pubs.acs.

org/CR Review

Influence of Oxygen-Containing Functional Groups on the

Environmental Properties, Transformations, and Toxicity of Carbon
Nanotubes
Alyssa R. Deline, Benjamin P. Frank, Casey L. Smith, Leslie R. Sigmon, Alexa N. Wallace,
Miranda J. Gallagher, David G. Goodwin, Jr., David P. Durkin, and D. Howard Fairbrother*

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ABSTRACT: Carbon nanotubes (CNTs) have unique physical and chemical properties
that drive their use in a variety of commercial and industrial applications. CNTs are
commonly oxidized prior to their use to enhance dispersion in polar solvents by deliberately
grafting oxygen-containing functional groups onto CNT surfaces. In addition, CNT surface
oxides can be unintentionally formed or modified after CNTs are released into the
environment through exposure to reactive oxygen species and/or ultraviolet irradiation.
Consequently, it is important to understand the impact of CNT surface oxidation on the
environmental fate, transport, and toxicity of CNTs. In this review, we describe the specific
role of oxygen-containing functional groups on the important environmental behaviors of
CNTs in aqueous media (e.g., colloidal stability, adsorption, and photochemistry) as well as
their biological impact. We place special emphasis on the value of systematically varying and
quantifying surface oxides as a route to identifying quantitative structure−property
relationships. The role of oxygen-containing functional groups in regulating the efficacy of
CNT-enabled water treatment technologies and the influence of surface oxides on other
carbon-based nanomaterials are also evaluated and discussed.

CONTENTS 7.2. Stability Toward Microbial Biodegradation 11669

7.3. Microbial Uptake and Toxicity 11669
1. Introduction 11652 7.4. Uptake, Translocation, and Biodistribution
2. CNT Surface Oxidation 11653 in Organisms 11670
3. Quantification of Surface Oxides 11655 7.5. Potential Routes of Cellular Toxicity 11671
4. Colloidal Stability and Transport 11657 7.6. Biopersistence 11673
4.1. Homoaggregation Behavior 11659 7.7. Implications for CNT Design 11674
4.2. Influence of Divalent Cations 11660 8. Applications in Water Treatment 11674
4.3. Influence of Other Media Components 11660 8.1. Impact of CNT Surface Oxygen on Mem-
4.4. Heteroaggregation and Transport 11662 brane Preparation 11674
5. Adsorption Properties 11662 8.2. Antibiofouling Properties of O-CNT Mem-
5.1. Adsorption of Organic Molecules 11663 branes 11675
5.2. Adsorption of Natural Organic Matter 8.3. Removal of Organic and Inorganic Contam-
(NOM) 11664 inants by O-CNT Membranes 11675
5.3. Adsorption of Metal Ions 11665 8.4. Water Desalination with O-CNT Membranes 11676
5.4. CNT-Facilitated Contaminant Transport and 8.5. O-CNT Filters in Advanced Oxidation Pro-
Trojan Horse Effects 11666 cesses 11677
6. Photochemical Transformations and ROS Gen-
eration 11666
6.1. Intentional CNT Photooxidation 11667
Received: April 23, 2020
6.2. Photodecarboxylation of O-CNTs 11667
Published: September 22, 2020
6.3. ROS Generation by Irradiation of O-CNTs 11667
6.4. Effects of ROS Interactions on O-CNTs 11668
7. Environmental Risk and Toxicity 11669
7.1. Stability During End-of-Life Incineration 11669

© 2020 American Chemical Society https://dx.doi.org/10.1021/acs.chemrev.0c00351

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Chemical Reviews
9. Impact of Surface Oxides on Other Carbon
Nanomaterials 11677
9.1. Colloidal Properties 11678
9.2. Adsorption Behavior 11679
9.3. Photochemical Transformations 11680
9.4. Toxicity 11680
10. Summary and Future Outlook 11681
Author Information 11682
Corresponding Author 11682
Authors 11682
Notes 11683
Biographies 11683
Acknowledgments 11683
Abbreviations 11684
References 11684
1. INTRODUCTION
Carbon nanotubes (CNTs) represent a versatile class of
engineered nanomaterials with potential in a wide range of
applications due to their unique physical, chemical, and
electronic properties.1,2 CNTs are composed of graphene
sheets rolled into seamless cylinders with ends that are either
open or capped with rounded, fullerene-like structures.3,4
CNTs can be single-wall (SWCNTs) or multiwall
(MWCNTs), depending on how many concentric cylindrical
layers of rolled graphene sheets make up the CNT diameter.4
SWCNTs are a single layer thick with diameters on the order
of 1−2 nm, while MWCNTs typically contain 2−30 concentric
layers resulting in a range of diameters on the order of 2−50
nm.4,5 The length of CNTs is variable but is commonly on the
order of tens of micrometers, resulting in large aspect ratios
that contribute to many of the desirable properties and
applications of CNTs.6
For example, CNTs possess great mechanical strength, with
tensile strengths approximately 100 times stronger and elastic
strain capacities 50 times greater than the strongest steel while
maintaining a much lower density.7,8 CNTs are also highly
thermally stable and possess thermal conductivities exceeding
that of copper and in some cases diamond.9−11 The electronic
properties of SWCNTs in particular are highly tunable: by
varying the chirality and nanotube radius, SWCNTs can be
controllably produced as metallic conductors, small band gap
semiconductors, or large band gap semiconductors.4,12
Conversely, MWCNTs are metallic and possess electronic
properties similar to graphite.13 Defect-free CNTs can also
conduct electrons inelastically, allowing for the conduction of
high currents without the loss of energy as heat.4,6 Collectively,
these properties have driven commercial applications of CNTs
in the reinforcement of composite materials, protective
coatings, microelectronics, energy storage, and biosensing.1
Notably, most CNT-enabled products are produced from
composite materials, in which CNTs are integrated into a
polymer matrix.1,5
Despite their many useful properties, as-produced CNTs are
not readily dispersible in aqueous or organic solvents and
commonly require extensive sonication for dispersion.14−16
This is a consequence of strong van der Waals forces between
individual CNTs, which lead to their aggregation into bundled
or rope-like structures, diminishing their desirable properties
and decreasing composite quality.15,17,18 Chemical functional-
ization of CNTs can overcome these limitations by tuning
interfacial properties through surface modification.19 Chemical
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modification of CNTs generally falls into one of two
categories: covalent modification of the CNT structure or
noncovalent adsorption of materials onto the exterior surface
of the CNT.19 The chemistry of CNT functionalization has
been reviewed previously.15,18,19
Noncovalent modification compromises neither the struc-
ture of the CNT nor the complete sp2 carbon hybridization of
CNTs; therefore, the desirable electronic and mechanical
properties of CNTs will persist while dispersion properties are
improved.20 For example, entrapment within surfactant
micelles can facilitate improved CNT dispersion in a variety
of solvents; this method is particularly effective with surfactants
possessing aromatic moieties due to attractive π-stacking
interactions with the hydrophobic CNT sidewalls while the
hydrophilic portion of the surfactant is free to interact with the
surrounding media.21 Additionally, larger molecules, such as
proteins, deoxyribonucleic acid (DNA), and polymers
containing sufficient hydrophobic regions can adsorb to and
wrap around the exterior of CNTs to yield stable
dispersions.19,21−24 Despite the number of useful applications
(e.g., medicine, chemical sensing, and photovoltaic devi-
ces),23,25 noncovalent modification has a number of disadvan-
tages. Noncovalent functionalization methods are driven by
equilibrium processes and are therefore dependent on
concentration, ionic strength, temperature, solvent character-
istics, and other factors.26−28 Furthermore, the interactions
between CNTs and modifying moieties that facilitate non-
covalent functionalization (e.g., π stacking, van der Waals
attractions, and hydrogen bonding) are weak and can easily be
nullified by the presence of solvents or other chemical
constituents with stronger affinities for modifiers.24,26−29
Covalent modification involves incorporating new functional
groups onto the CNT end-caps or sidewalls. As compared to
noncovalent approaches, covalent modification is largely
irreversible, which is critical for prolonged dispersion in
many solvents and for conducting further chemistry on
CNTs.30,31 CNTs can be covalently modified to introduce a
variety of functionalities, including fluorine moieties, alkyl
chains, polymers, amino acids, and small peptides.30−40 Strong
oxidizing agents (e.g., HNO3) or highly reactive chemical
reagents (e.g., carbenes, azomethine ylides) are usually
required to functionalize nanotubes because of the chemical
stability of CNT surfaces.19,41−43 The highly strained fullerene-
like structure of CNT end-caps results in more reactivity
toward modification techniques than the highly stable
graphenic CNT sidewalls, allowing for the selective function-
alization of these different CNT areas.2,13,39,44 Among the
various types of covalent surface modification strategies,
deliberately grafting oxygen-containing functional groups at
the ends and sidewalls of CNTs is by far the most popular and
versatile approach to functionalization.45,46 For this reason, the
effect of oxidation on the environmentally relevant properties
of CNTs is the focus of this review article.
Ultimately, the quantity of raw CNT materials and the
number of CNT-enabled products is increasing rapidly, with
current CNT production capacity exceeding several thousand
tons per year worldwide.1 As CNTs are produced, used, and
disposed of, they will inevitably be released into the natural
environment, which has inspired a growing body of research
on the environmental fate, transport, and toxicity of CNTs.5,47
As surface oxidation of CNTs is commonly required to enable
their use in many applications, CNTs can be expected to enter
the environment with a range of surface oxygen concentrations.
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Furthermore, once in the environment, the surface oxygen
content of CNTs can be further modified: for example, pristine
CNTs may be oxidized as a result of exposure to naturally
occurring reactive oxygen species in surface waters, while
oxidized CNTs (O-CNTs) may be decarboxylated as a result
of exposure to UVC irradiation during advanced wastewater
treatment processes.48,49 The primary goal of this review is to
provide the current state of knowledge on the specific role of
CNT surface oxidation in regulating the behavior and toxicity
of CNTs in environmentally relevant aqueous media. An
emphasis is placed on the quantitative relationships that have
been established between CNT surface oxidation and behavior,
as these relationships better enable the prediction and control
of the overall environmental risk of CNTs. This review does
not describe the impacts of other CNT properties (e.g., length)
in detail, except to provide relevant background information in
cases where these properties are directly influenced by
oxidative treatments or complicate the reported conclusions
regarding surface oxidation. The performance of CNT-enabled
water treatment technologies is discussed in addition to
environmental behavior, as these technologies directly relate to
the trade-off between the beneficial use of CNTs in
environmental applications and the potential negative environ-
mental impact of increased CNT production and consequent
release into aquatic ecosystems. Other CNT applications (e.g.,
medical and commercial) are absent from this review, as these
do not directly pertain to evaluating the effect of CNT surface
oxides on environmental risk.
The organization of this review is as follows: Section 2
describes the processes that can be used to introduce oxygen-
containing functionalities onto CNT surfaces. Section 3
discusses the analytical methods that have been developed to
assess the identity, concentration, and spatial distribution of
CNT surface oxides. Next, the focus shifts to detailing the
influence of surface oxides on important environmental
behaviors of CNTs. Section 4 covers the colloidal stability
and transport properties of CNTs in both simple and complex
aquatic media. Section 5 discusses the adsorption of organic
contaminants, metal ions, and natural organic matter (NOM)
onto CNTs. Section 6 summarizes the photochemical
transformations of CNTs, which can affect the quantity and
distribution of surface oxides. This section also discusses the
photogeneration of reactive oxygen species (ROS) when O-
CNTs are irradiated. Section 7 broadly encompasses topics
related to the environmental risk and toxicity of CNTs,
beginning with their relative resistance to thermal and
enzymatic degradation, continuing with details of their uptake
and toxicity to a variety of organisms and concluding with
implications for the design of environmentally benign CNTs.
Following these sections summarizing environmental effects
and behavior, section 8 describes the application of CNTs in
water treatment, specifically concentrating on the relationship
between CNT surface oxidation and the efficacy of CNT-
enabled membrane technologies. Section 9 extends the overall
analysis of the role of surface oxidation to other classes of
carbon-based nanomaterials, with a focus on the similarities
and differences with respect to CNTs. Section 10 concludes
the review with a summary of the relative impact of CNT
surface oxidation on environmental behavior. The remaining
knowledge gaps in this area of research are identified and
discussed.
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2. CNT SURFACE OXIDATION
When CNTs are prepared for a given application, surface
oxidation methods can be intentionally applied to enhance
dispersibility and/or create surface oxide platforms for further
modification. Surface oxides can also be formed unintention-
ally during common CNT purification techniques that use wet
chemical oxidants to remove metal catalyst impurities.50,51 As
part of intentional surface modification, functionalities such as
carboxyl, hydroxyl, and carbonyl groups can be grafted onto
CNT surfaces using wet chemical oxidation methods, plasma
treatments, microwave irradiation, photo-oxidation, or gas-
phase reactions.19,44,45,52−59 These strategies generate O-CNTs
that readily disperse in water or other polar solvents unlike
their pristine counterparts, allowing for homogeneous
dispersions and improved composite materials.46
In addition to improving dispersion and stability, the
deliberate addition of surface oxides is a means to introduce
chemical functionality and provide convenient handles for
conducting further chemistry on CNTs.39,60 For example,
carboxylic acid groups on CNTs can be chemically
manipulated, via coupling with ethylenediamine or other
reagents, to provide amine-terminated sites through which
DNA, enzymes, and other biomolecules may be covalently
linked to CNT surfaces, enabling the use of O-CNTs as
cellular delivery agents or in biosensing applications.61−65
Oxides on CNTs can also serve as attachment points for
metallic and semiconducting nanoparticles or their precursors,
which can facilitate controlled synthesis of nanoparticles (NPs)
directly on CNT surfaces.60,66 In this respect, O-CNTs
decorated with metal NPs (e.g., Ru, Mn, Co, and Ag) are
highly useful as electrodes in supercapacitors and lithium ion
batteries for energy storage; they also have applications in
energy production as components of flexible and optically
transparent electrodes in solar cells.67−71 Using CNTs as
supports for catalytic metal NPs provides advantages over
traditional supports, such as carbon black, due to the unique
structural and electronic properties of CNTs, including high
conductivity and surface area.60,66,72
It is important to note that CNT oxidation can also have
drawbacks. For example, sonication and treatment with strong
acids introduces defects and bends.54,55 If chemical oxidation
processes are allowed to proceed too far, they can lead to
decreased CNT structural integrity, shortening, or break-
age.45,52,54,55,73 Some chemical and photooxidation processes
cause the unzipping and removal of outer MWCNT layers,
decreasing the outer CNT diameter.74−76 “Oxidative debris”
created by oxidation processes can include these released outer
layers, other CNT fragment types, and partially oxidized
carbonaceous matter; the presence of this debris can confound
experimental data or impact CNT surface chemistry though
adsorption to sidewalls.77−79 Another potential result of CNT
overoxidation is the increased disruption of the continuous sp2
carbon hybridization, which can result in the loss of the unique
electronic properties of CNTs as they become insulat-
ing.46,54,71 Overall, even in studies where CNT surface oxygen
has been successfully controlled and quantified, it is also
important to evaluate the effects of the oxidation method on
other relevant structural and electronic characteristics.
The oxidation method chosen will continue to affect CNT
behavior after disposal of CNT-enabled products and
subsequent release of CNTs into the environment, as these
methods determine the resultant concentration of surface
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oxides in addition to their chemical structure and spatial
distribution. Each of these characteristics can impact the
environmental fate, transport, and toxicity of CNTs. Therefore,
to best evaluate the influence of CNT oxidation on
environmental behavior, researchers must be able to system-
atically vary the concentration and nature of oxygen moieties
while avoiding changes to other CNT properties.
Several functionalization approaches are particularly useful
for systematic tuning of surface oxidation. Wet chemical
methods, in which CNTs are refluxed or sonicated in an
oxidizing solution, are widely utilized due to their simplicity
and accessibility. This strategy can be utilized to vary both the
overall extent of oxidation and the identity of the specific
functional groups imparted. For example, Smith et al. showed
that adjusting the w/w % concentration of HNO3 used for
refluxing offers great control in altering the total surface oxygen
concentration of MWCNTs (Figure 1a).80 While this work
Figure 1. (a) Controlled surface oxidation of MWCNTs by varying
the concentration of HNO3 oxidant used. Reproduced with
permission from ref 80. Copyright 2009 American Chemical Society.
(b) Results of chemical derivation in conjunction with XPS analysis,
used to show the impact of different oxidants on the relative
contributions of different oxygen-containing functional groups on
MWCNTs. Reproduced with permission from ref 83. Copyright 2010
Elsevier.
found that HNO3 treatment generates mainly carboxylic acids,
others have shown that the initial CNT properties can affect
the identity of functional groups imparted. Hydrothermal
treatment in varying concentrations of HNO3 produced mainly
hydroxyl groups for both SWCNTs and large diameter (25−40
nm) MWCNTs, while MWCNTs with a similar diameter to
those used by Smith et al. (10−20 nm) were primarily
functionalized with carboxylic acids.81,82 Each of these studies
reported a strong correlation between total surface oxidation
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and HNO3 concentration, with no effect on the proportional
contribution of different functional groups, indicating that this
facile method also offers superior control of surface chemistry.
Alternatively, changing the identity of the oxidant (e.g.,
KMnO4 vs HNO3) can alter both the overall extent of
oxidation and the relative amounts of different types of oxygen-
containing functional groups in the resultant O-CNTs, as
shown in Figure 1b.83 Studies by Wepasnick et al., Datsyuk et
al., and Avilés et al. have compared the effects of different
oxidants on MWCNT functionalization.52,54,83 These studies
found that the greatest total surface oxygen concentrations can
be achieved using concentrated HNO3 or strong oxidizing
mixtures like HNO3/H2SO4 (in a 3:1 ratio) or KMnO4/
H2SO4. Wepasnick et al. reported that carboxylic acids make
up the majority of the functional groups imparted by these
mixtures (Figure 1b),83 in good agreement with previous
studies.84,85
Weaker oxidants include dilute acids, H2O2, and O3.52,54,83
H2O2 and O3 treatments were shown to primarily add carbonyl
groups (Figure 1b),83 but other studies have reported greater
quantities of hydroxyl (with H2O2 treatment) or ether (with
O3 treatment) functionalities forming, depending on the initial
CNT characteristics (e.g., SWCNT vs MWCNT) and the
temperature and length of treatment.86−88 Other oxidants that
impart high levels of hydroxylation include NaOH and
NaAlO2.89 Beyond wet chemical methods, photooxidation
with ultraviolet (UV) light can also be employed to increase
the total surface oxygen concentration as a function of
irradiation time, with mainly ether and epoxy groups formed.57
Similarly, the extent of CNT surface oxidation can be varied
through increasing exposure to a plasma discharge (e.g., an
oxygen, hydrogen, or argon-fed plasma).59,90
It is important to note that unlike increasing the
concentration or strength of the oxidant, increasing the
exposure time will not always result in a greater concentration
of surface oxygen. In some instances, periodic cycling between
low and high oxygen concentrations has been observed for
both H2SO4/HNO3 and UV/H2O2 treatments.74,75 Once a
maximum surface oxygen concentration is reached in these
conditions, extending the reaction time causes the outer layers
of the MWCNTs to unzip and shed, which reveals a pristine
MWCNT layer with low functionalization density.74,75
Oxidation using a KMnO4/H2SO4 treatment is also known
to cause unzipping and shedding of outer layers, due to the
ability of the oxidant to act as an intercalant.76 This reinforces
the idea that when the surface oxidation is varied using
different oxidant mixtures or oxidation times chemical
information on the degree of oxidation must be accompanied
by structural analysis to ensure that there are not
accompanying differences in the diameter or number of layers
of the resultant O-MWCNTs.
Further variation of the proportion of different oxygen-
containing functional groups can be achieved after any
oxidative treatment through the thermal treatment of O-
CNTs under vacuum. Initially, at temperatures between 225
and 525 °C, carboxylic acid functional groups decompose
while hydroxyl and carbonyl groups remain intact.80,91 The
remaining functional groups are then removed at higher
temperatures, with the vast majority of all oxygen-containing
functional groups eliminated after thermal treatment at 1025
°C.91 Detailed mechanisms for the thermal decomposition of a
variety of oxygen-containing functional groups were presented
by Chernyak et al.92 This work showed that the activation
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energy for decomposition is linearly correlated to the O/C
ratio of the functional group, which is consistent with
observations that decomposition temperature increases in the
order of carboxyl < anhydride < hydroxyl ≤ ether
functionalities.92 Notably, the temperature ranges of decom-
position can vary depending on the heating rate,92 which
should be considered when utilizing thermal treatment
methods reported in the literature.
Overall, methods for controlling the nature and concen-
tration of CNT surface oxygen are well-established, although
certain oxidation methods provide greater systematic control
over those two factors than other methods. Considering the
totality of the literature discussed in this section, treatment of
CNTs with HNO3 at increasing concentrations provides the
most straightforward and least resource-intensive route toward
obtaining CNTs with well-controlled surface oxygen concen-
trations. To control the nature of oxygen functional groups the
most versatile and well-established method is a two-step
approach utilizing using wet chemical oxidation methods
followed by thermal treatment to remove specific functional
groups (e.g., carboxylic acids). Figure 2 illustrates different
Figure 2. Summary of commonly utilized pathways for the oxidation
of CNTs and the selective removal of specific functional groups.
pathways to the selective variation of different functional
groups. Future work in the area of controlled CNT oxidation
should determine the exact role that initial CNT characteristics
such as diameter and defect density play in dictating the
specific proportion of different oxygen containing functional
groups, which will better enable the predictive design of
oxidative treatments.
3. QUANTIFICATION OF SURFACE OXIDES
Once O-CNTs are functionalized, their surface properties must
be rigorously characterized to enable predictive relationships
between CNT surface oxidation and environmental behavior.
The full suite of available analytical techniques for character-
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izing CNTs has been previously reviewed.93 In this section, we
focus primarily on techniques that can be used to define the
total surface oxygen concentration, the nature of different
functional groups present on O-CNTs, and the spatial
distribution of functional groups.
Most analytical techniques applied to CNT surface
characterization are effectively bulk measurements, either by
the nature of the analysis or due to the small diameters of
CNTs. Elemental combustion analysis can be used to
determine the mass fractions of C, H, and N within a sample
of O-CNTs, with the remaining mass difference assumed to be
the concentration of O.94 This technique can be impacted by
the presence of metal oxide catalyst impurities residual from
CNT synthesis, which will result in an overrepresentation of
the oxygen concentration. While destructive, this technique
requires a relatively small amount of sample (∼1−2 mg).
Similar to the subtractive approach of elemental analysis,
thermogravimetric analysis (TGA) can also be used to
determine the weight percentage of functional groups on
CNT surfaces. In TGA, functionalized CNTs are thermally
degraded in the presence of oxygen in multiple stages: initial
mass losses from 100 to 180 °C correlate to release of
moisture, mass losses from 180 to 450 °C correlate to
functional groups covalently bound to CNTs, and mass losses
above 450 °C correlate to CNT combustion, with remaining
ash attributed to metal impurities.95,96 Furthermore, if the
identity of the functional groups is known through another
method, the molar percentage can be estimated. Like TGA,
temperature-programmed desorption (TPD) also involves
heating CNTs to remove functional groups as volatile
species.97,98 However, in TPD, the volatile products are
collected and analyzed by mass spectrometry to enable the
identification and quantification of the desorbed species. The
major disadvantage of both TGA and TPD is that the similar
structures, surface bonding, and decomposition products of
many oxygen-containing surface functionalities result in an
inability to discern the contributions of different functional
group types in a single O-CNT sample. TPD in particular
requires the deconvolution of broad overlapping peaks with a
low signal-to-noise ratio to report these concentrations. Both
techniques also require a relatively large amount of sample (∼5
mg) and are intrinsically destructive measurements.99 While
these techniques can complement other analyses, they lack the
sensitivity and chemical information provided by other
methods and are not a reliable source of data on CNT surface
oxidation.
Another commonly utilized bulk analysis technique is energy
dispersive X-ray spectroscopy (EDX or EDS), in which the
elemental composition of a sample is determined through the
release of characteristic X-rays. EDX can be used to quantify
the total atomic percentage of oxygen on O-CNTs using a very
small amount of sample (≪1 mg), but cannot determine the
specific type of functional groups present or distinguish oxygen
present in metal oxide catalyst impurities from oxygen present
in surface functional groups.83,100,101 Often, bulk analysis
techniques that measure total oxygen concentration are used as
an orthogonal complement to Fourier transform infrared
(FTIR) spectroscopy. FTIR spectroscopy allows for the
identification of organic functional groups present in a sample
through the measurement of vibrational modes associated with
time-dependent changes in the molecular dipole moment. IR
spectroscopy serves as a useful supplement to other analytical
techniques but cannot be employed as the standalone measure
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of CNT surface chemistry due to its nonquantitative nature
and lack of sensitivity for some functional groups.93
Another approach to characterizing CNT surface chemistry
is the use of wet chemical titration methods that exploit
differences in pKa between different oxygen-containing
functionalities to provide both quantitative and qualitative
information. In Boehm titrations, acidic functional groups are
neutralized by a suite of bases with varying basicity, typically
NaOH, NaHCO3, and Na2CO3.102 The difference in the
quantity of each base required for neutralization is used to
calculate the concentration of carboxyl, hydroxyl, and lactonic
(i.e., a cyclic carboxylic ester) functional groups on CNT
surfaces.103−105 Alternatively, potentiometric titrations are
performed with a single strong base (i.e., NaOH), where the
change in pH with each known volume of base is recorded and
utilized to develop a proton binding isotherm, which is then
analyzed to determine the concentration and acid-strength
(i.e., pKa value) of each functional group present.106,107 Results
from potentiometric titrations correlate strongly to Boehm
titrations due to the dependence on functional group pKa in
both approaches, and results can be quantitatively identical
when the pH value of the potentiometric titration end point is
chosen to reflect the equilibrium pH of the Boehm base
utilized.108 These titration-based analyses are useful in that
they provide the absolute concentrations of each different
functionality type, but they are limited in that aprotic
functionalities will not be detected and there can be overlap
of pKa values between some functional groups.93 While these
techniques require more sample material than many
spectroscopic methods (>10 mg), they are rapid and facile
quantitative analyses that can be performed routinely without
specialized equipment.
Because of its surface sensitive nature and ability to provide
detailed information about both chemical composition and
bonding, X-ray photoelectron spectroscopy (XPS) is one of the
most widely utilized techniques for examining the surface
properties of CNTs. In this method, CNT samples are
irradiated with X-rays, ejecting photoelectrons that travel with
distinct kinetic energies, as a result of their different binding
energies that are regulated by the element and surrounding
chemical bonding environment from which they originate. The
total oxygen composition is determined by comparing the
overall peak areas of the C 1s and O 1s signals. The oxygen
concentrations measured via XPS directly correlate to those
measured via EDX (R2 = 0.70), with the surface sensitivity of
the XPS technique resulting in higher values for at. % O
overall.83 Oxygen concentrations measured via XPS are less
likely to be impacted by oxygen arising from the presence of
metal catalyst impurities than those measured via bulk
analyses, as these catalysts are present within the hollow
CNT interior as opposed to CNT surface.93
Determination of the relative amounts of different oxygen-
containing functional groups by XPS is more complicated than
determining the overall surface oxygen concentration. This
requires deconvolution of the C 1s spectra into multiple peaks
arising from C−C, C−O, CO, and O−CO bonding
environments as well as a π−π* shakeup feature. When carbon
is bonded to atoms with increasing electronegativity, there is a
shift in the binding energy and, as a result, multiple peak
components arise in the C 1s region of the spectra. Peak fitting
of these components to determine their relative contributions
is often subjective, as the results are highly dependent on the
full width at half-maximum and binding energy values assigned
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to each feature during data analysis, as discussed by Wepasnick
et al.93 Peak fitting may also be affected by the binding energy
resolution of the instrument used to collect the data as well as
the signal-to-noise ratio achieved during collection. To
overcome limitations in peak fitting, selective chemical
derivatization reactions can be used in conjunction with XPS
analysis to quantify specific functional groups. Several chemical
derivatization schemes have been applied to O-CNTs for this
purpose,109,110 most notably the gas-phase fluorine-labeling
method originally developed by Langley et al. for the analysis
of a wide variety of carbonaceous materials.58,83,111−114
Wepasnick et al. further refined this technique for CNTs.83
In this method, the derivatizing agents trifluoroacetic acid,
trifluoroethanol, and trifluoroethyl hydrazine are utilized to
specifically react and tag hydroxyl, carboxylic acid, or carbonyl
functional groups, respectively.111 For each individual reaction
and tagged product, the F 1s signal is directly representative of
the quantity of the specific functional group labeled, except in
the case of carboxylic acid groups, where the N 1s and F 1s
signals must be used in tandem due to the formation of an N-
acyl urea in a side reaction.83 This method has been used to
quantify the contribution of different oxygen-containing
functional groups to the total oxygen concentration imparted
by a variety of oxidants (Figure 1b).83 While chemical
derivatization is a powerful tool for quantifying the most
common CNT oxygen-containing functionalities, some func-
tional groups like ethers and esters cannot be labeled, instead
requiring a subtractive approach to estimate their relative
contribution.83,93 In addition, XPS analysis used in conjunction
with chemical derivatization requires a relatively large amount
of sample, on the order of 1−2 mg per derivatization reaction
for a total of approximately 5 mg per CNT sample analyzed
(depending on sample preparation and instrument capabil-
ities).93
Two additional advanced techniques for the identification of
specific O-containing functional groups are electron energy
loss spectroscopy (EELS) and near-edge X-ray absorption fine
structure (NEXAFS). EELS is used to analyze the energy
distributions of incident electrons that are inelastically
scattered as they interact with atoms in the CNT sample.
This energy loss is greater than or equal to the binding energy
of the electrons in the CNT sample that interact with the
incident electrons, which results in absorption edges in the
EELS spectrum at element-specific energies. The spectral
intensity of the oxygen adsorption edge can be compared to
that of other elements to determine the atomic percentage of
oxygen in a CNT sample, while the near-edge structure of the
C K-edge (C 1s) spectra provides information on the local
bonding environment (i.e., sp2- and sp3-hybridized carbon and
the ratio of σ* to π* antibonding orbital character).115 Similar
to EELS, NEXAFS also creates element specific absorption
edges, with a near-edge structure that provides information on
the local bonding environment. NEXAFS requires a tunable X-
ray source typically provided by a synchrotron, limiting the
ease of its routine use. The challenges in deconvoluting the fine
structure to determine relative contributions of different
bonding environments are similar to those in XPS peak fitting,
due to the close proximity of different spectral components.93
NEXAFS has been used to quantify the relative amounts of
carboxylic acid groups and hydroxyl groups on O-CNT
surfaces, with results in good agreement with potentiometric
titration techniques.116
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Figure 3. TEM micrographs showing MWCNTs treated with (from left to right): no oxidants (final concentration of 0.9 at. % O), H2O2 (4.5 at. %
O), a mixture of H2SO4 and HNO3 (5.1 at. % O), and KMnO4 (5.3 at. % O). Arrows indicate amorphous carbon, and circles indicate sidewall
defects. Reproduced with permission from ref 83. Copyright 2010 Elsevier.
In addition to the total oxygen concentration and the
specific functional groups present on O-CNTs, it is important
to also consider that the spatial distribution of these functional
groups can impact environmental behaviors in multiple ways.
Differences in the oxidation of CNT tips vs sidewalls have
important implications for contaminant rejection and water
flux through the CNT tubular structure when CNTs are used
in water filtration membranes,117 while the formation of high
local concentrations of oxygen groups results in electrostatic
patches that are known to control nanoparticle aggregation and
membrane disruption properties.118,119 Although spectroscopic
in nature, EELS and NEXAFS can also provide spatial
information. EELS can be used in conjunction with trans-
mission electron microscopy (TEM) to develop high
resolution elemental maps, which have been applied to
CNTs to show the location of sulfur atoms present in
thiolated functional groups as well as the distribution of boron
dopants in the CNT structure.120,121 At this time, direct
imaging of oxygen-containing functional groups using EELS is
limited to a resolution of ∼5 nm using the carbon K-edge,
requiring rigorous statistical analysis and peak deconvolution
for data interpretation.122 However, recent advancements in
imaging fluorine and other light elements at the single-atom
level using EELS could enable its use in conjunction with
chemical derivatization to examine the spatial distribution of
specific functional groups with enhanced resolution, a powerful
path forward in CNT surface characterization.123 Currently the
resolution of NEXAFS imaging is limited to approximately 25
nm, precluding the imaging of individual moieties on CNT
surfaces, though resolution continues to improve.124 Despite
current limitations, both EELs and NEXAFS are used for O-
CNT surface characterization without imaging.125−127
Another technique for examining the spatial distribution of
oxygen on CNT surfaces is the labeling of carboxylic acids with
titanium dioxide nanoparticles (TiO2 NPs), which are then
imaged using atomic force microscopy, TEM, or scanning
electron microscopy (SEM).128 The TiO2 NPs covalently
attach to the carboxylic acids via an ester-type linkage through
hydroxyl groups present on TiO2. While the increase in TiO2
NP density observed by X. Li et al. for CNTs exposed to more
aggressive oxidation methods is in qualitative agreement with
the increase in carboxylic acids observed by Wepasnick et al.
using chemical derivatization, the specificity of TiO2 NP
labeling to carboxylic acid groups in particular has not been
experimentally verified.83,128 In a similar labeling approach that
offers enhanced spatial resolution, Marichy et al. labeled CNT
surface oxygen groups using atomic layer deposition of TiO2,
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allowing for CNT defect sites to be imaged using a
combination of high-resolution TEM (HR-TEM) and high-
angle annular dark-field scanning transmission electron
microscopy (HAADF-STEM)129 HAADF-STEM has also
been used to image Eu [III] ion labels that covalently bind
to CNT surface oxides.130,131 While these labeling techniques
offer some advantages in the visualization of CNT surface
oxygen groups, some spatial information can be obtained
without the application of labels. TEM imaging alone can be
used to visualize the presence of defects that accompany
aggressive oxidation techniques as well as the presence of
surface adsorbed amorphous impurities, as described in detail
by Wepasnick et al.83 Figure 3 illustrates how TEM analysis
can be utilized to provide spatial information regarding the
impact of different oxidizing agents on both amorphous carbon
and sidewall defects.
Ultimately, rigorous characterization using complementary
techniques will enable the strongest conclusions to be drawn
on the impact of CNT surface properties to environmental fate
and toxicity. In addition to surface characterization, it is
important to characterize other properties like defect formation
and CNT size before and after oxidative treatments, to ensure
that CNT surface functionalization is the only parameter
varied within a study. The presence of defects can be
quantified with Raman spectroscopy using the characteristic
D-band and G-band peaks, which appear at 1330 and 1590
cm−1, respectively.83,132−134 Here, the G-band corresponds to
sp2 carbon atoms present in the graphenic sidewalls of CNTs,
while the D-band corresponds to sp3 carbon atoms present at
defects.83,132−134 The D-band is also impacted by the presence
of surface adsorbed amorphous carbon.134 The ratio of D- and
G-band intensities (ID:IG) therefore signifies the relative
quantity of defects and impurities.83 The distributions of
CNT lengths and diameters are typically assessed using atomic
force microscopy (AFM) or electron microscopies (SEM/
TEM), while HR-TEM is used to determine the number of
concentric MWCNT layers. The following sections in this
review will detail the use of the analytical techniques discussed
here to determine the impact of CNT surface oxidation on key
environmental behaviors of CNTs.
4. COLLOIDAL STABILITY AND TRANSPORT
Colloidal stability is the predominant factor controlling the
environmental risk of engineered nanomaterials like
CNTs.135,136 The propensity for CNTs to aggregate with
themselves (homoaggregation) or other colloidal materials
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Table 1. Methods Used in Studies of the Effect of CNT Oxygen Concentration on Colloidal Stability
CNT O content methods used for primary method used for examining
(at. % O) quantifying O content media tested stability ref
0.4−13.7 SEM with EDX 5% infasurf in saline, RPMI media CNT aggregate size via DLS Hamilton Jr.
et al.100
not quantified not quantified RPMI media, BEGM CNT aggregate size via DLS and TEM Ursini
et al.143
0.01−0.16 O/Ca XPS water, ethanol, hexane CNT aggregate size via Coulter counter, Ma et al.144
surface energies of CNT films
pristine vs 1.3 TGA 0−0.05% BSA in PBS, 10% FBS in DMEM CNT concentration after settling via Allegri et al.96
mol %b UV−vis
2.5−9.5, elemental analysis, XPS pH 1.5−11, 0−240 mM NaCl, 0−2 mM CaCl2, 0−100 CNT concentration after centrifugation via Bai et al.94
5.4−16.3 mg/L fulvic acid UV−vis
1.5−5.7 XPS TG201 media, MHRW, and M7 media each with CNT concentration after settling via Glomstad
added SR-NOM; natural fresh lakewater UV−vis et al.145
pristine vs manufacturer reported MHRW with added SR-NOM CNT concentration after settling via Kennedy
1.23−1.76 UV−vis et al.142
wt %c
2−4 XPS MES, MOPS, or HCO3 buffered to pH 5 or 7, SRHA CNT concentration after settling via Schwyzer
or SRFA added, 0−2 mM CaCl2 UV−vis et al.146
0.9−7.0 XPS MOPS buffered to pH 7 with SRHA added, 0−2 mM CNT concentration after settling via Schwyzer
CaCl2 UV−vis et al.147
2.8−7.3, elemental analysis, XPS ultrapure water CNT concentration after centrifugation via Zhang
1.4−13.8 UV−vis et al.103
2−10.8 XPS with chemical acetate or HCO3 buffered to pH 4−8, NaCl Initial CNT aggregation rate via TR-DLS Smith et al.80
derivatization
1.2−8.1 XPS with chemical pH 3−10, 0−200 mM Na2SO4, 0−900 mM NaCl, 0−8 Initial CNT aggregation rate via TR-DLS Smith et al.58
derivatization mM MgCl2, 0−6.2 mM CaCl2
14.7−34.8 SEM with EDX 0−300 mM NaCl, 0−50 mM MgCl2 Initial CNT aggregation rate via TR-DLS Wu et al.101
C/COOHd
pristine vs 1.6 manufacturer reported 0−20 mM NaCl, 0−0.6 mM CaCl2 CNT concentration after heteroaggregation Bouchard
wt %e with sediments via UV−vis et al.148
3.1−11.5 XPS with chemical pH 4−10, 0−4.1 mg DOC/L SR-NOM, 0−1000 mM Transport of CNTs through porous media Yang et al.113
derivatization NaCl, 0−100 mM CaCl2 via column experiments
6.3−10.6 XPS with chemical HCO3 buffered to pH 7.1, 0−1000 mM NaCl, 0−10 Initial CNT aggregation and deposition Yi and
derivatization mM CaCl2 rates via TR-DLS and QCM-D Chen112
a
CNT oxidation was reported as the O/C ratio as opposed to % elemental composition. bCNT functionalization was estimated for one reference
CNT and assumed to apply to all CNTs studied. cCNT functionalization with COOH and OH was reported by manufacturer as wt % and not
further quantified. dCNT oxidation was reported as the C/COOH ratio, all O was assumed to be from COOH. eCNT functionalization with OH
was reported by manufacturer as wt % and not further quantified.

present (heteroaggregation) determines their transport in
ground and surface waters, which defines CNT exposure and
bioavailable dose.137,138 In surface water, aggregation controls
whether CNTs remain in suspension in the water column or
settle out of solution into sediment, while in groundwater,
aggregation controls whether CNTs deposit in porous media
or maintain their mobility.135 Aggregation processes also alter
the effective surface area and size distribution of CNTs, which
can control reactivity and thus affect toxicity.138,139
Oxidative treatments are often utilized to improve CNT
dispersibility in industrial and commercial applications;
consequently, these treatments will continue to affect colloidal
stability after CNTs are released into environmental systems.80
In this section, trends linking CNT surface oxidation to
colloidal stability and transport will be discussed, with special
emphasis placed on quantifiable relationships that contribute
to predictions of environmental behavior when the properties
of both the CNTs and surrounding media are known.
Several experimental methods have been utilized to examine
the impact of oxygen-containing functional groups on CNT
colloidal stability, as summarized in Table 1. Qualitative
evaluation of visual changes to CNT suspensions over time has
the benefit of rapid, facile comparisons between large
differences in CNT stability. This method is commonly used
as supplemental evidence in conjunction with the quantitative
measurements necessary to establish predictive relationships.
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One type of quantitative comparison is the evaluation of CNT
aggregate size distribution after exposure to the media of
interest by utilizing SEM, TEM, Coulter counting, nanoparticle
tracking analysis, or dynamic light scattering (DLS). These
static size measurements are valuable, but they do not allow for
kinetic modeling and they are highly susceptible to
experimental artifacts. For example, a static DLS measurement
may not capture all particles if some have settled out of
solution, while CNT aggregates observed via SEM or TEM
may be impacted by drying effects. Another quantitative
approach is the monitoring of CNT concentration in
suspension over time using ultraviolet−visible/near-infrared
(UV−vis/NIR) spectroscopy or total carbon analysis. CNT
settling data has been modeled using the simple exponential
decay equation (t) = C0e−kt, in which k is the observed rate
constant of sedimentation and C0 is the initial CNT
concentration.140−142 From this data, half-life (t1/2) and k
values can then be compared between suspensions with
different CNT or media properties.140−142 This approach can
be used to examine CNT homoaggregation with other CNTs
or heteroaggregation with model colloids and natural sedi-
ments.
The most powerful methods for establishing quantitative
relationships between CNT stability and surface oxidation
allow for the modeling of colloidal stability and transport using
classical Derjaguin−Landau−Verwey−Overbeek (DLVO
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theory).136 These include time-resolved dynamic light
scattering (TR-DLS), quartz crystal microbalance with
dissipation monitoring (QCM-D), and packed bed column
experiments. DLVO theory defines the probability of attach-
ment between two colliding particles as the sum of van der
Waals and electric double-layer potential.149,150 Particle
stability is imparted by electrostatic repulsion, which for
CNTs is controlled by the magnitude of negative surface
charge.136 To achieve stability, electrostatic repulsion must
outweigh attractive van der Waals forces.149,150
With TR-DLS, the initial aggregation rate can be determined
by finding the slope of the initial linear increase in the
hydrodynamic diameter (Dh) over time,( dDh dt )t → 0 . In solutions
with high ionic strength, the energy barrier to aggregation
caused by electrostatic repulsion is eliminated, resulting in a
“diffusion-limited” fast aggregation rate of ( dDh dt )fast . In
solutions with lower ionic strength, aggregation is “reaction-
limited” and requires the energy barrier to be overcome,
resulting in a slower, ionic strength-dependent aggregation rate
of ( KDh Kt )slow . Normalizing the slow aggregation rate by the fast
aggregation rate results in the aggregation attachment
efficiency (αa), assuming that the initial number concentration
of particles (N0) is equivalent in both conditions, as shown in
eq 1.151
1 dD
( h dt )t → 0,slow
N0
αa = 1 dD
( h dt )t → 0,fast
N0 (1)
αa represents the probability that a collision between two
particles will result in permanent attachment. The minimum
concentration of a given electrolyte required to reach fast,
diffusion-limited aggregation where αa = 1 is the critical
coagulation concentration (CCC). A higher CCC indicates
CNTs that are more resistant to aggregation than those with a
lower CCC. The Schulze−Hardy rule dictates that the CCC
for an electrolyte with a given charge valence (Z) will be
proportional to Z−2 for CNTs with low ζ-potentials and Z−6
for CNTs with high ζ-potentials, with the dependence for most
nanomaterials falling between these extremes.152
Similarly, QCM-D can be used to examine the deposition
behavior of CNTs on model surfaces. Analogous to αa, the
deposition attachment efficiency (αd) is the ratio of the initial
deposition rates measured in reaction-limited vs diffusion-
limited conditions. αd is the probability that a collision
between a CNT and the model surface will result in permanent
attachment and can be determined from shifts in measured
frequency that result from mass deposited on the QCM-D
crystal. Likewise, the critical deposition concentration (CDC)
is the minimum concentration of electrolyte required to reach
rapid, diffusion-limited deposition. Packed-bed column trans-
port experiments can also be used to determine αd and CDC
by analyzing the concentration of CNTs in the column effluent
after they pass through a porous medium (e.g., quartz sand).
As discussed in detail by Elimelech et al., the transport of
CNTs and other colloids through porous media is controlled
by particle advection, dispersion, and deposition (filtra-
tion).153−155 When the effluent CNT concentration is modeled
using the one-dimensional advection-dispersion equation with
an additional term for particle deposition, the first-order
deposition rate coefficient kd can be determined experimentally
under a range of ionic strength conditions. Comparing the
ratio of kd values measured in reaction-limited vs diffusion-limit
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conditions enables the calculation of αd and CDC for the
specific CNT, collector, and media conditions utilized.
In studies of CNTs, quantifiable metrics like αa, αd, CCC,
and CDC values can be used to determine predictive
relationships between surface oxygen content and colloidal
stability or transport. Overall, the facile and quantitative nature
of TR-DLS makes this technique the best choice for studying
CNT homoaggregation in a variety of solution conditions, as
well as heteroaggregation in systems where a relevant model
colloid can be procured in a monodisperse suspension. When
natural colloids and sediments are studied, the most efficient
method for comparing the extent of CNT heteroaggregation is
a subtractive approach where large heteroaggregates are
separated using filtration or centrifugation before CNTs
remaining in suspension are quantified using UV−vis analysis.
Collectively, the techniques discussed in this section have
enabled the discovery of many useful quantitative relationships
between CNT surface oxidation and aggregation behavior.
4.1. Homoaggregation Behavior
The effects of oxygen concentration and oxygen functional
group distribution on CNT stability are most evident in
ultrapure water or monovalent electrolyte solutions. In these
simple media, CNT functionalization with carboxylic acid and
hydroxyl groups has consistently been shown to increase the
magnitude of negative surface charge, enhancing colloidal
stability by increasing electrostatic repul-
sion.58,80,94,101,103,144,156 While individual studies have shown
that CNT electrophoretic mobilities, ζ-potentials, and surface
charge densities can all be affected by surface oxidation, the
most systematic relationship has been observed between the
surface charge density determined by potentiometric titration
and the surface oxygen concentration determined by XPS.80
Smith et al. used a suite of CNTs functionalized to achieve 12
different surface oxygen concentrations ranging from 1.0 to
10.8 at. % to show the magnitude of surface charge density had
a strong linear correlation to surface oxidation (R2 = 0.89),
with slope increasing with pH. Carboxylic acid groups, assayed
by XPS in combination with vapor-phase chemical derivatiza-
tion, were shown to have the strongest contribution to this
effect. The surface concentration of carboxylic acid groups
described 72% of the variability in CCC, but CCC remained
most correlated to the total concentration of surface oxygen,
indicating that other functional groups also contribute to
stability. Ultimately, a coplanar relationship was discovered
that links colloidal stability to the solution pH and CNT
surface oxygen concentration, revealing that CNTs behave in
accordance with classical DLVO theory (Figure 4).80
These results are corroborated by other studies that show a
similar linear dependence of colloidal stability on surface
oxidation and pH. Bai et al. found that CCC systematically
increased with oxygen content regardless of whether XPS (R2 =
0.92) or elemental combustion analysis (R2 = 0.95) was used
to determine oxygen concentration.94 However, the range of
CNT oxygen concentration was greater when measured with
XPS (5.4−16.3 at. % O) than with elemental analysis (2.5−9.5
at. % O), resulting in a steeper slope when oxygen content was
determined with elemental analysis.94 Caution should there-
fore be used in comparing specific regression equations
between studies utilizing different methods for determining
oxygen concentration, as the surface sensitivity and limit of
quantification differs between methods. The range of NaCl
CCC values determined in this study at pH 7 (6.2−108.1 mM)
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Table 2. Reported CCC Values for NaCl vs CaCl2 in Studies

of Oxidized CNTs
CNT O Content CCC, mM CCC, mM Z
(at. % O) NaCl CaCl2 ratio ref
8.1 93 1.2 Z−6.3 Smith et al.58

6.3 53 0.9 Z−5.7 Yi and

10.6 210 1.0 Z−7.9 Chen112

pristine 60 ∼2.0 Z−4.9 Bouchard

1.6 wt % OH 90 ∼2.0 Z−5.5 et al.148

2.0 2.0 0.11 Z−4.2 Bai et al.94

Figure 4. Three-dimensional plot illustrating the coplanar depend-
ence of critical coagulation concentration (CCC) on CNT surface
oxygen concentration and solution pH. Reproduced with permission
from ref 80. Copyright 2009 American Chemical Society.
were similar to the range of values determined by Smith et al.
at pHs 6 and 8 (50−180 mM).80,94 Other studies with two-
point comparisons between oxidized vs pristine CNTs or high
vs low oxidation CNTs also reported the expected increase in
NaCl CCC for CNTs with greater oxidation.58,112,157
Only one study reported a deviation from a linear increase in
CCC vs % O: Z. Wu et al. showed that while CCC values
increased systematically from 9.7 to 13.4 wt % O, they reached
a maximum of 169 mM NaCl and remained stable from 13.4 to
14.5 wt % O.101 This difference from other studies is likely
because the oxygen content was determined by EDX, which is
less sensitive to changes in surface chemistry than XPS analysis,
increasing the likelihood that the final data points had no
significant difference in O content. Additionally, the microwave
digestion procedure used to oxidize CNTs in this study
resulted in CNT shortening at the longer exposure times
required for higher oxidation levels, introducing another
experimental variable (i.e., CNT length) that could affect
colloidal stability.101 In general, identifying the impact of CNT
oxidation requires rigorously characterized materials to ensure
that differences in CNT aspect ratio, defect content, methods
for quantifying oxygen, or the type of oxygen-containing
functional groups present do not confound individual results or
comparisons to existing literature.
4.2. Influence of Divalent Cations
The clear trends in the effects of surface oxidation on CNT
stability are suppressed by the presence of divalent cations like
Ca2+ and Mg2+. As shown in Table 2, reported CCC values of
CNT suspensions are much smaller for CaCl2 than for NaCl.
The valence ratios of the decrease in CCC are typically near
the value of Z−6 predicted by the Schulze−Hardy rule and
decrease as oxidation increases.152 For CNTs with a surface
oxygen concentration above 10 at. %, the valence ratios range
from Z−6.9 to Z−8.0, lower than the predicted value. This has
been attributed to the capacity for Ca2+ ions to form bidentate
complexes with adjacent carboxyl groups, thus readily
neutralizing the negative surface charge of highly oxidized
CNTs.94,112 As a result, increasing the surface density of
carboxyl groups also increases the probability of bidentate
complexing by divalent cations, which decreases the stabilizing
effect of surface oxidation. Stability imparted by hydroxyl
groups has also been shown to be disproportionately impacted
by CaCl2 solutions: Bouchard et al. found no observable
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5.4 6.2 0.21 Z−4.9
8.2 22.5 0.36 Z−6.0
12.1 57.9 0.48 Z−6.9
16.3 108.1 0.42 Z−8.0
differences in electrophoretic mobility, CCC, or αa values
between pristine and hydroxyl-functionalized (OH-) CNTs in
CaCl2 solutions, implying that charge neutralization through
bidentate complexing remains relevant for functional groups
other than carboxylic acids.148
Differences in settling behavior between pristine and
oxidized CNTs were also diminished in the presence of
Ca2+. In a study examining a suite of 10 different CNT types,
Schwyzer et al. found that only the two oxygen-functionalized
CNTs had a measurable fraction (approximately 25%)
remaining in suspension after 5 d of settling in background
media containing pH-adjusted MOPS buffer and sodium azide
(used to prevent bacterial growth).147 When 2 mM CaCl2 was
added to the same background media, these CNTs also
became undetectable in the supernatant.147 Similarly, Kennedy
et al. did not observe large differences in the CNT supernatant
concentration for three CNT types studied in moderately hard
reconstituted water (MHRW) containing both Ca2+ and
Mg2+.142 However, the half-lives indicated that OH-CNTs
remained in suspension the longest (t1/2 = 51 ± 4 min),
followed by carboxylated (COOH-) CNTs (t1/2 = 21 ± 3 min)
and pristine CNTs (t1/2 = 7 ± 1 min), suggesting that some
differences in kinetics remain.142
4.3. Influence of Other Media Components
As media complexity increases to include natural organic
matter (NOM), proteins, and other components relevant to
cell culture or toxicological media, the importance of surface
chemistry on CNT stability continues to lessen. The effects of
CNT surface oxidation on homoaggregation behavior in these
types of media have been primarily studied through the
evaluation of settling behavior as opposed to the comparison of
CCC or αa values. Using stability after centrifugation to
represent long-term sedimentation stability, Bai et al. studied
the behavior of CNTs in varying concentrations of fulvic acid,
with no ions present.94 Highly oxidized CNTs were shown to
have the greatest fraction remaining in solution after
centrifugation regardless of the absence or presence of fulvic
acid, but fulvic acid was also shown to have a stabilizing effect
on CNTs with a low degree of surface oxidation. Fulvic acid
100 mg/L increased the stability of pristine CNTs (0.1 at. %
O) by more than a factor of 10 and lowly oxidized CNTs (2.5
at. % O) by a factor of 2 but had no impact on highly oxidized
CNTs (3.6−9.5 at. % O).94 Using a similar centrifugation
technique, but a more complex artificial groundwater media
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Figure 5. Optical images of vials containing settled CNTs A1) in 20 mg/L SRHA and B1) in 20 mg/L SRHA with 2 mM CaCl2. SEM images of
settled CNTs from a sample containing A2) 20 mg/L SRHA and B2) 20 mg/L SRHA with 2 mM CaCl2. Black dots on SEM images are holes in
filter paper. Reproduced with permission from ref 146. Copyright 2013 Elsevier.
that included both NOM and Ca2+, Smith et al. found a linear
relationship between the fraction of CNTs remaining in
suspension and the concentration of NOM added (R2 = 0.97−
0.99) that was independent of CNT oxygen content (5.1−9.0
at. % O).114 The colloidal stability imparted by adsorbed
NOM was shown to be a result of steric repulsion between
NOM-coated CNTs, as opposed to a change in electrostatic
repulsion.114
This key difference in the importance of nascent surface
properties to CNT stability in the presence of NOM alone vs
the combination of NOM and Ca2+ was also observed by
Schwyzer et al.147 The fraction of CNTs remaining in
suspension after 20 d of media exposure and 5 d of settling
could be effectively modeled by eq 2 in the presence of
Suwannee River humic acid (SRHA) with no added Ca2+ (R2 =
0.82):
CNTs suspended (%) = −11.7 + 6.2 × O content (at. %)
+ 1.6 × CNT diameter (nm)
However, when 2 mM CaCl2 was present along with the
SRHA, there was no dependence on surface oxidation. Instead,
CNT diameter alone was predictive of 94% of variability in
CNT suspension concentrations.147 In a follow-up study
comparing two CNT types, the authors found that the CNTs
possessing both higher oxygen content and larger diameters
were more stable in suspension across a range of pH values,
Ca2+ concentrations, and NOM types and concentrations.146
This is in some ways counter to DLVO theory: while a higher
oxygen content would increase the electrostatic repulsion
between CNTs (thus increasing colloidal stability), a larger
diameter would increase van der Waals attraction between
CNTs (thus decreasing colloidal stability). However, the
authors affirmed that a larger set of CNT types would need to
be examined to validate the positive correlation between CNT
diameter and stability.147 Interestingly, analysis of the settled
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material showed that the media composition also affected
CNT aggregate structures: a mixture of SRHA and Ca2+
resulted in netlike structures due to Ca2+ bridging behavior,
while SRHA alone resulted in compact spheroidal bundles
(Figure 5).146 In another study, Glomstad et al. tested CNT
sedimentation in three commonly used toxicological media
with NOM added, and compared these to behavior in natural
surface water.145 For each of the synthetic media, OH- and
COOH- functionalized CNTs remained in suspension at
higher concentrations than pristine CNTs. However, the
differences between oxidized and pristine CNTs were reduced
as the complexity of media increased, with higher Ca2+
concentrations resulting in a lower degree of stability imparted
by functionalization.145
Often, toxicological studies utilize media containing
proteins, antioxidants, and other materials designed to
optimize cell and organism health. While NOM has been
shown to have a stabilizing effect on CNTs, the effects of other
(2)
materials can vary. In one toxicological study, COOH-
functionalized CNTs were more colloidally stable than pristine
CNTs in phosphate buffered saline (PBS) but less stable in
both PBS media containing bovine serum albumin and Eagle’s
medium containing fetal bovine serum.96 Here, sedimentation
behavior was monitored using UV−vis spectroscopy, but in
other toxicology-focused studies, the discussion of aggregation
is often limited to a simple comparison of mean aggregate size
using DLS, which has resulted in inconsistencies in reported
trends comparing the impact of oxidation within the same
media.96 For example, Hamilton Jr. et al. found that aggregate
sizes were greatest for O-CNTs, while Ursini et al. found that
aggregate sizes were smallest for O-CNTs.100,143 Both studies
utilized RPMI-1640 media, a common cell culturing media
with an ionic strength of approximately 150 mM, higher than
nearly all reported CCC values for CNTs. This media also
contains compounds such as glutathione, cobalamin, and 4-
aminobenzoic acid, which have not been systematically studied
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for their effects on CNT stability. Discerning the true effect of
CNT oxidation in this media is not possible using only this
static DLS data, as the reported lengths and diameters of
CNTs utilized differed both within and between the two
studies.100,143 Additionally, even if initial CNT size parameters
were equal, it is likely that the high ionic strength resulted in
sedimentation that eliminated the largest aggregates from the
measurement and thus affected the measured aggregate sizes.
4.4. Heteroaggregation and Transport
Clearly, increasingly complex media reduces the importance of
CNT surface oxygen content on determining colloidal stability.
While the results discussed so far in this section have been
focused on homoaggregation behavior, these general trends
also apply to heteroaggregation and deposition. For example,
Yi and Chen used QCM-D to study the deposition of O-CNTs
onto a model silica surface in the presence of monovalent vs
divalent cations.112 The CDC of CNTs with 10.6 at. % O was
330 mM NaCl, more than twice the CDC of 150 mM NaCl
measured for CNTs with 6.3 at. % O. With CaCl2, the
difference was eliminated, and CDCs were comparable at 1.1
mM and 1.6 mM for 6.3 at. % and 10.6 at. % O, respectively.112
Similar results were obtained by Yang et al., who employed
column transport studies to examine deposition interactions
between CNTs and glass beads.113 For experiments conducted
in NaCl, CDC values increased from 24.4 mM to 27.3 mM and
93.7 mM for CNTs with 3.0, 7.1, and 11.5 at. % O,
respectively. In CaCl2, CDC values ranged from 2.4 to 3.0 mM
for CNTs, with oxygen concentrations ranging from 5.1 to 8.3
at. %. This study also examined the effects of NOM, which was
shown to increase mobility of all CNTs regardless of surface
oxidation. Just as in homoaggregation studies, the degree of
stability imparted by NOM was greatest for less-oxidized
CNTs, and the differences in αd between different CNTs were
eliminated when Ca2+ was present.113
In addition to the solution properties, the properties of the
collector surfaces and colloids are also important, further
decreasing the impact of CNT surface oxidation. In transport
studies, pH had a greater effect on CDC values than surface
oxygen even in monovalent electrolyte solutions because the
pH affects the surface charge of both the glass beads and the
CNTs, while the oxygen concentration affects only the
CNTs.113 Bouchard et al. compared the heteroaggregation
attachment efficiencies, αa,hetero, for pristine and OH-function-
alized CNTs with two different natural sediments.148 The
differences between properties of the sediments were shown to
outweigh the effects of CNT functionalization. αa,hetero values
were very similar for the two CNT types regardless of
electrolyte type and content, but one sediment type had 4.0−
5.3 times greater αa,hetero values in NaCl than the other
sediment type. It was proposed that the greater concentrations
of aluminum hydroxide in one sediment provided more
positively charged sites for CNTs to deposit, resulting in the
increased rate of heteroaggregation. Using QCM-D to probe
CNT deposition onto aluminum hydroxide surfaces, it was
shown that this heteroaggregation is irreversible if the
background electrolyte concentration is maintained, consistent
with DLVO theory.148
In other studies of CNT heteroaggregation with positively
charged model colloids, it has been shown that negatively
charged CNTs will rapidly aggregate as the ratio of
colloids:CNTs increases, eventually reaching a maximum due
to the oversaturation of positively charged colloids, causing a
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charge reversal and leading to electrostatic repulsion between
heteroaggregates.156,158 While neither of these heteroaggrega-
tion studies methodically varied the oxygen concentration of
the CNTs utilized, it can be hypothesized that increasing the
surface oxygen concentration will increase the density of
negatively charged binding sites and shift the maximum
heteroaggregation rate to a higher ratio of colloids:CNT. It
should be noted that, to date, the vast majority of studies
examining the effect of CNT oxidation on colloidal stability
have focused on homoaggregation, with only a few studies
considering heteroaggregation, deposition, and transport
(Table 1). Moving forward, it will be important to elucidate
relationships between surface oxidation and αa,hetero in
particular, as this is an important parameter in predictive
models determining the concentrations of nanomaterials in
specific environmental compartments as well as their
propensity for trophic transfer.159,160
Overall, there exist clear relationships that allow for both
qualitative and quantitative predictions of CNT colloidal
stability when the properties of both the CNT surface and the
surrounding media are known. As media grows more complex
with the presence of divalent cations, NOM, and heteroge-
neous natural colloids, the importance of surface oxidation is
diminished. The diminishing impact of surface chemistry as
media complexity increases has also been observed for other
nanomaterials. For example, the initial surface coatings or
capping agents of gold nanoparticles were shown to have less
of an impact on colloidal stability than interactions with NOM
or exposure to raw wastewater,161,162 although certain surface
coatings (i.e., polyethylene glycol) imparted steric stability that
prevented aggregation even in natural river water or other
media containing NOM.163,164 Ultimately, the colloidal
stability of CNTs will affect many other aspects of CNT
behavior described in this review, as the persistence of CNTs
in the water column will dictate which molecular species (e.g.,
ROS) and organisms will interact with CNTs and the time
scale over which these interactions will occur.
5. ADSORPTION PROPERTIES
Understanding the adsorption properties of CNTs is critical to
predicting and controlling CNT behavior in environmental
systems. Incidental adsorption of ubiquitous materials like
proteins or organic acids to CNT surfaces results in the
formation of ecological or biological coronas, which drastically
impact the fate and toxicity of nanomaterials.165 Other
potential adsorbates, such as heavy metal ions or organic
contaminants, have known toxicological impacts. Here,
adsorption can affect the mobility and bioavailability of these
contaminants as well as the toxicological properties of the
CNTs. In addition to the incidental adsorption behaviors
associated with CNTs released into the environment, CNT
adsorption properties are also intentionally engineered to
optimize contaminant removal in water treatment applications,
as discussed in section 8. CNT adsorption behaviors, both
incidental and intentionally engineered, depend on a variety of
factors, including available CNT surface area (SA) for
adsorption, water chemistry parameters, adsorbate structure
and properties, and the physicochemical properties of the
CNTs.166−168 In this section, we discuss the quantitative
relationships between CNT adsorption behaviors and the
character and quantity of CNT surface oxygen. The chemical
mechanisms controlling the adsorption of different classes of
adsorbates (i.e., nonpolar organics vs metal ions) will also be
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discussed to elucidate the role of surface oxygen in predicting
adsorption behavior.
CNT adsorption behavior is modeled by plotting adsorption
isotherms, which relate the equilibrium concentration of the
adsorbate in the solid phase (qe, reported in units of
mass adsorbate
or mass adsorbate ) to the equilibrium concentration
mass adsorbent SA adsorbent
of the adsorbate in the liquid phase (Ce, reported in units of
mass adsorbate
). Values of q e and C e are experimentally
solution volume
determined through batch adsorption experiments in which
CNT/adsorbate mixtures are equilibrated at a constant
temperature before the solid and aqueous phases are separated
for analysis. 14C-radiolabeling of organic adsorbates can
enhance quantification by enabling the discrimination of
carbon present in the adsorbate from carbon present in
CNTs or other media components (e.g., NOM).169 The
experimental data is then fit to a model adsorption isotherm to
determine fitting parameters such as the maximum adsorption
capacity of the CNT adsorbent or the relative affinity of the
adsorbate to binding sites. The appropriate choice of
adsorption isotherm, however, depends on the nature of the
adsorbate, as will be discussed.
5.1. Adsorption of Organic Molecules
The most commonly applied models for the adsorption of
organic molecules are the Freundlich model (eq 3) and the
Polanyi-based Dubinin−Ashtakhov model (DAM) (eq 4);
both consistently produce good fits based on both R2 values
and mechanistic considerations.169−175 These models are
appropriate for organic molecule adsorption because they
permit multilayer adsorption; that is, qe will continuously
increase with Ce without reaching a plateau.175,176 Here, the
CNT surface acts as the initial adsorption site for organic
molecules, which can then adsorb onto each other through π-
stacking interactions.175,176
qe = KFCe1/ n (3)
iε y
− jjj sw zzz
b determined from the Polanyi-based Dubinin−Astikov adsorption
k E {
log qe = log qmax
(4)
In eq 3 (i.e., the Freundlich model), KF is the Freundlich
coefficient and 1/n is the Freundlich exponent of nonlinearity.
KF is a measure of the relative adsorption capacity, while 1/n is
a measure of the relative strength of adsorption; these values
are convenient for direct comparisons between different CNT
adsorbents.177 In eq 4 (i.e., the DAM), qmax is the maximum
adsorption capacity, E is the correlating divisor, b is the fitting
parameter; and εsw is the effective adsorption potential equal to
εsw = RT ln (−Cs/Ce), where R is the universal gas constant, T
is the absolute temperature, and Cs is the water solubility of the
adsorbate. qmax can be compared between different CNT
adsorbents, while εsw can be compared for different adsorbates.
Both the Freundlich model and DAM are empirical fits and
should not be used to extrapolate qe values outside of the
experimentally measured range.178 When applying these
adsorption models to collected data, it is important to consider
that factors such as data transformations and weighting, the
step size and number of iterations used to achieve a fit, the
number of data points collected, and the range of equilibrium
concentrations examined will all impact the deviation of the
fitted isotherm from the true isotherm.167,176 In addition, the
aggregation state of the CNTs, a property closely intertwined
with CNT surface oxidation, influences the total surface area
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available for adsorption. Therefore, water chemistry and CNT
surface chemistry must each be systematically varied to achieve
a complete understanding of the mechanisms dictating
adsorption behavior.
The relationships between CNT surface oxygen and
adsorption behavior change drastically for different adsorbate
types. Within the broad category of “organic molecules,”
quantitative trends are most evident when examining nonpolar,
unsubstituted aromatic contaminants like naphthalene and
phenanthrene in simple electrolyte solutions. In these
conditions, an increase in CNT surface oxidation causes a
decrease in the adsorption of nonpolar organic mole-
cules.169,173,179,180 Using a suite of nine CNTs with surface
oxygen concentrations ranging from 3.3 to 14.0 at. % as
measured by XPS, Cho et al. found that the DAM qmax values
for naphthalene systematically decreased with increasing CNT
oxygen content (eq 5, Figure 6):
qmax ( μL g ) = 118 − 6.6 × O content (at.%) (5)
Figure 6. Maximum adsorption capacity (q′ad,max) of naphthalene
model vs MWCNT surface oxygen concentration. Open circles
represent MWCNTs oxidized with HNO3, and solid circles represent
MWCNTs oxidized with KMnO4 or H2O2. Reproduced with
permission from ref 169. Copyright 2008 American Chemical Society.
This result indicates that approximately 5.9% of the total
sorption capacity is removed for each additional percentage of
surface oxides,169 a relationship that was later reiterated in
another study.173 Notably, CNT surface oxidation only affects
the adsorption capacity, while the isotherm shapes and
adsorption energies remain unchanged.169,174 While π-electron
donor−acceptor (π-EDA) bonding between the aromatic rings
of organic adsorbates and the extended sp2 π-conjugated
carbon system in the CNT backbone has been reported as the
primary mechanism of adsorption for nonpolar organic
molecules to pristine CNTs,181−183 hydrogen bonding
interactions are also critically important to understanding
adsorption behavior for O-CNTs.167 Specifically, oxygen-
containing functional groups like carboxyl or hydroxyl groups
create hydrophilic regions on the CNTs where hydrogen
bonding with the surrounding water molecules is more
energetically favorable relative to n−π or π−π EDA
interactions with the adsorbate.167,169,174 Consequently, as
the degree of CNT oxidation increases the fraction of the
surface that is unavailable for organic compounds to sorb
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increases, thus decreasing the total sorption capacity.167,169,174
However, those regions of the CNT surface where the sp2 π-
conjugated carbon system remains intact exhibit the same
strength of sorbate interaction, meaning that the sorption
energy remains unaffected.167,169,174
For substituted aromatic compounds, the effect of CNT
surface oxidation on adsorption depends on the specific
electronic properties and polarity of a given adsorbate. As
CNT oxidation increases, the adsorption of aromatic molecules
substituted with ionizable functional groups decreases: this
relationship has been observed for hydroxyl-,174,184−191
carboxyl-,187,189 sulfonamide-,192,193 and amino-substituted
aromatics,174,188,194 although in some cases the effect is only
observed after data is normalized to the specific surface area
(SSA) of CNTs.174 These adsorption interactions are highly
pH dependent due to electrostatic repulsion between the
oxygen-containing functional groups of the CNTs and the
ionizable functional groups of the adsorbates, with the
repulsion typically greatest for conditions where pH >
pKa.186−188,195 The effects of solution pH and CNT oxidation
on adsorption were also observed for ionizable molecules
lacking aromaticity, including perfluoroalkyl substances
(PFAS), a family of prominent persistent organic pollu-
tants.189,196 Adsorption of polar nonionizable aromatic
molecules (e.g., nitro-and halogen-substituted aromatics) also
decreases for O-CNTs compared to pristine or thermally
graphitized CNTs.174,197,198
CNT surface oxidation consistently decreases the adsorption
capacity of a given organic molecule with no effect on the
adsorption strength, as indicated by the unchanging values of
1/n (when using the Freundlich model) or E (when using
DAM).167,169,174 However, when the relative influence of CNT
surface oxidation on adsorption is compared for multiple
organic molecules, the properties of the organic adsorbate
control the extent of the decrease in adsorption capacity and
can also affect the adsorption strength.174 W. Wu et al.
compared the adsorption behavior of a suite of 10 polar and
nonpolar organic molecules on four MWCNT types with total
surface acidic group content (Nacidic groups) ranging from 0.021
to 0.382 mmol/g as determined by the Boehm titration
method.174 While there were differences in SSA between the
MWCNT types, this was controlled for by normalizing the
resultant DAM-derived qmax to the measured SSA. The
relationship between the SSA-normalized adsorption capacity,
qmax,SA, and the acidic group content of the MWCNTs was
determined to fit eq 6, with R2 values ranging from 0.853 to
0.999:
qmax,SA = S × Nacidic groups + C (6)
Here, S and C are linear regression coefficients determined
for each adsorbate. S therefore describes the amount by which
qmax,SA is altered by the acidic surface oxide groups on the
CNTs. S is negative for all organic molecules examined
because CNT oxidation always reduced the surface area
normalized adsorption capacity. The extent of this reduced
adsorption varied with adsorbate properties, as shown in
Figure 7. E, a DAM fitting parameter representative of the
adsorption energy, is unchanged by CNT oxidation for a
specific organic species but is strongly dependent on the
solvatochromic parameters of the organic species (e.g., the
potential for hydrogen bonding and the π-electron polar-
izability).174,197 The linear correlation between S and E values
(R2 = 0.741) indicates that organic molecules with higher
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Figure 7. Relationship between the decrease in qmax,SSA with oxidation
(S) and the average E values (the Dubinin−Astikov adsorption model
parameter representative of the adsorption energy) measured for the
adsorption of organic compounds on four MWCNTs. Each E value
was unaffected by MWCNT oxidation and is therefore presented as
an average of the four MWCNT types tested. Reproduced with
permission from ref 174. Copyright 2012 American Chemical Society.
polarity, and thus larger E values, lose less adsorption capacity
when CNTs are oxidized. This behavior was attributed to the
potential for the more polar compounds to occupy adsorption
sites of intermediate hydrophilicity on O-CNTs in addition to
the hydrophobic sites represented by sp2 π-conjugated carbon,
while nonpolar organic compounds could only occupy
hydrophobic sites.174
Overall, CNT oxidation has been consistently shown to
decrease adsorption for a wide variety of organic molecules.
Exceptions to this include two studies of the antibiotic
ciprofloxacin, one of which showed increasing qmax,SA with
increasing CNT oxidation,199 and one of which showed
increasing adsorption for COOH-MWCNTs < graphitized
MWCNTs < OH-MWCNTs.200 These trends were both
assumed to be caused by a combination of enhanced π−π EDA
interactions between ciprofloxacin and phenolic groups on
CNT surfaces and the enhanced CNT dispersion achieved
through oxidation. Another exception was for benzene,
toluene, ethylbenzene, and p-xylene (BTEX) mixtures, which
were adsorbed in greater quantities for more highly oxidized
CNTs.201 While this increase was attributed to enhanced π−π
EDA interactions, the conclusion is weakened by the use of
only two concentrations of BTEX compounds (as opposed to
the measurement of adsorption isotherms), variable SSA values
for the different O-CNTs, and a lack of data on the aggregation
behavior of the CNTs. These studies highlight the importance
of systematic variation in the CNT and adsorbate properties to
determine the underlying mechanisms driving adsorption
behavior, as well as decoupling adsorption behavior from
SSA or dispersion properties through experimental control or
data normalization.
5.2. Adsorption of Natural Organic Matter (NOM)
The adsorption of NOM by CNTs can impact aggregation,
toxicity, and competition for other adsorbates. Because of the
ubiquity of NOM in the natural environment, understanding
the impact of CNT surface oxidation on NOM adsorption is
necessary to evaluate the overall environmental impact of
CNTs.
Similar to other organic molecules, NOM adsorption
capacity decreases as CNTs become more oxidized.114,192,202
Smith et al. found that KF values for NOM collected from the
Great Dismal Swamp systematically decreased from 20 mg/g
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for pristine CNTs (2.7 at. % O) to <4 mg/g for highly oxidized
CNTs (7.9−8.1 at. % O).114 This decrease in NOM
adsorption capacity for O-CNTs compared to pristine CNTs
was also observed in studies using humic acid.192,202 Unlike
other organic molecules, where CNT oxidation had no effect
on the strength of adsorption, the Freundlich 1/n value
increased with CNT oxidation, indicating that the NOM was
occupying lower energy adsorption sites on O-CNTs relative
to pristine CNTs. It was concluded that NOM adsorption is
driven by π−π EDA interactions between the aromatic
fractions of the NOM and CNTs and that this process is
negatively impacted by a combination of the lack of CNT
aromaticity in oxidized regions and the increasing electrostatic
repulsion between acidic functional groups present on NOM
and O-CNTs.114 Notably, increasing NOM aromaticity while
maintaining CNT surface chemistry increased both the NOM
adsorption capacity and NOM adsorption strength (as
modeled using KF and 1/n, respectively), further evidence
for a π−π EDA interaction mechanism.203 The adsorption of
NOM is highly pH-dependent for O-CNTs, decreasing as pH
is increased, while pH has a more limited effect on the
behavior of pristine or graphitized CNTs.114,192,204 This is
because electrostatic repulsion between the ionizable func-
tional groups on NOM and O-CNTs is controlled by pH-
dependent deprotonation, while pristine CNTs are not affected
by these interactions.114,192
The presence of NOM is known to decrease the adsorption
of competing compounds by CNTs,171,172,187,192,205−207 which
can result in the decreased impact of CNT surface oxidation
on adsorption behavior. Mechanistically, NOM can decrease
adsorption through competition for available binding sites,
molecular sieving, and the blockage of pore spaces within the
CNT aggregate structure.114,192 Zhang et al. demonstrated that
the presence of NOM had a greater impact on the adsorption
of organic compounds to CNTs than ionic strength or pH,
although increased CNT surface oxidation slightly suppressed
the effects of NOM.172 This was due to a decrease in CNT-
NOM interactions for O-CNTs, limiting NOM surface
coverage and thus increasing the CNT surface area available
for contaminant adsorption.172 In some cases, the presence of
NOM can effectively eliminate differences in adsorption
behavior between pristine and oxidized CNTs: Zindler et al.
observed that CNT oxygen content only affected phenan-
threne adsorption in media without added NOM.170 Overall,
existing literature on NOM interactions with CNTs shows that
the presence and properties of NOM will play a large role in
the ability to use CNTs for contaminant removal in a given
media. As the NOM concentration in the aquatic environment
increases, so will the extent of NOM adsorption to CNT
surfaces, consequently decreasing the impact of CNT surface
oxidation on contaminant removal.
5.3. Adsorption of Metal Ions
In addition to organic contaminants, the fate, transport, and
adsorptive removal of heavy metals from aquatic systems are
also affected by CNT surface oxidation. Adsorption of metal
ions to CNTs is most commonly modeled using a Langmuir
isotherm (eq 7). This model is appropriate for metal cations
and oxyanions because it represents monolayer adsorption in
which qe reaches a plateau after all adsorption sites on the
CNT surfaces are occupied.208−210 Unlike organic compounds,
metal ions do not have the capacity to adsorb onto one
another.
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KLCe
qe = qmax
1 + KLCe (7)
Here, KL is the Langmuir adsorption constant, which
represents the adsorption affinity of the surface sites. As
written in eq 7, the model represents monolayer adsorption to
a fixed number of energetically equivalent sorption sites, but
the model can be extended to a more complex multisite form,
where each site type has its own qmax and KL parameters.
CNT surface oxidation has consistently been shown to
increase sorption of metal ions, with several quantitative
relationships emerging in the literature.209,211−218 For example,
Cho et al. observed a strong linear correlation between qmax,SA
for Zn[II] adsorption and the CNT surface oxygen
concentration (eq 8, R2 = 0.97).217
qmax,SA ( μmol m 2 ) = 0.063 × O content (at. %) + 0.35
(8)
The positive y-intercept suggests that while there is a clear,
pH-dependent electrostatic attraction between negatively
charged carboxyl functional groups (quantified by a combina-
tion of XPS analysis and chemical derivatization) and
positively charged metal ions, graphenic carbon must also
contribute to metal adsorption. A two-site Langmuir model
used to represent a finite number of more energetically
favorable carboxylic sites (KL = 0.0061 L/μmol) and less
favorable graphenic sites (KL = 0.00026 L/μmol) was shown to
describe the behavior of a suite of 16 MWCNTs with oxygen
concentrations ranging from 2.1−10.8 at. % (R2 = 0.93−
0.99).217 This result indicates that carboxylic acid groups on
functionalized CNTs are approximately 24 times more
energetically favorable for Zn[II] sorption than the graphenic
carbon that composes pristine CNTs.217
H. Wang et al. also concluded that oxygen-containing
functional groups played the largest role in metal cation
adsorption in a study of Pb[II] adsorption to O-MWCNTs.212
In this study, the adsorption behavior of pristine MWCNTs
was compared to that of MWCNTs oxidized by refluxing in
concentrated HNO3 for 1, 2, 6, and 10 h. Furthermore, a
sample of the O-MWCNTs prepared by 6 h of HNO3 refluxing
was annealed in argon gas at 800 °C to remove surface oxides,
forming a graphenic surface similar to pristine MWCNTs with
a directly comparable SSA. These methods produced a suite of
MWCNTs with varying SSA values (162.16−253.89 m2/g)
and surface oxide concentrations (0.89−9.34 wt % as
determined by Boehm’s titration and TGA analyses).
Adsorption capacity increased with increasing CNT surface
oxidation even without SSA normalization. Furthermore, by
comparing the adsorption capacities of 6 h acidified MWCNTs
before and after annealing, it was calculated that the physical
adsorption of Pb[II] to unfunctionalized CNT surfaces
accounts for 24.7% of total adsorption (for this specific O-
MWCNT studied), while adsorption to oxygen-containing
functional groups accounted for the remaining 75.3%.212
The effect of CNT surface oxidation on the adsorption of
metal cations is well understood, but not all metal
contaminants are present in cationic form in the environment.
J. Li et al. observed that while CNT oxidation increased the
adsorption capacity for cationic Cu[II], oxidation decreased
the adsorption capacity for Cr[VI], and As[V] oxyanion
species.208,219 This is due to electrostatic repulsion between
negatively charged functional groups on O-CNT surfaces (i.e.,
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hydroxyl and carboxylic acid groups) and negatively charged
HCrO4− and H2AsO4− complexes, an effect exacerbated by
increases in pH.208
Ultimately, the surface oxygen concentration of CNTs can
be tuned for the favorable adsorption of both organic and
metal contaminants, increasing their potential for use in water
treatment (section 8). The properties of the CNTs, adsorbates,
and surrounding media all play a role in adsorption behavior.
Several correlative relationships between CNT surface oxygen
content and adsorption behavior have been defined, which can
be used in predicting and controlling CNT adsorption. As
discussed further in section 9, the effect of oxygen on CNT
adsorption is in many ways analogous to the effect of oxidation
on the adsorption properties of other carbon-based nanoma-
terials. However, these relationships are often easier to
determine for CNTs than for commonly used carbon sorbents
like activated carbon. This is, in part, because pristine CNTs
are readily available and often have close to or no surface
oxygen. Moreover, the degree of CNT surface oxidation can be
tuned and easily quantified by surface spectroscopies as the
vast majority of the oxygen atoms are located at the CNT
surface. While the surface oxidation of activated carbon can be
varied using oxidation or reduction processes, quantification of
the oxygen content is complicated by the internal porosity.
Moreover, the internal pore structure of activated carbon can
itself be altered by oxidative processes, thus affecting the total
surface area available for sorption. Collectively, these factors
favor the use of CNTs to determine quantitative relationships
between surface oxidation and adsorption behavior that are far
less readily observable in activated carbons, making CNTs a
useful model system for understanding the effects of surface
chemistry on contaminant removal.
5.4. CNT-Facilitated Contaminant Transport and Trojan
Horse Effects
The adsorption of contaminants by CNTs and other
nanomaterials can have broader environmental implications
on contaminant mobility (i.e., facilitated transport) and
bioavailability/toxicity (i.e., Trojan horse and other coexposure
effects).220,221 Several factors are required for CNT adsorption
behavior to significantly alter these effects: (1) CNTs must be
present at sufficient concentrations relative to the concen-
tration of the contaminant, (2) the contaminant must adsorb
strongly onto the CNT and desorb slowly relative to the time
scale of the transport or toxicological behavior being studied,
and (3) the mobility or toxicity of the CNT-adsorbed
contaminant must differ from that of the free contami-
nant.220,221 As CNTs with a variety of surface oxygen
concentrations are expected to enter the environment, and
oxygen-containing functional groups are known to impact the
adsorption of contaminants onto CNTs, it follows that CNT
surface oxidation can affect facilitated transport and Trojan
horse effects by altering adsorption−desorption hysteresis
behavior.
Adsorption−desorption hysteresis behavior is defined as the
nonsingularity of the adsorption and desorption isotherms;
that is, the condition where the adsorbent (i.e., the CNT)
loading follows a different path than its regeneration via
desorption, in terms of the qe vs Ce isothermal shape.222
Adsorption−desorption hysteresis can be caused by reversible
capillary condensation of adsorbates in pore spaces within
CNT aggregates, irreversible adsorbate entrapment driven by
the deformation of these pore spaces, or irreversible binding of
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the contaminant to the CNT surface.222−224 In studies where
CNT surface oxidation is systematically varied, the relationship
between hysteresis behavior and surface oxide content has
been attributed to the irreversible formation of covalent bonds
or surface complexes between the contaminant and the surface
functional groups of the CNTs. 208,223 W. Wu et al.
demonstrated that amidation reactions between the amino
functional groups of organic contaminants (e.g., atrazine,
aniline) and the carboxyl or lactonic functional groups of O-
CNTs results in irreversible adsorption to CNT surfaces that
increases with CNT surface oxidation, while other contaminant
functional groups (e.g., phenol, nitro) that are unable to form
covalent bonds to CNT surface oxides did not exhibit
adsorption−desorption hysteresis.223 However, care must be
taken when generalizing these results from the media tested
here (a pH 8.0 solution containing 0.01 M CaCl2 and 200 mg/
L NaN3) to other aqueous systems: the amidation reaction is
endothermic and affected by conditions that decrease the
nucleophilicity of the amino functional group, while NOM
compounds may also covalently bind aniline through this
mechanism and prevent this irreversible adsorption to CNTs
from occurring.223,225 For heavy metal contaminants, the effect
of CNT surface oxides on adsorption−desorption hysteresis
depends on the charge of the metal ion. Hysteresis for Cu[II],
Cd[II], Ni[II], and Pb[II] cations increases with CNT surface
oxidation, while hysteresis for Cr[IV] and As[V] oxyanions
decreases.208,218 The adsorbed cations can later be released if
the O-CNTs are exposed to acidic media (e.g., gastric
fluids).218,226 Therefore, highly oxidized CNTs could poten-
tially impact the transport, biodistribution, and toxicity of
cationic metal contaminants.
In some cases, the irreversible adsorption of contaminants to
COOH-functionalized CNTs has been directly shown to
decrease bioavailability and subsequent toxic effects, as
observed for Pb[II] cations toward Daphnia magna, and the
synthetic estrogen 17α-ethinylestradiol toward cultured
adenocarcinoma cells.227,228 In contrast, another study showed
a drastic increase in toxicity when a mixture of Ag+ ions and
COOH-functionalized SWCNTs were exposed to sea urchins,
as compared to the toxicity of the individual components.229
Increased accumulation in the gut was observed for Ag+
adsorbed to COOH-SWCNTs compared to free Ag+, and
higher mortality rates were observed for the mixture during the
recovery period after acute exposure, suggesting that Ag+
adsorption to CNTs effectively increased the exposure time
of sea urchins to Ag+ ions.229 The overall impact of CNT
surface oxidation on facilitated transport and toxicity of
adsorbed contaminants is complex and requires further
study. Different mechanisms of toxicity should be evaluated
in conjunction with systematic variation of CNT surface
oxidation and detailed adsorption and desorption kinetics
relative to the kinetics of uptake and depuration by exposed
organisms. Similarly, the role of CNT surface oxidation and
desorption hysteresis on contaminant transport through
porous media merits further study.
6. PHOTOCHEMICAL TRANSFORMATIONS AND ROS
GENERATION
CNTs can undergo photochemical transformations after
release into natural waters and water treatment systems.
Therefore, the impact of photochemical transformations on
key CNT properties (i.e., surface oxidation) will have
implications for the ultimate fate and toxicity of CNTs.
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Phototransformations of CNTs can occur through either direct
or indirect photolysis. In direct photolysis, transformations are
driven by photons being absorbed by CNTs, while indirect
photolysis is characterized by interactions between CNTs and
reactive oxygen species (ROS) created by the interaction of
photons with species in the surrounding media. Oxidized
CNTs can also produce ROS themselves as a result of
irradiation, which can then contribute to CNT photo-
transformation processes and have consequences for CNT
toxicity.
The relationships between CNT surface oxidation, photo-
chemical transformations, and environmental behavior are
challenging to quantify due to competing processes that can
either increase or decrease the amount of surface oxygen as
well as alter the distribution of different functional group
types.49 In this section, we describe CNT photooxidation and
decarboxylation reactions as well as the photoinduced
production and reactions of ROS involving CNTs.
6.1. Intentional CNT Photooxidation
Several studies have examined the deliberate functionalization
of CNTs through photochemistry. For photooxidation to
occur, a photon’s energy must be high enough to excite an O2
molecule from the triplet state to the more reactive singlet
state, which promotes chemisorption of O2 onto the CNT
surface.230 For this reason, the majority of studies intentionally
photo-oxidize CNTs using wavelengths between 254 nm (4.9
eV) and 400 nm (3.1 eV), a range that includes UVA, UVB,
and UVC light. For example, Alvarez et al. investigated CNT
photooxidation through UV irradiation of CNTs in aqueous
solution.231 After irradiation with 254 nm light, SWCNTs
showed an increase in surface hydroxyl groups, as observed by
changes to the FTIR spectra coupled with an increase in the
atomic concentration of oxygen measured via XPS, in a process
referred to as photohydroxylation.231
CNT powders can also be photooxidized by UV light. For
example, Parekh et al. oxidized MWCNTs using UV irradiation
under atmospheric pressure and vacuum ultraviolet (VUV)
irradiation.57 Under atmospheric conditions, the CNT surface
oxygen concentration increased from 2 to 7.5 at. % after 4 h of
irradiation with a combination of 185 and 254 nm light.57
Larger increases in the degree of surface oxidation (9.5 at. %)
were recorded after 2 h of pristine MWCNT exposure to a
microwave argon plasma (essentially a line source of radiation
at 104.8 and 106.7 nm) kept under vacuum, where oxygen and
argon were flowed through the plasma chamber and into a low-
pressure (39−47 Pa) reaction chamber, resulting in the direct
exposure of MWCNTs to electronically excited oxygen
atoms.57 On the basis of the spectral deconvolution of the C
1s XPS envelope, the authors concluded that for both methods
the new species were primarily epoxide and ether groups, an
indication that photooxidation is a gentler form of oxidation
compare to acid treatments, which invariably produce a
proportionately high concentration of more highly oxidized
carboxyl groups. However, once VUV exposure times exceeded
2 h, the oxygen content began to decrease, an effect attributed
to the formation and desorption of CO and CO2.57 The overall
effects of UV exposure on MWCNTs therefore represent a
balance between photooxidation processes that add oxygen-
containing functional groups, and photoreduction processes
that lead to their removal.
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6.2. Photodecarboxylation of O-CNTs
Direct photolysis of oxidized CNTs suspended in water causes
photodecarboxylation (PDC), the removal of carboxyl groups
via photochemistry (Figure 8). The PDC process eliminates
Figure 8. Summary of the photodecarboxylation (PDC) process as
induced by direct photolysis. Adapted with permission from ref 49.
Copyright 2014 The Royal Society of Chemistry.
colloidal stability imparted by negatively charged carboxylic
acid groups, resulting in aggregation and sedimentation of
CNTs that can be monitored by DLS or UV−vis.49 There is no
significant mass loss or structural change to the O-CNTs from
PDC processes driven by direct photolysis; instead, colloidal
destabilization and sedimentation are directly caused by
changes to the CNT surface chemistry.49 Bitter et. al showed
that the irradiation time required for CNT aggregation to
occur is dependent on the pH and ionic strength of the
surrounding media (ranging from 12 to 48 h), with longer
irradiation times required for aggregation at high pH and lower
ionic strength.49 These trends were in line with the greater
colloidal stability of O-MWCNTs under these conditions,
which therefore required the loss of larger concentrations of
carboxylic acid groups to reach a point of colloidal instability.49
Additionally, the study showed that when 254 nm UVC light is
used for irradiation, PDC of O-CNTs occurs through a single
photon process and does not involve ROS. Similar to the
photochemical transformations of organic molecules, photo-
excitation promotes the carboxylic acid groups to a localized
excited singlet state, which are then expelled as CO2.49
UVA light (320−400 nm) present in natural solar irradiation
can also drive PDC; however, under UVA irradiation PDC
does involve interactions with ROS as discussed later in this
section. 48 In both UVC and UVA studies, chemical
derivatization used in conjunction with XPS revealed that
the loss of carboxylic acid groups was the only significant
change to the distribution of oxygen-containing functional
groups.48,49 Because the O-MWCNTs studied also contained a
range of other functional groups that were unaffected by
photolysis, the observation of CNT aggregation and
sedimentation in these studies provides support for the idea
that these other functional groups (e.g., hydroxyl and epoxide)
play at most a minor role in determining overall CNT colloidal
stability.
In the environment, O-MWCNT surfaces will almost
certainly be modified by the presence of other materials like
NOM or proteins. Their presence could absorb photons and/
or modify other factors that contribute to the photo-
decarboxylation process, which would likely alter CNT
phototransformations in complex media.
6.3. ROS Generation by Irradiation of O-CNTs
Prior to photodecarboxylation and subsequent sedimentation,
irradiation of CNTs in natural surface waters can cause the
production of ROS, a process which is impacted by CNT
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properties, solution chemistry, and irradiation condi-
tions.232,233 While pristine CNTs do not produce ROS,
multiple types of ROS are produced when carboxylic acid
functionalized CNTs are irradiated with UVA light, including
singlet oxygen (1O2), superoxide (O2•−), and hydroxyl radicals
(•OH).48,232−234 These ROS have also been produced in
natural sunlight, as shown by Chen et al.232 The differences in
ROS production between functionalized and pristine CNTs
have been attributed to the defects that form in the sp2
hybridized carbon network due to covalent functionaliza-
tion.232,233 This has been proposed to result in a lower band
gap energy for initial photon adsorption by COOH-CNTs,
increasing their photochemical reactivity.235 Notably, semi-
conducting COOH-SWCNTs are much more photoreactive
than their semimetallic COOH-MWCNT counterparts; here,
it has been suggested that the larger band gap of the SWCNTs
results in excited triplet states with higher energy and longer
lifetimes, increasing 1O2 generation.236 Under dark conditions,
only minimal amounts of •OH are produced by COOH-
CNTs,2 and no 1O2 or O2•− can be produced by COOH-
CNTs without the addition of an external electron
donor.48,232−234 Thus, both irradiation and the presence of
CNT surface oxygen are necessary for significant ROS
production in simple electrolyte solutions.
While nearly all studies to date have focused exclusively on
COOH-CNTs, Chen and Jafvert compared the ROS
generation behavior of pristine SWCNTs, COOH-SWCNTs,
and SWCNTs functionalized with polyethylene glycol
(PEG).233 The EDX-determined oxygen concentration varied
from 5.73 at. % for the unfunctionalized SWCNTs to 16.52
and 16.60 at. % for the COOH-SWCNTs and PEG-SWCNTs,
respectively. For each ROS type examined (1O2, O2•−, and
•
OH), steady-state concentrations reported for COOH-
SWCNTs and PEG-SWCNTs were on the same order of
magnitude. There were, however, slight differences in the
relative amount of each type of ROS generated: O2•− and •OH
production were slightly greater for PEG-SWCNTs, while 1O2
production was slightly greater for COOH-SWCNTs. This
suggests that the specific structure of oxygen-containing
functional groups could play a role in ROS production
behavior, although differences in the SWCNT contents of
sidewall defects, amorphous carbon, and metal impurities were
also suggested by the authors as potential contributing
factors.233 Notably, there have been no studies that system-
atically vary the degree of CNT surface oxidation or the
proportion of different oxygen-containing functionalities to
determine the effect on the photogeneration of ROS by O-
CNTs.
Overall, irradiation of oxidized CNTs results in decarbox-
ylation and subsequent sedimentation, removing O-CNTs
from the water column and limiting their exposure to aquatic
organisms. However, during the period that O-CNTs are
colloidally stable, irradiation can result in the production of
ROS, with important consequences for toxic effects (section
7).
6.4. Effects of ROS Interactions on O-CNTs
Interactions with ROS can have a significant impact on the
surface properties of CNTs, regardless of whether these ROS
were generated by CNT photolysis, formed naturally in surface
waters, or produced during advanced water treatment
processes. Using externally generated ROS, the effects of 1O2
and •OH on COOH-functionalized CNTs have been
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independently investigated.48,237 In a study by Qu et al.,
reactions with 1O2 were shown to decrease the quantity of
carboxylic acid groups while increasing the quantity of
hydroxyl and carbonyl groups, resulting in a net zero effect
on the total oxygen content after 3 d of exposure.48 Reactions
with •OH also decreased the quantity of carboxylic acid
groups, but there were no effects on the concentrations of
other O-containing functionalities, resulting in a net decrease
of the total oxygen content.48,237 The decarboxylation
processes observed for interactions with 1O2 and •OH are a
result of the oxidation of both new and existing carboxylic acid
functional groups to CO2, which is then desorbed from the
CNT surface as shown in Scheme 1.48 As •OH is more reactive
Scheme 1. Reactions of CNTs with •OH, Resulting in
Oxidation, Decarboxylation of New and Existing COOH
Groups, and CO2 Productiona
a
Adapted with permission from ref 48. Copyright 2013 American
Chemical Society.
than 1O2, photodecarboxylation by •OH is much faster: a
similar decrease in carboxyl group content was achieved in
only 2 h for •OH vs 72 h for 1O2, even though the steady-state
concentration of 1O2 was several orders of magnitude higher.48
The effect of •OH on other oxygen-containing groups is more
challenging to identify, as several concurrent processes are
known to occur (Scheme 1).48
Qu et al. concluded that although there was no clear change
to hydroxyl and carbonyl concentrations under •OH exposure,
the continuous production of CO2 and the high reactivity of
•
OH suggest that rather than a lack of reactivity, a steady-state
was reached as depicted in the chemical reactions of Scheme
1.48,238
In studies where no external ROS were added, enough ROS
was produced by the irradiation of COOH-MWCNTs to
measurably decrease the total oxygen content (by ∼2−3 at. %)
after 7 d of UVA irradiation, with significant mineralization
(CO2 production) detected.48,234 Qu et al. showed that this
process primarily affects carboxylic acid groups with no other
functional groups measurably affected, consistent with studies
examining reactions with externally produced •OH.48 In a
separate experiment, the addition of Na2SO3 to the solution as
a known scavenger for •OH prevented these transformations
from occurring, further indicating that •OH is the driving ROS
species even though 1O2 was produced at greater concen-
trations. The underlying mechanism for this difference has yet
to be determined, but it is likely a consequence of the greater
reactivity of •OH relative to 1O2, the potential for electron−
hole pair formation and its impact on •OH, and/or differences
in the reaction rates of different surface oxides with •OH.48
Reactions with •OH can also impact the colloidal and
structural stability of O-CNTs. Similar to the PDC processes
under direct photolysis, O-CNTs exposed to •OH lose the
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colloidal stability and negative surface charge imparted by
carboxylic acid groups, resulting in increased sedimentation
behavior compared to unexposed O-CNTs.48,237 However,
reactions with •OH can also impact other structural properties
of O-CNTs unaffected by directed photolysis. Partial
mineralization of the CNT structure has been observed after
extended exposure to •OH, with 8 to 25% of CNT carbon
converting to CO2 before a plateau is reached.48,237 The
quantity of amorphous carbon impurities also affects the
reactivity of •OH with O-CNTs. Hou et al. compared the
structures of base-washed and as-received COOH-function-
alized SWCNTs using a combination of TGA, IR, and Raman
analyses, and showed that exposure to •OH eliminated
amorphous carbon impurities in a similar manner to base-
washing.237 Compared to the as-received COOH-SWCNTs,
base-washed COOH-SWCNTs reached a point of colloidal
destabilization more quickly during •OH exposure. This was
attributed to a shielding effect by the amorphous carbon,
limiting •OH interaction with COOH-SWCNT sidewalls until
these amorphous carbon fragments were degraded.237
7. ENVIRONMENTAL RISK AND TOXICITY
For any nanomaterial, the environmental health and safety risk
is a function of both hazard (i.e., the toxicity of the material)
and exposure (i.e., the route or duration of contact with
organisms of interest).239 Therefore, the toxicity and
persistence of CNTs are both critical factors in determining
their overall environmental impact. The exposure, uptake,
translocation, biopersistence, and resultant toxicity of CNTs
can all be affected by the presence of oxygen-containing surface
functionalities. In this section, we first discuss how surface
oxidation impacts CNT resistance to degradation after
consumer use; then we explore the effect of CNT oxidation
on CNT uptake and toxicity toward bacteria and other
organisms.
7.1. Stability During End-of-Life Incineration
At the end of their consumer lifetime, one possible route of
disposal for CNT-enabled products involves incineration, after
which CNTs may be released into the environment as
incinerator ash.240,241 The thermal stability of CNTs as a
function of surface oxidation is important to consider, as
incineration offers the possibility of transformation prior to
environmental release. In typical incineration processes, waste
is combusted in air at temperatures exceeding 1000 °C, which
provides enough heat to mineralize the majority of CNTs, as
graphitized carbon thermally degrades in air at temperatures of
600−700 °C.242,243 In general, this threshold for the onset of
thermal decomposition is unaffected by the presence of surface
oxygen on CNTs.132,244,245 While most CNTs will be
eliminated during waste incineration, oxygen may be unable
to adequately reach the CNTs in some consumer products
(e.g., batteries) during incineration, resulting in a fraction of
the CNTs remaining intact within the ash.246,247 This
incomplete combustion process may instead thermally anneal
CNTs, which can decrease the number of surface defect sites
and remove surface oxygen groups, potentially impacting the
toxicity of the CNTs that persist after incinera-
tion.132,245,248−252
7.2. Stability Toward Microbial Biodegradation
Another important relationship to assess is the effect of surface
oxygen on the susceptibility of CNTs to microbial biode-
gradation, as variations in the rate of degradation will control
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the risk of exposure to other organisms. The cytotoxicity of
CNTs coupled with the recalcitrance of their aromatic
structure causes their degradation by microorganisms to be
generally slow or nonexistent,253 although surface oxidation or
exposure to mixed culture bacteria has been shown to promote
enzymatic degradation of CNTs.254−256 O-CNTs have been
shown to promote enzyme activity (which corresponds to
increased enzymatic degradation) when exposed to white rot
fungi, suggesting that oxidized CNTs may indeed be more
prone to biodegradation than pristine CNTs.257,258
Microbes can also transform the surface chemistry of CNTs:
upon exposure to soil-dwelling Trabusiella guamensis, only
marginal degradation of pristine MWCNTs was observed, but
interestingly, the CNT surface was oxidized after bacterial
exposure.259 The impact of such microbially induced surface
transformations may be more relevant to toxicological risk than
CNT biodegradation behavior, as both pristine and oxidized
CNTs are expected to persist for time scales well beyond those
needed for transport and exposure to other organisms in the
environment. Notably, CNTs encased in biodegradable
polymer composites also persist despite complete degradation
of the polymer component; this results in the formation of a
contiguous mat of exposed CNTs that can now directly
interact with microbes and other organisms.260−262
7.3. Microbial Uptake and Toxicity
As CNTs are generally expected to be stable to microbial
degradation after environmental release, their toxic effects
toward microorganisms are relevant to consider. The
cytotoxicity of CNTs toward environmental microorganisms
and how surface oxidation alters these interactions is highly
relevant to their overall environmental risk and impact on key
processes such as nutrient cycling. Indeed, both pristine CNTs
and O-CNTs have been reported as cytotoxic to bacteria, but
the precise mechanism of this toxicity is unclear.263 The
toxicity of pristine CNTs toward microorganisms is reported to
manifest through a few routes, the most common being
disruption (i.e., interactions with the cell membrane that create
perforations or other damage), uptake into cellular mem-
branes, or induction of ROS production.264−267 While pristine
CNTs primarily interact externally with cells, O-CNTs have
been shown to be available for uptake by algae, enabling the
internal disruption of cellular processes.268,269 An important
behavior shown to impact the bacterial toxicity of O-CNTs is
their improved dispersion in aqueous media, which effectively
increases the exposed surface area and concentration of O-
CNTs due to decreased aggregation and sedimenta-
tion.142,270−273 For example, Zheng et al., reported that while
neither pristine nor oxidized SWCNTs disrupted cell
membranes, O-SWCNTs were cytotoxic to Paracoccus
denitrificans, an important denitrifying bacterial species. Here,
the toxicity was attributed to interference in gene expression
caused by passive O-SWCNT uptake with no observable
membrane disruption, which was increased by virtue of their
improved dispersibility while pristine SWCNTs exhibited no
cytotoxic effect.271 The cytotoxicity of O-CNTs does not
necessarily require dispersion in aqueous media, however, as
polymer nanocomposites embedded with O-CNTs have been
shown to inhibit biofilm formation by Pseudomonas aeruginosa,
suggesting that microbe−CNT contact (which can be
influenced by CNT oxidation) is the key prerequisite for
CNT toxicity.263
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Beyond changes in cytotoxicity stemming from the extent of
surface oxidation, Gilbertson et al. established that the precise
functionality of CNT surface oxygen also affects microbial
toxicity as determined using acellular assays and the selective
thermal reduction of carboxylic acid groups.252 Specifically, O-
CNTs functionalized with carbonyl groups were found to have
high antimicrobial activity, while COOH-CNTs had reduced
antimicrobial activity.252 Glutathione oxidation, used here as
an acellular indicator of antimicrobial activity, can be caused by
both CNT-produced ROS and CNT-mediated electron
transfer from O2 to adsorbed glutathione.274 Glutathione
oxidation activity has been directly linked to decreased
bacterial viability, suggesting that the effects of different
functional groups on CNT toxicity are related to chemical, as
opposed to physical, mechanisms.252 The decreased anti-
microbial activity of COOH-CNTs is likely related to the
hydrogen-bonding character of the carboxyl groups blocking
glutathione access to active sites on the CNT surface.252 The
increased reactivity of the carbonyl-functionalized CNTs was
attributed to the electron-donating capacity of carbonyl groups
like quinones as well as their potential to form radical
intermediates.252 Because of the competing effects of carboxyl
and carbonyl functional groups, there was no correlation
between the total surface oxygen concentration and anti-
microbial activity. Importantly, this study did not examine the
effects of surface oxygen groups on physical mechanisms of
toxicity (e.g., membrane interactions). When considering
complex organisms, both physical and electrochemical
mechanisms of toxicity are relevant, as discussed in the
following sections.
7.4. Uptake, Translocation, and Biodistribution in
Organisms
Upon exposure to organisms, both pristine and oxidized CNTs
are prone to uptake. At this point, their translocation into the
bloodstream and subsequent biodistribution is important to
consider, as potential cytotoxic effects will be most relevant to
cells present at the sites of CNT deposition. Accurate
determination of CNT uptake and biodistribution in organisms
is challenging due to the complexity of biological systems and
the ubiquitous presence of background carbon species, thus
necessitating strategies for CNT labeling and tracking. Popular
means to detect CNTs in vivo include the use of radiolabels or
the detection of the inherent near-infrared (NIR) fluorescence
of pristine SWCNTs. Radiolabels (e.g., 14C, 111In, and
86 275,276
Y) are highly sensitive to quantification even in
complex media277−279 and generally do not contribute to
toxic effects, making them an excellent option for the detection
of CNTs after uptake.280,281 However, radiolabeling is not
always a viable option, as certain radiolabels can be removed
during surface oxidation processes (e.g., acid oxidation) and
other bulkier radiolabels (e.g., 125I, 86Y, and 64Cu) can be
released in complex media.276 Carbon (14C) radiolabeling,
while expensive, avoids these issues as 14C radiolabels remain
embedded within the CNT structure after oxidation or
exposure to complex media.279 Detection of pristine SWCNTs
via NIR fluorescence is more accessible than radiolabeling, but
this technique is less sensitive to detection and more
vulnerable to signal attenuation in complex
media.14,279,282,283 Additionally, NIR fluorescence is sup-
pressed after covalent functionalization, especially when the
functionalization involves electron-withdrawing groups like
those present after surface oxidation.284,285 Therefore, the
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detection of O-SWCNTs by NIR fluorescence is impractical.
Another CNT detection strategy relies on the quantification of
residual catalysts that remain within CNTs after syn-
thesis.286,287 However, surface oxidation often decreases the
content of such catalysts, thereby limiting the applicability of
this strategy. The stability and sensitivity of these analytical
approaches must be considered when using these techniques to
monitor the uptake and biodistribution of pristine and oxidized
CNTs within organisms.
As different routes of CNT uptake are possible and each
offers potentially different in vivo behavior, a variety of
exposure scenarios must be considered. Translocation within
the body typically proceeds from the site of primary exposure
into the bloodstream, which renders CNTs available for
transport to a range of organs.288,289 The injection of CNTs
into model organisms enables the study of the CNT
biodistribution behavior that occurs after initial translocation
to the bloodstream from primary sites of exposure. For
example, after injection of CNTs dispersed in a biocompatible
serum into the bloodstream of rodents, pristine CNTs and O-
CNTs have typically been found to accumulate in the liver,
kidneys, and spleen, although deposition in the lungs has also
been reported.277,290−292 Once transported to these organs,
CNTs have been shown to persist for months to years,
underlining the importance of understanding their toxicity and
interactions with cells during this span.277,291,292 Schipper et al.
reported that pristine, noncovalently PEGylated, and oxidized/
covalently PEGylated SWCNTs were each transported to the
liver and kidneys after injection and persisted for four months,
suggesting that surface chemistry does not notably alter the
deposition sites of CNTs after injection.292 Similarly, J. Wang
et al. found OH-SWCNTs throughout the body of mice two
months after injection into the bloodstream, with the highest
concentrations in the liver, kidneys, and stomach.293
Inhalation is another important exposure pathway to
investigate, as CNTs accumulated in the lungs are typically
considered to be available for translocation into the blood-
stream. In general, immediately after aspiration, CNTs are
concentrated in the lungs where they are slowly removed over
the timespan of months or years, partially due to translocation
into the bloodstream.276,277,291 After arrival in the bloodstream,
CNTs are available for further transport to the liver, spleen,
and bone marrow.276,277,294 The hydrophilicity imparted by
surface oxidation leads to increased uptake, dispersion, and
residence within the lungs after inhalation, though both O-
CNTs and pristine CNTs have been shown to later translocate
from the lungs to the same final deposition sites.295,296
As opposed to the in vivo mobility of CNTs after inhalation,
exposures via ingestion or dermal contact offer low availability
for translocation and biodistribution in terrestrial mammals
and invertebrates.297,298 As a result of the poor permeability of
CNTs through intestinal barriers, ingestion of CNTs primarily
leads to excretion in feces.277,291 In a study by Czarny et al.,
95% of ingested CNTs labeled with 14C were found in the
gastrointestinal tract and feces of mice after 24 h, leading to
complete removal after 4 d with none found in the spleen or
liver.277 O-MWCNTs have also been shown to be unavailable
for transport across dermal and intestinal barriers, suggesting
that both types of CNTs are relatively transient in vivo upon
ingestion.299 For example, Petersen et al. exposed model worm
species to both pristine and oxidized CNT-dosed soil and
found that bioaccumulation was minimal for both CNT types
after 28 d of exposure,297 indicating that surface oxidation of
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CNTs has a negligible effect on uptake and in vivo residence
time after exposure via dermal and gastrointestinal routes. One
exception may be for the hydroxylation of very small SWCNTs
(diameter = 1.4 nm, length = 300 nm); H. Wang et al.
observed that these OH-SWCNTs could be detected in the
kidney, lungs, and bone in addition to the stomach 3 h after
oral exposure to mice.300 A very similar biodistribution pattern
was observed for the OH-SWCNTs when administered via
injection, further evidence that the ingested OH-SWCNTs
were able to enter the bloodstream.300 O-CNT accumulation
has also been observed in the gills and digestive tract of
freshwater and marine organisms.301−304 O-SWCNTs were
observed in the gut, intestines, lipid vesicles, and phagocytes of
Artemia salina 24 h after the exposure period was ended.301
Similarly, both oxidized and pristine MWCNTs have been
observed in the gut of Daphnia magna for at least 24 h after the
exposure period was ended and normal feeding was resumed,
though between 50 and 85% of the ingested O-MWCNTs
were determined to be excreted (comparable calculations were
not performed in the P-MWCNT study).303,304
Overall, the translocation and biopersistence of CNTs has
been shown to be primarily dependent on exposure pathway
rather than the degree of surface oxidation. Many hypothesize
that agglomerate size is the driving factor, which is consistent
with the observation that oxidation increases mobility and
urinary excretion only for small SWCNTs.276 As described in
detail in the review by Jacobsen et al., the large agglomerate
size of most CNTs tested is likely what causes accumulation
within the liver after injection because excretion through the
renal system requires passage through perforations <20 nm in
size.276 Confirmation of the agglomerate size in vivo is
challenging but could help identify the mechanisms of CNT
biodistribution and the potential relevance of oxidation for
well-dispersed CNT materials.
7.5. Potential Routes of Cellular Toxicity
Because of the availability of CNTs for distribution throughout
the body, a variety of organs are likely to be exposed to CNTs
and O-CNTs, necessitating the determination of toxic effects
toward a range of cell types. The nature and extent of these
cytotoxic effects are somewhat complex, however, as they can
manifest through a variety of mechanisms.
Research to date has established that both SWCNTs and
MWCNTs are cytotoxic to a variety of cells and organisms, the
extent of which is dependent on size,266,305−307 dose,305,308,309
purity,310−313 and aggregation state.314,315 As such, keeping as
many physicochemical factors as consistent as possible is
crucial when identifying the influence of oxidation on CNT
toxicity, especially because there is no single, well-accepted
underlying mechanism of these toxic effects. Indeed, it seems
more likely that a variety of different mechanisms can
contribute to the overall cytotoxicity of CNTs. Consequently,
identifying the effect of CNT surface oxidation on the wide
range of potential mechanisms of toxicity is necessary.
One widely accepted mechanism of CNT and O-CNT
toxicity involves damage to cellular components and eventual
apoptosis after cellular uptake via endocytosis/phagocytosis
(which requires CNTs to be small enough to enable uptake),
or nanopenetration (i.e., piercing through the cellular
membrane).316,317 One example of this mechanism of toxicity
is described by Fraczek-Szczypta et al., who exposed
macrophage cells to pristine and acid-oxidized MWCNTs.318
The O-MWCNTs in this study were shown to greatly decrease
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cell proliferation due to their increased uptake into cells (which
was attributed to a combination of endocytosis and passive
uptake) as observed using an inverted microscope, leading to
the disruption of mitotic processes (i.e., cell division).
Conversely, pristine MWCNTs did not interfere with the
mitotic pathway, as their relative surface hydrophobicity led to
the formation of agglomerates too large for uptake.318 This
increased uptake of O-CNTs is consistent with data obtained
by Bai et al., where rat endothelial cells and mouse macrophage
cells exhibited increased uptake of COOH-CNTs compared to
the pristine form, resulting in alterations in gene expression.319
Small particulate residues that form during enzymatic
oxidation of CNTs may be similarly bioavailable for inducing
genotoxicity.320 Pan et al. showed that increased exposure to
horseradish peroxidase (HRP) resulted in SWCNT fragment
formation and increased DNA damage, as measured through
Comet assays and an electrochemiluminescent screening
array. 320 In general, the increased hydrophilicity and
dispersibility of O-CNTs increases availability and subsequent
cellular uptake, heightening interactions with interior cellular
components and DNA compared to pristine CNTs.321−323
However, internal interaction between cells and CNTs is not
the only potential mechanism of toxicity. External interactions
with cell membranes have also been shown to lead to cell death
and ROS response, especially if the CNT is large enough to
spur frustrated phagocytosis (caused by cells straining to
uptake a large particle).324 Because of the difficulty of directly
observing these disruptive effects using live cells, model
phospholipid membranes are often used to assess interactions
between CNTs and cell surfaces. Such studies indicate that
pristine MWCNTs typically have increased interactions with
cell membranes compared to O-MWCNTs, dependent on the
extent of CNT dispersion in the cellular media.325,326 For
example, using giant unilamellar vesicles, the hydrophobic
surface of pristine MWCNTs has been found to facilitate the
penetration of membrane bilayers while O-MWCNTs remain
outside the phospholipid layer, driving nondisruptive pore
formation.325 In a separate study, pristine MWCNTs failed to
penetrate a model cell membrane, instead irreversibly
depositing on the bilayer in solutions of 0.5 mM CaCl2 or
low pH (2).326 McGeachy et al. used second harmonic
generation (SHG) and sum frequency generation (SFG)
spectroscopies combined with QCM-D of supported lipid
bilayers to demonstrate that while O-MWCNTs deposited on
model membranes at ionic strengths of 100 mM (typical ionic
strength 0.05−0.25 M in vivo),327 the deposition was only
minimal and drove no membrane disruption.328
Results from studies utilizing model membranes should be
considered with caution. While they successfully model toxic
interactions which stem from CNT disruption of cell
membranes, they do not account for other cytotoxic
mechanisms which may be influenced by surface oxidation.
For example, oxidation improves the dispersibility of CNTs,
resulting in a higher exposure to cells as described in the
previous section involving microbial toxicity. The higher
effective concentration of O-CNTs exposed to cells leads to
increased uptake via endocytosis, potentially heightening
internal toxicity, an effect which cannot be captured by
model membrane studies.329 Indeed, as CNT−microbe
contact has been reported as crucial for toxic effects to
manifest,263 the increased dispersibility of O-CNTs is likely to
contribute strongly to potential toxicity.
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In addition to the potential for membrane disruption caused
by CNTs, the promotion of cellular oxidative stress through
other physical interactions and the indirect production of ROS
by CNTs are common mechanisms of toxicity for CNTs and
O-CNTs.330 These pathways of oxidative stress are mechanis-
tically unique as interfering with natural cellular quenching
(i.e., interfering with antioxidants) of ROS typically requires
CNT uptake, while external ROS can be produced by surface-
adsorbed metal catalysts residual from CNT synthesis or
produced by cells exposed to CNTs of large sizes (i.e., too
large for cellular uptake leading to frustrated phagocyto-
sis).310−312,319,324,331 Many studies report that oxidation of the
CNT surface results in deceased inflammatory response, which
is often attributed to the increased dispersibility and reduced
membrane disruption caused by the hydrophilic surface or
reduced metal content after acid-washing of the O-
CNTs.100,295,332,333 However, other studies indicate that
CNTs promote increased inflammatory response after surface
oxidation due to either increased exposure (due to
dispersibility) or ROS production (by oxygen-containing
surface groups). 334−338 The different routes of ROS
production caused by the exposure of cells to CNTs
necessitate studies which systematically vary the degree of
surface oxidation in order to determine the overall effect of
surface oxidation on toxicity.
One such study was done by Hamilton Jr. et al., which
investigated MWCNTs with a range of surface oxidation (5−
15 at. % O as measured by EDX) and confirmed that increased
oxidation resulted in a decrease in both inflammatory response
and autophagy (a cellular process involving the removal of
damaged cell components as would be required after
nanoparticle-induced toxicity), which was observed both in
vivo and in vitro for A549 epithelial cells exposed to
MWCNTs.295 Similarly, Jain et al. reported a steady decrease
in inflammatory response (Figure 9) by mice as a function of
surface oxidation (0−6 μmol/mg COOH, measured with
TGA).332 CNT oxidation has also been observed to impart
Figure 9. (a) TNF-α and (b) IL-6 cytokine production of mice
treated for 7 d with various surface oxidized MWCNTs (0−6 μmol/
mg COOH, with increasing oxidation indicated by the increasing acid
treatment time in h on the x-axis) at 10 mg/kg. Increased oxidation
density led to an overall reduction in inflammatory cytokine response.
Reproduced with permission from ref 332. Copyright 2011 American
Chemical Society.
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protective effects. Using a mixed theoretical−experimental
approach, González-Durruthy et al. developed a combination
perturbation theory-quantitative structure−property relation-
ship (PT-QSPR) model from experimental studies of nine
different CNTs interacting with mitochondria isolated from rat
livers.339 While pristine CNTs caused mitotoxic effects,
COOH- and OH-functionalized CNTs could prevent and
reduce mitochondrial swelling, with the greatest protection
achieved using COOH-MWCNTs.339 It was hypothesized that
this effect could be caused by the adsorption of the Fe2+ and
Ca2+ ions that induce mitochondrial permeability.339 Results
from the predictive model suggested that increasing the
functionalization density would increase protection.339 These
systematic studies provide evidence that surface oxidation of
CNTs leads to a reduction in inflammatory response and
resultant toxicity due to decreased interactions with the
nonpolar components of cell membranes compared to pristine
CNTs, and that this enhanced biocompatibility may even
extend to protective effects in some cases.
In contrast, an in vitro study performed by Singh et al. as a
follow up to the previously discussed in vivo study by Jain et al.
used the same suite of oxidized MWCNTs but found the
opposite trend in the effects of functionalization.340 As shown
in Figure 10, MWCNTs with higher carboxylic acid densities
exhibited greater toxicity to the RAW 264.7 cell line, a model
for liver Kupffer cells.340 Thus, caution is warranted when
attempting to relate toxic effects toward isolated external cells
to overall toxicity to an organism. This stems from the
complicated interplay between mechanisms of toxicity when a
complex biological system is considered for in vivo studies. For
example, damage to cells may be exacerbated in vitro due to
increased CNT localization (and dosage), leading to increased
cellular uptake and subsequent internal damage that would not
be experienced within an organism where CNT concentrations
are diminished.340 Another interesting aspect of this study is
that both the uptake and toxicity of O-MWCNTs were
dramatically decreased after neutralizing the charge of surface
oxygen groups using poly-L-lysine or polyethylene glycol.340
This suggests that the surface charge is a key parameter driving
Figure 10. Apoptosis of RAW 264.7 cells after 24h. Exposure to 100
μg/mL MWCNTs with 0−6 μmol/mg COOH density (with
increasing oxidation indicated by the increasing acid treatment time
in h on the x-axis). Percent of apoptotic cells was determined by
TUNEL (white bars) and annexin V (black bars) DNA fragmentation
assays. Reproduced with permission from ref 340. Copyright 2012
American Chemical Society.
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toxicity, consistent with work by Gilbertson et al. discussed in
section 7.3.251
However, it should be noted that the H2SO4/HNO3
oxidation method applied in both the in vitro and in vivo
studies resulted in systematic shortening of the
MWCNTs.332,340 When the in vitro cellular uptake of the
full suite of pristine, oxidized, and charge-neutralized
MWCNTs was modeled using multiple linear regression
analysis, both surface charge and MWCNT length were
shown to play a role (eq 9, Pearson’s coefficient = 0.955).340
uptake = 8.158 − (0.006 × ζ potential)
− (0.180 × length)
(9)
The complicated interplay between functionalization and
length has been further explored in other in vitro studies. Yu et
al. examined a suite of MWCNTs with two discrete length
ranges (10−30 μm and 0.5−2.0 μm) and three surface
chemistries (pristine, 3.86 wt % COOH, and 5.58 wt %
OH).341 Here, it was discovered that the impact of
functionalization depended on CNT length; surface oxidation
increased cytotoxicity of longer MWCNTs toward the human
hepatoma cell line HepG2 but decreased cytotoxicity of
shorter MWCNTs.341 In another study using the same CNT
length ranges on a different cell line (THP-1 alveolar
macrophages isolated from mice), it was shown that
carboxylation eliminated the in vitro toxicity of MWCNTs
regardless of length.100 As previously discussed, the different
effects of functionalization-length combinations are likely
caused by differences in the mechanisms of toxicity; the
inhibitory effects observed for HepG2 cells were caused by
intracellular ROS production, while THP-1 cells experienced
inflammation caused by membrane interactions.100,341 There-
fore, structure−property relationships describing the impact of
CNT functionalization must consider potential differences in
cellular uptake and mechanisms of toxicity before they can be
extrapolated to different cell types.
Considered collectively, the various and often conflicting
studies describing the effects of oxidation on CNT toxicity can
be understood by the differential interaction of CNTs with
cells based on aggregation state and the specific mechanism of
toxicity, both of which vary depending on the organism of
interest.342 Surface oxidation can promote toxic effects which
manifest through certain pathways (e.g., DNA damage) but
reduce toxic effects which emerge via others (e.g., membrane
disruption) by virtue of the changes in dispersibility and
membrane interactions produced by the addition of surface
oxygen groups. Because of the complexity of biological
systems, multiple mechanisms likely contribute to the overall
effect of surface oxidation on CNT toxicity. As such, studies
which first isolate the effect of surface oxidation on toxicity,
specifically in terms of how the underlying mechanism(s)
change as a function of CNT surface oxidation, are
prerequisites to understanding the overall impact of CNT
surface oxidation on toxicity toward an organism. Furthermore,
studies which allow for the comparison of a variety of O-CNTs
by systematically controlling (e.g., via acid oxidation and
subsequent annealing) and quantifying (e.g., via XPS in
conjunction with chemical derivation) the degree of surface
oxidation will be invaluable for identifying the effect of surface
oxidation on the cytotoxicity of CNTs.
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7.6. Biopersistence
One other contributing factor in determining the effect of
surface oxidation on the biological impact of CNTs are the
changes to biopersistence that could be induced by oxidation.
As biological impact is highly dependent on exposure duration,
the in vivo residence time of CNTs and O-CNTs is of
heightened importance. The biopersistence of CNTs is
primarily dictated by their resistance to cellular enzymes, a
property which is impacted by the degree of surface oxidation.
These enzymatic routes of degradation that occur within
organisms are distinct from those experienced in the natural
environment outside of organisms, as they often take place in
acidic conditions (e.g., in lysosomes) or in the presence of
different concentrations and types of oxidants than would be
otherwise encountered.
Work done with HRP has shown that enzymatic degradation
is initiated at defect sites in the CNT structure, meaning that
oxidized CNTs are degraded to a greater extent than pristine
CNTs.343,344 Russier et al., showed that O-SWCNTs degraded
entirely over 60 d in a HRP/H2O2 system, and O-MWCNTs
were degraded to a lesser extent over the same time period as
illustrated with TEM, DLS, and Raman spectroscopy; this
difference between the two O-CNT types was attributed to the
multiple concentric layers of MWCNTs, which SWCNTs
lack.345 Furthermore, this study also investigated the enzymatic
degradation of MWCNTs with two different degrees of surface
oxidation and found that the more highly oxidized CNTs were
most extensively degraded; it was hypothesized that the
enzymatic degradation process is initiated at defect sites
present in the CNT sidewalls, which increase in quantity as
CNTs become more oxidized.345 A study by Liu et al. further
supports the theory that defect sites are needed to drive the
enzymatic degradation of CNTs.346 O-SWCNTs oxidized via
acid carboxylation were enzymatically degraded in acidic
phagolysosomal simulant fluid (PSF) for 90 d, which resulted
in a decrease in length (Figure 11) that was measured with
TEM, SEM, and DLS. Conversely, pristine SWCNTs and O-
SWCNTs that were oxidized via ozonolysis and aryl
sulfonation (i.e., oxidation strategies which do not impart
many defect sites) did not degrade under the same
conditions.346
Despite the majority of studies which report decreased
biopersistence of CNTs after surface oxidation, other studies
show that O-CNTs possess considerable biopersistence/
resistance to enzymatic degradation.258,347 For example, Sato
et al. reported that tangled O-CNTs, which were too large for
uptake by macrophages, persisted for 2 y in intercellular spaces
within subcutaneous tissues.347 Additionally, certain enzymes
are less effective at degrading O-CNTs, as each enzyme has a
distinct pathway of degradation that interacts differently with
surface oxygen groups. An illustrative example of this enzyme
dependence was described by Zhang et al., who exposed
pristine and oxidized SWCNTs to lignin peroxidase,
manganese peroxidase, and laccase.348 Of these three enzymes,
none could degrade the O-SWCNTs while only manganese
peroxidase degraded the pristine SWCNTs, as shown by
Raman, NIR, and TEM.348 This improved resistance of O-
SWCNTs to manganese peroxidase was attributed to the
complexation of Mn2+ by surface carboxyl groups, thus
disrupting the enzymatic pathway of manganese peroxidase
by interfering with its oxidation to Mn3+ at the enzyme’s active
site.
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Figure 11. Biodegradation of O-SWCNTs before and after exposure
to phagolysosomal simulant fluid (PSF). (a) SEM of initial O-
SWCNTs before enzymatic treatment. (b) Histogram of O-SWCNT
lengths before enzymatic treatment as compiled from the SEM
measurements of ∼300 nanotubes. (c) Histogram of O-SWCNT
lengths after 90 d exposure to PSF compiled from the SEM
measurements of ∼300 nanotubes. Reproduced with permission from
ref 346. Copyright 2010, Elsevier.
The biopersistence of O-CNTs is dependent upon the
specific classes of enzymes encountered during their in vivo
residence time and therefore the biodistribution of CNTs.
Degradation can be expected to occur over prolonged
timespans. Sato et al. implanted O-MWCNTs inside of rat
subcutaneous tissue for a 2 y period.347 Larger aggregates
remained in intercellular spaces and did not degrade, while
smaller aggregates entered macrophages and underwent some
degradation inside of lysosomes.347 Even after 2 y, only partial
degradation of the outermost O-MWCNT layer was observed
in vivo, as characterized using Raman spectroscopy and HR-
TEM analyses.347 Overall, biodegradation of CNTs is limited,
meaning that CNT and O-CNT toxicity will still be of relevant
concern after uptake. As such, it would befit manufacturers to
intelligently design O-CNTs to minimize the toxic potential of
O-CNTs while still enabling their use.
7.7. Implications for CNT Design
The surface oxidation of CNTs can impart drastic variations in
the toxic interactions of CNTs with a range of cells and
organisms. As surface oxidation is often a prerequisite for the
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utilization of CNTs in commercial products, a balance must be
struck at the point of manufacture between the extent of
oxidation required for the practical application of CNTs and
minimizing their potential downstream toxicity. The desire to
achieve this balance necessitates the ability to control the
degree of CNT surface oxidation. One option to obtain this
control involves thermal annealing of O-CNTs in inert
atmosphere, allowing for a “safer by design” approach to the
synthesis of CNTs and CNT-enabled products.251,274,349,350
Gilbertson et al., in particular, have utilized such techniques to
control the toxicity of CNTs.251,252,349 Although the impact of
CNT surface oxidation on toxicity depends on the mechanism
of action, strategies exist which provide control over such
interactions, and thus CNT toxicity and persistence, offering
manufacturers a low-cost and scalable method for minimizing
the environmental impact of CNTs.
8. APPLICATIONS IN WATER TREATMENT
The need for more efficient and selective membrane separation
technologies for water purification has led to increased interest
in using CNTs as a potential filtration material. CNTs have the
advantages of high porosity, large surface area to volume ratios,
desirable adsorptive interactions, and beneficial electrochem-
ical properties.351,352 Despite these promising characteristics,
there are challenges to preparing CNT-modified membranes,
including CNT entanglement and low dispersibility of CNTs
in polar solvents frequently used for membrane preparation.353
This aggregation and nonuniform dispersion results in
inefficient transfer of stress and decreases the mechanical
properties of the modified membranes. Deliberate oxidation of
CNT surfaces prior to membrane fabrication improves CNT
dispersion in a solvent/polymer matrix, increasing composite
homogeneity. Ultimately, incorporation of O-CNTs into
membranes provides additional control over the pore size,
roughness, and surface chemistry of the composite membrane.3
This tunability facilitates superior treatment performance
metrics such as increased contaminant rejection, increased
permeability, and fouling resistance.3 Furthermore, O-CNTs
can be utilized as electrochemical filters and thereby enable the
degradation of target contaminants, which is not possible with
conventional water filtration methods. In this section, we
describe the implications of CNT surface oxidation on the
efficacy of CNT-enabled water treatment technologies.
8.1. Impact of CNT Surface Oxygen on Membrane
Preparation
CNT-enabled membranes can be classified into three
categories based on the orientation of SWCNTs or MWCNTs
within the polymer membrane matrix: vertically aligned CNT
(VACNT) membranes, horizontally aligned CNT (HACNT)
membranes, and mixed matrix (MM) membranes (Figure
12).354 For each membrane type, CNT surface oxidation can
improve membrane preparation and performance.
In a VACNT membrane, CNTs are typically synthesized
perpendicular to the support layer via chemical vapor
deposition, followed by polymer infiltration to fill the gaps
between nanotubes. An etching process is conducted to
remove excess surface polymer and open the tips of the CNTs.
Separation of aquatic contaminants occurs as water is
transported through the inner diameter of the CNTs. Here,
plasma oxidation can introduce carboxylic surface groups to
the tips of the CNT nanopores after assembly to further
improve rejection of charged contaminants.117 As opposed to
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Figure 12. Conceptual diagram of CNT-enabled membranes with
various structures based on CNT orientation: (a) vertically aligned
CNT membrane (VACNT), (b) horizontally aligned CNT
membrane (HACNT), (c) mixed matrix (MM) CNT membrane.
vertical arrangement, CNTs may also be positioned parallel to
the support layer to form a HACNT membrane. 355
Preparation of a HACNT membrane requires a homogeneous
dispersion of CNTs in water or another solvent, followed by
vacuum filtration to deposit CNTs into a thin layer on the
membrane surface.356 CNTs can be oxidized prior to
deposition by acid treatment or after deposition via plasma
oxidation to generate a highly porous, hydrophilic bar-
rier.357,358 Unlike HACNT membranes, in which CNTs are
deposited on the surface of the support layer, MM membrane
CNTs are directly embedded into the support layer. This is
achieved by casting a solution of solvent, dissolved polymer,
and dispersed CNTs into a flat sheet, allowing the CNTs to
randomly orient themselves within the polymer matrix.359 Both
HACNT and MM membranes require good dispersion of
CNTs within the casting solution to achieve enhanced
mechanical properties and filtration performance.353,360 This
can be accomplished through premodification of CNTs with
surface oxygen groups. For example, MM membranes prepared
with an active layer of O-CNTs had a greater Young’s modulus
(by 85.5%), tensile strength (by 48.0%), and stress at break
value (by 21.4%) as compared to the same membrane without
an O-CNT layer.360 Overall, CNT oxidation overcomes the
major challenges inherent to using pristine CNTs in CNT-
enabled membranes through the formation of hydrophilic
surface sites and improved compatibility with the solvent
during membrane preparation.
The advantages of integrating O-CNTs in composite
nanofiltration membranes extend beyond improvements to
membrane preparation, playing a critical role in membrane
fouling resistance and water treatment performance.
8.2. Antibiofouling Properties of O-CNT Membranes
An effective method to control membrane fouling is tuning the
chemistry of the membrane surface to decrease interactions
with biofouling material. Many organic foulants are hydro-
phobic; thus, increasing the hydrophilicity of a membrane via
incorporation of O-CNTs enhances fouling resistance. As
discussed in section 7, CNTs can also exhibit strong
antibacterial activity, which can further improve fouling
resistance by imposing biocidal properties to the membrane.361
For example, Vatanpour et al. fabricated an O-MWCNT/
poly(ether sulfone) MM membrane that exhibited higher flux
recovery when exposed to a fouling protein solution compared
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to that of a pristine poly(ether sulfone) membrane.362 While
the concentration of CNT surface oxygen was not quantified,
FTIR was used to confirm oxidation via the presence of CO
and O−H stretching modes in the O-CNT structure and in the
assembled membranes, while contact angle measurements
confirmed an increase in membrane hydrophilicity compared
to the unmodified PES membrane. The charged carboxylic
groups of the O-MWCNT act as binding sites for water
molecules, which presumably leads to the formation of a
surface water layer that prevents protein adsorption, resulting
in decreased fouling.362 Similarly, another study examined MM
ultrafiltration membranes composed of polyvinylidene fluoride
(PVDF) and pristine vs oxidized MWCNTs. The membranes
containing O-MWCNTs had a 99.3% greater pure water flux
and a 21.7% greater rejection of bovine serum albumin, a
model hydrophobic foulant.363
While the incorporation of O-CNTs reduces membrane
biofouling, the O-CNT mass loading must be balanced to limit
the formation of aggregated CNT clusters. Although O-CNTs
are less prone to aggregation than pristine CNTs, at high
loadings they may form clusters and reduce pure-water
membrane flux. CNT aggregation facilitates foulant adsorption
by roughening the membrane surface and decreases biocidal
properties relative to well-dispersed CNTs, further enabling
biofilm growth.360 For example, deposition of O-CNTs on a
polyamide reverse osmosis HACNT membrane resulted in
improved rejection of the biomolecular foulant Pseudomonas
aeruginosa; however, at O-CNT loadings greater than 0.2 wt %,
the dispersed O-CNTs began to aggregate on top of the
substrate membrane layer.360 Consequently, a decline in pure
water flux was observed for this sample, as biological foulants
were able to adsorb in the macroporous spaces between CNT
aggregates and clog the membrane.360 Additionally, even in
filtration applications where fouling is not a concern, CNT
loading cannot be increased monotonically without inevitably
compromising water flux due to aggregation alone.364
8.3. Removal of Organic and Inorganic Contaminants by
O-CNT Membranes
Numerous studies have utilized CNT oxidation to improve the
removal efficacy of CNT membranes toward inorganic and
organic contaminants in aqueous solution. Elsehly et al.
demonstrated the improved removal of iron from aqueous
solution by an O-CNT filter compared to a pristine CNT filter
due to greater adsorptive interactions of the positively charged
Fe2+ ions with the negatively charged oxygen binding sites
available on O-CNT surfaces.365 Removal of other metal
contaminants has also been studied. For example, when the
concentration of surface oxygen was increased from 2.78 at. %
for pristine CNTs to 6.79 at. % for O-CNTs, Zn2+ removal
with CNT-enabled water filtration membranes increased from
68% to 85%.366 This relationship between functional group
density and metal ion removal has also been observed for other
CNT-enabled treatment technologies. Using paper adsorbents
composed of SWCNT−graphene nanohybrids, Dichiara et al.
found that the maximum Cu2+ adsorption capacity increased
from 49 μg·mg−1 for pristine hybrids to 63 and 256 μg·mg−1
for hybrids containing COOH-SWCNTs (2.7 wt % COOH)
and OH-SWCNTs (3.9 wt % OH), respectively.367
The removal efficacy of CNT membranes toward organic
contaminants primarily occurs through mechanisms discussed
in section 5 (e.g., π−EDA interactions); thus the sorption
capability of membranes containing pristine CNTs is limited to
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nonpolar species. Surface modification of CNTs with oxygen-
containing functional groups enhances electrostatic interac-
tions with polar organics, thereby broadening treatment
applications of a contaminant filtration membrane. For
example, an O-CNT-enabled polysulfone MM membrane
achieved better removal of polar organic contaminants than a
pristine CNT-enabled polysulfone MM membrane.368 Specif-
ically, the membrane rejection performance for 2-naphthol
[Naphthol]
(calculated as 1 − [Naphthol] effluent ) was 0.3 for the O-CNT
feedsolution
membrane vs 0.1 for the pristine CNT membrane, confirming
the repulsive behavior between polar contaminants and the
polar surface of O-CNTs.368 For nonpolar organic contami-
nants, however, highly oxidized CNTs can decrease treatment
efficacy due to undesired electrostatic interactions. Y. Wang et
al. compared removal efficiencies of PVDF membranes
prepared with SWCNTs, MWCNTs, and O-MWCNTs with
4.1, 3.3, and 6.0 at. % surface oxygen (as determined by XPS),
respectively, for the removal of the common pharmaceutical
and personal care products acetaminophen, triclosan, and
ibuprofen via adsorptive filtration.369 While all CNT-enabled
membranes performed better in triclosan removal than the
unmodified PVDF membrane due to the overall hydro-
phobicity of both the CNTs and the triclosan (Figure 13),
Figure 13. Breakthrough curve of triclosan at pH 7. In the absence of
CNTs, triclosan passed through the PVDF membrane within 25 min,
achieving a C/C0 value of 0.8 (less than 20% removal). In comparison,
the breakthrough of triclosan toward CNT-containing membranes
was appreciably slower with C/C0 values remaining below 0.2.
Reproduced with permission from ref 369. Copyright 2015 Elsevier.
feed solution pH directly impacted the adsorptive removal
capacity of the O-MWCNT membrane. The presence of more
oxygenated groups on the CNT surface of the O-MWCNT
membrane resulted in an increase in negative charge with an
increase in feed solution pH. At pH values greater than 7,
triclosan and ibuprofen exist primarily as deprotonated ions
and electrostatic repulsion is the predominant interaction
between the negatively charged contaminant and negatively
charged CNT surface. Consequently, the O-MWCNT
membrane presented lower adsorptive removal for triclosan
and ibuprofen compared to the pristine CNT membranes.369
Along with contaminant removal, water flux must be
considered when designing filtration technologies. For MM
ultrafiltration membranes, both the extent of CNT oxidation
and the loading of O-CNTs within the membrane has proven
to impact pure water flux and the rejection of bovine serum
albumin (BSA), a model protein.370 Ma et al. found that PVDF
membranes with 1 wt % loading of oxidized versus pristine
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MWCNTs had dramatic differences in hydrophilicity, porosity,
and pure water flux, while differences in BSA rejection were
more modest.370 Compared to a pure PVDF membrane, the
O-MWCNT-PVDF membrane offered an 1100% increase in
pure water flux while the P-MWCNT-PVDF membrane
offered only a 78% increase. This was attributed to increased
hydrophilicity imparted by the oxygen-containing functional
groups, which also improved phase separation and pore
formation during membrane preparation.370 Similarly, when
the O-MWCNT loading was varied (0, 0.2, 0.5, 1, and 2 wt %),
the water contact angle decreased and the porosity increased
until a plateau was reached for the 1 wt % formulation. This
formulation had the most advantageous balance of pure water
flux and BSA rejection.370
Overall, O-CNTs can improve rejection efficiency of both
polar organic and inorganic contaminants compared to pristine
CNTs, but negatively charged functional groups on the surface
of the O-CNTs can reduce the adsorption, and thus the
rejection efficiency, of nonpolar organics due to electrostatic
repulsion. CNT surface oxidation can also control the porosity
of membranes, allowing for the optimization of water flux
versus contaminant rejection.
8.4. Water Desalination with O-CNT Membranes
Current water desalination techniques rely on reverse-osmosis
polymer membranes to filter out fine solids and dissolved salts.
These processes require high pressures for successful treat-
ment, resulting in high energy consumption and high cost.
These disadvantages can be mitigated using O-CNTs.
Specifically, the trade-off between increased ion selectivity
and decreased water flux in desalination processes can be
tuned by optimizing both the degree of surface oxidation in O-
CNTs and the overall O-CNT loading in the final membrane
assembly.
Two CNT-enabled membrane types have been explored for
desalination applications. In the case of VACNT membranes,
computational modeling demonstrates that addition of oxygen-
containing moieties to CNT openings improves rejection of
salt ions but reduces the flow rate of water molecules through
the inner wall of the CNTs.371 Experimentally, VACNT
membranes utilizing O-CNTs have been successfully employed
for the removal of salt ions,372 although CNT surface oxidation
has not yet been systematically varied in these studies.
Filtration and water quality parameters are also important to
performance outcomes, further complicating the relationship
between CNT surface oxygen and desalination performance.
Increased feed concentration, increased operating temperature,
and increased flow rate have all been shown to decrease the
efficacy O-VACNT membranes.373 Despite excellent water
permeability and high salt rejection, the preparation of
VACNT membranes is difficult, which hinders scale-up for
practical implementation.
HACNT membranes have also been explored for desalina-
tion. The most systematic study of the influence of CNT
surface oxidation on desalination performance to date was
performed by Yang et al. using membranes enabled by
ultralong (100−200 μm) MWCNTs.374 Rather than oxidizing
the CNTs prior to membrane assembly, CNTs were deposited
onto a mixed cellulose ester support and then oxidized using
either acid or plasma modification techniques. Plasma
treatments resulted in a greater increased of surface oxygen
(as measured by XPS) and defect density (quantified by the
Raman ID/IG ratio) and also imparted severe structural damage
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to the outer walls of the O-MWCNTs. As oxidation and
defects increased, so did NaCl removal, which was
accomplished through the ultrahigh adsorption capacity of
the MWCNTs as opposed to osmotic removal. At the highest
plasma treatment time (10 min exposure), the NaCl
adsorption capacity reached 400% by weight (4 g NaCl/g
CNT). This portable technology enables the treatment of
brackish waters with limited energy requirements, but further
studies are needed to evaluate their use for the purification of
more complex high salinity waters.374
O-CNT-enabled membranes offer great promise in desali-
nation applications, with surface oxidation generally increasing
performance. However, optimization of material properties is
complicated by strong influence of water quality, requiring
careful balance between CNT oxidation, loading, and filtration
parameters.
8.5. O-CNT Filters in Advanced Oxidation Processes
A recent focus has been the application of O-CNTs in “next
generation” electrooxidative filters. The aim of this water
treatment strategy is the oxidative degradation of target
pollutants (or anodic mineralization) by •OH in addition to
removal through filtration. The quantity and nature of surface
oxygen groups directly influences the performance of CNTs in
electrochemical filters. By using a suite of well-characterized
CNTs that were oxidized under different conditions, Oulton et
al. showed that the efficiency with which •OH are produced
when CNT filters are exposed to ozone increases systematically
as their surface oxygen content is increased.375 The electro-
oxidation kinetics of CNT filters are surface group dependent,
resulting in different oxidation strengths and pathways. Gao et
al. examined how the type of oxygen-containing functional
group (i.e., carboxylic acid vs hydroxyl) influenced the overall
anodic potential of a CNT filter. Compared to unmodified
CNTs, anodic mineralization performance decreased 2-fold for
CNTs with predominantly carboxylic acid groups while anodic
performance increased 2-fold for CNTs containing primarily
hydroxyl groups. This trend is observed due to the production
of more surface bound •OH upon oxidation of the primarily
hydroxylated CNTs.376 The oxidation of a hydroxyl functional
group generates a strongly oxidizing, surface-bound •OH. In
contrast, oxidation of a carboxyl group results in the formation
of a weakly oxidizing carbon radical upon decarboxylation. O-
CNTs have also been used by Omi et al. for the layer-by-layer
self-assembly of CNTs on polysulfone ultrafiltration mem-
branes, with CNT bilayers alternating between amine-
functionalized MWCNTs and COOH-MWCNTs.377 Five-
bilayer thick conductive membranes achieved 100% inactiva-
tion of Escherichia coli and 99% removal of methyl orange at an
applied potential of 3 V.377 The low applied electrical potential
required for contaminant removal and the resilience of these
CNT-enabled membranes against physical and chemical wear
show that these technologies hold great promise.377 The
electrochemical properties of O-CNTs used in next-generation
filters can be further tuned through the creation of holey O-
CNTs. Metal catalysts that remain embedded in pristine CNTs
catalyze the mineralization of sidewall carbon when heated in
air, forming holes.378 After acid oxidation is used to purify and
functionalize the holey O-CNTs, both the SSA and the
electrochemical capacitance are significantly improved com-
pared to pristine CNTs.378
In summary, a wide range of studies have sought to exploit
CNTs in water treatment applications, and CNT surface
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oxidation is one variable that has important implications for
the efficacy of CNT-enabled treatment technologies. While
CNT surface oxidation resolves some of the challenges
associated with applications of pristine CNTs (e.g., dispersi-
bility and contaminant rejection), preparation of O-CNT
membranes is complex, especially for VACNT membranes.
9. IMPACT OF SURFACE OXIDES ON OTHER CARBON
NANOMATERIALS
It is useful to evaluate the extent to which the structure−
property relationships that describe how surface oxidation
regulates the behavior of CNTs in aquatic systems can be
qualitatively extrapolated to the broader family of carbona-
ceous nanomaterials (CNMs). This class of nanomaterials
includes both intentionally engineered nanoparticles with well-
defined structures and properties (e.g., graphenes, fullerenes)
and incidental nanoparticles produced from the pyrogenic
breakdown of larger materials to form heterogeneous and
complex nanostructures (e.g., black carbon).379
Within the engineered CNMs, the allotropes that have
attracted the most research interest are CNTs, fullerenes, and
the graphene family.380−382 Fullerenes are zero-dimensional
nanomaterials composed of 20 + 2n carbon atoms arranged
across the surface of a hollow cage; of these, the spherical C60
archetype is the most widely produced and studied.383,384 C60
is stabilized through resonance structures, but its unique
electronic properties, similar to those of an electron deficient
alkene, enable covalent functionalization with oxygen moieties
at the surface while maintaining icosahedral symmetry.385,386
In water, unfunctionalized C60 molecules spontaneously
aggregate to form stable nanocrystalline assemblies 25−500
nm in diameter (n-C60).2,387 C60 is produced on the order of
tens of tons per year and has numerous biomedical, optical,
and electronic applications.388,389
Graphenes are two-dimensional CNMs composed of a single
atomic layer of sp2-hybridized carbon atoms arranged in a
hexagonal lattice and can be understood as an atomically flat
sheet that forms a SWCNT when rolled into a tube.384 The
lateral dimensions of graphenes can range from the microscale
(i.e., microsheets) to the nanoscale (e.g., nanosheets, nanorib-
bons, or graphene quantum dots).390 Graphene oxide (GO) is
the oxidized form of graphene; like O-CNTs, GO is defined by
sp3-hybridized carbon defect sites covalently linked to
hydroxyl, epoxide, carbonyl, and carboxyl functional groups.391
The oxygen content of GO is much greater than that of O-
CNTs, with C:O atomic ratios typically near 2:1.390 Reduced
GO (rGO) can be readily formed using a variety of chemical,
thermal, and photochemical reduction methods to systemati-
cally decrease the oxygen content of GO, eventually creating a
highly reduced product that resembles graphene but maintains
some structural defects and oxygen-containing functional
groups.392 The graphene family of materials have numerous
applications in polymer composites, electronics, energy
storage, catalysis, and biomedical devices.392
In contrast with CNTs, fullerenes, and graphenes, black
carbon (BC) nanoparticles are unwanted byproducts that are
generated incidentally through incomplete combustion in both
natural and engineered processes as opposed to being
intentionally manufactured.393 BC is ubiquitous in the air,
with global emissions estimated to be 1 kiloton.394 Unlike
engineered CNMs, the chemical and structural properties of
BC particles are highly variable and not well-defined; these
properties depend heavily on the source of the BC (e.g., diesel
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exhaust vs burning wood).393 The elemental carbon content of complex.80,402,403 The preparation method of n-C60 (e.g.,
BC ranges from approximately 2−90% and is most often less sonication vs stirring) affects both the ζ-potential and the
than 50%.393 Primary particle diameters vary from 15 to 600 colloidal stability of the particles while leaving van der Waals
nm, with the aggregate and agglomerate sizes ranging from forces unaffected, resulting in aggregation that increases with
tens of nanometers up to micrometers and even millimeters.393 ionic strength as predicted by DLVO theory.404 The
The surface chemistry of BC is also variable, but BC particles electrostatic repulsion between n-C60 particles is hypothesized
are known to exist with various oxygen contents and to form to be related to oxygen-containing functional groups: the
carboxylic acid and phenolic surface groups as a result of magnitude of negative ζ-potential values and the oxygen
natural oxidation processes.393,395,396 It should be noted that content measured via XPS were both observed to increase after
there remains much ambiguity regarding the nomenclature for stirring in water, suggesting that dissociated surface oxides
BC and other carbon-based particulate matter. For example, contribute to colloidal stability.404 Specifically, the formation of
the term “carbon black” is also used throughout the literature, [6,6]-closed epoxides on n-C60 surfaces has been shown to be a
but these materials differ from BC in that they are intentionally key driving force in achieving colloidally stable n-C60
manufactured, well-graphitized materials with high elemental suspensions.405 However, the highly negative ζ-potential of
carbon content. These nuances have been described in detail n-C60 at low pH values (where pH < pKa of all surface oxide
by Long et al.393 groups) suggests there are likely additional contributing
In this section, we evaluate the similarities and differences of factors.404,406 These could include the surface energy of n-
CNTs to other CNMs, focusing on the impact of surface C60 (41.7 mJ/m2, higher than many hydrophobic particles) or
oxidation on the key environmental behaviors discussed the preferential adsorption of hydroxide ions.402,404,407,408 A
throughout this review. systematic evaluation of the impact of surface oxygen on n-C60
colloidal stability has not yet been performed due to synthetic
9.1. Colloidal Properties challenges in achieving reliable control over the oxidation level
Similar to pristine CNTs,397 rGO and C60 nanomaterials are of n-C60, as the reactivity of fullerene materials often results in
difficult to disperse in aqueous solution due to strong van der rapid and complete oxidation even under mild conditions.409
Waals attractive forces and hydrophobic interactions.398−401 In contrast, quantitative relationships between surface
However, n-C60 is much more stable in aqueous media, with oxygen and colloidal stability have been established for GO
CCC values for monovalent cations 2−4 times greater than and rGO materials. Jiang et al. used thermal reduction methods
highly reduced GO and 1.5−60 times greater than pristine to prepare a suite of five rGO nanomaterials with different
CNTs (Table 3). While the colloidal stability of highly reduced surface oxygen contents; these materials were also physically
GO and pristine CNTs has been attributed to the crumpled using capillary compression to simultaneously
deprotonation of the oxygen-containing surface functional evaluate the impact of morphology and surface chemistry on
groups present in low concentrations at defect sites of these aggregation behavior.403 The carboxylic acid contents of the
materials, the origin of n-C60 electrostatic stability is more crumpled rGO (as determine by XPS analysis in conjunction
with peak fitting of the C 1s region) were highly correlated to
Table 3. Reported CCC Values for Carbon Nanomaterials CCC values (R2 = 0.89−0.95).403 This is due to the capacity of
in Monovalent and Divalent Aqueous Solutions carboxylic acid groups to deprotonate at the studied pH value
of 6.0 pH, increasing electrostatic repulsion between the rGO
carbon CCC, mM CCC, mM nanosheets and therefore resulting in higher CCC values.403
nanomaterial NaCl CaCl2 ref These mechanisms are analogous to those driving the colloidal
pristine CNTs 25 2.6 Saleh et al.397 stability of O-MWCNTs, which is also reliant on carboxylic
∼60 ∼2 Bouchard et al.148 acid content.80 O-CNTs and GO materials are both highly
2 0.1 Bai et al.94 tunable in their surface oxide content and possess well-defined
morphological structures and surface chemistries, making these
O-CNTs 93 1.2 Smith et al.58 predictive relationships relatively easy to observe in media
∼90 ∼2 Bouchard et al.148 containing simple electrolytes with no other materials (e.g.,
53-210 0.9−1 Yi and Chen112 NOM or proteins) present.
6.2−108.1 0.21−0.42 Bai et al.94 The colloidal behavior of CNTs, n-C60, and GO/rGO
materials have generally been in good agreement with
nC60 120 4.8 Chen and Elimelech151 predictions based on classical DLVO theory.58,136,151,402,403,410
85 4.1 Mchedlov-Petrossyan Unlike engineered CNMs, the colloidal behavior of BC
et al.399 particles is significantly impacted by Lewis acid−base
interactions (i.e., hydration forces), thus requiring the use of
GO 68.7 1.57 Jiang et al.403 extended DLVO (XDLVO) modeling.411−414 While pH and
44 0.9 Chowdhury et al.410 ionic strength can be altered to decrease electrostatic repulsion
∼200 ∼0.7 Chowdhury et al.400 between BC particles by decreasing the magnitude of negative
210 >0.5 Qi et al.401 surface charge, BC particles are primarily stabilized through
hydration forces that persist even in media with low pH or high
rGO ∼30−35 ∼0.7 Chowdhury et al.400 ionic strength.411 As a result, the CCC values of BC particles
41−113 ∼0.5 Qi et al.401 are much higher than other CNMs, including highly oxidized
CNTs (Table 3). The colloidal stability of BC particles has
BC >800 60 Xu et al.411 also been shown to be highly dependent on pyrolysis
250 8.5 Yi et al.419 temperature and carbon source.412,414,415 Plant-based BC
183−274 38.1−61.4 Yang et al.414 particles were shown to have higher stability than BC from
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municipal waste sources; this was attributed to greater
hydration forces imparted by a higher density of carboxyl,
phenolic, and ether surface functional groups (as detected by
FTIR).415 Specifically, the high density of hydrophilic
functional groups creates several layers of water molecules
on the BC surface through hydrogen bonding interactions,
resulting in enhanced repulsion between adjacent BC particles
due to the energy required to perturb the ordered structure of
the hydrate complexes.416 Similarly, lower pyrolysis temper-
atures result in greater concentrations of surface oxides, leading
to enhanced colloidal stability.414 Overall, the impact of surface
oxygen on BC colloidal stability is more challenging to evaluate
than other CNMs due to the non-DLVO hydration forces
involved, heterogeneous surface properties, complexity in BC
pore structure, and mixed crystalline/amorphous charac-
ter.411,417−419
9.2. Adsorption Behavior
Adsorption processes for other CNMs are by and large
regulated by the same mechanisms as CNT adsorption.
Organic contaminants are adsorbed via π−EDA interactions
between the aromatic rings of the adsorbate and the extended
sp2 π-conjugated carbon system present in CNTs, graphene-
family nanomaterials, n-C60, and BC.181,182,420−424 Increasing
the amount of surface oxygen groups for CNMs allows for
hydrogen bonding with water molecules, creating hydrophilic
regions where π−EDA interactions with adsorbates are no
longer favorable, decreasing adsorption.167,169,174 This negative
correlation between surface oxidation and adsorption of
hydrophobic contaminants has been observed for each of the
CNMs discussed in this review, but the most systematic
evaluations have been performed for CNTs and GO/rGO
materials.169,421,423,425,426 Using a suite of six GO and rGO
nanosheets with O/C atomic ratios ranging from 0.10 to 0.49
(as determined via XPS analysis), X. Wang et al. established a
strong linear correlation between the adsorption capacities of
GO/rGO for phenolic compounds and degree of reduction (as
indicated by decreasing O/C ratio) of the GO/rGO
materials.421 13C nuclear magnetic resonance (NMR) analysis
was used to show that GO reduction increased π−π
interactions between the graphene structure and organic
molecules, consistent with established adsorption mecha-
nisms.421
Larger organic materials, like proteins, interact differently
with CNMs depending on the properties of both the protein
and the CNM. Kenry et al. measured the adsorption and
conformational changes of albumin, globulin, and fibrinogen
exposed to three types of CNMs (COOH-CNTs, graphene,
and porous GO).427 Albumin, which contains hydrophobic
amino acids with aromatic functionalities, exhibited greater
adsorption to pristine graphene than for the more highly
oxidized COOH-CNTs and GO materials, with all three
CNMs offering a similar strength of adsorption. Globulin and
fibrinogen both exhibited the greatest adsorption to GO, which
contained the greatest concentration of surface oxygen.
COOH-CNTs exhibited only a slightly greater adsorption
capacity for these proteins than graphene, but both COOH-
CNTs and GO had stronger binding affinities compared to
graphene. No conformational effects were observed for
albumin and globulin, but GO was able to cause fibrinogen
denaturation through the unraveling of the α-helix. Taken
together, these results suggest that CNM morphology and
surface oxygen each play a role in dictating protein
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interactions, along with protein structure and hydrophobic-
ity.427
Other studies have also examined the importance of the
differences in the physical structures of CNMs on their
adsorption properties. For example, the mass-normalized
adsorption capacities of five different CNT and graphene
family materials for organic contaminants were strongly
correlated to the BET-derived SSA and micropore volume.428
This reliance on SSA and pore volume can be further exploited
for CNTs by substituting SWCNTs for MWCNTs428 or by
using alkali activation methods in increase porosity,429
resulting in dramatically improved performance over classical
adsorbents like activated carbon. To effectively evaluate the
impact of surface chemistry on CNM adsorbents, differences in
these physical properties must be synthetically controlled or
considered during data interpretation.
Unlike organic molecules, metal cations have stronger
interactions with the oxygen-containing functional groups of
CNTs and other CNMs than with the sp 2 carbon
system.209,211−217,430−434 Because of to their low oxygen
content (typically <3 at. %), n-C60 materials have limited
adsorption sites for metal ions, and as such have not been
evaluated as adsorbents for metal ion removal; however,
fullerenol (C60(OH)n) has been shown to bind Cu2+ ions and
increase their transport through porous media (i.e., facilitated
transport).435 Again, the most systematic studies on the impact
of surface oxides have been performed using GO/rGO
materials. Wang and Chen reduced GO materials using
different chemical and thermal methods to vary the surface
oxide content and character of the resultant rGO and used
these materials to show that the adsorption of metal cations
(here, Cd2+) is highly dependent on the presence of oxygen-
containing functional groups.433 Adsorption of Cd2+ was
greatest for unreduced GO materials (greater than all rGO
materials tested), followed by the rGO materials possessing the
highest concentration of carboxylic acid groups.433 The
attractive electrostatic interactions driving increased adsorption
of divalent metal ions onto CNMs with greater surface
oxidation (e.g., oxidized n-C60 derivatives or GO materials), as
well as the observed importance of carboxylic acid functional
groups to this process is consistent with the mechanisms
driving O-CNT adsorption.217
One important mechanistic difference in adsorption
behavior between CNTs and some other CNMs is the
contribution of structural complexity to desorption hysteresis.
The adsorption of nonpolar organic compounds to pristine and
O-CNTs is typically noncovalent and highly reversi-
ble.170,221,223,224,436−438 In addition, these compounds have
been shown to adsorb to the outer surfaces of CNT sidewalls,
as opposed to becoming trapped in the inner cavities or pore
spaces within CNT bundles.28,224,436 While the structural
similarities between graphene family materials and CNTs
result in a similar lack of hysteresis with limited influence of
surface oxygen groups,439,440 the pore structure of n-C60 and
BC aggregates can result in strong hysteresis behavior for
organic contaminants that can be impacted by surface
oxidation.224,441,442 In a study by Cheng et al., only 11% of
the total adsorbed naphthalene was shown to desorb from n-
C60 over a 60 d period in aqueous media.441 This behavior has
been attributed to the formation of closed interstitial spaces
within n-C60 aggregates due to rearrangement after initial
adsorption has occurred, resulting in entrapment of the organic
adsorbates.224,441 Similarly, desorption of organic molecules
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from the inner micropore structure of BC can be prevented
due to pore blockage by NOM or leachable pyrogenic organic
carbon that occurs after initial contaminant adsorption.443,444
While dispersion and thus aggregate pore structure are known
to be affected by surface oxygen, the functionalization or
annealing methods used to control surface chemistry can also
impact aggregate microstructures. Therefore, quantifiable
relationships between surface oxidation and adsorption−
desorption behaviors for these materials are more difficult to
identify. Overall, the strong adsorption−desorption hysteresis
observed for organic contaminants interacting with BC and n-
C60 could alter contaminant transport behavior to a greater
extent than CNTs, which has implications for exposure risk.221
9.3. Photochemical Transformations
Photochemical transformations play a major role in regulating
the surface properties of CNMs. For example, n-C60 can be
irradiated with UVC light or natural sunlight to form surface
oxidized, hydrophilic C60 derivatives with increased solubility
in water as a result of new oxygen-containing surface functional
groups (e.g., epoxide, ether, and hydroxyl).445−447 The indirect
photolysis mechanism driving these processes has been
proposed to to rely on the formation of the excited triplet
state of C60 (3C60) through photoexcitation and conversion
from the singlet state (1C60); the 3C60 then reacts with 1O2
species to form oxidized C60 species.448,449 Highly oxidized n-
C60 materials, modeled using fullerenol, are then susceptible to
degradation and partial mineralization as a result of direct
photolysis.447,450 Similarly, GO materials are also known to
partially mineralize under direct photolysis by both UVC and
solar irradiation.451,452 When exposed to sunlight, GO
undergoes a rapid (<10 h) reaction to form smaller fragments
of rGO materials, CO2, and low molecular weight photo-
products, in a process that has been hypothesized to be driven
by electron−hole pair reactions.452 Continued irradiation up to
the equivalent of two months of natural sunlight exposure
results in slower transformation and further production of both
oxidized (i.e., CO2) and reduced (i.e., rGO fragments) product
species, with the relative proportion of CO2 vs rGO fragments
depending on the presence or absence of dissolved O2 in
solution.452 In this aspect of their behavior n-C60 and GO differ
markedly from O-CNTs, which do not undergo structural
degradation due to direct photolysis, only a photodecarbox-
ylation process that reduces total surface oxidation and
colloidal stability.49
Like O-CNTs, other CNMs can form ROS when irradiated.
As discussed in section 6, surface oxidation is required for
CNTs to photogenerate ROS. Similarly, increased surface
oxidation increases the rate of ROS generation for BC, n-C60,
and GO materials, but the mechanism driving the relationship
between CNM oxidation and ROS generation differs in each
case. For O-CNTs, which are known to produce •OH, 1O2,
and O2•− under irradiation with UVA light, the dependence of
ROS generation on surface oxidation has been attributed to
defects in the extended sp2 carbon network and a resultant
lower band gap for initial photon absorption.232,233,235 While
n-C60 and its oxidized derivatives also form 1O2 and O2•−
under irradiation with UV and visible light, the increased
production for oxidized C60 derivatives (e.g., fullerenol) was
attributed to enhanced dispersion in aqueous media as
opposed to a change to the electronic properties of the
material.453−456 GO materials produce a wider variety of ROS
under solar irradiation than CNTs and n-C60 materials,
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including H2O2, •OH, 1O2, and O2•−, as well as electron−
hole pairs that can further produce ROS and interact with the
surrounding media.451,452,457−459 rGO materials also produce
•
OH, 1O2, and O2•− under solar irradiation but at much lower
concentrations than GO.459 Unlike CNTs and n-C60, the
increase in ROS production for more highly oxidized GO
materials was attributed to the electron donation potential of
surface oxygen groups.459 Additionally, the relationship
between band gap and oxidation for GO/rGO is non-
monotonic and does not independently explain the increase
in ROS production.460 The relationship between surface
oxidation and ROS generation for BC materials is less
understood. Fu et al. showed that BC materials chemically
reduced by NaBH4 had a lower quantum yield of 1O2 (3.18%
vs 4.07% for the original BC), suggesting that carbonyl-
containing chromophores play a key role, but not the only role,
in 1O2 photogeneration.461 Furthermore, the same study
showed that O2•− generation was driven by electron transfer
reactions between hydroxyl groups present in the organic
portions of BC and inorganic silica constituents.461
There are also differences between CNMs in the mechanism
and extent of production for individual ROS types, as
exemplified by examining 1O2 production. CNTs, n-C60, and
BC nanomaterials each have the same mechanism of 1O2
production, in which CNMs are photosensitized to an excited
triplet state which then transfers energy to dissolved O2 in
solution.232,453,461,462 In contrast, 1O2 production by GO
materials is believed to be caused by the interactions of
photogenerated transient electron−hole pairs produced by
irradiation with dissolved O2.452 Despite the difference in
mechanism, O-CNTs and GO materials produce similar
steady-state 1O2 concentrations, on the order of 10−14
M.232,233 This is an order of magnitude lower than the amount
of 1O2 known to be produced by the photosensitization of
NOM.459 In contrast to engineered CNMs, water-soluble BC
materials generate 1O2 from solar irradiation 2−3 times more
efficiently than well-studied NOM materials.461 The difference
in 1O2 production rates between O-CNTs and BC is likely due
to differences in factors such as carbonyl content, aromaticity,
and smaller molecular sizes, each of which has been shown to
increase the generation of triplet excited states for photo-
sensitizers.461,463,464
9.4. Toxicity
The toxic effects and negative environmental impacts of CNMs
have been shown to be affected by surface oxidation in similar
ways to CNTs, with both the mechanism and extent of toxicity
changing with oxidation. As discussed in section 7, oxidation of
CNTs can promote toxic effects that manifest through CNT
uptake and internal damage but reduce toxic effects that
manifest through mechanisms of membrane disruption or
inflammatory response. Similarly, for GO and rGO materials,
the oxygen content of the graphene structure has been shown
to alter the mechanism of action toward E. coli, with GO
toxicity caused by ROS production and rGO toxicity caused by
wrapping and isolation of bacterial cells.465 A quantitative
relationship was established showing that the concentration
required to reduce viability by 50% (EC50 value) decreases as
the oxygen content of the GO materials decrease, indicating
that the net effect of reducing GO to rGO is to increase
toxicity (eq 10).465
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μg
EC50 , = − 16.422 × (C:O at. ratio) + 217.34, (R2
L that oxidation increased the toxic response of BC, in direct
= 0.91) (10)
This shift from chemical to physical mechanisms of
microbial toxicity with decreased oxidation is consistent with
other studies of CNMs. A similar wrapping mechanism was
observed for rGO interactions with human sperm, which
decreased sperm mobility, while exposure to COOH-SWCNTs
had no effect.466 Additionally, CNTs with decreased oxidation
have been consistently shown to have stronger physical
interactions with cell membranes.325,326 Another factor in the
long term environmental impact of surface oxides on GO and
O-CNT materials is that covalent functionalization results in
defects to the sp2 structure, which serve as sites accessible to
enzymes and microbes, leading to increased biodegradation
and thus decreasing the risk of exposure to these materials,
albeit over prolonged time scales.345,467,468
Just as observed for CNTs, the impact of surface oxidation
on CNMs depends on whether studies are performed in vivo
or in vitro. For example, while n-C60 materials are generally
understood to have low to no toxicity in comparison to other
CNMs,469,470 there remains some evidence that oxidative
damage can be imparted by n-C60 and that this toxicity can be
affected by functionalization with surface oxides.471 Sayes et al.
reported that exposure to pristine n-C60 resulted in greater
membrane damage and cell death than exposure to three
different oxidized C60 derivatives; this difference was attributed
to decreased ROS production by oxidized C60 derivatives (in
the absence of irradiation with light).472 However, when this
comparison was made in a whole organism study as opposed to
cell lines, there were no observable differences between
oxidized and pristine n-C60.473 Similar to studies of CNT
toxicity, the challenge of extrapolating the mechanistic
understanding derived from well-controlled systems to more
complex studies (e.g., uptake and toxicity in whole organisms)
results in some ambiguity on the effects of surface oxidation.
While CNT toxicity has been examined under a variety of
exposure pathways, the toxicity of BC particles has primarily
been studied in the context of global ambient air pollution,
leading to some differences in the observed effects of surface
oxidation. Along with other constituents present in fine
particulate matter (PM2.5), human exposure to BC and other
PM2.5 through inhalation is known to cause negative
cardiovascular and respiratory health outcomes as well as
premature mortality.394 Overall, BC oxidation through ozone
exposure has been shown to increase toxicity through damage
to both in vitro lung cell models and in vivo lung health.474−476
This behavior has been connected to the ROS production
activity of pristine vs oxidized BC through the measurement of
the overall oxidation potential (i.e., the total contribution of all
ROS produced) via the dithiotreitol (DTT) assay.474,477,478 In
addition to ROS, genetic effects have also been observed. Kong
et al. showed that ozone-induced oxidation of BC altered the
genetic pathways regulating the toxic response of A549
epithelial cells to BC, although the observed toxic end points
and inflammatory responses were similar between pristine and
oxidized BC.479 However, damage from oxidized BC may be
easier to repair; An et al. found that while both pristine and
oxidized BC particles induced oxidative DNA damage and cell
apoptosis in A549 cells, the oxidized BC induced more
extensive DNA damage repair response through the up-
regulation of genes promoting cell cycle arrest, resulting in less
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DNA damage overall.480 While the majority of studies found
contrast to CNTs, BC literature is currently limited to two-
point comparisons of oxidized vs pristine BC as opposed to
systematic variation of surface oxidation and focuses on
relatively few exposure pathways and mechanisms of toxicity.
In summary, the determination of CNM structure−property
relationships requires that both the CNM and the system of
interest are well-characterized. Additionally, quantitative
predictive relationships are best developed through the
systematic modification of the quantity and identity of
oxygen-containing surface functional groups.
10. SUMMARY AND FUTURE OUTLOOK
Oxygen-containing functional groups (surface oxides) can be
introduced into the graphenic sidewalls of CNTs through a
variety of different processes, some deliberate (e.g., acid
treatment) and some unintentional (e.g., photolysis). To
determine the impact of CNT surface oxidation on the
environmental behavior and toxicity of CNTs, it is necessary to
control and quantify the concentration and type of oxygen-
containing functional groups on O-CNTs. Controlled
oxidation is best accomplished using different wet chemical
oxidants in combination with annealing methods to selectively
produce and remove specific surface oxide types, respectively.
After functionalization, XPS is perhaps the most widely used
technique to quantify the extent of oxidation, although more
detailed information on the proportional contribution of each
type of functional group (e.g., carboxylic acid vs hydroxyl) can
be obtained using techniques such as chemical derivatization in
conjunction with XPS analysis. Importantly, techniques for
characterizing the spatial distribution of CNT surface oxides
currently fall far behind techniques developed for surface oxide
identification and quantification. Improvements in spatial
distrubution methods require advances in chemical imaging
techniques and would provide information useful not only for
understanding the impact of the spatial distribution of oxygen-
containing moieties on environmentally relevant behaviors but
in enabling control of covalent modification strategies that rely
on surface oxides as attachment points for further modification.
After release into natural waters and engineered water
treatment systems, surface oxidation can affect CNT colloidal
stability. In systems containing monovalent electrolytes, there
exist quantitative relationships that enable prediction of CNT
colloidal stability when the properties of the CNT surface (i.e.,
concentration of total oxygen and concentration of carboxylic
acid functional groups) and aquatic media (i.e., pH and ionic
strength) are known. Here, increased CNT surface oxidation
results in enhanced colloidal stability, and this behavior is
primarily driven by carboxylic acid groups as opposed to other
functionalities. In media containing destabilizing Ca2+ ions,
NOM, or natural colloids, the influence of surface oxides is
diminished and the relationships between CNT surface
oxidation and colloidal stability are not as apparent. The
impact of surface oxidation on CNT aggregation behavior in
the presence of materials like extracellular polymeric
substances or algal colloids has not yet been systematically
explored, and these studies could provide key insights into the
uptake, toxicity, and trophic transfer of CNTs.
Surface oxidation can also affect the adsorption of materials
to CNT surfaces, which may be an incidental (e.g., adsorption
of NOM in natural waters) or intentionally engineered (e.g.,
adsorption of heavy metal ions in water treatment) behavior.
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Chemical Reviews
For nonpolar organic molecules, increasing CNT surface
oxidation results in a systematic decrease in adsorption
capacity; this is also observed for polar organic molecules
and NOM, although the effect is lessened as the polarity of the
adsorbate molecule increases. In contrast, the adsorption of
metal cations is systematically increased with increasing CNT
surface oxidation due to preferential interactions with
negatively charged surface oxides, principally deprotonated
carboxylic acid groups; conversely, CNT surface oxidation
decreases adsorption of metal oxyanions due to electrostatic
repulsion. Less is known regarding the impact of CNT surface
oxidation on competitive adsorption of multiple contaminant
types, information which is particularly important in complex
environmental matrices and for water treatment applications.
Although CNT surface oxidation is known to increase
desorption hysteresis through the irreversible formation of
covalent bonds with amino-substituted organic contaminants
or surface complexes with metal cations, the overall impact of
this hysteresis behavior on facilitated transport and Trojan
horse mechanisms of toxicity is less understood.
O-CNTs can undergo several concurrent photochemical
processes under irradiation. Photodecarboxylation can occur as
a result of UV irradiation which causes O-CNTs to become
colloidally unstable. While pristine CNTs do not generate ROS
under irradiation, O-CNTs generate a variety of ROS in
natural sunlight, including •OH, 1O2, and O2•−. To date, there
have been no systematic studies on ROS production via the
irradiation of O-CNTs with varied total surface oxygen
concentrations or different proportions of individual oxygen-
containing functionalities. Information from these studies
would provide valuable insights into the mechanisms of ROS
production. There is also a need to elucidate the potential for
electron−hole pair formation by O-CNT irradiation, and the
role these species play in CNT phototransformations.
Compared to other environmental behavior, the impact of
CNT surface oxidation on toxicity to cells and organisms is
more variable and ambiguous. This is in part because different
mechanisms of toxicity are modulated by the presence of
oxygen-containing functional groups in distinct ways. Specif-
ically, while CNT oxidation generally increases uptake through
improved dispersibility thereby increasing damage to internal
cellular components, the hydrophilicity imparted by surface
oxides decreases interactions with cellular membranes,
reducing membrane damage and related oxidative stress
responses. In contrast to other properties (e.g., adsorption),
studies of toxicity require the most rigor to evaluate the effects
of CNT surface oxidation, and they are the most prone to
experimental artifacts and misinterpretation. These studies not
only require systematic control over the type and concen-
tration of CNT surface oxygen group but are also particularly
affected by other variables such as metal catalyst content or
oxidation-induced CNT shortening. Overall, many toxicology
studies lack the rigorous CNT characterization necessary to
draw broad conclusions about potential unifying mechanisms
for the impact of surface oxides on CNT toxicity across
different organisms and media types, a weakness which should
be remedied in future studies.
CNT surface oxidation also has important implications for
the efficacy of CNT-enabled treatment technologies. Surface
oxidation increases the colloidal stability of CNTs in the
solvents and polymers required for filter manufacturing,
therefore increasing the ease with which CNT water treatment
filters can be manufactured. The oxygen-containing moieties
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on the surface of CNTs play a crucial role in the separation
performance and pure water flux of nanocomposite mem-
branes. Next-generation membrane capabilities, including
biofouling resistance and electrochemical performance, can
be imparted by tuning the concentration and type of CNT
surface oxides in addition to the total O-CNT loading. Because
of the established cytotoxicity of CNTs, leakage risk must also
be assessed prior to implementation in real water treatment
devices. While O-CNTs resolve challenges (e.g., dispersibility
and contaminant rejection) inherent in using pristine CNTs,
difficulties persist in manufacturing O-CNT membranes cost
effectively and uniformly on a commercial scale.
Quantitative relationships between surface oxidation and
behavior have also been established for other carbon
nanomaterials, with graphene family (GO and rGO) materials
behaving most similarly to CNTs due to their structural
similarities. The impact of oxidation on the behavior of
fullerene materials is more challenging to explore, as synthetic
yields are currently low and the range of possible surface
oxygen concentrations is narrow. There are also complications
in developing reliable structure−property relationships for
naturally occurring BC materials, due to their heterogeneous
surface chemistries and pore structures. Despite these
challenges, many of the experimental strategies developed to
control, quantify, and evaluate the impact of surface oxidation
for CNTs are also effective in studies of other CNMs. These
strategies may also prove valuable in the study of other
important environmental compartments, including the soil−
water−root interface and the troposphere.
In summary, it is apparent that the introduction of oxygen-
containing functional groups onto CNT surfaces often results
in profound changes to the properties of CNTs. To develop a
conclusive in-depth understanding of these effects, the optimal
and most convincing experimental approach is to create a suite
of oxidized CNTs where both the overall extent of oxidation
and the type of oxygen-containing functional groups have been
controlled and quantified. Results from such a systematic,
reductionist approach can not only clearly identify important
qualitative trends in behavior but have also been shown to be
capable of uncovering detailed structure−activity relationships.
This type of information can form the basis to develop
predictive capabilities that can inform not only risk assessment,
but also help guide the development of CNTs for commercial
and environmental applications.
AUTHOR INFORMATION
Corresponding Author
D. Howard Fairbrother − Department of Chemistry, Johns
Hopkins University, Baltimore, Maryland 21218, United
States; orcid.org/0000-0003-4405-9728;
Email: howardf@jhu.edu
Authors
Alyssa R. Deline − Department of Chemistry, Johns Hopkins
University, Baltimore, Maryland 21218, United States;
orcid.org/0000-0002-7309-3979
Benjamin P. Frank − Department of Chemistry, Johns Hopkins
University, Baltimore, Maryland 21218, United States;
orcid.org/0000-0001-9727-3774
Casey L. Smith − Department of Chemistry, Johns Hopkins
University, Baltimore, Maryland 21218, United States;
orcid.org/0000-0001-6177-223X
https://dx.doi.org/10.1021/acs.chemrev.0c00351
Chem. Rev. 2020, 120, 11651−11697
Chemical Reviews
Leslie R. Sigmon − Department of Chemistry, Johns Hopkins
University, Baltimore, Maryland 21218, United States;
orcid.org/0000-0001-6591-6237
Alexa N. Wallace − Department of Chemistry, Johns Hopkins
University, Baltimore, Maryland 21218, United States
Miranda J. Gallagher − Department of Chemistry, Rice
University, Houston, Texas 77005, United States; orcid.org/
0000-0003-1139-1257
David G. Goodwin, Jr. − Department of Chemistry, Johns
Hopkins University, Baltimore, Maryland 21218, United
States; orcid.org/0000-0002-5979-3581
David P. Durkin − Department of Chemistry, United States
Naval Academy, Annapolis, Maryland 21402, United States;
orcid.org/0000-0001-5979-8449
Complete contact information is available at:
https://pubs.acs.org/10.1021/acs.chemrev.0c00351
Notes
The authors declare no competing financial interest.
Biographies
Alyssa R. Deline earned her Ph.D. in Environmental Engineering from
Oregon State University in 2018 under the guidance of Jeffrey Nason.
During this time, she was awarded a National Science Foundation
Graduate Research Fellowship and conducted research on the labeling
and detection of metal oxide nanomaterials. She is currently a
postdoctoral fellow in Howard Fairbrother’s research group at Johns
Hopkins University, where she studies the environmental photo-
chemistry of carbon nanomaterials and the use of nanobiopolymers in
agriculture. In 2020, Dr. Deline will join the Department of Chemical
Sciences at Bridgewater State University as an Assistant Professor.
Her research interests are centered in the application of nanoenabled
technologies toward global sustainable development.
Benjamin P. Frank earned his B.S. degree in Chemistry from the
University of Pittsburgh, where he conducted research on piezo-
electric self-assembling monolayers in Geoffrey Hutchison’s research
group. In 2014, Benjamin began his Ph.D. research in the Fairbrother
research group at Johns Hopkins University. His research focuses on
understanding the environmental transformations of nanocellulose
and carbon dot materials.
Casey L. Smith completed her undergraduate studies at Virginia Tech
where she earned B.S. degrees in Chemistry and Biochemistry and
conducted research on gas phase reaction mechanisms of chemical
warfare agents and metal organic frameworks with John Morris. In
2018, Casey started her Ph.D. studies in Chemistry at Johns Hopkins
University under the guidance of Howard Fairbrother. Her Ph.D.
research focuses on the release and transformation of additives from
polymers exposed to accelerated weathering conditions.
Leslie R. Sigmon received her B.S. degree in Chemistry and Biology
from the University of North Carolina at Asheville, where she
performed research with Dr. Oksana Love. She is currently a Ph.D.
student in the Fairbrother research group at Johns Hopkins University
and a recipient of the National Science Foundation Graduate
Research Fellowship. Her research interests focus on environmentally
sustainable nanotechnology, including carbon dots and nanoenabled
agricultural fertilizers.
Alexa N. Wallace completed her undergraduate studies at Temple
University, where she earned a B.S. degree in Chemistry and
conducted research on the hole transport layer of solar cells with
Graham Dobereiner. In 2017, Alexa started her Ph.D. studies in
Chemistry at Johns Hopkins University under the guidance of
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Howard Fairbrother. Her Ph.D. research focuses on oxidized black
carbon in the atmosphere.
Miranda J. Gallagher earned a B.S. in Chemistry and a B.A. in French
from Hartwick College in 2009. She subsequently taught English at La
Faculté de Science, Université de Nice. She received her Ph.D. from
the Department of Chemistry at the Johns Hopkins University with
Professor D. Howard Fairbrother in 2018. During her graduate
studies, Miranda developed methods for the detection of the
environmental transformations of the surfaces of composite nanoma-
terials. She then joined the laboratory of Professor Christy F. Landes
at Rice University as a Postdoctoral Research Associate, where her
research detects surface transformations of plasmonic nanomaterials
with spectroscopy.
David G. Goodwin, Jr., graduated with a B.S. in Chemistry from
Lafayette College in 2010 and received his Ph.D. in Chemistry from
the Johns Hopkins University in 2016. David’s Ph.D. work focused on
microbial interactions with carbon nanotube/polymer nanocompo-
sites and quantification of surface oxygen functional groups on
carbonaceous nanomaterials. Since 2016, David completed his
National Research Council (NRC) Postdoctoral Associateship at
the National Institute of Standards and Technology (NIST) and
continues to work at NIST as a research chemist. At NIST, David
conducts photodegradation studies on various types of polymer
nanocomposites using the state-of-the-art NIST SPHERE and
evaluates the durability and performance of fiber reinforced polymer
(FRP) composite retrofits used for strengthening, repair, and seismic
retrofit of civil infrastructure.
David P. Durkin is a career Naval Officer serving as a Permanent
Military Professor at the United States Naval Academy. Born in
Scranton, PA, he spent his operational career as a military helicopter
pilot. In 2018, he earned a Ph.D. in Chemistry from Johns Hopkins
University in Baltimore, MD. His research focuses on developing
advanced biocomposite systems using novel ionic liquids, biopol-
ymers, and nanomaterials, and studying the impact ionic liquids have
on biopolymer structure after partial dissolution. He is also actively
involved in evaluating the fundamental structure−property relation-
ships of binary ionic liquid systems, the chemistry of surrogate
military jet fuels, and chemical modifications for additive manufactur-
ing of functional composites.
D. Howard Fairbrother received his B.A. from Oxford University,
England, in 1989 and a Ph.D. in Chemistry from Northwestern
University in 1994. Following a postdoctoral position at the
University of California, Berkeley, he joined the Chemistry Depart-
ment at Johns Hopkins University in Baltimore in 1997. His research
interests in environmental science are focused on understanding the
properties of carbon-based materials. Dr. Fairbrother received a NSF
CAREER award from the National Science Foundation in 2000. He
served as the Secretary and Chair of the Colloids and Surface Science
Division of the ACS and was elected as an ACS Fellow in 2011. He is
currently a senior editor of the ACS Journal of Physical Chemistry.
ACKNOWLEDGMENTS
We gratefully acknowledge the financial support that led to
much of the work described in this review, including the
National Science Foundation (grant nos. BES0731147 and
CBET 1236493), the Environmental Protection Agency (grant
no. RD-83385701-0), and the Institute for Nanobiotechnology
(INBT) at Johns Hopkins University. L.R.S. is supported by
the National Science Foundation Graduate Research Fellow-
ship Program under grant no. DGE-1746891. We would also
https://dx.doi.org/10.1021/acs.chemrev.0c00351
Chem. Rev. 2020, 120, 11651−11697
Chemical Reviews pubs.acs.org/CR Review

like to thank Ronald S. Lankone for his insightful suggestions TEM = transmission electron microscopy
throughout the preparation of this manuscript. TGA = thermogravimetric analysis
TOC = total organic carbon
ABBREVIATIONS TPD = temperature programmed desorption
BC = black carbon TR-DLS = time-resolved dynamic light scattering
BEGM = bronchial epithelial growth medium UV = ultraviolet
BSA = bovine serum albumin UV−vis = ultraviolet−visible
BTEX = benzene, toluene, ethylbenzene, and p-xylene VACNT = vertically aligned carbon nanotube
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