Science of the Total Environment 668 (2019) 566–576

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Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Review

Antibacterial activity of chitosan nano-composites and carbon

nanotubes: A review
Assaad Kassem, George M. Ayoub, Lilian Malaeb ⁎
Civil and Environmental Engineering Department, American University of Beirut, P.O. Box 11-0236, Beirut, Lebanon

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Chitosan and carbon nanotubes are ef-

fective bacterial disinfectors with no
byproducts.
• Nanotechnologies based on these mate-
rials have proved to be promising.
• Mechanisms of disinfection and the
methods of preparation still hold com-
plexities.
• The lack of a disinfection residue is a
common disadvantage of many
nanomaterials.
• Studies on economic feasibility and sus-
tainability are yet needed.

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

Article history: Bacteriological contamination of water sources is a major challenge that has a detrimental impact on both the en-
Received 3 January 2019 vironment and human health. This imposes the search for the most efficient disinfectant. Despite their antibac-
Received in revised form 27 February 2019 terial efficiency, traditional methods can often form disinfection byproducts through their reaction with
Accepted 27 February 2019
organic and inorganic compounds. Substitutes for conventional bacterial inactivation methods should not pro-
Available online 01 March 2019
duce harmful byproducts and must also be cost effective. Nanotechnology is an attractive option that is suited
Editor: Kevin V. Thomas for surface reactions as nanostructures offer large surface to volume ratios. Technologies using chitosan-
modified nanocomposites and carbon nanotubes have proven to offer promising alternatives for bacterial inacti-
Keywords: vation. To enhance their antibacterial efficiency, such technologies have been modified chemically and physically
Carbon nanotubes (CNTs) and have as well been associated with other treatment techniques. However, despite their high bacterial disin-
Chitosan fection efficacy and lack of treatment byproducts, the vagueness in bacterial inactivation mechanisms and com-
Microorganisms plexity in materials preparation have often obscured their wide scale application. The aim of this manuscript is to
Nanoparticles review the recent advances in bacterial disinfection using nanomaterials, in the form of chitosan and carbon
nanotubes. The rapid rate of research and the notable progress in this area dictate the frequent compilation
and dissemination of recent introductions to this field. Existing gaps in the literature are thus also highlighted
and reported discrepancies are pinpointed so that roadmaps for future studies may be figured.
© 2019 Elsevier B.V. All rights reserved.

⁎ Corresponding author.
E-mail address: lm75@aub.edu.lb (L. Malaeb).

https://doi.org/10.1016/j.scitotenv.2019.02.446
0048-9697/© 2019 Elsevier B.V. All rights reserved.
 A. Kassem et al. / Science of the Total Environment 668 (2019) 566–576 567

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 567
2. Chitosan antibacterial activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 567
2.1. Experimental considerations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 569
2.2. Applications and implications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 569
2.3. Mechanisms of removal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 570
3. Carbon nanotubes antibacterial activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 571
3.1. Experimental considerations and mechanisms of disinfection of CNTs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 571
4. Conclusions and recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 574
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 574

1. Introduction
Improper exploitation of natural water resources worldwide has
exerted pressure on the quantity and quality of water supplies (Van
Vliet et al., 2017). Water scarcity is attributed mainly to the rapid increase
in global population, over exploitation and uneven geographic distribu-
tion of water resources around the world (Sadoff, 2017). Increase in global
water demand has resulted in stressed resources, a situation that promul-
gated the need for technological advances directed at improving water
quality and quantity (European Environment Agency, 2017). Solutions
to the problem of quantity are often advanced through the introduction
of more efficient water management policies, resorting to the application
of cost-effective desalination technologies and/or the adoption of water
recycling strategies to supplement raw water sources. Qualitatively, the
introduction of more efficient treatment processes has contributed to
the amelioration of the quality of water; however, pollution of water re-
sources due to uncontrolled discharges of wastewater from varied sources
remains to be a major contributor to the deterioration of water quality.
One major component of pollution is that of a microbiological nature
(Wright et al., 2004). Bacteriological contamination of water sources is a
major parameter to address as it has a detrimental impact on both the en-
vironment and human health; especially when many water bodies have
been characterized by the presence of high bacterial counts (Schaffter
and Parriaux, 2002). Microbial accumulation in water bodies leads to an
increase in waterborne diseases as well as to inducing a toxic environ-
ment to many aquatic species when present in amounts that exceed set
acceptable levels (Peters et al., 2012). Furthermore, bacterial presence po-
tentially lead to operational problems in water treatment processes such
as membrane fouling and the production of toxic byproducts, which re-
sult in increased system operational costs (Chellam and Cogan, 2011;
W. Li et al., 2013; X. Li et al., 2013). Consequently, disinfection of water
prior to any usage is deemed to be mandatory. This in turn imposes the
selection of the most efficient disinfectant needed to achieve the set ob-
jective. The renowned conventional chemical disinfectants of bacteria
are chlorine, chloramines, ozone, chlorine dioxide, and Ultraviolet (UV) ir-
radiation (Savage and Diallo, 2005). Ozonation and chlorination are well
recognized for their powerful sterilization and residual impact on a
wide range of waterborne pathogens (bacteria and viruses) (Crittenden
et al., 2012; Lee et al., 2018). Despite their antibacterial efficiency, these
traditional methods can often form disinfection byproducts through
their reaction with organic and inorganic compounds in water
(Richardson, 2003). Most of the byproducts released are labeled as endo-
crine disruptors, carcinogens, mutagens and teratogens, thus threatening
human and environmental health (Richardson et al., 2007; Li et al., 2008a,
2008b; Pereira et al., 2011). UV radiation is known to have a powerful
disinfecting impact and does not impart toxic byproducts, yet its main dis-
advantage is the high cost involved as well as the inability to maintain a
residual, which is considered an important part of the overall disinfection
process. The shortcomings associated with conventional disinfectants
hence constantly favor the search for novel ones that will alleviate the
aforementioned disadvantages.
Substitutes for conventional bacterial inactivation methods, in addi-
tion to the requirement of strong disinfection capabilities, should not
produce harmful byproducts and must also be cost effective. Nanotech-
nology is an attractive entrant to replace traditional disinfection
methods since in most applications no harmful byproducts are pro-
duced. Moreover, it is well suited for surface reactions as nanostructures
offer large surface to volume ratios (Hornyak et al., 2008).
Nanomaterials using various types of materials and composites have
proven their antibacterial efficiency when applied to different types of
bacteria (Ahmed et al., 2016; Bijelic et al., 2018; Hossain et al., 2018;
Seo et al., 2018; Anand et al., 2019).
Technologies using chitosan-modified nano-composites and carbon
nanotubes, solely or combined, have proven to offer promising alterna-
tives for bacterial inactivation. Their highly desired physiochemical
characteristics have indicated that bacterial inactivation, which leads
to complete removal, achieved in most cases simply by physical contact
for a short duration with a reasonable amount of nano-composite mate-
rial (Shang et al., 2013; Pramanik et al., 2017). To enhance their antibac-
terial efficiency, chitosan and carbon nanotubes have been modified
chemically and physically and have as well been associated with other
treatment techniques (Qu et al., 2015; Dos Santos et al., 2012; Garcia
Peña et al., 2017; Smith and Rodrigues, 2015; Dong and Yang, 2015).
Despite their high bacterial disinfection efficacy and lack of treatment
byproducts, the vagueness in bacterial inactivation mechanisms and
the complexity in materials preparation have obscured their desirable
application and kept them at the laboratory level (Divya and Jisha,
2018; Sarkar et al., 2018). The aim of this manuscript is to review the re-
cent advances in bacterial disinfection using nanomaterials, in the form
of chitosan and carbon nanotubes. Although reviews on these topics
were presented earlier by Li et al. (2008a, 2008b) and Hossain et al.
(2014), the rapid rate of research and the notable progress in water
and wastewater treatment using nanotechnologies dictate the frequent
compilation and dissemination of recent introductions to this field and
the identification of existing gaps in the literature that would help
guide and set needed roadmaps for future studies.
2. Chitosan antibacterial activity
Conventional disinfection processes have recognized drawbacks
displayed by the byproducts generated from their use, whereas a simple
virtue of chitosan based products is that their backbone is biodegrad-
able. This results in reduced secondary pollution as well as alleviated
costs of supplementary processing (Yang et al., 2014). Chitosan is a de-
gradable biopolymer that is derived from the deacetylation of chitin
present in the shells of crustaceans, the cuticles of insects, and the cell
walls of most fungal biomass (Hossain et al., 2014; Desbrières and
Guibal, 2017). It is composed of glucosamine and acetyl-glucosamine
monomers associated via (1 → 4) (Desbrières and Guibal, 2017). Chito-
san is known for its disinfection capabilities that override other disinfec-
tants due to its effective and broad spectrum of antimicrobial activities
and low toxicity for animals and human beings (Kang et al., 2008a,
2008b). In water treatment, the antimicrobial properties of chitosan
vary with the physical and chemical environment of the treatment pro-
cess. Its disinfection efficacy generally depends on the availability of
charged amino groups, molecular weight, chitosan dose, type of
 568
Table 1
Published work on Chitosan (2013–2018).

Ref. Modified chitosan Type of water PH Temperature Chitosan dose Retention time Targeted Method of Disinfection efficiency
microorganism/s treatment

Capelete and Chitosan Eutrophic water 7 ≥2 mg /L Microcystis Coagulation 95–100%

Brandão aeruginosa
(2013)
Yang et al. Quaternary ammonium salt grafted chitosan Synthetic wastewater 6–9 20 ± 1 °C. 150 mg/L E. coli Flocculation 95%
(2014) (carboxymethyl chitosan- graft-poly[(2-
-methacryloyloxyethyl) trimethylammonium
chloride]
Motshekga Chitosan cross-linked with glutaraldehyde and Ag, Bacteria contaminated 6.3 36 ± 1 °C 0.3, 0.4, and Dependent on bacterial E. coli Shaking Reaches 100% but and depends on
et al. (2015) ZnO, and Ag-Zn0 chitosan bentonite nanocomposites water 0.5 g concentration and E. faecalis bacterial initial concentration and

A. Kassem et al. / Science of the Total Environment 668 (2019) 566–576

Chitosan composite chitosan composite
Cadogan et al. Chitosan glycerol Municipal wastewater 7.9 25 °C E. coli Microfiltration N 95%
(2015)
Mukherjee et al. Mixed matrix membrane consisting of Fe3O4 and PAN Surface water 7.4 120 min E. coli Membrane 99.90%
(2016) coated with chitosan filtration
Masheane et al. Chitosan-alumina/functionalized-multiwalled carbon Water 6–9 37 °C 2 mL/mL 24 h E. coli Batch 100%
(2016) nanotube nanocomposites Klebsiella
pneumoniae
Klebsiella
oxytoca
Pseudomonas
aeruginosa
Proteus mirabilis
Shigella sonnei
Shigella boydii
Enterococcus
faecalis
Bacillus cereus
Enterobacter
cloacae
Ma et al. (2016) Dual and composite coagulant of chitosan-aluminum Drinking water 8.4 18.5 °C 2.6 mg/L 53 min M. aeruginosa Coagulation 97.8% of intact cells 53.08% of
chloride chitosan and extracellular microcystins 100%
7.5 mg/L Al-Cl extracellular organic matter
Unuabonah Chitosan modified hybrid clay composite Contaminated water 6.1 Room temp. 3 mg/mL 120 min Vibrio cholerae Batch 4.07 × 106 cfu/mL
et al. (2017) 180 min Escherichia coli adsorption 1.95 × 106 cfu/mL
270 min Salmonella technique 3.25 × 106 cfu/mL
Motshekga and Chitosan-Bentonite composites Bacterial contaminated b6 27 h E. coli Fixed bed 1 × 104 cfu/mL
Ray (2017) drinking water and column
river water
Garcia Peña Chitosan-silver nanoparticles-cork granules Bacterial contaminated Room temp. 8h E. coli Filtration 100%
et al. (2017) water
Rasool et al. ZnO-interlinked chitosan nanoparticles Seawater Room temp. 250 168 h Sulfate reducing Batch reaction
(2018) microg/mL bacteria
Garrido-Maestu Low molecular weight chitosan Liquid media 7 37 °C 0.1–0.2% 6h E. coli Incubation 100%
et al. (2018) High molecular weight chitosan containing chitosan,
bacteria broth, and
bacteria
 A. Kassem et al. / Science of the Total Environment 668 (2019) 566–576
targeted bacteria, pH, pka, ionic strength, surface area, disinfection time,
chelating capacity, and presence of organic matter (Kong et al., 2010).
Several recent studies have been reported on testing the efficacy of chi-
tosan for bacterial disinfection. Table 1 summarizes the most recent
published work on this topic and the associated experimental setups.
As can be noted from the conditions and results of these studies, high re-
moval efficiencies have been reported for chitosan based products over
a varying range of experimental conditions including temperature, pH,
retention time, type of water used in addition to the targeted microor-
ganisms. The applications also vary over a wide selection of water treat-
ment processes.
2.1. Experimental considerations
Chitosan has proven its flexibility when functionalized with certain
composites or materials. Taking into consideration parameters such as
surface area, pH, and particle size it is possible to target several types
of bacteria, though at different efficiencies, regardless of their charge
(gram negative or positive) and structure (Yang et al., 2014; Ma et al.,
2016, and Garcia Peña et al., 2017). Some studies were conducted to op-
timize the process for complete inactivation of Escherichia coli and En-
terococcus faecalis in terms of the nano-composite quantity used and
contact time (Dos Santos et al., 2012). Silver and zinc oxide containing
bentonite chitosan composites were prepared and results showed that
contact time and bacterial inactivation are directly proportional
(Motshekga et al., 2015). Previous studies reported that silver and
zinc-oxide bentonites when used alone had removal efficiencies of
51%, whereas when these composites were introduced with chitosan
the removal efficiency increased to at least 78% and also produced a sta-
ble leachate making it suitable for large scale water disinfection pro-
cesses (Kong et al., 2010; Regiel et al., 2012). Results also
demonstrated that 6.3 is the optimal working pH at which chitosan's
positively charged groups easily interact and form a bridge with the
negatively charged bacterial surface causing lysis and eventually leak-
age of intracellular material leading to death. In addition to pH, particle
size and surface area played a major role in optimizing the bacterial in-
activation process (Zheng and Zhu, 2003; Chang and Juang, 2004; Li
et al., 2008a, 2008b; Raafat and Sahl, 2009; Kittinaovarat et al., 2010;
Guibal et al., 2013; Takahashi et al., 2008).
Due to the structural difference between E. coli and E. faecalis, the ben-
tonite chitosan had higher inactivation efficiency against E. coli. Because of
its gram-negative nature, Escherichia coli is characterized by not having an
outer cell membrane thus resulting in a quicker and easier cell penetra-
tion compared to the gram-positive E. faecalis (Kim et al., 2007). However,
even with the post-experimental analysis, it remains unknown in this
study if the nano-composites acted as an adsorbent, a disinfectant or
both, thus suggesting that further investigation is needed to understand
the actual comportment of the cross-linked nano-composites.
Garrido-Maestu et al. (2018) conducted a study in which two chito-
san cross-linking agents namely sodium sulfate versus tripolyphosphate
were compared when tested under various conditions that could possi-
bly affect removal efficiency (molecular weight of chitosan, sonication
treatment, time and power). The objective was to optimize the antimi-
crobial activity of the matrix (2018). Experiments were conducted on
E. coli and the resulting analyses indicated that the protein and
liposaccharides existing in its outer membrane were damaged. Similar
rational was reported by earlier studies (Helander et al., 2001; Jeon
et al., 2014; Liu et al., 2004).
Chitosan is also known for its thermal instability and high solubility,
however the addition of supplementary nano-composites has proven to
enhance thermal stability and reduce its solubility (El-Sawy et al., 2010;
Sagheer et al., 2009). Masheane et al. (2016) conducted a study that
aimed at overcoming the apparent disadvantages of chitosan. In this
study an enhanced nano-composite was prepared by adding alumina
functionalized with multi-walled carbon nanotube to chitosan, which
resulted in largely improving its prospective for use as a biocide.
569
Alumina played a role in enhancing thermal stability, solubility and ad-
sorption due to its large surface area (W. Li et al., 2013; X. Li et al., 2013).
Experimental results showed complete bacterial removal, which may be
attributed to that the positively charged nanocomposites active sites
interacted with the negatively charged bacterial cell walls of the twelve
bacterial strains examined in the study (Masheane et al., 2016).
2.2. Applications and implications
A non-nugatory characteristic of chitosan is its versatility in the
scheme in which it can be used, whereby it may be applied as a filter, co-
agulant and an adsorbent (Roussy et al., 2005). A study conducted by
Capelete and Brandão (2013) to assess the use of chitosan as a disinfec-
tant through coagulation in the presence of chlorine on lake water that
contains M. aeruginosa cells, has shown that chitosan did not contribute
to the formation of trihalomethanes even after the oxidative processes
that took place between the cells and chlorine. This ensued despite
the fact that chitosan is of an organic origin and is expected to contrib-
ute to the formation of trihalomethanes (Rizzo et al., 2008; Vasyukova
et al., 2010). In addition, Chitosan showed to be more effective as a co-
agulant than aluminum sulfate (Capelete and Brandão, 2013).
Chitosan has also been tested for its filtering efficiency. A study was
conducted by Cadogan et al. (2015) utilizing synthesized chitosan glyc-
erol membrane for microfiltration of bacteria from municipal wastewater.
Glycerol was used as a porosifier which supplied the membrane with
greater elongation and tensile strength. As a result, N95% E. coli disinfec-
tion was achieved. As for the fouling phenomenon, hydraulic experimen-
tal studies demonstrated that it is best illustrated by the cake formation
model at which membranes pore size b1 μm formed a physical barrier
and assisted in rejecting bacterial species with a removal efficiency of
95% (Rana and Matsuura, 2010; Abbasi et al., 2010). Another study on
membrane filtration application of chitosan was reported by Mukherjee
et al., 2016 in which chitosan was coated with iron oxide polyacrylonitrile
(PAN) to produce a mixed matrix membrane (MMM), though the high-
light of this membrane type is that it is designed to act as an anti-fouler.
The study indicated the operating conditions that played a role in achiev-
ing high removal efficiencies (99.9%) to be MMM stability, cross flow rate,
and transmembrane pressure. Also high removal efficiency could be at-
tributed to the addition of iron oxide, which instigated a positive charge
on the membrane surface exhibiting an adsorptive interaction with the
bacteria thus resulting in cellular damage leading to 99.9% removal
(Prucek et al., 2011; Mukherjee and De, 2015).
Chitosan can also be used as a flocculent exhibiting bactericidal ac-
tion by damaging bacterial cell membrane (Renault et al., 2009). A
study by Yang et al. (2014) performed on a chitosan-based flocculent
(Quaternary ammonium salt grafted chitosan) revealed an advantage
over other chitosan-based flocculants by exhibiting a wider pH range
of solubility (1–13) and more efficient bactericidal effects due to the
larger flocculation sites available. Upon the application of an optimal
flocculent dosage, the flocculation process undergoes various reactions
before being concluded.
It may be observed that the introduction of chitosan to the water
treatment industry would serve various sectors. The oil and gas indus-
tries form major energy sectors that suffer from fouling and toxic
byproducts released by bacteria. Rasool et al. (2018) tackled this issue
by targeting sulfate reducing bacteria through a batch reaction using
zinc oxide interlinked with chitosan nanoparticles. They reported a
high rate, undisclosed by the study, of inactivation of the bacteria. The
removal efficiency was evaluated based on the amount of sulfate pro-
duced rather than colony counts.
Chitosan composites also were highly active in destroying
M. aeruginosa, being a toxic bacterium in addition to causing fouling
problems (Li et al., 2012). In a study performed by Ma et al. (2016), chi-
tosan was mixed with aluminum chloride at different dosing orders
(aluminum chloride added first or vice versa) to act as a coagulant.
This process resulted in strong bridging abilities, where optimal
570 A. Kassem et al. / Science of the Total Environment 668 (2019) 566–576

Fig. 1. Mechanism for ‘on-demand’ microbial control showing the encapsulate antimicrobial agents matrix (Qu et al., 2013).

conditions, with chitosan added first, attained 97.8% removal of intact
cells, 53.08% of extracellular microcystins and 100% extracellular or-
ganic matter by a reaction that followed bridging and subsequently en-
trapment of M. aeruginosa as proposed indicated by earlier researchers
(Bo et al., 2012; Wei et al., 2009; Renault et al., 2009; Hu et al., 2013).
It is important to note that long term efficacy is also a major concern
since antimicrobial nanomaterials that rely on the release of biocidal
ions will be eventually depleted (Qu et al., 2013). A potential “on de-
mand” release strategy that has been proposed is to encapsulate antimi-
crobial agents into a matrix gated by materials that are responsive to
microorganisms and that can be further coupled with recognition
mechanisms for targeted release as shown in Fig. 1 (Qu et al., 2013).
2.3. Mechanisms of removal
Clays are well known for their water treatment capabilities (Usmani
et al., 2017), while oxides are denoted as good water disinfectants
(Upadhyay et al., 2014). On the other hand alum is an established floc-
culent and Carica papaya seeds were successful in treatment of organic
and inorganic pollutants in water (Unuabonah et al., 2009). Based on
the characteristics of these materials, Unuabonah et al. (2017)
conducted a study by synthesizing a mixture of Kaolinite clay, chitosan,
ZnCl2, Alum, and Carica papaya seeds and used the mixture as a disinfec-
tant. From the impending results, they were unable to determine the re-
moval mechanism, however the most plausible account is that removal
occurs as a result of the presence of an electrostatic interaction; this is
because chitosan chains have the ability to interact with negatively
charged compounds thus disrupting the bacterial outer structure lead-
ing to lysis (Raafat et al., 2008; Undabeytia et al., 2014). It is important
to note that several factors have a role in achieving high removal effi-
ciencies which include surface area of adsorbent sites, polymers molec-
ular weight and hydrophobicity (Smith and Rodrigues, 2015).
As a flocculent, an important reaction is that related to the attraction
of the flocculent to the bacteria through a bridging mechanism ascribed
to ionic attraction, which eventually leads to settling accompanied by
the breakage of the bacterial cell wall and death as shown in Fig. 2.
(Strand et al., 2002; Zhao and Zhang, 2013; Yang et al., 2014).
Motshekga and Ray (2017) complemented previous work that was
conducted by Motshekga et al. (2015) where the behavior of chitosan
bentonite composites was studied in a fixed bed column. Results
showed these composites to be highly effective by leaving no bacteria
behind after 27 h of exposure. Even though the inactivation mechanism

Fig. 2. Mechanisms leading to bacterial disinfection using modified chitosan (Yang et al., 2014).
 A. Kassem et al. / Science of the Total Environment 668 (2019) 566–576
deemed not to be fully understood, all chitosan composites have
followed the same course of action whereby the active surfaces were
characterized by being positively charged serving as a biocidal agent
through interaction and disruption of negatively charged cell mem-
brane (Li et al., 2008a, 2008b; Biswas and Bandyopadhyaya, 2016;
Haider et al., 2016). An important parameter that determined removal
efficiency was bed mass, as it was shown that the larger the bed mass
the greater is the surface area resulting in more bacteria being anchored
and inactivated by the matrix (Motshekga and Ray, 2017). Garcia Peña
et al. (2017) tested a filtering system using a chitosan and silver nano-
particles medium where complete bacterial removal was achieved in
8 h. The filter is distinguished by its anti-fouling ability which prevented
bacteria from attaching and proliferating on the surface of the filter. The
precise mechanism that led to inactivation was not fully understood;
however, it was proposed that the generated reactive oxygen species
disrupted the cell membrane, and/or the binding of positively charged
surface that disassembles vital bacterial functions resulting in cell
death (Xu et al., 2011; Choi and Hu, 2008; Le Ouay and Stellacci,
2015). In the study discussed above by Rasool et al. (2018), which
targeted sulfate reducing bacteria using zinc oxide interlinked with chi-
tosan nanoparticles, the suggested inactivation mechanism did not in-
clude oxidative stress since the production of reactive oxygen species
requires the presence of oxygen (Maurer-Jones et al., 2013; Liu et al.,
2011; Kong et al., 2010); which was not the case in this study as sulfate
reducing bacteria exist under anaerobic conditions. Consequently, it
was suggested that physical contact with NH2 group lead to inactivation
by cell destruction. It has to be noted that the exact biocidal activity of
nanostructures are not yet fully understood, yet hypothetical mecha-
nisms that are most commonly reported (Seo et al., 2018) include accu-
mulation and dissolution of nanoparticles in the bacterial membrane,
oxidative damage to cellular structures and uptake of metallic ions if
present in the nanoparticles.
3. Carbon nanotubes antibacterial activity
Carbon nanotubes (CNTs) have shown promising applications due
to their exceptional properties in comparison to various nanomaterials.
CNTs are composed of nano-cylindrical material that is purely made out
of carbon that only extends to a few millimeters in range and are distin-
guished by their highly conductive properties. In addition to that, stud-
ies showed that CNTs are excellent antimicrobial agents (Setaro, 2017).
Depending on the layering of the tubes, CNTs range from single-walled
to multi-walled carbon nano-tubes (Fig. 3). CNT's efficiency in microbial
removal is affected by several operational conditions such as tempera-
ture, pH, retention time, solute and solvent composition (Smith and
Rodrigues, 2015). Table 2 summarizes the most recent advances in the
utilization of carbon nanotubes in the inactivation of microorganisms.
Fig. 3. Rolling layers of graphite can form SWCNT and MWCNT (Hammond et al., 2016).
571
3.1. Experimental considerations and mechanisms of disinfection of CNTs
To demonstrate the microbial removal activity of carbon
nanotubes, Salam et al. (2017a, 2017b) performed a study to assess
the effectiveness of polypyrrole and silver nanoparticles in the
presence of carbon nanotubes when added at different concentra-
tions. The results have shown that the percentage of bacteria
removed as a result of adsorption in an overnight contact time
using a nanocomposite of pyrrole, CNTs, and silver nanoparticles
ranged from 87.5% to 95%.
The overall mechanism of disinfection is related to the individual ef-
fect imparted by each element forming the synthesized nanocomposite,
whereby silver nanoparticles cause cell death by attacking the cell
membrane (Ghosh et al., 1998), the positively charged polypyrrole mol-
ecules stick to the negatively charged cell membrane of the bacteria
causing growth inhibition (Smith and Rodrigues, 2015), while CNTs,
given their large surface areas and damaging capabilities of cell mem-
brane through oxidation, hold exceptional disinfection efficiency
(Cioffi and Rai, 2014; Ghosh et al., 1998).
The introduction of CNTs resulted in added advantages to the study
in that higher thermal stability was recorded besides that the large sur-
face area of CNTs proved to enhances bacterial inactivation efficiency
Salam et al., 2017a, 2017b. A similar study was conducted by Das et al.
(2014) to assess the microbial removal activity of multi-walled carbon
nanotubes which indicated similarity to single-walled carbon nano-
tubes in that interaction by direct contact with bacterial cell membrane
led to inactivation. Bai et al. (2015) performed a study using MWCNT in
a mixture of surfactants containing hexadecyltrimethyl ammonium
bromide and octylphenol ethoxylate. The presence of MWCNT has
shown to form stable dispersion in the aqueous phase with strong bac-
terial cell inactivation capabilities.
As noted earlier, metal oxides play a significant role in the bacteri-
cidal ability of carbon nanotubes. Engel et al. (2018) assessed the re-
moval of E. coli and its mutants using single walled carbon nanotubes
mixed with iron oxides where the resulting removal efficiency ranged
from 86 to 100%. The reported inactivation mechanism was explained
by the fact that the cell membrane of the bacteria is composed of lipo-
polysaccharides which act as a barrier, whereby its structural integrity
can be degraded when exposed to carbon based nanomaterials. Degra-
dation of E. coli was verified when displayed under SEM showing cell
deformation. This has been established to be due to the oxidative toxic-
ity of CNTs which causes oxidative stress in microbial cells that will lead
to inactivation (Engel et al., 2018).
Carbon nanotubes have proven their versatility in the way they op-
erate. In a study by Dong and Yang (2015), a dual functional carbon
nanotube filter was developed to capture and inactivate bacteria. Two
MWCNTs, having different outer layer diameters (8 nm and
10–20 nm), were used to coat commercially available isopore polycar-
bonate hydrophilic membranes. This was adopted because it was
established that surface area plays a major role in bacterial inactivation
by inhibiting the vital metabolic functions of bacteria (Wang et al.,
2012). Test results showed that Bacillus anthracis viability was reduced
by up to 97.19%. Through further analysis it was shown that bacterial
deactivation occurred by adsorption onto nisin (an antimicrobial pep-
tide) which has shown to have the capability to inhibit both gram pos-
itive and gram-negative bacteria (Severina et al., 1998; Willey and van
der Donk, 2007; Karam et al., 2013).
Carbon nanotubes can be assimilated with supplementary materials
to enhance their activity. Dong et al. (2018) conducted an experiment
by incorporating SWCNTs and MWCNTs to carbon quantum dots since
it was found to demonstrate antimicrobial activities in the presence of
light (Dong and Yang, 2015; Brady-Estévez et al., 2008). Ionic strength
was the most important parameter that researchers were able to
heighten through the addition of NaCl (Brady-Estévez et al., 2010),
thus enhancing bacterial removal rates by 1 log and achieving disinfec-
tion efficiency of 94.21% (Dong et al., 2018).
 572
Table 2
Published work on carbon nanotubes (2013–2018).

Reference Type of modified nanotube Type of water pH Temperature CNT amount Retention Targeted Way of Disinfection
time microorganism/s treatment efficiency

Al-Hakami et al. (2013) Functionalized Carbon nanotubes with 1-octadecanol Bacterial stock Room 2 g/300 mL 10 s E. coli Adsorption under 100%
groups (C18) solution temperature microwaves
Bhaduri et al., 2018 Ag-Fe3O4- single walled carbon nanotube Bacterial stock 25C 1 g/300 mL 2h Bacillus Batch adsorption 100%
solution megaterium
E. coli
Su et al. (2013) Ag-doped multi-walled carbon nanotube nanoparticles Bacterial stock 7 25C 3 mg/27 mL 6h E. coli Batch experiment 99.98%%
solution under fluorescent
irradiation
Sui et al. (2013) ZnO coated multi-walled carbon nanotubes Bacterial stock – Room 0.256–0.512 – E. coli Batch experiment 100%
solution temperature mg/mL

A. Kassem et al. / Science of the Total Environment 668 (2019) 566–576

Hai et al. (2014) Multiwalled carbon nanotubes Wastewater 7.2–7.6 21 ± 3C 1 and 20 mg/L Short term Proteobacteria Triplicate 62.5 ± 5.5%
MWCNT exposure: 1 Actinobacteria sequencing batch
day Bacteroidetes reactors
Long term Chloroflexi
exposure: Rhodobacter
180 days
Rananga and Magadzu (2014) Silver doped multi-walled carbon nanotube/β-cyclodextrin Bacteria – – 100 mg/20 mL 10 min E. coli Batch experiment 100%
nanocomposite contaminated
water
Dinh et al., 2015 Silver- carbon nanotube Bacterial stock 37C 50 μg/mL 24 h E. coli Paper-disc diffusion –
solution Staphylococcus method
aureus
Bai et al. (2015) Mixed surfactant CTAB and TX100 (hexadecyltrimethyl Water – Room temp. 15 mg CNT added 1h S. aureus Batch adsorption 6 h growth
ammonium bromide, octylphenol ethoxylate) -functionalized to 100 mL mixed delay and
multi walled carbon nanotube surfactant achieved 4.5 log
Dong and Yang (2015) Multiwalled carbon nanotubes 1: b8 nm in diameter Water – Room temp. 1.2 mg 6h Bacillus anthracis Batch adsorption
multiwalled carbon nanotubes 2: 10–20 nm in diameter
Zhu et al. (2015) Carboxyl-functionalized multi-walled carbon nanotubes Contaminated – – – 20 min E. coli Conductive N99.99%
blended with polysulfone polymer in the presence of electric deionized 40 min S. aureus membrane reactor
current water
Rananga and Magadzu (2015) Silver nanoparticles coated on multi-walled carbon Bacteria – – 100 mg/20 mL 10 min E. coli Batch experiment 100%
nanotubes/β-cyclodextrin contaminated
water
Hassouna et al. (2016) Natural kaolin carbon nanotube Tap water – 25C 0 .1mg/L 2h K. Pneumonae Batch adsorption 70% Salmonella
Underground E. coli 70% K.
water Salmonella Pneumonae
Surface water 60% for E. coli
Wastewater isolates.
Salam et al. (2017a, 2017b) Nanocomposites of polypyrrole/carbon nanotubes/silver nano Water – Room temp. (40 & 60% CNT w/w – E. coli Column adsorption 87.5–95%
particles of pyrrole) S. aureus
Hussein et al. (2018) Polyaniline, graphene nanosheets, and carbon nanotubes Bacteria – – 200 mg/(column 1 0.5 L/min E. coli Column adsorption 99.2%
contaminated cm ∗ 1 cm) S. aureus 99.5%
water
Engel et al. (2018) Single walled carbon nanotubes and iron oxides Saline solution – Room temp. 0.5 mg 2h E. coli Batch adsorption 86–100%
E. coli mutants
Dong et al. (2018) Multiwalled carbon nanotubes with carbon quantum dots Water – Room temp. 3 mg MWCNTs 4 min E. coli Filtration 73–95.25%
B. subtilus
 A. Kassem et al. / Science of the Total Environment 668 (2019) 566–576
Fig. 4. Possible antibacterial mechanisms of nanoparticles on bacterial inactivation. *NP: nanoparticle.
Activated sludge is a basic process applied in wastewater treatment
facilities. This setup displays the presence of the highest variety of mi-
crobial fauna, thus testing the capability of CNTs in bacterial removal
under these conditions is a challenge, besides generating important
and crucial information to be added to the literature (Goyal et al.,
2010). In a study performed by Hai et al. (2014) the authors addressed
this issue by placing MWCNTs in synthesized activated sludge while
measuring its efficiency to remove nutrients and bacterial communities.
Microbial entities were exposed to different MWCNT concentrations;
this was done in order to determine the optimal experimental condi-
tions in terms of CNT concentration. Exposure lasted for 180 days during
which microbial activities were inhibited by various cytotoxic mecha-
nisms. The main inactivation mechanisms were reported to be the gen-
eration of reactive oxygen species that led to oxidative stress in addition
to the destruction of cell membrane resulting from the direct physical
contact with CNTs (Han et al., 2012; Yan et al., 2006; Kang et al., 2008).
Another application of CNTs was reported by Hassouna et al. (2016)
in which Kaolin clay was loaded with carbon nanotubes. The agglomer-
ation effect between kaolin clay and the nanotubes led to the formation
of a MWCNT with some non-functionalized suspended carbon nano-
tubes (Bae et al., 2010). Antimicrobial activity of the adsorbent was
tested using E. coli and Salmonella species, Klebsiella, and Shigella flexneri.
Direct contact was hard to achieve with the non-functionalized carbon
nanotubes due to the small surface area (Hossain et al., 2014; Jain and
Pradeep, 2005), nevertheless it was found that loading membrane fil-
ters with single-walled carbon nanotubes has resulted in the deactiva-
tion of 80%, 90%, 80%, 70%, and 80% of E. coli, Salmonella spp.,
K. pneumoniae, K. aerogenes, and Shigella flexneri respectively in just
b2 h of contact time and under the absence of bacterial growth.
On the other hand, the deactivation efficiency of CNTs-clay has de-
creased appreciably when conducting the treatment process under the
effect of bacterial growth resulting in 20% - 0% removal (Hassouna
et al., 2016). Other than the fact that activity of carbon nanotubes re-
quires direct physical contact with the targeted organisms to inhibit
their activity, in some cases this process can be enhanced through the
introduction of thermal processes (Kang et al., 2008; Qi et al., 2004;
Morones et al., 2005; Lyon et al., 2006; Kang et al., 2007). Al-Hakami
et al. (2013) have adopted this approach by functionalizing CNT with
1-octadecanol groups (C18) under the effect of microwaves, whereby
the researchers aimed to compare the efficiency of raw CNT with func-
tionalized CNT-(C18). Both of these composites were placed under the
effect of microwaves. The results showed that the raw CNT and the func-
tionalized CNT-C18 had removal efficiencies of 5 and 3% respectively
however when microwaves were applied the raw CNT was able to
achieve 98% removal of E. coli, while the functionalized CNT-C18
showed a removals of up to 100%. As a result the authors hypothesized
that the heat produced from microwaves causes polarization which
573
resulted in rupturing the cell walls of the bacteria. Also the functional-
ized CNT-C18 had a higher removal efficiency due to the larger number
of C\\C bonds which absorbed more heat than raw CNT. Fig. 4 shows a
schematic of possible destruction mechanisms that occur due to nano-
particles applied to different microorganisms.
Another study was conducted by Bhaduri et al. (2018) to determine
the antibacterial activity of Ag-Fe3O4 functionalized SWCNT. The results
showed complete inactivation of the targeted bacteria. Clear disruptions
of the cell wall integrity was noted which has mainly occurred due to
the release of Ag+ ions from the composite. These ions have been re-
ported earlier to be toxic to microorganisms (Cronholm et al., 2013;
Choi et al., 2008; Ivask et al., 2013; Kittler et al., 2010; Sotiriou and
Pratsinis, 2010). The experiment was carried out under two different
conditions, in the presence and absence of dissolved organic matter
(DOM) in order to assess its effect on the composite's antibacterial activ-
ity as it was previously reported (Wirth et al., 2012; Liu and Hurt, 2010)
that DOM tends to compete with bacteria for available surface area thus
limiting its direct contact with the nanocomposite. Results showed that
the presence of DOM has resulted in decreasing bacterial removal from
6 folds to 4 folds.
The promising biocidal effects of carbon nanotubes triggered re-
searchers to investigate CNTs in combination with various metals
using different preparation methods as this affects the degree of
functionalization of CNTs. Dinh et al. (2015) used a photochemical pro-
cess in order to activate CNT-silver nanoparticles and Graphene Oxide-
Silver (GO-Ag) nanoparticles; where results suggested that with direct
physical contact between bacteria and CNT-Ag, the Ag ions possessed
the leading role in the deactivation of bacteria. Despite the fact that
both composites had biocidal activities, GO-Ag displayed a more prom-
ising removal activity due to the enhanced dispersion of particles along
the nanocomposite, as suggested by Liu et al. (2010), Wu et al. (2011),
Baro et al. (2013) and Bao et al. (2011), that lead to greater surface
area for bacterial contact when compared to CNT-Ag.
Several attempts were explored to dope carbon nanotubes with sil-
ver, this is because silver ions when released exhibit biocidal activities
resulting in the rupture of the bacterial cell wall. To determine the
mechanism responsible for the inactivation of the microorganisms, Su
et al. (2013) used a silver doped multi-walled carbon nanotube as a re-
sult of which they suggested that bacterial inactivity occurred due to the
generation of reactive species. On the other hand, Rananga and
Magadzu (2014) performed a similar study with silver doped carbon
nanotubes-cyclodextrin where results showed damage of bacterial cell
wall prior to direct physical contact. In another attempt by Rananga
and Magadzu (2015) utilizing β-cyclodextrin and silver doped carbon
nanotubes confirmed that high bacterial removal was a result of crystal-
lite magnitude of silver. A number of studies, which tested the use of
Zinc Oxide coated MWCNTs, reported weak activity (Sui et al., 2013;
574 A. Kassem et al. / Science of the Total Environment 668 (2019) 566–576
Arias and Yang, 2009; Jia et al., 2005). Electrical current has been also
utilized in combination with CNTs to enhance their activity. Zhu et al.
(2015) prepared carboxyl-functionalized multi-walled carbon nano-
tubes to be used in the presence of current (AC and DC) where results
showed 99.9% bacterial removal, making this method a promising one.
It is to be noted that a composite could behave differently with dif-
ferent bacterial species. Since different types of carbon nanomaterials
possess distinct features depending on their lateral size, surface charge,
and functionalization, their cytotoxicity and biocompatibility for differ-
ent bacteria should be deeply considered for safe biomedical applica-
tions (Anand et al., 2019). In this context Hussein et al. (2018)
prepared a hybrid polyaniline/graphene/carbon nanotube to remove
S. aureus and E. coli, where S. aureus exhibits high negative charge
whereas E. coli exhibits a weaker negative charge (Li et al., 2014).
Their structural and ionic differences explain their different ion-ion in-
teraction with the positively charged adsorbent (Salam et al., 2017a,
2017b). Despite the diversity between the two species, the tested com-
posite was successful in deactivating 99.5% and 99.2% of the S. aureus
and E. coli respectively. As reported by Klahn and Bronstrup (2017), hy-
brids, in contrast to single components, avoid the complex handling of
dual profiles for efficacy, pharmacokinetics and toxicities. However, sys-
tematic studies on resistance and resistance mechanisms are still
needed especially for actively transported conjugates.
4. Conclusions and recommendations
Advances in water purification using nanomaterials are mainly
driven by their high efficiency in biological, physical, and chemical con-
taminants removal at the nano-scale (Baruah et al., 2016). It is to be
noted that extensive research investments have recently been spent
and earmarked for the future in this area due the tremendous impact
and potential that nanotechnologies have shown in various applications
and particularly in water and wastewater sanitation. Classified under
the category of nanomaterials, chitosan and their modified composites
along with carbon nanotubes, were found to be effective bacterial
disinfectors. Despite their antibacterial capabilities, the mechanisms of
disinfection and the methods of preparation still hold complexities
that impede their commercial application in water and wastewater
treatment. On the other hand, experimental studies for bacterial disin-
fection using chitosan and carbon nanotubes have demonstrated one
of its advantages is in eliminating the release of treatment byproducts
compared to other conventional disinfection methods (ozonation and
chlorination). Although the existing gaps in determining the inactiva-
tion mechanisms associated with using nanomaterials are diminishing
as a result of ongoing research advances in this field, r more defined
studies are needed on this issue to arrive at more confirmative conclu-
sions. Moreover, it has to be highlighted that the lack of a disinfection
residue, which is crucial for controlling microbial growth during water
storage and distribution is a common disadvantage of many
nanomaterial based disinfection processes (Qu et al., 2013). Long term
efficiencies and fouling that may be caused by direct contact are also
major concerns that need to be addressed in future studies. Another
gap that is very apparent in the literature includes studies on economic
feasibility and sustainability of the novel disinfection methods being
researched. This requires special attention as the ultimate adoption of
any of these methods for practical application will depend on the cost
advantages that they offer to the water treatment industry. Future re-
search also needs to consider the development of hybrid compounds
with enhanced stability and low toxicity. Nanocomposites that exhibit
great synergy with conventional antibiotic agents can be significant
for the treatment of highly resistant bacteria. Moreover, the
nanomaterial design approaches need to be established in a way to
eliminate undesired adsorption of biomolecules and enhance antibacte-
rial activity without compromising biocompatibility. Any structural de-
fect will significantly affect the properties and effectiveness of the
nanomaterial. Large-scale synthesis is also a major challenge due to
difficulty in reproducibility is some cases. Last but not least, the poten-
tial adverse effects of nanomaterials to humans and the environment re-
mains a crucial topic in future research.
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