Microbial toxicity of different functional groups-treated carbon nanotubes

CHAPTER

Microbial toxicity of different functional groups-treated carbon nanotubes

2

Ahmad Amiri1, Hadi Zare-Zardini2,3,4, Mehdi Shanbedi5, Salim Newaz Kazi1, Asghar Taheri-Kafrani4, Bee Teng Chew1 and Ali Zarrabi2 1

Department of Mechanical Engineering, University of Malaya, Kuala Lumpur, Malaysia Department of Biotechnology, University of Isfahan, Isfahan, Iran 3Pediatric Hematology and Oncology Research Center, Shahid Sadoughi University of Medical Sciences and Health Services, Yazd, Iran 4Young Researchers and Elite Club, Yazd Branch, Islamic Azad University, Yazd, Iran 5Department of Chemical Engineering, Ferdowsi University of Mashhad, Mashhad, Iran

2

2.1 INTRODUCTION Annually, numerous people die across the world from infectious diseases such as dysentery and pneumonia. To avoid this disaster, scientists have utilized conventional antibacterial agents, such as kanamycin, spectinomycin, and penicillin. Unfortunately, overuse of these antibacterial agents neutralizes the desired disinfection function, resulting in gradual resistance of bacteria. This fact dictates that the health communities continuously discover/develop novel antibacterial agents. Recently, carbon nanostructures with high surface area, such as carbon nanotubes (CNTs) and graphene, have promised to alleviate the gradual resistance phenomenon of various strains (Zardini et al., 2014; Amiri et al., 2012b; Zardini et al., 2012; ZareZardini et al., 2015). CNTs with promising properties, such as having high special surface area, being less dispersive in environment, and the potential of loading different biofunctional groups can be used in this field of study. Despite the toxic nature of CNTs, the functionalized samples were suggested to comprise less-toxic properties and can be considered as an alternative both in vitro and in vivo (Kang et al., 2009b; Sayes et al., 2006). To enhance the antibacterial activity of CNTs, they were combined with different functional groups such as metallic nanoparticles as well as biochemical functionalities (Pantarotto et al., 2003). Regarding biofunctional groups, the antibacterial property of biofunctional CNTs may originate from amino acid moieties. The positively charged groups loaded on the surface of CNTs were shown to be responsible for effective adsorption and so damage of negatively charged phospholipid membranes of bacteria (Amiri et al., 2012b; Zardini et al., 2012). It can be Surface Chemistry of Nanobiomaterials. DOI: http://dx.doi.org/10.1016/B978-0-323-42861-3.00002-9 © 2016 Elsevier Inc. All rights reserved.

33

34

CHAPTER 2 Functional group-dependent toxicity of CNT

concluded that different functional groups can impose different bioproperties on CNTs. Therefore, in this chapter, the effect of the morphology and structure of CNTs on microbial toxicity and/or antibacterial activity is investigated. It is obvious that the special morphological structure of CNT, strong intertube van der Waals interactions and π π orbital interactions makes them insoluble in different kinds of fluid, which has reduced the number of CNT applications (Amiri et al., 2011, 2012a, 2014; Shanbedi et al., 2015). Therefore, to realize different applications, functionalization has been suggested as an excellent method. To address this issue, functionalization of CNTs is first described in detail and followed by investigation of the influence of different functional groups on antibacterial and cytotoxicity.

2.1.1 NON-COVALENT FUNCTIONALIZATION When CNTs are attached to other adjacent tubes, producing a good dispersion in various solvents is extremely difficult. The mentioned adhesion can be decreased in the presence of π π interaction by surface adsorption of surfactants (Shanbedi et al., 2013), polymers, polynuclear aromatic compounds, and biomolecules (Zhang et al., 2003; Thostenson et al., 2001; Murakami and Nakashima, 2006). Noncovalent functionalization is more interesting and attracts numerous researchers in different fields. This method is simple, quick, cost-effective and also the main structure of CNT remaining intact after functionalization. However, the CNT dispersibility is strongly dependent on the type and concentration of molecules on the surface. CNTs can be classified into four branches.

2.1.1.1 Functionalization with surfactant In order to increase dispersibility of CNT in aqueous media, there are four surfactants that are commonly applied, gum arabic (GA), Sodium dodecyl sulfate (SDS), sodium dodecyl benzene sulfonate (SDBS), and Triton X-100. According to previous results (Figure 2.1), the sequence of CNT dispersibility in the presence of the above-mentioned surfactants is as follows: GA . SDBS . Triton X-100 . SDS

SDBS and Triton X-100 have a benzene function, which produces the powerful π π interaction with the CNT surface. It is noteworthy to mention that SDBS has a higher dispersibility than Triton X-100. This issue is attributed to the steric hindrance of tip chains in Triton X-100, which results in a low concentration of Triton on the CNT surface. In addition, GA has attracted numerous researchers because of promising properties (Islam et al., 2003; Azizi et al., 2013).

2.1.1.2 Functionalization with aromatic molecules There are numerous reports in the field of functionalization of CNT with pyrene, anthracene, and porphyrin comprising of hydrophobic or hydrophilic chains.

2.1 Introduction

FIGURE 2.1 Surfactant adsorption on the surface of CNT.

According to earlier results, zinc porphyrin can provide a homogeneous suspension of SWNT and polar solvents such as methanol and dimethylformamide. They have also demonstrated that this suspension has remained stable for more than 6 months in the vessel (Murakami et al., 2003). In another similar work, Li et al. (2004) synthesized a new kind of porphyrin that absorbed on the surface of CNT and resulted in higher dispersion of CNT in chloroform. Chichak et al. (2005) showed that two pyridine ligands in the porphyrin played a key role in increasing dispersibility of CNT in the aqueous media. As a result, there are numerous researches in this field describing new applications with the aromatic compounds (Guldi et al., 2005). Chen et al. (2001) suggested the attachment of N-succinimidyl-1-pyrenebutanoate on the surface of CNT in the presence of π π interactions among the graphitic structure of CNT sidewall and the pyrene-group. The N-succinimidyl-1-pyrenebutanoate showed a good adsorption onto the CNT surface. The sidewall functionalization of CNT with N-succinimidyl-1-pyrenebutanoate via π-stacking interactions is shown in Figure 1-11. The similar π-stacking interactions between CNTs and 17-(1-pyrenyl)-13-oxa-heptadecanethiol [PHT] resulted in decoration of CNT through gold nanoparticles (Liu et al., 2003).

35

36

CHAPTER 2 Functional group-dependent toxicity of CNT

In another study, a pyrene molecule, including an ammonium ion, was applied to attain a transparent solution of CNT in water (Nakashima et al., 2002).

2.1.1.3 Functionalization with polymers It is obvious that polymer can wrap around the CNT structures in a periodic approach (McCarthy et al., 2000). The polymer can play a role like bridge between the adjacent CNTs that significantly reduces the interactions among CNTs. In addition, characterization studies confirmed a reaction between the polymer and CNTs with the same or different diameters (Dalton et al., 2000). The decoration of CNTs with some polymers was also illustrated as being an appropriate purification technique to increase the quality of CNTs (Murphy et al., 2002).

2.1.1.4 Functionalization with biomolecules Studies using CNTs for the immobilization of biomolecules showed that a wide range of proteins and peptides can be bound on the nanotube surface and provide good conditions for improving CNT dispersibility (Tsang et al., 1995). Noncovalent functionalization of CNT with DNA was investigated by numerous researchers. The previous results confirmed that single-walled carbon nanotube (SWCNT) has remained stable in aqueous media for more than 6 months at 5  C (Tsang et al., 1995; Barisci et al., 2004; Zhou et al., 2009).

2.1.2 COVALENT FUNCTIONALIZATION Adding functional groups to the main backbone of CNT has been introduced as the covalent functionalization. This type of functionalization changes the main structure of CNT and introduces numerous defects on the CNT surface. Covalent functionalization disrupts some aromatic π-electrons on the CNTs surface along with the alteration of sp2 hybridized carbon (graphitic carbon) to sp3 (amorphous/disordered carbon) (Shanbedi et al., 2011, 2014; Amiri et al., 2013). However, functional groups attaching to the main structure of CNT can decrease some promising properties of CNT such as electrical conductivity (Hirsch and Vostrowsky, 2005). On the other hand, covalent functionalization can provide more stable conditions for CNT in different applications and realize numerous purposes, due to the improvement in their reactivity. Covalent functionalization can be classified into two groups in terms of effective site and added functional groups: 1. Tip functionalization. 2. Sidewall functionalization.

2.1 Introduction

2.1.2.1 Tip functionalization There are different viewpoints for tip and sidewall functionalizations of CNT. CNTs are capped with two fullerene hemispheres, which are active sites for functionalization because of the pentagonal structure of CNT. However, the curvature of sidewall of CNT is lower than various fullerenes, which results in C 5 C bonds with weaker reactivity as compared to the tip and end of CNTs (Hirsch and Vostrowsky, 2005). Therefore, one can conclude that tip functionalization is more simple and the main reason for increasing dispersibility. It is obvious that dispersibility of CNT in organic solvents increases when hydrophobic functional groups are decorated on the CNT surface (Amiri et al., 2011, 2012a, 2014). The first report on increasing dispersion of CNT had suggested the functionalization of SWCNTs with octadecylamine and later investigated the dispersibility of CNT after functionalization in different media. They observed a good solubility of CNT in organic solvent. Amidation, carboxylation, hydroxylation, and esterification are different types of tip functionalization, which are illustrated in Figure 2.2. In addition, electrostatic interaction between CNTs and biological molecules is also possible and this concept was employed for synthesizing environmentally friendly products. Covalent-ionic functionalization with different molecules has also been introduced as another approach to add functional groups on CNT surfaces (Figure 2.3) (Furtado et al., 2004). In advanced studies, tips of carboxylated multiwalled counterparts (MWCNT) were connected to the gold substrate covered with silicon. The dispersibility of CNT in some organic solvents is increased in the presence of esterification with pentanol (Hamon et al., 2002; Tasis et al., 2006). In another study, Gooding (2005) utilized the carboxylated CNT as a bridge for functionalization with other

FIGURE 2.2 Tip functionalization of CNT with different functional groups.

37

38

CHAPTER 2 Functional group-dependent toxicity of CNT

FIGURE 2.3 Covalent-ionic functionalization with different molecules.

FIGURE 2.4 Installing CNT on Au substrate.

functional groups. They first functionalized CNT-COOH with aminothiol was then installed on a gold substrate (Figure 2.4) (Tasis et al., 2006). The oxidized CNTs were applied as the potential carriers in different cells. CNTs have a promising ability for transferring active biocompounds in this type of cell. Thermal conductivity of CNTs along with some properties of biomaterials decorated on CNTs provide a great chance for inventing novel kinds of systems, set-ups, and drugs. Biosensors are a typical example and model of this invention. CNTs can bridge or link to the chain of enzyme by the carboxylic groups functionalized on their tip and end. This connection has been applied in manufacturing biosensors. Numerous researchers in various fields have investigated different types of biosensors. It is of note that a majority of them focused on the connection

2.1 Introduction

FIGURE 2.5 Difference in structure of CNT and flurrene.

of CNT on Au substrate. Overall, the numerous reports in the field of tip functionalization of CNT confirm the importance of this issue for biological studies.

2.1.2.2 Side-wall functionalization of CNT Side-wall covalent functionalization is another method to increase the lack of interactivity of CNTs. Two types of carbon bond are obvious in Figure 2.5. 1. Some with a circular surface area, those are vertical on the central axle of CNT as well as parallel-aligned. 2. The angle between π bonds (orbitals) of adjacent carbons, which is about zero in flurrene. The zero angles in flurrene are mainly for its active interaction with other materials. It is confirmed that the morphology and structure of carbon allotropes play a key role in the physical and chemical properties. It is worth mentioning that SWCNTs have a developed structure full of lower-energy bonding orbital (Niyogi et al., 2002).

39

40

CHAPTER 2 Functional group-dependent toxicity of CNT

FIGURE 2.6 Side-wall functionalization of CNTs with different functional groups.

It could be noteworthy that there are numerous studies in the field of functionalization of CNTs and different methods and functional groups were employed to reach this goal. Figure 2.6 represents some functionalization processes reported recently. Some functionalization reactions such as fluoridation, dipolar cycloaddition, adding cyclonitrile compounds, reaction with aryldiazonium salts, and electro addition (Ghiadi et al., 2013; Zardini et al., 2014) have been reported. Recent investigations have shown that the simple reductive reaction of CNTs with Li and Na could result in higher dispersibility in polar aprotic solvents.

2.2 METHODS OF FUNCTIONALIZATION Different methods and instruments have been employed to functionalize CNT and there are advantages and disadvantages in each of the methods as described here. This comparison may open a gateway to select the best technique for the required functional groups.

2.2 Methods of Functionalization

2.2.1 HEAT-REFLUXING In this method, CNTs with functional groups are poured into a kettle or boiler with the circulation system. Then, the mixture is heated up to the boiling temperature of the functional groups. The vapors of functional groups along with CNTs are commonly passed through a cycle including a spiral condenser and an evaporator for 24 h. The heat-refluxing method has several advantages, such as high degree of functionalization, treatment of different functional groups even acidic groups, economical and cost-effective, simple set-up, etc. On the other hand, this method is time-consuming and holds some problem for functional groups at high boiling temperature.

2.2.2 MIXING A hot plate stirrer and ultrasonic instruments are two conventional devices for mixing CNTs in the liquid phase. Ultrasound was introduced as an oscillating sound pressure wave in high frequency, undoubtedly higher than the maximum amount of the human hearing range. Overall, ultrasound devices commonly operate at frequencies of 20 kHz up to several gigahertzes (Messmer, 1998). Ultrasonication offered enormous capability in the liquids by enhancing the mixing and chemical reactions. Ultrasonication prepares irregular low- and highpressure waves in the base-fluids, which result in the generation and severe collapse of miniature bubbles, which are called cavitations and lead to high-speed impinging liquid jets and strong hydrodynamic shear-forces. Commonly, the mentioned properties are applied for de-agglomerating of micro- and nanostructures. It is obvious that ultrasonication can be an alternative to high-speed agitators and mixers. In addition, CNT chemical functionalization commonly benefits from producing free radicals during cavitation phenomena as well as heat and mass transfer through the boundary layers. Sometimes, a few reduction reactions are generated in the reaction time under sonication waves (Messmer, 1998). As a result, the vibrations of the sonication method provide the suitable condition for more effective collision, which results in a higher degree of functionalization. A hot plate stirrer is commonly applied for functionalization with sensitive materials. As compared with the ultrasonic method, stirring is weaker and results in a lower degree of functionalization. Overall, the mixing method introduces numerous defects on the surface of CNTs and is more time-consuming than other methods.

2.2.3 PLASMA In this method, a reaction chamber (plasma chamber) is designed to undergo high temperature. The input and output entrances for gas, a vacuum pump, and several controllers for adjusting temperature and pressure are the main instruments of

41

42

CHAPTER 2 Functional group-dependent toxicity of CNT

FIGURE 2.7 Schematic of plasma chamber with microwave irradiation (Kalita et al., 2008).

set-up. By injection of semiactive gas, such as CH4 in high temperature and pressure in reaction chamber, the degree of CNT functionalization increases considerably. In order to eliminate noncondensed gas into the reaction chamber, a vacuum pump is employed. This equipment can be used along with microwave irradiation with low modifications in design. Figure 2.7 illustrates a schematic of a plasma chamber with microwave irradiation (Kalita et al., 2008). Although the plasma method leads to a high degree of functionalization and rapid reaction, it generates defects on the surface and backbone of CNT, high temperature; applying complex controllers and high cost are the main problems that have limited the utilization of this method. In addition, this method is being used only for functional groups with low chains and small molecules. Some catalysts are also used to increase the functionalization performance.

2.2.4 MICROWAVE METHOD In this method, microwave irradiation is used for functionalization of carbon nanostructures with various functional groups (Amiri et al., 2015a, 2015b). Dipolar polarization, conduction, and interfacial polarization (Maxwell Wagner phenomenon) mechanisms have been reported as the main reason for good functionalization under microwave irradiation. As the CNTs are placed under microwave irradiation, severe absorptions are obtained, intense heating is observed, and light emission is produced. Some electrically conductive impurities, like metals and carbon, could support the conduction heating mechanism. According to the conduction heating mechanism, the microwaves do not heat the carbon nanostructure directly. It was believed that movement of the electrons is induced and boosted by the electric field, resulting in extra heat in samples and preparing some superheating positions in the effect of inducing Joule heating by the metal nanoparticles.

2.3 Antimicrobial Activity

On the other hand, some studies showed that magnetic nanoparticles have no effect on microwave irradiation, while the elimination of metal nanoparticles has little influence on the microwave absorption of CNTs. Another possible source of superheating positions should be the production of gas plasma under microwave radiation (as mentioned above) from absorbed gases (typically H2) in CNTs. As another mechanism, some researchers have concluded that there is no dipolar polarization in CNTs since they have no electric dipoles. On the other hand, CNTs with one-dimensional structure were illustrated as ballistic conductors, implying their resistances were quantified and independent of length. Thus, no energy was dissipated because of electron motion. Accordingly, the current generated during microwave irradiation is not changed into heat. However, CNTs have generally structural defects, which lead to the deterioration of ballistic transport, permitting Joule heating to happen in the CNTs as well as producing some superheating. A special model for elucidating microwave-induced heating of CNTs into mechanical vibrations was suggested by alteration of electromagnetic energy. According to the proposed model, CNTs exposed to the microwave irradiation undergo ultraheating because of a transverse parametric resonance, which is obtained by the CNTs’ polarization under microwave irradiation. In the presence of nonpure CNTs, Joule heating happens due to the defects and impurities which dampen the transverse vibration mode. Also, CNTs cannot vibrate in the viscous media. As a result, transverse resonance and Joule could not describe the dissimilar results of absorption for various solvents that are reported by other researchers. This method has been considered as a promising protocol due to some advantages as follows: generating few defects on CNTs’ surface, rapid, effective, and one-pot are the main advantages of this method as compared with other abovementioned methods.

2.3 ANTIMICROBIAL ACTIVITY We reviewed all the methods of functionalization to investigate the bioproperties of nanotubes. Antibiotic-resistant microorganisms have become one of the common and most serious health obstacles over recent decades (Fedorka-Cray, 2014; Viksveen, 2003). These microorganisms are capable of inducing some severe diseases (Heinemann et al., 2000). The mentioned microorganisms can easily pollute plants, animals, humans, and their ecosystems. As an example, water treatment is one of the critical challenges in twenty-first century. Most water has different microbial pathogens and pollutions (Qu et al., 2013). To eliminate the different kinds of pathogens, the development of novel agents and systems is essential, and traditional antibiotics cannot inhibit a majority of pathogens. Nowadays, nanostructures are considered as a new candidate for inhibition of microbial growth in different media. Mass production of numerous nanomaterials with good antibacterial activities, such as metal and metal oxide nanoparticles (silver (Ag), silver oxide (Ag2O), titanium dioxide (TiO2), zinc oxide (ZnO), gold

43

44

CHAPTER 2 Functional group-dependent toxicity of CNT

(Au), calcium oxide (CaO), silica (Si), copper oxide (CuO), and magnesium oxide (MgO)) provide suitable changed applicable conditions (Iqbal et al., 2014; Wahab et al., 2013; Ramani et al., 2014; Giri, 2014; de Azeredo, 2013). CNTs are the best compounds due to their promising properties. CNTs have been considered for use in different technologies such as electrical devices, superconductors, and especially in biological systems such as biosensors, drug delivery, gene delivery, medical imaging, etc. (He et al., 2013; Shao et al., 2013). One of the CNT applications which has recently been considered and attracted numerous scientists’ attention is their application as the antimicrobial agents to inhibit tmicrobial growth in different environments (Dong et al., 2012; Aslan et al., 2010; BradyEste´vez et al., 2008). It has been proven that CNTs exhibit high antimicrobial activity. Different studies indicated that SWCNTs and MWCNTs showed unique antimicrobial properties. CNTs have been applied for biological purposes in both forms of pristine and functionalized samples (Kang et al., 2008a; Varghese et al., 2013; Amiri et al., 2012b; Zardini et al., 2014; Zare-Zardini et al., 2013; Zardini et al., 2012). Different factors influence the antimicrobial activities of CNTs. Thus, the antimicrobial activity of CNTs was not equal in different forms, size, chemical characteristics, and environments. In this chapter, the antimicrobial activity of pristine as well as functionalized CNTs is studied. The aim of this chapter is to summarize the investigation of different methods of functionalization, antimicrobial activity of CNTs, and the influence of different functional groups on antimicrobial activity.

2.3.1 ANTIMICROBIAL ACTIVITY OF PRISTINE CNTs In 2007, Kang et al. (2007) for the first time showed that SWCNTs had a strong antimicrobial activity against Gram-negative bacteria (Escherichia coli). The suitable biological activity of SWCNTs was confirmed by different researchers in different fields. In 2008, other groups showed that MWCNTs also have great antimicrobial activity and proved that this activity is less than for SWCNTs. According to several studies (Kang et al., 2008a; Vecitis et al., 2010), SWCNTs have a more toxic effect on bacteria than their MW counterparts. Some studies reported that CNTs can directly contact microbial cells and inhibit their growth by generation of a disturbance in membrane integrity, metabolism processes, and morphology (Kang et al., 2008b). They also indicated that SWCNTs penetrate into the cell wall with higher performance than MWCNTs and finally disturb DNA (Zhang et al., 2010). In 2010, researchers showed that the SWCNTs with higher length have stronger antimicrobial activity due to their improved aggregation with bacterial cells (Yang et al., 2010). In addition, Dong et al. (2012) demonstrated that the type of surfactant used to synthesize solutions influences the antibacterial properties of CNTs. Overall, it can be concluded that SWCNTs have higher antimicrobial activity than MWCNTs (Kang et al., 2008a). Based on a

2.3 Antimicrobial Activity

recent study (Liu et al., 2009), bacteria incubated with sulfadiazine and SWCNTs had a much higher death rate in comparison to bacteria incubated with sulfadiazine in the absence of SWCNTs. The effect of CNTs on human health, environments, and natural flora is considered as the main concern in recent studies (Du et al., 2013; Petersen, 2014). The best strategy for maximizing CNTs’ application potential and minimizing their risks is functionalization. As mentioned above, the method of CNT functionalization and their functional groups were discussed. In the following sections, the functional groups that can improve antimicrobial activity will be introduced.

2.3.2 ANTIMICROBIAL ACTIVITY OF FUNCTIONALIZED CNTs As mentioned in previous sections, CNTs are bundled with strong van der Waals interaction. Thus, the dispersion of CNTs in organic and inorganic solutions is a big challenge (Hertel et al., 1998; Dumlich and Reich, 2011). Different methods, such as mixing, sonication, and the microwave method are employed to enhance the dispersivity of CNT in different media (Huang and Terentjev, 2012). With the increase in dispersivity of CNTs, a majority of bioapplications could be realized. In addition to the improvement of their dispersion, such functional groups change the biological activity of CNTs, especially antimicrobial activity (Amiri et al., 2012b; Zardini et al., 2012, 2014). Well-dispersed CNTs can easily move in solution and have a higher chance of colliding with bacterial cells (Liu et al., 2010). To address this issue, there are many functional groups used to change the antimicrobial activity of pristine CNTs. For instance, the antimicrobial activity of three different functionalized SWCNTs (hydroxylated SWCNTs (SWCNT OH), carboxylated SWCNTs (SWCNT COOH), and amine treated SWCNTs (SWCNT NH2)) were investigated in the presence of Salmonella typhimurium. The results showed that SWCNT OH and SWCNT COOH have antimicrobial activities at B50 μg/ml, while SWCNT NH2 showed poor antimicrobial activity at high concentration. Meanwhile, MWCNTs functionalized with OH, COOH, and NH2 did not show any antimicrobial activities against different bacterial cells up to 500 875 μg/ ml (Arias and Yang, 2009). On the other hand, another study reported that the carboxylated MWCNTs treated by sonication method present stronger antimicrobial activity than those of a pristine sample (Kang et al., 2008b). Furthermore, SWCNTs have also been functionalized with sugars, such as mannose or galactose, resulting in a significant drop in the number of bacterial spores (Gu et al., 2005; Wang et al., 2006; Luo et al., 2009). Sugar is one of the special compounds for capturing some bacteria such as E. coli and Bacillus anthracis. Arias and Yang also indicated that SWCNT-COOH and SWCNT-OH can improve the antimicrobial activity of CNTs against Gram-positive and Gramnegative bacteria. They also illustrated that carboxylation can improve the dispersion of MWCNTs, but their sample exhibited no significant effect on the antimicrobial activity (Arias and Yang, 2009).

45

46

CHAPTER 2 Functional group-dependent toxicity of CNT

Several researchers investigated the antimicrobial activity of pristine and functionalized SWCNTs via hydroxyl, carboxyl, and amino groups. The results suggested a sequence for antibacterial activity of functionalized sample as follows: SWCNT-OH . SWCNT-COOH .SWCNT-NH2 (Arias and Yang, 2009). The antimicrobial activity of Cu-treated CNT nanocomposite was investigated against Gram-negative (Providencia sp.) and Gram-positive (Bacillus sp.) at different concentrations, the results of which demonstrated its strong antimicrobial activity against various microorganisms (Sunil Kumar et al., 2012). MWCNTs decorated with silver nanoparticles (Ag NPs) can increase the chemical and antimicrobial activities. After both E. coli and Staphylococcus aureus had been cultivated with a fixed amount of Ag/MWCNTs for 24 h, no bacterial colonies of E. coli and S. aureus can grow in that media. The MIC value of CNT-Ag was lower than those of silver nanoparticles and pristine CNTs against both Gram-negative and Gram-positive bacteria due to the excellent antimicrobial activity of functional groups, good dispersion of the Ag nanoparticles on the CNTs surfaces, and good water dispersion. The antimicrobial properties of Cu-MWCNT were also investigated against some bacteria. Cu-MWCNT killed about 75% of tested bacteria (Mohan et al., 2011). We reported that functionalization of MWCNTs by positive amino acids (arginine and lysine) can improve the dispersion and antimicrobial activity of these nanostructures. According to the antibacterial results, arginine-treated MWCNTs (MWCNTs-Arg) and lysinetreated MWCNTs (MWCNTs-Lys) have stronger antimicrobial activities against Gram-positive and Gram-negative bacteria, as well as fungal pathogens, compared with pristine sample. The sequence of antibacterial activity against S. aureus, E. coli, and S. typhimurium bacteria was MWCNT-arginine . MWCNT-lysine . pristine MWCNTs (Amiri et al., 2012b; Zardini et al., 2012). Based on the antifungal activity of lysine-treated MWCNTs and pristine MWCNTs, lysine functionalization can increase the activity of lysine-treated MWCNTs 1.92, 2.35, 2.36, 1.5, 1.3, 1.1, 2.54, 1.42, 1.23, and 2.1 times against Aspergillus niger, Candidate albicans, Aspergillus fumigatus, Saccharomyces cerevisiae, Penicillium chrysogenum, Fusarium culmorum, Microsporum canis, Trichophyton rubrum, Trichophyton mentagrophytes, and Penicillium lilacinum, respectively. Similar results were repeated for the antifungal activity of arginine-treated MWCNTs (Zare-Zardini et al., 2013). We also showed that ethanolamine MWCNTs have strong antimicrobial activity against E. coli, Klebsiella pneumonia, S. typhimurium, and Pseudomonas aeroginosa as the Gram-negative bacteria and S. aureus, Bacillus subtilis, Streptococcus pneumonia, and Bacillus cereus as the Gram-positive bacteria (Zardini et al., 2014). Qi et al. (2012) in their study claimed that the immobilization of the antibiotic cefalexin on the surface of MWCNTs can improve the antimicrobial properties against Pseudomonas aeruginosa, E. coli, S. aureus, and B. subtilis. This functionalized MWCNT has higher antimicrobial activity than that of the pristine sample (Qi et al., 2012).

2.3 Antimicrobial Activity

According to the results of a chitosan CNT composite, there is an upward trend between its antimicrobial activity and the concentration of CNT in composite (Venkatesan et al., 2014). Surprisingly, functionalized CNT can easily remove the harmful microbial strains without side effects on natural flora. To follow this issue, a mixture (blend) of functionalized CNT and amphotericin B (AMB) exhibited strong antifungal activity without significant toxic effects on Jurkat cells. The antifungal activity of the treated CNTs with functional group and amphotericin B (f-CNT-AMB) against a series of bacteria, as well as clinical fungal strains, demonstrated better results as compared to the pure AMB. To increase the validity of the study, the microbial activity was compared with sodium deoxycholate (e.g., amphotericin B deoxycholate (AMBD)). The results showed that AMBD-resistant Candida strains were susceptible to the f-CNT-AMB (Benincasa et al., 2010). We summarize the antimicrobial assay of some different functionalized CNTs in Table 2.1. According to all references, in all of these functionalized CNTs, their antimicrobial activities were significantly higher than pristine CNTs. Functionalization of CNTs (SWCNTs and MWCNTs) by different agents improved their antimicrobial activity.

2.3.3 MECHANISM OF ANTIMICROBIAL ACTIVITY OF CNTs The recognized antimicrobial mechanism of CNTs plays a key role in selecting and programming CNTs as an antimicrobial agent. Thus, a good understanding of the mechanism can be utilized to remove microorganisms without adverse side effects on human cells and environments. There are several hypotheses in the field of the antimicrobial mechanism of nanostructures. The different proposed mechanisms are described below.

2.3.3.1 Destruction of bacterial membrane The study of the antibacterial activity of CNTs on human gut bacteria indicated that the mechanism of antibacterial activity of CNTs is a function of their diameter-dependent piercing and length-dependent wrapping on the lysis of microbial membranes, which resulted from releasing the intracellular components DNA and RNA. It can decrease the bacterial membrane potential for selective diffusion and can destruct bacteria significantly. According to the results, thin and rigid SWCNTs illustrate stronger membrane piercing on spherical bacteria than their MW counterparts (Kang et al., 2007, 2008a, 2008b, 2009a). The mechanism of antimicrobial activity of CNT is shown in Figure 2.8. According to this figure, the interaction of CNTs with bacteria can induce changes in bacterial morphology (Liu and Chen, 2012). It should be noted from the results that the CNTs physically interact with bacterial membrane and develop a pore(s) in the bacteria membrane and disrupt its integrity. The hypothesis of antimicrobial activity of SWCNTs was induced

47

Table 2.1 Antimicrobial Activities of CNTs and Their Functionalization with Different Compounds Type of Functionalization Silver nanoparticles MWNT-COOH MWNT-Dapsone MWNT-Dapsone-imine MWCNT-Dapsoneimine Copper complex Chitosan

Copper Cefalexin

Silver nanoparticles

Copper

Type of Microbes Chlorophenols Arthrobacter E. coli S. aureus E. coli S. aureus E. coli S. aureus E. coli S. aureus S. aureus E. coli Candida tropicalis E. coli Vibrio cholerae P. aeruginosa S. aureus E. coli B. subtilis S. aureus E. coli B. subtilis Salomnella Providencia Bacillus

Type of Antimicrobial Test

Value of Antimicrobial Activity

References

Inhibition zone in mm

30 mm

Gao et al. (2012)

Inhibition zone in mm Inhibition zone in mm Inhibition zone in mm Inhibition zone in mm Inhibition zone in mm Inhibition zone in mm Inhibition zone in mm Inhibition zone in mm Colony counting Colony counting Colony counting Colony counting Colony counting Colony counting (% kill) Colony counting (% kill) Colony counting (% kill) Colony counting (% kill) MIC MIC MIC MIC Colony counting (% kill rate) Colony counting (% kill rate)

8 mm 0 mm 14 mm 10 mm 12 mm 15 mm 16 mm 8 mm 4 CFU (1 3 1010) 8 CFU (1 3 1010) 2 CFU (1 3 1010) 7 CFU/100 ml 0 CFU/100 ml B80% B85% B50% B90% 1 0.13 mg/ml 0.5 mg/ml 0.25 mg/ml 99.11%

Azizian et al. (2014)

38.89%

Azizian et al. (2014) Azizian et al. (2014) Azizian et al. (2014) Venkatesan et al. (2014)

Lukhele et al. (2011) Qi et al. (2012)

Hyosuk et al. (2013)

Sunil Kumar et al. (2012)

SWCNT coupled with near-infrared radiation Functionalized with Lys

Functionalized with Arg

B. anthracis

Colonies forming (CFU/ml)

B2 3 106/ml

Dong et al. (2013)

S. typhimurium S. aureus E. coli A. niger A. fumigatus C. albicans P. chrysogenum S. cerevisiae F. culmorum M. canis T. mentagrophytes T. rubrum P. lilacinum S. typhimurium S. aureus E. coli A. niger A. fumigatus C. albicans P. chrysogenum S. cerevisiae F. culmorum M. canis T. mentagrophytes T. rubrum P. lilacinum

MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC

2 μg/ml 6 μg/ml 2 μg/ml 12 μg/ml 9 μg/ml 11 μg/ml 10.8 μg/ml 9.8 μg/ml 10.12 μg/ml 8.69 μg/ml 13.4 μg/ml 13.8 μg/ml 15.7 μg/ml 1.8 μg/ml 5.5 μg/ml 1.9 μg/ml 13 μg/ml 10 μg/ml 12 μg/ml 13.25 μg/ml 12.45 μg/ml 11.2 μg/ml 10.36 μg/ml 14.6 μg/ml 14.2 μg/ml 16.3 μg/ml

Zare-Zardini et al. (2013), Amiri et al. (2012b), Zardini et al. (2012)

Zare-Zardini et al. (2013); Amiri et al. (2012b); Zardini et al. (2012)

(Continued)

Table 2.1 Antimicrobial Activities of CNTs and Their Functionalization with Different Compounds Continued Type of Functionalization Ethanolamines

mono-

di-

tri-

Composite with PVC Porphyrin Hydroxyapatite

Type of Microbes

Type of Antimicrobial Test

Value of Antimicrobial Activity

E. coli K. pneumonia P. aeruginosa S. typhimurium B. cereus B. subtilis S. aureus S. pneumonia E. coli K. pneumonia P. aeroginosa S. typhimurium B. cereus B. subtilis S. aureus S. pneumonia E. coli K. pneumonia P. aeroginosa S. typhimurium B. cereus B. subtilis S. aureus S. pneumonia S. typhimurium S. aureus B. subtilis P. aeruginosa C. albicans

MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC MIC Inhibition zone in mm % survival MIC MIC MIC

6.32 μg/ml 5.38 μg/ml 5.23 μg/ml 8.65 μg/ml 11.86 μg/ml 12.85 μg/ml 28.12 μg/ml 10.36 μg/ml 4.23 μg/ml 3.36 μg/ml 5.15 μg/ml 8.23 μg/ml 9.32 μg/ml 9.63 μg/ml 20.4 μg/ml 9.10 μg/ml 4.22 μg/ml 2.87 μg/ml 3.12 μg/ml 6.95 μg/ml 8.2 μg/ml 7.13 μg/ml 14.22 μg/ml 7.56 μg/ml 13 mm B20% . 1000 μg/ml . 1000 μg/ml . 1000 μg/ml

References Zardini et al. (2014)

Amiri et al. (2012c) Banerjee et al. (2010) Khalid et al. (2014)

2.3 Antimicrobial Activity

FIGURE 2.8 Mechanism of antimicrobial activity of CNTs. (a) Schematic image for antimicrobial activity. (b) SEM image of damage to bacterial membrane by MWCNTs.

by the direct physical contact between bacterial cell membranes and SWCNT aggregates and then extirpation of membrane integrity. Another similar study showed that E. coli cells that adhered to the SWCNT were inactivated. This mechanism was accepted by a majority of researchers. Most attempts have proposed that the antibacterial activity of SWCNTs results from the damage to the bacterial membrane based on the direct connection between CNT and bacteria. To confirm this idea, some researchers investigated the interaction of SWCNTs and bacterial strain and effect of this nanomaterial on membrane by studying the release of internal material of bacterial cells into the environment using a UV-visible technique. From the results it is noted that the absorbance of the environment increases by 26 nm after incubation of bacteria with SWCNTs. This increase in absorbance is related to the release of DNA from bacteria into the environment. The result showed that bacterial death is directly associated with the damage to the bacterial membrane. An SEM image of incubation of SWCNTs and bacteria proved the damage to the bacterial membrane (Li et al., 2014). Recent studies indicated that the antibacterial activity of SWCNTs is dependent on the physical damage to the outer membrane of the cells. Bacterial cells may collide with CNTs by incubation of bacteria with them. The collision between bacterial cells and SWCNTs can directly damage bacterial cells (Kang et al., 2007; Rodrigues and Elimelech, 2010; Arias and Yang, 2009; Kang et al., 2008a, 2008b, 2009a).

51

52

CHAPTER 2 Functional group-dependent toxicity of CNT

2.3.3.2 Induction of oxidative stress Some studies showed that CNTs damage cell membrane as an oxidant agent and induce various oxidative stresses such as ROS stress. Moreover, CNTs can induce expression of bacterial genes that are involved in the oxidative stress response. Researchers showed that an oxidation reduction reaction occurred in SWCNTs dispersed in different solutions. Thus, the oxidative stress can be selected as the most possible mechanism for the antibacterial activity of SWCNTs. Klaine et al. (Klaine et al., 2008) have demonstrated that fullerene exerts ROS-independent oxidative stress on bacterial cells. According to some attempts, the antibacterial activities of CNTs may be partially related to oxidative stress. One of the stresses is oxidation of thiol groups by ROS or other oxidants that exist on some types of bacterial proteins. Thus, SWCNT can oxidize some proteins inside or outside of bacterial membranes. Due to the problem of penetration of SWCNTs to cells, they significantly oxidize the membrane of proteins and induce strong oxidative stress on the bacteria (Guo et al., 2007; Kang et al., 2007; Klaine et al., 2008; Pulskamp et al., 2007; Li et al., 2008; Vecitis et al., 2010).

2.3.3.3 Chemical effects Besides the physical interaction between bacteria and CNTs, some scientists claimed that chemical properties of CNTs may influence bacteria and play an essential role in inhibition of their growth (Yang et al., 2013). Because of functional groups on CNTs, specially functionalized CNTS, the chemical absorbance between CNTs and chemical groups on the membrane of bacteria is possible.

2.3.3.4 Destruction of genetic material (DNA or RNA) The unique form of CNTs can prepare conditions for CNTs entering bacterial cells and interacting with DNA or RNA. Thus, the nanostructure can disrupt the genetic structure of microbial pathogens and induce cell death (Ong et al., 2010).

2.3.3.5 Destruction of basic macromolecules In addition to the destruction of genetic structures, other biological compounds, such as coenzymes and cell wall proteins, can easily be disrupted by CNTs (Ong et al., 2010). According to Dhakras (2011) results, there are different proposed mechanisms for antimicrobial activity of nanostructures, especially CNTs. These mechanisms are shown in Figure 2.9.

2.3.4 PHYSIOCHEMICAL PROPERTIES AND ANTIMICROBIAL ACTIVITY The antimicrobial activity of CNTs is dependent on several factors. CNTs have promising physiochemical, mechanical, and thermal properties that have an

2.3 Antimicrobial Activity

FIGURE 2.9 The types of mechanisms of antimicrobial activity of CNTs.

influence on antimicrobial activity. Furthermore, physical factors such as size, electronic properties, concentration, impurities, the chemistry of solution, and incubation time all influence the antimicrobial activity of CNTs (Brady-Este´vez et al., 2008). The effects of the above-mentioned factors were studied and are described below.

2.3.4.1 Size Physiochemical properties of CNTs change with alterations to the size of the nanostructures. The size dependence of CNTs has been clearly observed in their antimicrobial activities. Kang et al. (2008a) indicated that the size (diameter) of CNTs plays a vital role in their antibacterial activities and effects. Klaine et al. (Klaine et al., 2008) compared the antibacterial activities of four stable fullerene water suspensions with various aggregate sizes. They reported that, as the size of the nanostructure decreases the antibacterial activity increases. Among two different types of CNTs (SWCNTs and MWCNTs), smaller-diameter SWCNTs have stronger antimicrobial activities than larger-diameter SW- and MWCNTs. Yang et al. (2010) examined three different lengths of SWCNTs (,1, 1 5, and B5 μm) and showed that CNTs with higher length exhibited stronger antimicrobial activity at constant weight concentrations. On the other hand, Aslan et al. (2010) suggested dissimilar results. They concluded that SWCNTs with shorter length showed stronger antimicrobial activities toward both E. coli and Staphylococcus epidermidis (Dong et al., 2012; Varghese et al., 2013; Aslan

53

54

CHAPTER 2 Functional group-dependent toxicity of CNT

et al., 2010; Kang et al., 2008a). Due to the increase in surface area of nanostructures with a decrease in size, their results may be more reasonable.

2.3.4.2 Concentration The concentration of antimicrobial agents is also a critical factor for obtaining the antimicrobial activity nanostructures. This factor is the most common factor employed to increase the antimicrobial activity of CNTs. A higher concentration of CNTs means a higher antibacterial activity, implying higher surface area. A study on functionalized SWCNTs confirmed that antimicrobial activity of SWCNT COOH and SWCNT OH increases with an increase in the concentration of CNTs. The antibacterial activities of SWCNT were investigated at different concentrations. According to the results, the antibacterial activity of SWCNTs is considerably dependent on the SWCNT concentration in suspensions. The researchers hypothesized that the higher concentration means a greater chance of contact between bacteria and CNTs, implying a higher cell death rate. As an example, when the concentration of the individually dispersed SWCNTs in Tween-20 saline solutions increases, the death rate of the microbial strain increases significantly (Arias and Yang, 2009).

2.3.4.3 Existence of impurities in CNTs For synthesis of CNTs, metals are commonly used as the catalyst. Thus, the biggest challenge in this way is the removing of metal residues from the reaction solution. This impurity induces toxicity on mammalian cells and their environment. In addition, there are various nanomaterial effects on the potency of the antimicrobial activity of CNTs. The studies in this field verified that this effect of metal is weak. For example, Kang et al. (2008b) investigated the effect of Fe as an impurity on the antimicrobial activity on MWCNT. Their results suggested that pure MWCNTs have a higher antibacterial activity than MWCNTs containing Fe residues. On the other hand, the mentioned difference was not significant. Thus, Kang et al. (2008) concluded that there is no correlation between residual metal and antibacterial activity of CNTs. Nevertheless, the metal impurity, as well as amorphous carbon, in CNTs can influence the antimicrobial activity. In another study, researchers investigated the effect of Co metal on antimicrobial activity of SWCNTs. Co was applied as the catalyst for synthesizing of SWCNTs. There was no considerable difference between SWCNT containing Co impurities and a pure sample in terms of antibacterial activity. The amount of DNA release due to puncture of the bacterial membrane was also similar. Interestingly, the obtained results were observed in low-SWCNT concentration. As the concentration enhanced, the antibacterial activity of the nanostructure solution compared to Co (NO3)2 was increased (Guo et al., 2007; Kang et al., 2008b; Wei et al., 2008).

2.3.4.4 Type of solution In CNTs antimicrobial activity studies indicate that the type of solution is one of the important factors that affects antimicrobial activity. The properties of a

2.3 Antimicrobial Activity

solution containing ionic strength, pH, and its dissolved natural organic matters are potent factors that affect antibacterial activity (Brady-Este´vez et al., 2010). Several surfactants, such as sodium dodecyl sulfate (SDS), SDBS, surfactant hydrogels, nonionic surfactants, and sodium cholate, efficiently disperse CNTs into different media, as discussed in section 2.1.1.1 (Rastogi et al., 2008; Duan et al., 2011; Botelho et al., 2011; Di Crescenzo et al., 2013). For increasing dispersibility of CNTs in common solutions such as distilled water, functionalization can be introduced as the best method. Functionalization of CNTs by different compounds and functional groups such as OH, COOH, NH2, amino acids, and hydrophilic groups can improve the solubility of CNTs in distilled water (Amiri et al., 2012b; Zare-Zardini et al., 2013; Arias and Yang, 2009). It is noteworthy to mention that antimicrobial activity of CNTs has undergone a great deal of change with a change in the base solution. According to recent results, the sensitivity of different bacterial strains to the type of solution is different so that some microbes are sensitive to some special solutions and some are sensitive to another set of solutions. Researchers investigated the antimicrobial activity of pristine and functionalized SWNCTs in various media, especially deionized water, NaCl, PBS buffer, and brain heart infusion broth. They found that the highest activities of SWCNTs were in the water and NaCl. The results showed that SWCNTs display no antimicrobial activities in PBS buffer and brain heart infusion broth. Ionic strength is a key factor affecting performance of CNT-based water. CNT filters can remove more viruses at higher ionic strengths. Different salts have diverse effects on antimicrobial activity, for example, adding CaCl2 improves the virus removal by CNT filters, whereas adding MgCl2 reduced the virus removal. The pH of a solution also influences virus removal using CNT filters. Using the solution with a pH of 3.9, CNT filters showed a higher virus removal rate than using the solution with a pH of 9.0. Researchers predicted that natural organic behavior may alter the surface charge, aggregation behavior, and mobility of CNTs in solution, thus modifying interactions between CNTs and bacteria. Conversely, a recent antimicrobial assay showed no significant differences when natural river organic matters are present. This issue is related to the low concentration of natural river organic matters presented in some studies (BradyEste´vez et al., 2010, 2010b). As an example, the antimicrobial activity of SWCNTs dispersed in Tween-20/ NaCl solutions was assessed. The results of this assessment showed that the highest exhibited antibacterial activity is related to Tween-20 NaCl solutions. According to the results, the authors suggested that the different antibacterial activities can be related to the distinct SWCNT aggregation states in these two solutions, due to numerous SWCNT aggregates that were observed during the incubation with bacteria in saline solutions but not in Tween-20 saline solutions. In one study, results showed that the release of DNA (after damage to membrane by SWCNTs) in Tween-20 saline solutions is higher than saline solutions (Shaobin, 2012).

55

56

CHAPTER 2 Functional group-dependent toxicity of CNT

2.3.4.5 Incubation period The life-time of CNTs in bacterial media affects the strength of antimicrobial activity. An increase in incubation time leads to an increase in the antimicrobial activity of CNTs. In different incubation time periods, the antimicrobial activity of CNTs is dependent on the type of bacterial strain. For example Kang et al. (2009a) showed that the destruction of Gram-positive bacteria (B. subtilis) increases with extending the incubation time from 60 to 240 min. Carboxylated and hydroxylated SWCNT also illustrated the time-dependent antimicrobial effect toward S. typhimurium in deionized water. In terms of incubation time, the time of shaking can also influence the antimicrobial activity of CNTs. Recently, researchers depicted that an increase in shaking speeds can enhance antimicrobial activity of SWCNTs significantly. It is obvious that as the movement of both SWCNTs and bacteria in a solution increases, the antimicrobial activity is also increased, which is due to the higher frequency and intensity of collisions between SWCNTs and bacteria. Liu Shaobin (2012) proposed that more physical interactions between SWCNTs and bacterial membranes result in a greater chance of membrane damage, which increases cell death rates. So, a longer time of shaking enhances these physical interactions (Dong et al., 2012; Kang et al., 2007; Arias and Yang, 2009; Vecitis et al., 2010).

2.3.5 BIOPOTENTIAL APPLICATIONS OF CNTs Due to the promising and strong antimicrobial activity of CNTs, especially SWCNTs, these materials can be used in different applications. Potential applications of these nanostructures are in numerous avenues and examples include antibacterial CNT filter and membrane, antimicrobial nanocomposites, etc. The discovery of antimicrobial activity has triggered the exploration of CNT applications in related fields.

2.3.5.1 Control of biofouling Biofilm formation around biological and environmental surfaces is one of the major problems that have challenged different science fields (Butler and Boltz, 2014; Chaturongkasumrit et al., 2011; Srey et al., 2013). Biofouling is the colonization of submerged surfaces by microorganisms such as bacteria and has destructive effects on artificial devices used in different fields (Varin et al., 2013; Yoon et al., 2013). Biofilm causes different problems such as a decrease in the halftime and efficiency of artificial devices (e.g., catheter, prosthesis and implants) and etc. (Prabhawathi et al., 2014; Li et al., 2012). There was a similar problem in different industries such as artificial membranes used in dialysis, water distillation, etc. (Marion-Ferey et al., 2003; Ramanathan et al., 2012). There are several strategies for inhibition of biofilm formation (Wang et al., 2014; Vega et al., 2014; Wang et al., 2013; Kumar et al., 2013). One of these is the use of antimicrobial agents (Atarijabarzadeh et al., 2011; van Heerden et al., 2009). Thus, researchers

2.3 Antimicrobial Activity

have tried to develop new and effective antimicrobial agents for the inhibition of biofilm formation by growth inhibition of microorganisms (Lv et al., 2014; Atarijabarzadeh et al., 2011; van Heerden et al., 2009). Antifouling coatings have important applications in the food industry and medical instruments. Nowadays, nanostructures have shown a broad spectrum of antimicrobial activities (Ramani et al., 2014; Mohan Kumar et al., 2013). CNTs are suitable compounds for inhibition of biofilm formation because of their unique antimicrobial activities. In some studies, it has been indicated that all microorganisms involved in biofouling could be effectively removed by membrane filters containing CNTs. SWCNT filters can efficiently remove various bacterial strains. Researchers showed that MWCNT filters could remove some viruses. In one study, a blend of two layers (SWCNT MWCNT) was synthesized and investigated for antifouling performance. The experimental results showed that the SWCNT MWCNT blend removes microbial pathogens more effectively than that of either SWCNT or MWCNT filter alone (Brady-Este´vez et al., 2010a). Ahmed et al. (Ahmed et al., 2011) tested the effects of SWCNTs/PVK composite films on planktonic cells and biofilms of E. coli and B. subtilis and showed that the SWCNTs/PVK composite film had antibacterial activity and potency to remove biofilms at all levels of concentrations. Functionalization of MWCNTs by antimicrobial molecules improves the antimicrobial activity. In this way, researchers found that the MWCNTs/nisin and MWCNTs/cephalexin composite films have strong antimicrobial properties (Qi et al., 2011, 2012). Rungraeng et al. applied CNTs/ polytetrafluoroethylene coating on the surface of a plate heat exchanger for inhibition of milk foulant (Rungraeng et al., 2012). In another study, CNTs/enzyme/ polymer composite films were synthesized. Because of the large surface area of CNTs, a large amount of enzymes can be loaded on this surface. The rate of enzyme proteolysis was greatly improved, which leads to the elimination of surface biofouling (Asuri et al., 2007). The decoration of CNT with other powerful antimicrobial agents such as Ag nanoparticles opens a new gateway to enhance antimicrobial activity of raw materials. Therefore, Ag-decorated MWCNTs with good dispersion in aqueous media have an excellent connection with bacteria and lead to higher antibacterial activity against biofilms (Gunawan et al., 2011). A schematic diagram of Ag/MWCNTcoated fiber membrane with antibacterial activity is shown in Figure 2.10.

2.3.5.2 Water treatment Pan and Xing (2008) showed that CNTs have higher efficiency on adsorption of various organic chemicals. These nanostructures have much higher adsorption capacity in the presence of bulky organic molecules, which can strongly adsorb different kinds of polar organic compounds. Thus, CNTs are considered as a suitable material to eliminate microbial strains from water. Moreover, oxidized (carboxylated) CNTs have presented an excellent capacity for absorbing various metal ions. Some surface functional groups, such as carboxyl, hydroxyl, and

57

58

CHAPTER 2 Functional group-dependent toxicity of CNT

FIGURE 2.10 Schematic diagram of Ag/MWCNT-coated fiber membrane with antibacterial activity.

phenol, are the major adsorption sites for metal ions and can remove these metals from water swiftly. Functionalization of CNTs with different molecule compounds can improve their antimicrobial activity along with performance of water treatment. Researchers showed that copper-treated CNTs are a suitable candidate for the removal of impurities throughout water (Upadhyayula et al., 2009). According to their results, Cu-treated MWCNTs were applied for water treatment and as an antibacterial material, obtaining great results in terms of antibacterial activity as well as water treatment. The Cu-treated MWCNTs plates can easily destroy most of the bacteria in a short period of time (Zeino et al., 2014). CNTs were also applied in membrane technologies for water treatment in desalination. This novel kind of membrane can remove both salts and microbial impurities (Das et al., 2014). These membranes are also very appropriate for desalination of both sea and brackish water (Figure 2.11). In order to control different kinds of impurities and microbial pathogens, CNT membranes can be utilized as the filter with antimicrobial activity, which can be a good replacement for chemical disinfectants (Savage and Diallo, 2005; Li et al., 2008; Nepal et al., 2008). Interestingly, different CNTs have prevented the formation of harmful byproducts (DBPs) such as trihalomethanes, haloacetic acids, and aldehydes, because they do not have strong oxidation tendency and are relatively inert in water (Ong et al., 2010).

2.3.5.3 Antimicrobial CNTs nanocomposites Various CNT polymer composites have been studied in terms of antimicrobial activity due to promising properties of CNTs. Nylon nanocompsite fibers infused with silver-decorated CNTs (CNT-Ag) are one of the composites that inhibit a majority of common microbial pathogens. CNT-Ag demonstrated great antimicrobial activity against common bacterial pathogens including Streptococcus

2.3 Antimicrobial Activity

FIGURE 2.11 Schematic of CNT membranes for water treatment.

pyogenes, S. aureus, Salmonella enterica, serovar Typhimurium and E. coli (Vijaya et al., 2010). Sule et al. (Sule et al., 2014) synthesized the CNT Cu nanocomposites to employ them in antimicrobial applications. Also, the antimicrobial activity of Cu powder at different concentrations was investigated against Providencia and Bacillus bacteria. This article suggests that CNT Cu nanocomposites may be utilized in the antibacterial controlling systems. They can be employed as an effective growth inhibitor against various microorganisms. Aslan et al. synthesized thin films by dispersed SWCNTs in PLGA. The SWCNT PLGA film can be coated on coverglasses and effectively decreases the growth of E. coli and S. epidermidis. Also, Aslan et al. (Aslan et al., 2010) used SWCNTs in electrospun polysulfone mats and applied them as a coating. The polymer mats with a low amount of SWCNTs showed strong antimicrobial activities against E. coli. A new film was designed with a blend of SWCNT, DNA, and lysozyme by Nepal et al. This composite showed long-term antimicrobial activities (Davis et al., 2009; Nepal et al., 2011). Composites including CNTs-Ag can be used as a bactericidal agent. The synthesized composite was prepared through a combination of SWCNTs and MWCNTs. The SWCNT amphiphile AgNP nanohybrids also exhibited significant killing ability against all bacteria (Larrude et al., 2014; Brahmachari et al.; Akhavan et al., 2011). Nanocomposites prepared by a combination of CNTs and titanium dioxide have shown a great of antimicrobial activity and are a promising material for coatings (Akhavan et al., 2010).

59

60

CHAPTER 2 Functional group-dependent toxicity of CNT

FIGURE 2.12 Antimicrobial activity of a new PVC nanocomposite contining MWCNTs.

The present authors (Amiri et al., 2012c) have reported a new antimicrobial PVC nanocomposite comprising of MWCNTs. The synthesized nanocomposite has a strong antimicrobial activity against some bacterial strains (Figure 2.12). These researchers have suggested that this new invention be used as a coating for different surfaces, such as windows, walls, etc., especially for isolation rooms in research environments, hospitals, etc. Banerjee et al. (2010) reported antimicrobial nanocomposite films (Figure 2.13) that were composed of MWCNTs and protoporphyrin IX (PPIX). This nanocomposite has effective antimicrobial activity against S. aureus. The conjugates of MWCNTs and PPIX effectively deactivate S. aureus in solution upon irradiation with visible light.

2.4 CONCLUSIONS In this chapter, the investigation reports on different methods of functionalization with various functional groups are systematically presented. Antibacterial activity of CNTs, mechanisms of this activity, and different applications of CNTs as antimicrobial agents are reviewed. According to the different studies, CNTs have strong antimicrobial activities against different pathogens. Studies showed that some factors, such as concentration, diameter, length, aggregation, functional groups, type of solution, and incubation time, influence the antimicrobial activity of CNTs. Functionalization of CNTs by amino acids, metals, nanoparticles, antibiotics, peptides, etc. improves their antimicrobial

Acknowledgments

FIGURE 2.13 Schematic of CNT porphyrin conjugates as an antimicrobial nanocomposite.

activity. Individually dispersed SWCNTs showed a higher antibacterial activity compared to the SWCNT aggregates. Different studies showed that the most possible hypothesis for antimicrobial activity of CNTs is bacterial death caused by damage to the cell membrane. In this hypothesis, it was mentioned that bacterial membranes were severely damaged with release of intracellular contents after incubation with CNTs. The volume and height of bacterial cells also decreased. Due to the antimicrobial activity of CNTs, these nanostructures can be applied in different cases, such as antimicrobial nonocomposites, water purification, antifouling agents, etc.

ACKNOWLEDGMENTS The authors gratefully acknowledge High Impact Research Grant UM.C/625/1/HIR/ MOHE/ENG/45 and UMRG Grant RP012B-13AET, Faculty of Engineering, University of Malaya, Malaysia for support to conduct this research work.

61

62

CHAPTER 2 Functional group-dependent toxicity of CNT

REFERENCES Ahmed, F., Santos, C.M., Vergara, R.A.M.V., Tria, M.C.R., Advincula, R., Rodrigues, D.F., 2011. Antimicrobial applications of electroactive PVK-SWNT nanocomposites. Environ. Sci. Technol. 46, 1804 1810. Akhavan, O., Azimirad, R., Safa, S., Larijani, M.M., 2010. Visible light photo-induced antibacterial activity of CNT-doped TiO2 thin films with various CNT contents. J. Mater. Chem. 20, 7386 7392. Akhavan, O., Abdolahad, M., Abdi, Y., Mohajerzadeh, S., 2011. Silver nanoparticles within vertically aligned multi-wall carbon nanotubes with open tips for antibacterial purposes. J. Mater. Chem. 21, 387 393. Amiri, A., Maghrebi, M., Baniadam, M., Zeinali Heris, S., 2011. One-pot, efficient functionalization of multi-walled carbon nanotubes with diamines by microwave method. Appl. Surf. Sci. 257, 10261 10266. Amiri, A., Shanbedi, M., Eshghi, H., Heris, S.Z., Baniadam, M., 2012a. Highly dispersed multiwalled carbon nanotubes decorated with Ag nanoparticles in water and experimental investigation of the thermophysical properties. J. Phys. Chem. C 116, 3369 3375. Amiri, A., Zardini, H.Z., Shanbedi, M., Maghrebi, M., Baniadam, M., Tolueinia, B., 2012b. Efficient method for functionalization of carbon nanotubes by lysine and improved antimicrobial activity and water-dispersion. Mater. Lett. 72, 153 156. Amiri, A., Zare-Zardini, H., Shanbedi, M., 2012c. Antimicrobial polyvinyl chloride composite (Iran patent). Industrial Property General Office-state organization for registration of deeds and properties, No. 74061. Amiri, A., Memarpoor-Yazdi, M., Shanbedi, M., Eshghi, H., 2013. Influence of different amino acid groups on the free radical scavenging capability of multi walled carbon nanotubes. J. Biomed. Mater. Res. Part A 101A, 2219 2228. Amiri, A., Shanbedi, M., Amiri, H., Heris, S.Z., Kazi, S.N., Chew, B.T., et al., 2014. Pool boiling heat transfer of CNT/water nanofluids. Appl. Therm. Eng. 71, 450 459. Amiri, A., Sadri, R., Ahmadi, G., Chew, B., Kazi, S., Shanbedi, M., et al., 2015a. Synthesis of polyethylene glycol-functionalized multi-walled carbon nanotubes with a microwave-assisted approach for improved heat dissipation. RSC Adv. 5, 35425 35434. Amiri, A., Sadri, R., Shanbedi, M., Ahmadi, G., Chew, B., Kazi, S., et al., 2015b. Performance dependence of thermosyphon on the functionalization approaches: an experimental study on thermo-physical properties of graphene nanoplatelet-based water nanofluids. Energy Convers. Manage. 92, 322 330. Arias, L.R., Yang, L., 2009. Inactivation of bacterial pathogens by carbon nanotubes in suspensions. Langmuir 25, 3003 3012. Aslan, S., Loebick, C.Z., Kang, S., Elimelech, M., Pfefferle, L.D., Van Tassel, P.R., 2010. Antimicrobial biomaterials based on carbon nanotubes dispersed in poly(lactic-coglycolic acid). Nanoscale 2, 1789 1794. Asuri, P., Karajanagi, S.S., Kane, R.S., Dordick, J.S., 2007. Polymer nanotube enzyme composites as active antifouling films. Small 3, 50 53. Atarijabarzadeh, S., Stro¨mberg, E., Karlsson, S., 2011. Inhibition of biofilm formation on silicone rubber samples using various antimicrobial agents. Int. Biodeterior. Biodegradation 65, 1111 1118.

References

Azizi, M., Hosseini, M., Zafarnak, S., Shanbedi, M., Amiri, A., 2013. Experimental analysis of thermal performance in a two-phase closed thermosiphon using graphene/water nanofluid. Ind. Eng. Chem. Res. 52, 10015 10021. Azizian, J., Hekmati, M., Dadras, O.G., 2014. Functionalization of carboxylated multiwall nanotubes with dapsone derivatives and study of their antibacterial activities against E. coli and S. aureus. Orient. J. Chem. 30 (2), 667 673. Banerjee, I., Mondal, D., Martin, J., Kane, R.S., 2010. Photoactivated antimicrobial activity of carbon nanotube 2 porphyrin conjugates. Langmuir 26, 17369 17374. Barisci, J.N., Tahhan, M., Wallace, G.G., Badaire, S., Vaugien, T., Maugey, M., et al., 2004. Properties of carbon nanotube fibers spun from DNA-stabilized dispersions. Adv. Funct. Mater. 14, 133 138. Benincasa, M., Pacor, S., Wu, W., Prato, M., Bianco, A., Gennaro, R., 2010. Antifungal activity of Amphotericin B conjugated to carbon nanotubes. ACS Nano 5, 199 208. Botelho, E.C., Edwards, E.R., Bittmann, B., Burkhart, T., 2011. Dispersing carbon nanotubes in phenolic resin using an aqueous solution. J. Braz. Chem. Soc. 22, 2040 2047. Brady-Este´vez, A.S., Kang, S., Elimelech, M., 2008. A single-walled-carbon-nanotube filter for removal of viral and bacterial pathogens. Small 4, 481 484. Brady-Este´vez, A.S., Nguyen, T.H., Gutierrez, L., Elimelech, M., 2010. Impact of solution chemistry on viral removal by a single-walled carbon nanotube filter. Water Res. 44, 3773 3780. Brady-Este´vez, A.S., Schnoor, M.H., Kang, S., Elimelech, M., 2010a. SWNT MWNT hybrid filter attains high viral removal and bacterial inactivation. Langmuir 26, 19153 19158. Brady-Este´vez, A.S., Schnoor, M.H., Vecitis, C.D., Saleh, N.B., Elimelech, M., 2010b. Multiwalled carbon nanotube filter: improving viral removal at low pressure. Langmuir 26, 14975 14982. Brahmachari, S., Mandal, S.K., Das, P.K., 2014. Fabrication of SWCNT-Ag nanoparticle hybrid included self-assemblies for antibacterial applications. PLoS One 9, e106775 e106785. Butler, C.S., Boltz, J.P., 2014. 3.6 Biofilm processes and control in water and wastewater treatment. In: Ahuja, S. (Ed.), Comprehensive Water Quality and Purification. Elsevier, Waltham. Chaturongkasumrit, Y., Takahashi, H., Keeratipibul, S., Kuda, T., Kimura, B., 2011. The effect of polyesterurethane belt surface roughness on Listeria monocytogenes biofilm formation and its cleaning efficiency. Food Control 22, 1893 1899. Chen, R., Zhang, Y., Wang, D., Dai, H., 2001. Noncovalent sidewall functionalization of single-walled carbon nanotubes for protein immobilization. J. Am. Chem. Soc. 123, 3838 3839. Chichak, K.S., Star, A., Altoe, M.V.P., Stoddart, J.F., 2005. Single-walled carbon nanotubes under the influence of dynamic coordination and supramolecular chemistry. Small 1, 452 461. Dalton, A.B., Stephan, C., Coleman, J.N., McCarthy, B., Ajayan, P.M., Lefrant, S., et al., 2000. Selective interaction of a semiconjugated organic polymer with single-wall nanotubes. J. Phys. Chem. B 104, 10012 10016. Das, R., Ali, M.E., Hamid, S.B.A., Ramakrishna, S., Chowdhury, Z.Z., 2014. Carbon nanotube membranes for water purification: a bright future in water desalination. Desalination 336, 97 109.

63

64

CHAPTER 2 Functional group-dependent toxicity of CNT

Davis, V.A., Simonian, A.L., Nepal, D., Balasubramanian, S., 2010. Preparation of precisely controlled thin film nanocomposite of carbon nanotubes and biomaterials (US Patent), No. US20100028960 A1. De Azeredo, H.M.C., 2013. Antimicrobial nanostructures in food packaging. Trends Food Sci. Technol. 30, 56 69. Dhakras, P.A. 2011. Nanotechnology applications in water purification and waste water treatment: a review. Nanoscience, Engineering and Technology (ICONSET), 2011 International Conference, November 28 30, 2011, 285 291. Di Crescenzo, A., Bardini, L., Sinjari, B., Traini, T., Marinelli, L., Carraro, M., et al., 2013. Surfactant hydrogels for the dispersion of carbon-nanotube-based catalysts. Chem. Eur. J. 19, 16415 16423. Dong, L., Henderson, A., Field, C., 2012. Antimicrobial activity of single-walled carbon nanotubes suspended in different surfactants. J. Nanotechnol. 2012. Dong, X., Tang, Y., Wu, M., Vlahovic, B., Yang, L., 2013. Dual effects of single-walled carbon nanotubes coupled with near-infrared radiation on Bacillus anthracis spores: inactivates spores and stimulates the germination of surviving spores. J. Biol. Eng. 7, 1 12. Du, J., Wang, S., You, H., Zhao, X., 2013. Understanding the toxicity of carbon nanotubes in the environment is crucial to the control of nanomaterials in producing and processing and the assessment of health risk for human: a review. Environ. Toxicol. Pharmacol. 36, 451 462. Duan, W.H., Wang, Q., Collins, F., 2011. Dispersion of carbon nanotubes with SDS surfactants: a study from a binding energy perspective. Chem. Sci. 2, 1407 1413. Dumlich, H., Reich, S., 2011. Nanotube bundles and tube-tube orientation: a van der Waals density functional study. Phys. Rev. B, 84. Fedorka-Cray, P.J., 2014. Microorganisms and resistance to antibiotics, the ubiquity of antibiotic resistance by microorganisms. In: Dikeman, M., Devine, C. (Eds.), Encyclopedia of Meat Sciences, second ed. Academic Press, Oxford. Furtado, C.A., Kim, U.J., Gutierrez, H.R., Pan, L., Dickey, E.C., Eklund, P.C., 2004. Debundling and dissolution of single-walled carbon nanotubes in amide solvents. J. Am. Chem. Soc. 126, 6095 6105. Gao, G.-H., Lei, Y.-H., Dong, L.-H., Liu, W.-C., Wang, X.-F., Chang, X.-T., et al., 2012. Synthesis of nanocomposites of silver nanoparticles with medical stone and carbon nanotubes for their antibacterial applications. Mater. Express 2, 85 93. Ghiadi, B., Baniadam, M., Maghrebi, M., Amiri, A., 2013. Rapid, one-pot synthesis of highly-soluble carbon nanotubes functionalized by L-arginine. Russ. J. Phys. Chem. A 87, 649 653. Giri, S., 2014. 3 - Nanotoxicity: aspects and concerns in biological systems. In: Das, S. (Ed.), Microbial Biodegradation and Bioremediation. Elsevier, Oxford. Gooding, J.J., 2005. Nanostructuring electrodes with carbon nanotubes: a review on electrochemistry and applications for sensing. Electrochim. Acta 50, 3049 3060. Gu, L., Elkin, T., Jiang, X., Li, H., Lin, Y., Qu, L., et al., 2005. Single-walled carbon nanotubes displaying multivalent ligands for capturing pathogens. Chem. Commun. 874 876. Guldi, D.M., Taieb, H., Rahman, G.M.A., Tagmatarchis, N., Prato, M., 2005. Novel photoactive single-walled carbon nanotube porphyrin polymer wraps: efficient and long-lived intracomplex charge separation. Adv. Mater. 17, 871 875.

References

Gunawan, P., Guan, C., Song, X., Zhang, Q., Leong, S.S.J., Tang, C., et al., 2011. Hollow fiber membrane decorated with Ag/MWNTs: toward effective water disinfection and biofouling control. ACS Nano 5, 10033 10040. Guo, L., Morris, D.G., Liu, X., Vaslet, C., Hurt, R.H., Kane, A.B., 2007. Iron bioavailability and redox activity in diverse carbon nanotube samples. Chem. Mater. 19, 3472 3478. Hamon, M.A., Hui, H., Bhowmik, P., Itkis, H.M.E., Haddon, R.C., 2002. Esterfunctionalized soluble single-walled carbon nanotubes. Appl. Phys. A 74, 333 338. He, H., Pham-Huy, L.A., Dramou, P., Xiao, D., Zuo, P., Pham-Huy, C., 2013. Carbon nanotubes: applications in pharmacy and medicine. BioMed. Res. Int. 2013, 12. Heinemann, J.A., Ankenbauer, R.G., Ama´bile-Cuevas, C.F., 2000. Do antibiotics maintain antibiotic resistance? Drug Discov. Today 5, 195 204. Hertel, T., Walkup, R.E., Avouris, P., 1998. Deformation of carbon nanotubes by surface van der Waals forces. Phys. Rev. B 58, 13870 13873. Hirsch, A., Vostrowsky, O., 2005. Functionalization of carbon nanotubes. In: Schluter, A.D. (Ed.), Functional Molecular Nanostructures. Springer, Berlin Heidelberg. Huang, Y.Y., Terentjev, E.M., 2012. Dispersion of carbon nanotubes: mixing, sonication, stabilization, and composite properties. Polymers 4, 275 295. Hyosuk, Y., Ji Dang, K., Hyun Chul, C., Chul Won, L., 2013. Antibacterial activity of CNT-Ag and GO-Ag nanocomposites against gram-negative and gram-positive bacteria. Bull. Korean Chem. Soc. 34, 3261 3264. Iqbal, J., Jan, T., Ismail, M., Ahmad, N., Arif, A., Khan, M., et al., 2014. Influence of Mg doping level on morphology, optical, electrical properties and antibacterial activity of ZnO nanostructures. Ceram. Int. 40, 7487 7493. Islam, M.F., Rojas, E., Bergey, D.M., Johnson, A.T., Yodh, A.G., 2003. High weight fraction surfactant solubilization of single-wall carbon nanotubes in water. Nano Lett. 3, 269 273. Kalita, G., Adhikari, S., Aryal, H.R., Ghimre, D.C., Afre, R., Soga, T., et al., 2008. Fluorination of multi-walled carbon nanotubes (MWNTs) via surface wave microwave (SW-MW) plasma treatment. Phys. E 41, 299 303. Kang, S., Pinault, M., Pfefferle, L.D., Elimelech, M., 2007. Single-walled carbon nanotubes exhibit strong antimicrobial activity. Langmuir 23, 8670 8673. Kang, S., Herzberg, M., Rodrigues, D.F., Elimelech, M., 2008a. Antibacterial effects of carbon nanotubes: size does matter! Langmuir 24, 6409 6413. Kang, S., Mauter, M.S., Elimelech, M., 2008b. Physicochemical determinants of multiwalled carbon nanotube bacterial cytotoxicity. Environ. Sci. Technol. 42, 7528 7534. Kang, S., Mauter, M.S., Elimelech, M., 2009a. Microbial cytotoxicity of carbon-based nanomaterials: implications for river water and wastewater effluent. Environ. Sci. Technol. 43, 2648 2653. Kang, Y., Liu, Y.-C., Wang, Q., Shen, J.-W., Wu, T., Guan, W.-J., 2009b. On the spontaneous encapsulation of proteins in carbon nanotubes. Biomaterials 30, 2807 2815. Khalid, P., Hussain, M.A., Rekha, P.D., Sanal, C., Suraj, S., Rajashekhar, M., et al., 2014. Interaction of carbon nanotubes reinforced hydroxyapatite composite with bacillus subtilis, P. aeruginosa and C. albicans. Indian J. Sci. Technol. 7, 678 684. Klaine, S.J., Alvarez, P.J.J., Batley, G.E., Fernandes, T.F., Handy, R.D., Lyon, D.Y., et al., 2008. Nanomaterials in the environment: behavior, fate, bioavailability, and effects. Environ. Toxicol. Chem. 27, 1825 1851.

65

66

CHAPTER 2 Functional group-dependent toxicity of CNT

Kumar, L., Chhibber, S., Harjai, K., 2013. Zingerone inhibit biofilm formation and improve antibiofilm efficacy of ciprofloxacin against Pseudomonas aeruginosa PAO1. Fitoterapia 90, 73 78. Larrude, D.G., Maia Da Costa, M.E.H., Freire, F.L., 2014. Synthesis and characterization of silver nanoparticle-multiwalled carbon nanotube composites. J. Nanomater. 2014, 7. Li, A., Wang, L., Li, M., Xu, Z., Li, P., Zhang, Z., 2014. The antibacterial activity of covalent-functionalized carbon nanotubes against Escherichia coli. Dig. J. Nanomater. Biostruct. 9, 599 607. Li, H., Zhou, B., Lin, Y., Gu, L., Wang, W., Fernando, K.A.S., et al., 2004. Selective interactions of porphyrins with semiconducting single-walled carbon nanotubes. J. Am. Chem. Soc. 126, 1014 1015. Li, J., Hirota, K., Goto, T., Yumoto, H., Miyake, Y., Ichikawa, T., 2012. Biofilm formation of Candida albicans on implant overdenture materials and its removal. J. Dent. 40, 686 692. Li, Q., Mahendra, S., Lyon, D.Y., Brunet, L., Liga, M.V., Li, D., et al., 2008. Antimicrobial nanomaterials for water disinfection and microbial control: potential applications and implications. Water Res. 42, 4591 4602. Liu, L., Wang, T., Li, J., Guo, Z.-X., Dai, L., Zhang, D., et al., 2003. Self-assembly of gold nanoparticles to carbon nanotubes using a thiol-terminated pyrene as interlinker. Chem. Phys. Lett. 367, 747 752. Liu, S., Chen, Y., 2012. Antimicrobial activity of carbon nanotubes. Antimicrobial Drug Discovery: Emerging Strategies. CAB International (Chapter 22). Liu, S., Wei, L., Hao, L., Fang, N., Chang, M.W., Xu, R., et al., 2009. Sharper and faster “nano darts” kill more bacteria: a study of antibacterial activity of individually dispersed pristine single-walled carbon nanotube. ACS Nano 3, 3891 3902. Liu, S., Ng, A.K., Xu, R., Wei, J., Tan, C.M., Yang, Y., et al., 2010. Antibacterial action of dispersed single-walled carbon nanotubes on Escherichia coli and Bacillus subtilis investigated by atomic force microscopy. Nanoscale 2, 2744 2750. Lukhele, L.P., Krause, R.W.M., Nhlabatsi, Z.P., Mamba, B.B., Momba, M.N.B., 2011. Copper and silver impregnated carbon nanotubes incorporated into cyclodextrin polyurethanes for the removal of bacterial and organic pollutants in water. Desalin. Water Treat. 27, 299 307. Luo, P.G., Wang, H., Gu, L., Lu, F., Lin, Y., Christensen, K.A., et al., 2009. Selective interactions of sugar-functionalized single-walled carbon nanotubes with bacillus spores. ACS Nano 3, 3909 3916. Lv, H.B., Chen, Z., Yang, X.P., Cen, L., Zhang, X., Gao, P., 2014. Layer-by-layer selfassembly of minocycline-loaded chitosan/alginate multilayer on titanium substrates to inhibit biofilm formation. J. Dent. 42, 1464 1472. Marion-Ferey, K., Pasmore, M., Stoodley, P., Wilson, S., Husson, G.P., Costerton, J.W., 2003. Biofilm removal from silicone tubing: an assessment of the efficacy of dialysis machine decontamination procedures using an in vitro model. J. Hosp. Infect. 53, 64 71. McCarthy, B., Coleman, J.N., Curran, S.A., Dalton, A.B., Davey, A.P., Konya, Z., et al., 2000. Observation of site selective binding in a polymer nanotube composite. J. Mater. Sci. Lett. 19, 2239 2241. Mohan, R., Shanmugharaj, A.M., Sung Hun, R., 2011. An efficient growth of silver and copper nanoparticles on multiwalled carbon nanotube with enhanced antimicrobial activity. J. Biomed. Mater. Res. Part B 96B, 119 126.

References

Mohan Kumar, K., Mandal, B.K., Appala Naidu, E., Sinha, M., Siva Kumar, K., Sreedhara Reddy, P., 2013. Synthesis and characterisation of flower shaped zinc oxide nanostructures and its antimicrobial activity. Spectrochim. Acta, Part A 104, 171 174. Murakami, H., Nakashima, N., 2006. Soluble carbon nanotubes and their applications. J. Nanosci. Nanotechnol. 6, 16 27. Murakami, H., Nomura, T., Nakashima, N., 2003. Noncovalent porphyrin-functionalized single-walled carbon nanotubes in solution and the formation of porphyrin nanotube nanocomposites. Chem. Phys. Lett. 378, 481 485. Murphy, R., Coleman, J.N., Cadek, M., McCarthy, B., Bent, M., Drury, A., et al., 2002. High-yield, nondestructive purification and quantification method for multiwalled carbon nanotubes. J. Phys. Chem. B 106, 3087 3091. Nakashima, N., Tomonari, Y., Murakami, H., 2002. Water-soluble single-walled carbon nanotubes via noncovalent sidewall-functionalization with a pyrene-carrying ammonium ion. Chem. Lett. 31, 638 639. Nepal, D., Balasubramanian, S., Simonian, A.L., Davis, V.A., 2008. Strong antimicrobial coatings: single-walled carbon nanotubes armored with biopolymers. Nano Lett. 8, 1896 1901. Nepal, D., Minus, M.L., Kumar, S., 2011. Lysozyme coated DNA and DNA/SWNT fibers by solution spinning. Macromol. Biosci. 11, 875 881. Niyogi, S., Hamon, M.A., Hu, H., Zhao, B., Bhowmik, P., Sen, R., et al., 2002. Chemistry of single-walled carbon nanotubes. Acc. Chem. Res. 35, 1105 1113. Novelline, R.A., 1997. Squire’s Fundamentals of Radiology, fifth ed. Harvard University Press. Ong, Y.T., Ahmad, A.L., Zein, S.H.S., Tan, S.H., 2010. A review on carbon nanotubes in an environmental protection and green engineering perspective. Braz. J. Chem. Eng. 27, 227 242. Pan, B., Xing, B., 2008. Adsorption mechanisms of organic chemicals on carbon nanotubes. Environ. Sci. Technol. 42, 9005 9013. Pantarotto, D., Partidos, C.D., Hoebeke, J., Brown, F., Kramer, E., Briand, J.-P., et al., 2003. Immunization with peptide-functionalized carbon nanotubes enhances virusspecific neutralizing antibody responses. Chem. Biol. 10, 961 966. Petersen, E.J., 2014. 9 - Ecotoxicological effects of carbon nanotubes: test methods and current research. In: Njuguna, J., Pielichowski, K., Zhu, H. (Eds.), Health and Environmental Safety of Nanomaterials. Woodhead Publishing. Prabhawathi, V., Thirunavukarasu, K., Doble, M., 2014. A study on the long term effect of biofilm produced by biosurfactant producing microbe on medical implant. Mater. Sci. Eng. C 40, 212 218. Pulskamp, K., Diabate, S., Krug, H.F., 2007. Carbon nanotubes show no sign of acute toxicity but induce intracellular reactive oxygen species in dependence on contaminants. Toxicol. Lett. 168, 58 74. Qi, X., Poernomo, G., Wang, K., Chen, Y., Chan-Park, M.B., Xu, R., et al., 2011. Covalent immobilization of nisin on multi-walled carbon nanotubes: superior antimicrobial and anti-biofilm properties. Nanoscale 3, 1874 1880. Qi, X., Gunawan, P., Xu, R., Chang, M.W., 2012. Cefalexin-immobilized multi-walled carbon nanotubes show strong antimicrobial and anti-adhesion properties. Chem. Eng. Sci. 84, 552 556.

67

68

CHAPTER 2 Functional group-dependent toxicity of CNT

Qu, X., Alvarez, P.J.J., Li, Q., 2013. Applications of nanotechnology in water and wastewater treatment. Water Res. 47, 3931 3946. Ramanathan, V., Riosa, S., Al-Sharif, A.H., Mansouri, M.D., Tranchina, A., Kayyal, T., et al., 2012. Characteristics of biofilm on tunneled cuffed hemodialysis catheters in the presence and absence of clinical infection. Am. J. Kidney Dis. 60, 976 982. Ramani, M., Ponnusamy, S., Muthamizhchelvan, C., Marsili, E., 2014. Amino acidmediated synthesis of zinc oxide nanostructures and evaluation of their facet-dependent antimicrobial activity. Colloids Surf. B Biointerfaces 117, 233 239. Rastogi, R., Kaushal, R., Tripathi, S.K., Sharma, A.L., Kaur, I., Bharadwaj, L.M., 2008. Comparative study of carbon nanotube dispersion using surfactants. J. Colloid Interface Sci. 328, 421 428. Rodrigues, D.F., Elimelech, M., 2010. Toxic effects of single-walled carbon nanotubes in the development of E. coli biofilm. Environ. Sci. Technol. 44, 4583 4589. Rungraeng, N., Cho, Y.-C., Yoon, S.H., Jun, S., 2012. Carbon nanotubepolytetrafluoroethylene nanocomposite coating for milk fouling reduction in plate heat exchanger. J. Food Eng. 111, 218 224. Savage, N., Diallo, M., 2005. Nanomaterials and water purification: opportunities and challenges. J. Nanopart. Res. 7, 331 342. Sayes, C.M., Liang, F., Hudson, J.L., Mendez, J., Guo, W., Beach, J.M., et al., 2006. Functionalization density dependence of single-walled carbon nanotubes cytotoxicity in vitro. Toxicol. Lett. 161, 135 142. Shanbedi, M., Heris, S.Z., Baniadam, M., Amiri, A., Maghrebi, M., 2011. Investigation of heat-transfer characterization of EDA-MWCNT/DI-water nanofluid in a two-phase closed thermosyphon. Ind. Eng. Chem. Res. 51, 1423 1428. Shanbedi, M., Zeinali Heris, S., Baniadam, M., Amiri, A., 2013. The effect of multi-walled carbon nanotube/water nanofluid on thermal performance of a two-phase closed thermosyphon. Exp. Heat Transfer 26, 26 40. Shanbedi, M., Heris, S.Z., Amiri, A., Baniadam, M., 2014. Improvement in heat transfer of a two-phased closed thermosyphon using silver-decorated MWCNT/water. J. Dispers. Sci. Technol. 35, 1086 1096. Shanbedi, M., Amiri, A., Rashidi, S., Heris, S.Z., Baniadam, M., 2015. Thermal performance prediction of two-phase closed thermosyphon using adaptive neuro-fuzzy inference system. Heat Transfer Eng. 36, 315 324. Shao, W., Arghya, P., Yiyong, M., Rodes, L. Prakash, S. 2013. Carbon Nanotubes for Use in Medicine: Potentials and Limitations. Shaobin, L. 2012. Antibacterial Activity of Carbon Nanomaterials (Thesis). School of Chemical and Biomedical Engineering. Nanyang Technological University. Srey, S., Jahid, I.K., Ha, S.-D., 2013. Biofilm formation in food industries: a food safety concern. Food Control 31, 572 585. Sule, R., Olubambi, P.A., Sigalas, I., Asante, J.K.O., Garrett, J.C., 2014. Effect of SPS consolidation parameters on submicron Cu and Cu CNT composites for thermal management. Powder Technol. 258, 198. Sunil Kumar, S., Maneet, L., Lata, Soumya Ranjan, K., Rakesh Behari, M., 2012. Synthesis of Cu/CNTs nanocomposites for antimicrobial activity. Adv. Nat. Sci. Nanosci. Nanotechnol. 3, 045011. Tasis, D., Tagmatarchis, N., Bianco, A., Prato, M., 2006. Chemistry of carbon nanotubes. Chem. Rev. 106, 1105 1136.

References

Thostenson, E.T., Ren, Z., Chou, T.-W., 2001. Advances in the science and technology of carbon nanotubes and their composites: a review. Compos. Sci. Technol. 61, 1899 1912. Tsang, S.C., Davis, J.J., Green, M.L.H., Hill, H.A.O., Leung, Y.C., Sadler, P.J., et al., 1995. Corrigenda. J. Chem. Soc. Chem. Commun. 2579 2580. Upadhyayula, V.K.K., Deng, S., Mitchell, M.C., Smith, G.B., 2009. Application of carbon nanotube technology for removal of contaminants in drinking water: a review. Sci. Total Environ. 408, 1 13. van Heerden, J., Turner, M., Hoffmann, D., Moolman, J., 2009. Antimicrobial coating agents: can biofilm formation on a breast implant be prevented? J. Plast. Reconstr. Aesthet. Surg. 62, 610 617. Varghese, S., Kuriakose, S., Jose, S., 2013. Antimicrobial activity of carbon nanoparticles isolated from natural sources against pathogenic gram-negative and gram-positive bacteria. J. Nanosci. 2013, 5. Varin, K.J., Lin, N.H., Cohen, Y., 2013. Biofouling and cleaning effectiveness of surface nanostructured reverse osmosis membranes. J. Memb. Sci. 446, 472 481. Vecitis, C.D., Zodrow, K.R., Kang, S., Elimelech, M., 2010. Electronic-structure-dependent bacterial cytotoxicity of single-walled carbon nanotubes. ACS Nano 4, 5471 5479. Vega, L.M., Mathieu, J., Yang, Y., Pyle, B.H., Mclean, R.J.C., Alvarez, P.J.J., 2014. Nickel and cadmium ions inhibit quorum sensing and biofilm formation without affecting viability in Burkholderia multivorans. Int. Biodeterior. Biodegradation 91, 82 87. Venkatesan, J., Jayakumar, R., Mohandas, A., Bhatnagar, I., Kim, S.-K., 2014. Antimicrobial activity of chitosan-carbon nanotube hydrogels. Materials 7, 3946 3955. Vijaya, K.R., Ghouse, M.M., Shaik, J., Angel, H., Komal, V., Shree Ram, S., et al., 2010. Synthesis of Ag/CNT hybrid nanoparticles and fabrication of their nylon-6 polymer nanocomposite fibers for antimicrobial applications. Nanotechnology 21, 095102. Viksveen, P., 2003. Antibiotics and the development of resistant microorganisms. Can homeopathy be an alternative? Homeopathy 92, 99 107. Wahab, R., Khan, S.T., Dwivedi, S., Ahamed, M., Musarrat, J., Al-Khedhairy, A.A., 2013. Effective inhibition of bacterial respiration and growth by CuO microspheres composed of thin nanosheets. Colloids Surf. B Biointerfaces 111, 211 217. Wang, H., Gu, L., Lin, Y., Lu, F., Meziani, M.J., Luo, P.G., et al., 2006. Unique aggregation of anthrax (bacillus anthracis) spores by sugar-coated single-walled carbon nanotubes. J. Am. Chem. Soc. 128, 13364 13365. Wang, H.-H., Ye, K.-P., Zhang, Q.-Q., Dong, Y., Xu, X.-L., Zhou, G.-H., 2013. Biofilm formation of meat-borne Salmonella enterica and inhibition by the cell-free supernatant from Pseudomonas aeruginosa. Food Control 32, 650 658. Wang, K., Yan, J., Dang, W., Xie, J., Yan, B., Yan, W., et al., 2014. Dual antifungal properties of cationic antimicrobial peptides polybia-MPI: membrane integrity disruption and inhibition of biofilm formation. Peptides 56, 22 29. Wei, L., Wang, B., Wang, Q., Li, L.-J., Yang, Y., Chen, Y., 2008. Effect of centrifugation on the purity of single-walled carbon nanotubes from MCM-41 containing cobalt. J. Phys. Chem. C 112, 17567 17575. Yang, C., Mamouni, J., Tang, Y., Yang, L., 2010. Antimicrobial activity of single-walled carbon nanotubes: length effect. Langmuir 26, 16013 16019. Yang, H., Tong, M., Kim, H., 2013. Effect of carbon nanotubes on the transport and retention of bacteria in saturated porous media. Environ. Sci. Technol. 47, 11537 11544.

69

70

CHAPTER 2 Functional group-dependent toxicity of CNT

Yoon, H., Baek, Y., Yu, J., Yoon, J., 2013. Biofouling occurrence process and its control in the forward osmosis. Desalination 325, 30 36. Zardini, H.Z., Amiri, A., Shanbedi, M., Maghrebi, M., Baniadam, M., 2012. Enhanced antibacterial activity of amino acids-functionalized multi walled carbon nanotubes by a simple method. Colloids Surf. B Biointerfaces 92, 196 202. Zardini, H.Z., Davarpanah, M., Shanbedi, M., Amiri, A., Maghrebi, M., Ebrahimi, L., 2014. Microbial toxicity of ethanolamines—multiwalled carbon nanotubes. J. Biomed. Mater. Res. Part A 102, 1774 1781. Zare-Zardini, H., Amiri, A., Shanbedi, M., Memarpoor-Yazdi, M., Asoodeh, A., 2013. Studying of antifungal activity of functionalized multiwalled carbon nanotubes by microwave-assisted technique. Surf. Interface Anal. 45, 751 755. Zare-Zardini, H., Amiri, A., Shanbedi, M., Taheri-Kafrani, A., Kazi, S., Chew, B., et al., 2015. In vitro and in vivo study of hazardous effects of Ag nanoparticles and argininetreated multi walled carbon nanotubes on blood cells: application in hemodialysis membranes. J. Biomed. Mater. Res. Part A. Zeino, A., Abulkibash, A., Khaled, M., Atieh, M., 2014. Bromate removal from water using doped Iron nanoparticles on multiwalled Carbon Nanotubes (CNTS). J. Nanomater. 2014, 9. Zhang, J., Lee, J.K., Wu, Y., Murray, R.W., 2003. Photoluminescence and electronic interaction of anthracene derivatives adsorbed on sidewalls of single-walled carbon nanotubes. Nano Lett. 3, 403 407. Zhang, Y., Ali, S.F., Dervishi, E., Xu, Y., Li, Z., Casciano, D., et al., 2010. Cytotoxicity effects of graphene and single-wall carbon nanotubes in neural phaeochromocytomaderived PC12 Cells. ACS Nano 4, 3181 3186. Zhou, Z., Kang, H., Clarke, M.L., Lacerda, S.H.D.P., Zhao, M., Fagan, J.A., et al., 2009. Water-soluble DNA-wrapped single-walled carbon-nanotube/quantum-dot complexes. Small 5, 2149 2155.