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Make it clean, make it safe: A review on virus elimination via adsorption

Lotfi Sellaoui, Michael Badawi, Antonio Monari, Tetiana Tatarchuk, Sonia

Jemli, Guilherme Luiz Dotto, Adrian Bonilla-Petriciolet, Zhuqi Chen

PII: S1385-8947(21)00280-1

DOI: https://doi.org/10.1016/j.cej.2021.128682

Reference: CEJ 128682

To appear in: Chemical Engineering Journal

Received Date: 14 September 2020

Revised Date: 21 December 2020

Accepted Date: 13 January 2021

Please cite this article as: L. Sellaoui, M. Badawi, A. Monari, T. Tatarchuk, S. Jemli, G. Luiz Dotto, A. Bonilla-

Petriciolet, Z. Chen, Make it clean, make it safe: A review on virus elimination via adsorption, Chemical

Engineering Journal (2021), doi: https://doi.org/10.1016/j.cej.2021.128682

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1

Make it clean, make it safe: A review on virus elimination via adsorption

Lotfi Sellaoui 1,2*, Michael Badawi 3**, Antonio Monari 3, Tetiana Tatarchuk 4, Sonia Jemli 5,6,

Guilherme Luiz Dotto 7, Adrian Bonilla-Petriciolet 8, Zhuqi Chen1,2***

1 Department of Environmental Engineering, School of Environmental Science and Engineering,

Huazhong University of Science and Technology, Wuhan 430074, PR China

2 Key Laboratory of Material Chemistry for Energy Conversion and Storage, Ministry of

Education, Hubei Key Laboratory of Material Chemistry and Service Failure, School

of Chemistry and Chemical Engineering, Huazhong University of Science and Technology,

Wuhan 430074, PR China

3 Laboratoire de Physique et Chimie Théoriques LPCT UMR CNRS 7019, Université de

Lorraine, Vandœuvre-lès-Nancy, France

4 Educational and Scientific Center of Material Science and Nanotechnology, Vasyl Stefanyk

Precarpathian National University, Ivano-Frankivsk, 76018, Ukraine

5 Laboratory of Microbial Biotechnology, Enzymatic and Biomolecules (LMBEB), Centre of

Biotechnology of Sfax, University of Sfax, Tunisia

6 Faculty of Sciences of Sfax, Biology department, University of Sfax, Tunisia.

7 Chemical Engineering Department, Federal University of Santa Maria–UFSM, 1000, Roraima

Avenue, 97105-900 Santa Maria, RS, Brazil

8 Instituto Tecnológico de Aguascalientes, Aguascalientes, 20256, México

Corresponding authors:

*Lotfi Sellaoui, sellaouilotfi@yahoo.fr , **Michael Badawi, michael.badawi@univ-lorraine.fr

***Zhuqi Chen, zqchen@hust.edu.cn

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Abstract

Recently, the potential dangers of viral infection transmission through water and air have

become the focus of worldwide attention, via the spread of COVID-19 pandemic. The

occurrence of large-scale outbreaks of dangerous infections caused by unknown pathogens and

the isolation of new pandemic strains require the development of improved methods of viruses’

inactivation. Viruses are not stable self-sustaining living organisms and are rapidly inactivated

on isolated surfaces. However, water resources and air can participate in the pathogens’

diffusion, stabilization, and transmission. Viruses inactivation and elimination by adsorption are

relevant since they can represent an effective and low-cost method to treat fluids, and hence limit

the spread of pathogen agents. This review analyzed the interaction between viruses and carbon-

based, oxide-based, porous materials and biological materials (e.g., sulfated polysaccharides and

cyclodextrins). It will be shown that these adsorbents can play a relevant role in the viruses

removal where water and air purification mostly occurring via electrostatic interactions.

However, a clear systematic vision of the correlation between the surface potential and the

adsorption capacity of the different filters is still lacking and should be provided to achieve a

better comprehension of the global phenomenon. The rationalization of the adsorption capacity

may be achieved through a proper physico-chemical characterization of new adsorbents,

including molecular modeling and simulations, also considering the adsorption of virus-like

particles on their surface. As a most timely perspective, the results on this review present

potential solutions to investigate coronaviruses and specifically SARS-CoV-2, responsible of the

COVID-19 pandemic, whose spread can be limited by the efficient disinfection and purification

of closed-spaces air and urban waters.

Keywords: coronavirus; SARS; wastewater; porous; carbon; MOF

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1. Introduction

Viruses are ubiquitous in nature and consequently their interactions with superior organism and

human beings are constant. Overall, the genetic diversity of viruses, their capabilities to change

and adapt, as well as their significant presence in nature are amazing. It has been estimated that

the total number of viral particles is significantly higher than the number of all cells of all the

organisms on Earth combined [1]. A virus is defined as a non-cellular infectious agent, and the

fundamental question whether they may or not be classified as living organisms is still debated.

Today, only 6,000 viruses are known while several millions viral strains exist but are unknown

[2]. The extreme diversity of the viral populations is also related to the problems encountered in

viruses’ eradication and to the various public health threats. Indeed, viruses are particularly

difficult to eliminate because they are continuous evolving under natural selection pressure,

allowing them to counteract the protection offered by vaccines or specifically targeted drugs.

Viral particles cannot subsist independently, and the first step of the diffusion is the infection of

a cell, that is invaded with the viral genomic and proteic material.

Almost all known viruses have their own specific target in a living organism, which implies the

existence of a specific receptor on the cell surface where the virus attaches itself to gain entry to

the cell [2], the preferred viral receptors also determine the cell types that will most probably

suffer from the infection. Once inside the cell the viral genome is replicated and translated, also

exploiting the cellular machinery, resulting in the production and maturation of novel viral

particles that can be expelled from the cell, usually killing the latter in the process, and

contribute to the further diffusion of the agent. Viral transmission is mostly achieved by the

expulsion of viral particle with bodily fluid or respiration and the subsequent contact with other

organisms. Normally, and once again due to the receptor specificity, the viral transmission is

mostly happening between organisms of the same, or closely related, species. However, the virus

mutation capability can also lead to zoonosis, i.e. overcoming the interspecies barrier greatly

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facilitating the transmissibility and contagious capacity. Indeed, zoonosis is usually recognized

as a crucial step in the early development of uncontrolled epidemics and outbreaks.

It is nowadays well established that viruses may represent a serious threat to public health, since

they can be extremely pathogenic and be at the origin of extremely dangerous diseases [1,3,4].

Indeed, since ancient times mankind had to cope with the diffusion of epidemic and pandemic,

whose periodic outbreaks have marked many historical periods. The constant threat of viral-

based diseases is also witnessed by the fact that in many ancient cultures its spreading was

attributed to the angers of Gods, see for instance Sekhmet in ancient Egypt or Artemis in

classical Greece. Viral-based diseases may indeed severely affect different organs, and their

spread is favored by the possibility of human-to-human contagion, that is determined by the

inherent viral infectivity rate.

Every year, humanity is facing challenges with new types of viruses that threaten the human

health and can cause epidemics and, in the worse scenario, pandemics [2], the most common,

and relatively innocent one being seasonal flu. A more dangerous example is constituted by the

Middle East respiratory coronavirus syndrome (MERS coronavirus) appeared in the spring of

2015 in South Korea. The outbreak took the South Korean authorities by surprise and forced

them to take urgent epidemiological measures [2]. MERS mortality ratio amounts to more than

35 % and, as stated in the World Health Organization (WHO) Newsletter, “there is currently no

specific treatment or vaccine for this disease”. This example alone justify the extreme

importance and interest devoted to the research on viruses and its vital importance to maintain

healthy environments for the society [5].

In 2020, humanity is facing new global social and economic challenges induced by the

apparition of a novel coronavirus in late 2019. The first cases of an unknown coronavirus were

recorded on 31th December in the Chinese city of Wuhan, which has a population of nearly 12

million [6]. The effects due to this disease were rapidly observed in mainland China neighboring

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countries: Thailand, Japan, South Korea and Taiwan [7]. Since then, the virus dissemination has

continued, with the epicenter moving from Asia, Europe and later Americas, the new

coronavirus was later named severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) to

differentiate it from the original SARS-CoV appeared in 2003, while the associated disease has

been styled as COVID-19. On March 11th 2020, WHO declared COVID-19 a pandemic [7]. As

late as November 18th 2020, more than 55 million people have been infected worldwide, new

daily cases and deaths are still globally increasing, although the original Asian hot-spots seem

under relative control. COVID-19 affects the respiratory system, the gastrointestinal tract or the

nervous system; it can cause bronchitis, pneumonia and, in severe cases, death [1,5,6]. SARS-

CoV-2 originally developed in animals, probably pangolins, which acted as the initial main

carriers. However, through zoonosis, the transmissibility via human-to-human contact became

possible and represent today the main contagious route [4], while recent studies have also

pointed to the possible airborne transmission of this virus via aerosols [8]. The mortality ratio of

SARS-CoV-2 is relatively low, especially when compared with SARS-CoV or MERS, and is

estimated to not exceed 1-2 %, severe complications and death usually appearing in aged patients

or in subject presenting significant comorbidity, such as diabetes or hypertension. However, the

transmissibility and diffusivity of the virus are extremely high, and are also facilitated by the

presence of asymptomatic, or barely symptomatic carriers contributing to its spreading.

COVID-19 pandemic and the effects to the related containing measures on the different aspects

of the daily life have been clearly highlighted, also towards the general public, the importance of

developing new strategies to minimize the corresponding infection risks via the reduction of

exposure routes for this and other viruses and to generate healthy environments. The

quantification of coronavirus particles in wastewater is indeed an interesting and original

approach to the study of the spread of the pathogens [9], since SARS-CoV-2 particles have been

found in wastewater in a quantity correlating well with the epidemic growing ratio [10], pushing

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many countries to begin a more systematic wastewater monitoring [11]. Indeed, the increases of

the number of SARS-CoV-2 particles in wastewater occur even before COVID-19 symptoms

appear in patients, hence its monitoring may allow the early detection of possible epidemic

outbreaks [12]. Even if interesting such an approach requires the use of concentration method to

overcome the low concentration of viral material and it relies on the use of adsorbents such as

anion exchange resin [13].

It is known that the dissemination of viruses can take place by different routes including direct

contact with infected animals and humans, or through dispersion of viral particles in water and

air [3,14–16]. As a consequence, it is necessary to establish high-quality water and air treatment

to contribute to the reduction of virus dissemination, lowering the infectivity and transmissibility

ratio, and hence preventing serious epidemic outbreaks [17,18]. Thus, to be effective and to

respect the public-health standards, purification of water and air should not be restricted to the

mechanical elimination of large particles, but should also include the removal of biological

pollutants like viruses and bacteria [19–22]. Indeed, infections can be transmitted via the

diffusion of viral particles by air-droplets, through moist soil, surfaces, and water [23]. The

diffusion of viral material in household occupied by infected persons is of particular concern. In

some instances, infection can be propagated by the ingestion of contaminated food, such as

vegetable or fruits, or by drinking non-sanitized water. Viruses may reach the surfaces of fruits

and vegetables when they are fertilized with non-disinfected wastewater. If the contamination

through infected water and food is at the moment well managed in developed countries, the more

difficult access to alimentary resources in developing or underdeveloped areas still represents a

serious public-health issue, seriously undermining human health development.

Furthermore, the quantification of virus content, i.e. the precise determination of the type and

concentration of virus is far from being an innocent subject, and many important scientific

breakthroughs have been realized in the last years. Virus quantification is fundamental not only

7

for the analysis and purification of effluent or wastewater but also for the production of viral

vaccine, antiviral agents, or recombinant proteins. Historically, the more common virus

quantification methods included plaque titer assay, fluorescent focus assay (FFA), and 50 %

tissue culture infection dose (TCID50). Without entering into too much details, that will be out of

the scope of the present review, those methods are based on microbiology techniques in which

hosts cells are exposed to viral samples and the number of infected cells that will lyse eventually

identified by immunostaining, is recorded giving an indication of the virus quantity. The actual

quantification in this case is achieved providing either the number of plaques formed by the

lysed cells, or of the stained foci, expressed per unit of sample and volume, or by its logarithm

(log10). Conversely, TCID50, that yields the amount of virus needed to lyse half of the host cell, is

mostly used in clinical frameworks. More recently, direct measures of the amount of viral

material have emerged testing either specific viral protein or its genetic material. In particular,

quantitative polymerase chain reaction (qPCR) is used to amplify and detect the amount of viral

DNA or RNA, while enzyme-linked immunosorbent assays (ELISA) are sensible to the viral

proteins and acts through an antigenic mechanism. It is worthwhile to mention that the use of

transmission electron microscopy (TEM) may allow to quantify some virus via direct

visualization. In this case, the quantity of virus is expressed directly as the quantity of viral

material, or particles, per unit of sample and volume. Modern methods such as qPCR or

antigenic tests are much faster than the classical cellular based techniques, and have the

advantage to directly target the viral material, although they may be subjected in some instance

to contamination [17,24].

The presence of viruses in air and water can be faced using different technologies with a varied

degree of sophistication, operational costs, removal efficiency and energy consumption. These

technologies comprise mainly mechanical and electrical filtration using for example ceramic

filters [25–27], coagulations processes [28], saturated soil column [29], reclamation systems

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[30–32], membrane bioreactor process [33], photocatalytic disinfection [34,35], concentration

methods [36], ozone generators and UV irradiation [37], chemical disinfection and membrane-

based processes [38]. Among these technologies, membrane-based processes based on

adsorption appear as a low cost and efficient technique.

Different membranes have been proposed for virus removal from water and air: ultrafiltration

[39,40], nanofiltration [41] and reverse osmosis membranes [20,42–45]. Nowadays, a large

variety of materials has been proposed to this aim, also exploiting specific interactions with the

viral capsid. They include activated carbon [46–49], polysaccharide (PS)-based materials [50],

kaolinite and fiberglass [51], Cu and Ag compounds [52,53], quartz sand [54], functionalized

chitosan nanofibers [55], hydrochar [56], nano-TiO2 [57], resins [13], poly(ethylenimine) [58],

Fe/Ni nanoparticles [59] and zeolites [60]. Alternative strategies for fluid decontamination can

rely on the treatment of wastewaters with natural occurring or biocompatible organic

compounds, such as carbohydrates, that show high antiviral effect coupled with the absence of

unwanted side effects such as cytotoxicity. Note that the majority of these studies was focused

on the removal of the viruses from water but the results can be extended and used as a basis to

develop purification methods for air.

The present review will focus on the different strategies for the rational design of adsorbents

materials that can be easily implemented to eliminate viral particles from air or liquid fluids.

After describing in details the structure of viruses, this review will be organized in sections

corresponding to the main classes of adsorbents: carbon-based materials, oxide-based materials,

zeolites, silica, metal–organic frameworks, clays and carbohydrates. We will present and

critically comment the available practical technologies for removing viruses by adsorption and

our perspectives will be provided in the last section of this review.

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2. Description of virus structures

In addition, to the possible threats to public health system and social organizations, virus biology

is also complex and fascinating. By a general definition, viruses are small microorganisms that

do not possess a cellular structure. Overall, the classification of viruses may be diverse and

rooted either on molecular biology or phenomenological and phenotypical factors such as: 1) the

type of nucleic acid encoding the genetic information, 2) its structure (single- or double-chain,

linear, circular, fragmented, unregimented), 3) the structure, dimensions, type of symmetry and

number of capsomers (i.e. the subunits constituting the virus external shell, termed capsid, and

mainly constituted of proteins), 4) the presence or absence of the outer shell (super capsid), 5)

the antigenic structure, 6) the genetic interactions taking place, 7) the geographical distribution,

8) the route of infection transmission and 9) the type of host (animal, plant, bacteria) [4,61,62].

Based on the literature, the best known kind of viruses are: rotaviruses, adenoviruses, hepatitis

type A, B, C, poliomyelitis (poliovirus) [25] and coronaviruses. The size of the virus structural

units (virions) range from 20 to 300 nm [20]. The composition of virions includes nucleic acids,

either ribonucleic (RNA) or deoxyribonucleic (DNA) acids, enclosed by a membrane and a

protein shell constituting the capsid, see Figure 1. Protein capsid protects and encloses the viral

genome encoded by the nucleic acids. Thus, protein capsid and nucleic acids are globally known

as nucleocapsid. Note that at a microscopic level the capsid, and hence viruses, may assume

different shapes: cubic, spherical, rod-shaped, etc. [62]. The specific shape of the capsid and the

structural proteins defining the interactions with the cellular receptors will determine on the one

side the type of organisms and cells that can be infected by a given virus, and on the other side

the transmissibility and the possibilities for the interactions with external materials. For instance,

small size viruses can be diffused further with fluid emission and through air compared to

heavier and bigger structures.

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Figure 1. Illustration of a virus structure.

The most widespread classification of viruses depends on the nature and structure of their

genome rather than on the diseases that they can cause [3]. As a consequence, a basic difference

exists between DNA and RNA viruses, which may have single or double chains of genetic

material, see Figure 2. Furthermore, single chain RNA viruses are divided into RNAs with

positive polarity and RNAs with negative polarity [3]. Typically, DNA viruses replicate in the

nucleus of the host cell, while the replication process of RNA viruses takes place in the

cytoplasm. At the same time, some positive-polarity single-chain RNA viruses, called

retroviruses, although replicating in the cytoplasm, use a completely different strategy involving

the preliminary retro-transcription of RNA into DNA performed by the viral retrotranscriptase.

A further difference in viral strains can be related to the structural properties of the virions

leading to the definition of simple and complex particles [3].

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Figure 2. Schematic illustration of A) influenza A virus (i.e., RNA virus) and B) hepatitis B

virus (i.e., DNA virus) [4].

Simple viruses are constituted by an external shell, named capsid, formed by the specific

external proteins named capsomers, and whose shape determines the virus symmetry. Complex

viruses have an additional outer shell, the supercapsid, located on top of the capsid. The

supercapsid contains the inner protein layer, formed by the M-protein, and a more bulky layer of

lipids and carbohydrates, that is formed by molecular constituents extracted from the host cell

membranes [4]. In addition, viral glycoproteins penetrate into the supercapsid resulting in curly

protrusions (spikes, fibers) and act as receptor allowing the interaction with cell membrane

proteins and hence the infection [3]. Examples of different classes of viruses are illustrated on

Figure 3.

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Figure 3. Examples of viruses: A) Adenovirus, B) Sulfolobus turreted icosahedral virus I and C)

Mammalian orthoreo virus [62].

Although viral particles may, on a first approximation, be regarded as structured objects,

traditional separation methods like adsorption and capture have shown a generally low

efficiency, when used in practical applications. Probably, the reason for this lack of performance

may be associated to the specific physicochemical and biochemical properties of viral particles,

namely, their low diffusion mobility, that can be traced back to their molecular size, and the

complex multicomponent and rather labile structure of the virions [63,64]. Indeed, the structural

properties of the virus’ surface determine the mechanism of their interactions with the adsorbent

surface, its bio-affinity, and ultimately the adsorption rate, which is usually accompanied by the

formation of highly specific (or bio-affinity) ionic, hydrophobic and coordination bonds

[25,65,66]. Thus, the physicochemical properties of viruses such as their size, morphology,

surface charge, capsid conformation and the distribution of charged, hydrophilic, and

hydrophobic amino acids strongly affect the virus-material interaction [67,68] as schematically

reported in Figure 4.

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Figure 4. Capsid structure and hydrophilic/hydrophobic amino acid distribution of MS2 and

PhiX174 phages (bacteriophage). Adapted from [67] with permission from Elsevier.

Hence, the study, also at molecular level, of the specific interplay between the adsorption

processes and the specific nature of the viral envelope is essential for the development and the

improvement of separation methods and strategies for viruses capture and elimination. In

addition to structural optimization, mainly based on the adaptation of the adsorbent material to

the virus size [3], surface charged material could be used to exploit electrostatic effects to

enhance viruses adsorption and inactivation [26,69,70]. Some specific viral particles have been

extensively used to model the adsorption of viruses since they permit a sufficiently large

representation of the different structural and physico-chemical space spanned by the different

pathogens and, as reported in Figure 5, they include the bacteriophages male specific type 2

(MS2), fr, GA and Qβ.

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Figure 5. Structures of most common virus-like particles – bacteriophages MS2, fr, GA and Qβ

utilized as models in adsorption experiments. Reprinted with permission from [66].

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3. Carbon-based materials

Carbon-based materials are the most used adsorbents for water and air treatment and,

consequently, they have been also largely applied in virus removal. A summary of different

carbon-based materials used for virus adsorption is reported in Table 1 and critically analyzed in

the following. Two types of activated carbon, conventional granular activated carbon and an

activated carbon fiber composite, have been tested and applied for virus removal from water

[48]. The raw material was characterized by a rigid mass of interlocked fibers of an average

length of 0.1-0.4 mm and an average width comprised between 5 and 100 µm. The bacteriophage

MS2 (having a radius of approximatively 25 nm) was chosen as a model for this study. It has to

be noted that bacteriophage is easier and cheaper to grow and test, especially compared to viral

particles and, consequently, it is often used as a model virus especially to study water sanitation.

It was shown that the shape of activated carbon could either inhibit or enhance the removal of the

large bacteriophage particles. Indeed, the study confirmed that carbon fiber composite having a

lower total area (840 m2/g) was more efficient for virus adsorption than granular activated

carbon with larger total area (1050 m2/g) resulting in a higher virus removal due to different

shape and size fraction of the activated carbons.

Matsushita et al. [47] investigated the removal of the two bacteriophages Qβ (diameter 23.5 ±

0.8 nm) and MS2 (diameter 22.5 ± 1.0 nm) by adsorption on commercially available powdered

activated carbon (N-PAC) and super-powdered activated carbon (S-PAC). This study allowed to

pinpoint some crucial factors for virus removal, namely: (i) increasing the electrophoretic

repulsive force between virus and particles of powdered activated carbon results in the

decreasing of virus removal, (ii) the increase of N-PAC pore volume improved the virus

removal, a pore diameter of 20-50 nm was shown to be necessary to trigger adsorption, (iii) the

increase in hydrophobicity of the virus surface results in a higher removal, and (iv) the low

negative surface charge of AC surface enhanced the virus removal. Similar findings were

obtained by Nemeth et al. [72] who proposed multi-walled carbon nanotubes (MWCNT)

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sensitized by Cu2O, TiO2 and Fe2O3 NPs in order to build hybrid membranes for MS2

bacteriophages removal from contaminated water. Cu2O-coated MWCNT membrane (see Figure

6a) showed the highest activity in virus removal in the pH range comprised between 5.0 to 9.0,

yielding a 4-Log, i.e. 99.99 % lower bound, for the percentage of virus retention, and,

consequently, were considered promising for virion uptake (Figures 6b and 6c).

Table 1. Summary of some advantages and limitations of carbon-based materials used for virus

inactivation.

Adsorbents

Type of virus

Consequences and advantages

-Granular activated carbon (GAC);

-Activated carbon fiber composite

(ACFC)

-Bacteriophage MS2

-ACFC adsorbent was more efficient

for virus adsorption than GAC;

-Due to its shape, GAC was not the

best adsorbent for virus besides both

surface areas are comparable

-Commercially powdered activated

carbon (N-PAC);

-Super-powdered activated carbon (S-

PAC)

-Bacteriophages Qβ

-MS2

-Three factors enhanced the

adsorption of virus by these

adsorbents:

1-A large pore diameter of 20-50 nm;

2-The increase in hydrophobicity of

the virus surface;

3-A low negative surface charge of

activated carbon;

-Increasing the electrophoretic

repulsive force between virus and

particles of powdered activated carbon

results in the decreasing of virus

removal

-MWCNT sensitized by Cu2O, TiO2

and Fe2O3 NPs

-MS2 bacteriophages

-Cu2O-coated MWCNT membrane

showed the highest activity in virus

removal at pH 5 -9;

-CuO does not improve the virus

removal

-TiO2 and Fe2O3 NPs- MWCNT have

not significantly enhanced the virus

removal

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Figure 6. (a) TEM micrograph of Cu2O/MWCNT nanocomposite membrane with 25 % of

MWCNT, (b) MS2 bacteriophage removal using MWCNT-based nanocomposite membranes in

batch experiments and (c) MS2 bacteriophage removal using MWCNT-based nanocomposite

membranes in flow experiments. Adapted from [72].

4. Oxide-based materials

It is known that viral capsid surfaces are negatively charged, hence surface positively charged

nanoparticles may be well suited for virus removal through electrostatic interaction, at least at

suitable pH [73]. Indeed, electrostatic-mediated adsorption inactivates viruses and can be used

both for water and air disinfection. Table 2 provides a summary of oxide-based materials

employed to remove or inactivate viruses. Mazurkow et al. [71] reported spray-dried alumina

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granules modified with copper (Cu) and copper oxide (Cu2O) nanoparticles (NP) as effective

adsorbents against viruses, thanks to the capacity of the nanoparticles to create a high density of

adsorption sites. The experiments were conducted in flow reactor and showed a removal of 99.9

% of the MS2 bacteriophages by Cu2O and Cu, conversely CuO had no impact on virus removal.

Gutierrez et al. [73] performed batch and dynamic experiments in order to investigate the

removal of group A porcine rotavirus (whose diameter is of 74.57 ± 1.32 nm) and bacteriophage

MS2 (diameter of 25.42 ± 0.93 nm) using glass fiber coated with hematite Fe2O3 NPs having a

surface area of 80.75 m2/g and total pore volume of 0.0835 cm3/g. The batch mode disinfection

demonstrated a high removal of both rotavirus and bacteriophage MS2 quantified by 2.49 × 1011

plaque forming unit/g and 8.9 × 106 focal forming unit/g, respectively (Figures 7a and 7b), while

the concentration of hematite used was 0.043 and 0.26 g/L for virus and bacteriophage MS2,

respectively. Transmission electron microscopy (TEM) images confirmed the electrostatic

adsorption of MS2, while they also underlined structural damages to the rotavirus caused by the

interaction with hematite that also participate in the virus inactivation. (Figures 7c and 7d).

While hematite NPs present the advantage of offering more available adsorption active sites

coupled with strong electrostatic attraction, which can be beneficial in favoring virus depletion, it

was concluded that the inactivation of viral particle might depend on the specific proteins of its

capsids or the robustness of its structure [73], and hence its efficacy could vary considerably

between different viral strains. However, it is clear that hematite NPs may represent a most

valuable system to achieve virus removal from contaminated water and its use could be extended

to air treatment.

Table 2. Summary of some advantages and limitations of oxide-based materials used for virus

inactivation.

19

Adsorbents

Type of virus

Consequences and advantages

-Spray-dried alumina

granules modified with

copper (Cu) and copper

oxide (Cu2O)

nanoparticles (NP)

-MS2 bacteriophages

-A removal of 99.9 % of the MS2 bacteriophages by Cu2O and Cu;

-Glass fiber coated with

hematite Fe2O3NPs;

-Biosand filter filled with

iron oxide NPs

-Bacteriophage MS2;

-Rotavirus

-A high removal of both viruses;

-NPs have the advantage to provide more available adsorption sites

coupled with strong electrostatic attraction leading to virus depletion;

-Hematite NPs may represent a most valuable system to achieve virus

removal from contaminated water and its use could be extended to air

treatment;

-A significant higher removal of bacteriophage MS2 by an iron-

sensitized sand column compared to a sand-only column;

-The removal mechanism was explained by the electrostatic interaction

of negatively charged MS2 particles with the positively charged iron

oxides;

-It was concluded that the inactivation of viral particle might depend on

the specific proteins of its capsids or the robustness of its structure, and

so its efficacy could vary considerably between different viral strains

Magnesium oxyhydroxide

-Bacteriophages MS2

-PhiX174

-A favorable electrostatic interactions between the negatively charged

virion particles and the positively charged patches of magnesium

oxyhydroxides was improved the virus adsorption;

-Magnesium oxyhydroxide could be a good adsorbent for viruses also

due to its availability, high isoelectric point and low cost

-Diatomaceous-based

ceramic filter

-Enterobacteriaphage

MS2;

-Enterobacteria phage

PhiX174;

-Wild-type

bacteriophage

Siphovirida

-The experimental conditions were not optimized for virus removal;

-It is not very suitable for virus removal due to existence of repulsive

forces between the viruses and the filter surface besides steric clashes

caused by phage specific knobs.

Nano-TiO2-membranes;

Spherical Fe/NiNPs

-Bacteriophage f2

-Bacteriophages f2

-It is an effective adsorbent to remove the virus;

-Fast removal (after 60 min);

The virus removal was governed by the electrostatic attraction between

the opposite charged nano-TiO2 and phage f2 under acid conditions;

-Bacteriophages f2 were completely removed by Fe/Ni NPs after 30

minutes

Silica-decorated TiO2

NPs

-Bacteriophage MS2

-It was shown that doped-TiO2 including 5 % of SiO2 has a 37-fold

enhanced viral removal performance compared to pristine TiO2;

-It was suggested that this removal approach has the advantage of using

low-cost and green materials.

20

Figure 7. Removal of MS2 and rotavirus onto hematite NPs surface: (a) MS2 removal by

hematite NPs; (b) rotavirus removal by hematite NPs; (c) TEM image of MS2 bacteriophage

adsorbed onto hematite NPs surface; (d) TEM image of structurally damaged rotavirus particles

contacted with hematite NPs surface. Reprinted from [73].

Similarly, Bradley et al. [74] have studied the potential application of a biosand filter filled with

iron oxide NPs to remove virus, see Figures 8a and 8b. The iron oxides were obtained as result

of zero-valent iron particles corrosion, while the purification experiments were performed in

21

continuous flow process and showed a significantly higher removal of bacteriophage MS2 by an

iron-sensitized sand column (5log10) compared to a sand-only column (0.5log10) (Figure 8c). The

removal mechanism was again explained by the electrostatic interaction of negatively charged

MS2 particles with the positively charged iron oxides. In this same line of investigation,

Domagala et al. [75] used Cu2O/MWCNTs filters to remove MS2, finding that while the filters

were efficient, electrostatic interactions should not be held as the sole responsible of the

adsorption [75].

Figure 8. (a) Breakthrough curves of NaCl tracer from glass columns packed with sand and

zero-valent iron; (b) small-scale glass columns packed with iron oxides used for virus removal;

(c) the log10 reductions bacteriophage MS2 obtained by continuous flow through clean quartz

sand with no iron particles and sand mixed with 10 % (vol.) iron. Reprinted from [74].

Michen et al. [26] have proposed the use of magnesium oxyhydroxide, embedded into a ceramic

filter (10, 15, and 20 % of MgO), to improve viruses removal from water. These filters showed

an enhanced removal of about 4-log of bacteriophages MS2 and PhiX174. Once again, the

enhanced removal of the virus was attributed to the establishment of favorable electrostatic

interactions between the negatively charged virion particles and the positively charged patches of

22

magnesium oxyhydroxides. Furthermore, it was also concluded that viruses may be inactivated

in an alkaline environment and the presence of the slightly soluble Mg(OH)2 can indeed cause

the increase of water pH above 9. Albeit efficient for viral decontamination, the high increase of

pH alters the physico-chemical properties of water and, in particular, makes it not suitable for

drinking purposes; hence, a continuous flow mode was proposed for use of the ceramic filters.

Globally, the results suggested that magnesium oxyhydroxide could be a good adsorbent for

viruses also due to its availability, high isoelectric point and low cost.

The finding that viruses can be attracted by positively charged surface has been confirmed by

Wegmann et al. [42], in analyzing the impact of electropositive zirconium (hydr)oxide NPs

coatings on the performance of ceramic filters to remove viruses from water. Indeed, the internal

filter surface was coated by ZrO2 nanopowder via dip-coating and thermal treatment, resulting in

a considerable increase of the specific surface area of the filters going from 2 to 25.5 m2/g after

coating. The virus removal rate was also significantly increased, most notably achieving a 7-log

removal, equivalent to 99.99 % of the MS2 bacteriophages. Thus, zirconium oxide coating was

suggested as promising for virus filtration techniques with potential applications in both water

and air treatments.

On the other hand, the removal of positively charged viruses through negatively charged

surfaces has been investigated by Michen et al. [25]. Three bacteriophages, Enterobacteria phage

MS2 (isoelectric point (IEP) of 3.5, diameter 25 nm), Enterobacteria phage PhiX174 (IEP 6.6,

diameter 26 nm) and wild-type bacteriophage Siphovirida (IEP 2.7, diameter 60 nm), were used

as model viruses. The results have been rationalized through the use of the DLVO

(Derjaguin−Landau−Verwey−Overbeek) theory [25]. Most notably, it was shown that

diatomaceous-based ceramic filter, which is widely used to purify water, was not suitable for

virus removal due to repulsive forces between viruses and the filter surface besides steric clashes

caused by phage specific knobs.

23

Zheng et al. [57] reported the application of nano-TiO2-membranes for phage f2 removal from

water, see Figures 9a and 9b. This study showed that the removal of phage f2 was effective after

60 min and the results have been rationalized with the Freundlich adsorption model yielding a qe

= 27.4.Ce1.24. PolyVinyliDene Fluoride (PVDF) (0.20 μm) and PolyAcryloNitrile (PAN) (0.05

μm) membranes were used for TiO2 coupling in order to use nano-TiO2 membranes in flow

reactors for water treatment (Figures 9c and 9d). The experiments demonstrated higher virus

removal by PAN (3.88-log) compared to PVDF membrane (6.40-log). The mechanism of virus

removal was explained by the electrostatic attraction between the opposite charged nano-TiO2

and phage f2 under acid conditions. The coupled TiO2/membrane system was stable and can be

used for virus removal from contaminated water. Silica-decorated TiO2 NPs have been used by

Liga et al. [76] for the bacteriophage MS2 inactivation in water. It was shown that doped-TiO2

including 5 % of SiO2 has a 37-fold enhanced viral removal performance compared to pristine

TiO2. The authors suggested that this removal approach has the advantage of using low-cost and

green materials and, hence, is particularly appealing for water treatment.

24

Figure 9. (a) nano-TiO2 membrane adsorption reactor; (b) adsorption kinetics of nano-

TiO2 regarding phage F2. SEM images of (c) PVDF (PolyVinyliDene Fluoride) and (d) PAN

(PolyAcryloNitrile) flat membranes. Reprinted from [57].

Cheng et al. [59] reported the removal of bacteriophage f2 from water by spherical Fe/Ni

NPs (93 nm) under aerobic conditions, see Figure 10. Fe/Ni NPs were synthesized by a liquid-

phase method using NaBH4 solution. It was found that bacteriophages f2 were completely

removed by Fe/Ni NPs after 30 minutes treatment from a solution with an initial concentration of

4×106 PFU/mL (PFU: plaque-forming unit). The effect of the Fe:Ni ratio on virus removal was

investigated and results showed that the highest removal efficiency was obtained with a 5:1 ratio.

Oxygen condition, pH, initial virus concentration, adsorbent mass and temperature were also

25

tested and analyzed to determine their impacts on the removal of this virus. The inactivation

mechanism of bacteriophage f2 was explained by the oxidative stress produced by iron and by

the production of reactive oxygen species (OH• and O2•−) formed due to the oxidation of Fe0 and

catalyzed by Ni0 [59].

Figure 10. Removal of bacteriophage f2 in water by Fe/Ni nanoparticles. Reprinted from [59].

5. Zeolites

Zeolites are crystalline and porous materials with regular framework structures composed of

cages and pores of various size and shape [77]. Zeolites have exceptional chemical selectivity,

high adsorption capacity and are biocompatible and safe, consequently, they have attracted

considerable interest for biomedical applications. It is now possible to synthesize zeolites with

nanosized dimensions and stabilized in colloidal suspensions [78,79]. The high stability of

nanozeolites with regular micropores makes them suitable for selectively adsorbing and

desorbing different molecules based on their size allowing them to act as molecular sieves [80].

Furthermore, the tunable chemical composition of these crystalline materials allows them to

adapt to different chemical environments and thus to exhibit high stability in acidic and alkaline

media [81]. The interest of zeolites as antiviral adsorption agents also resides in the fact that their

properties can easily be tuned by the introduction of different metal cations in nanosized

26

materials, most notably altering their adsorption capacity [80,82–85]. Although this has mainly

be exploited for gas separation, its interest for purification stands out as well. Zeolites can also

be specifically functionalized, tuning their surface and interparticle porosity, in order to target a

specific tissue or cell type. As an example, antibody-nanozeolite bioconjugates have been

generated and successfully employed to target cancer cells [86]. As an extension, and because of

their favorable physico-chemical properties zeolites can be efficiently used to remove viruses,

also thanks to their high porosity and surface area (see Table 3).

Bright et al. [60] used zeolite as an adsorbent to remove coronavirus 229E from water. They

demonstrated that silver- and copper-doped zeolites can induce a significant reduction of the

presence of the coronavirus in water solution after 1 h treatment. Indeed, the functionalization of

zeolite via silver and copper, i.e. metals presenting known antibacterial properties, has been

shown to be an efficient way to inhibit SARS coronavirus, as well as other coronaviruses and

human norovirus (calicivirus) [60]. Even if experiences are still scarcer than for other materials,

the promising results show that metal-functionalized zeolites can be considered as an excellent,

and highly flexible, agent to reduce the contamination by all types of viruses from both water

and air.

6. Silica nanoparticles

Silica is a well-known adsorbent that has unique physicochemical properties: large surface area,

chemical purity, hydrophilicity, and significant adsorption capacity. Silica has the ability to

actively adsorb bioactive molecules, proteins, microorganisms, and viruses [36,87–89]. The

specific surface area of silica used for medical purposes is 300 m2/g, and is usually characterized

as a white powder consisting of spherical particles with a diameter of 9-10 nm. The surface of

silica particles contains silanol and hydroxyl groups, which are interacting via hydrogen bonds

[90]. In addition, water molecules are present at the silica surface both chemically bonded or

27

physically adsorbed. The concentration of silanol groups, which are the main adsorption sites, is

approximately 0.6-0.7 mmol/g or 2-2.5 μmol/m2 [91,92].

28

Table 3. Summary of some advantages and limitations of different alternative adsorbents used

for virus inactivation.

Adsorbents

Type of virus

Consequences and advantages

-Zeolite;

-Novel amine-

functionalized

magnetic

Fe3O4–SiO2–

NH2 NPs

-Coronavirus 229E

-SARS coronavirus;

-Bacteriophage f2

and Poliovirus-1

-Silver and copper-doped zeolites can induce a significant reduction of the

presence of the coronavirus in water solution after 1 h of treatment;

-The functionalization of zeolite via silver and copper, i.e. metals

presenting known antibacterial properties, has been shown to be an

efficient way to inhibit SARS coronavirus;

-The adsorption mechanism was explained by the surface charge,

hydrophobicity and surface properties of pathogens and NPs matrix;

-It was shown that the removal efficiency of Fe3O4–SiO2–NH2 NPs over

bacteriophage f2 and Poliovirus-1 are more than 97 %

-Silica

nanoparticles:

A variety of

NH2-containing

moieties can be

used to modify

silica, for

example,

lupamin, 3-3-

(ethylenediami

no) propyl,

aminopropyl,

3-

(diethylenetria

mino) propyl;

-Novel amine-

functionalized

magnetic

Fe3O4–SiO2–

NH2 NPs

-Bacteriophage MS-

2;

-Bacteriophage f2

and Poliovirus-1

-In general, they have large surface area, chemical purity, hydrophilicity,

and significant adsorption capacity;

-The modified functionalized silica particles show high efficiency towards

bacteriophage MS-2 removal (> 98 %).

-The mechanism of virus inactivation was explained by the high density of

positively charged NH2-groups, electrostatic interaction and hydrogen

bonds formation;

-The adsorption mechanism was explained by the surface charge,

hydrophobicity and surface properties of pathogens and NPs matrix;

-The removal efficiency of Fe3O4–SiO2–NH2 NPs over bacteriophage f2

and Poliovirus-1 are more than 97 %.

-Metal–Organic

Frameworks

(MOFs)

-Zika, Dengue,

human immune

deficiency virus-1

(HIV-1) and

Japanese

encephalitis virus

-It has been shown that the textural properties (pore size and volume),

crystal morphology and chemical functionality of MOFs can be modulated

to obtain specific performances for virus removal;

-MOFs-based materials have also been used to develop sensor for

detecting Zika, Dengue, human immune deficiency virus-1 (HIV-1) and

Japanese encephalitis virus with promising results

29

-Clay and clay

minerals

-Rotaviruses and

coronaviruses

-The experimental results demonstrated that clay-based adsorbents showed

good (70-90 %) to excellent (> 90 %) capability to remove bovine

rotavirus and bovine coronavirus

-Cyclodextrins

( CDs)

-Herpes simplex

virus (HSV);

-Respiratory

syncytial virus

(RSV);

-Dengue virus, and

Zika virus

-They showed that the modified CDs possessed in vitro broad-spectrum

virucidal properties at micromolar concentrations against these viruses

Silica has a significant protein adsorption capacity, for example, 1 g of silica can adsorb up to

200-300 mg/g of gelatin or 800 mg/g of albumin from aqueous solution at pH 5-6. Silica is an

active adsorbent of various kind of microorganisms: indeed 108 up to 1010 microbial bodies can

be adsorbed per 1 g of silica. The properties and structure of the active centers of the SiO2

surface, which determine the specific interaction with the biological objects, are described in

[93–96].

As such silica-based NPs are particularly attractive for virus removal as highlighted in Table 3.

Various methods of SiO2 surface modification have been described in order to increase its

adsorption selectivity towards microorganisms [97–101]. Chemically modified silicas are of

particular interest among nanoporous mineral oxides [102]. They have a developed surface and

are not only excellent adsorbents in their original form, but they are also capable of radically

changing their physicochemical properties as a result of chemical modification [103]. A variety

of NH2-containing moieties can be used to modify silica, for example, lupamin, 3-3-

(ethylenediamino) propyl, aminopropyl, 3-(diethylenetriamino) propyl [104]. Such modified

functionalized silica particles show high efficiency towards bacteriophage MS-2 removal (> 98

%). The mechanism of virus inactivation is explained by the high density of positively charged

NH2-groups, electrostatic interaction and hydrogen bonds formation.

30

As another example, magnetic silicon microspheres have been used for detection of Japanese

encephalitis virus [105]. Novel amine-functionalized magnetic Fe3O4–SiO2–NH2 NPs have been

investigated as adsorbent for bacteriophage f2 and Poliovirus-1 removal by Zhan et al. [106].

NPs were obtained through layer-by-layer method using Fe(acac)3, tetraethyl orthosilicate

(TEOS) and γ-amino propyltriethoxy-silane (APTES) as precursors. The adsorption mechanism

was rationalized by the surface charge, hydrophobicity and surface properties of pathogens and

NPs matrix. The electrostatic attraction between the negatively charged Poliovirus-1 walls and

the positively charged adsorbent surface was clearly identified, and it was shown that the

removal efficiency of Fe3O4–SiO2–NH2 NPs over bacteriophage f2 and Poliovirus-1 exceeded 97

%. Cademartiri et al. [107] have explored an alternative strategy in which four unmodified

phages were immobilized on anionic silica substrate via electrostatically-facilitated

physisorption, see Figure 11. The proposed adsorbents can be used to detect and control

pathogens, particularly drug resistant bacteria.

Figure 11. Electrostatic attraction model between phage and charged SiO2 particles. A: tail down

and non-specific adsorption, B: head down, C: head down saturated surface [107].

7. Metal–Organic Frameworks (MOFs)

31

MOFs are composed of inorganic nodes of metallic species/clusters and organic ligands. These

materials are very stable under different operating conditions (e.g., temperature and solvents)

[108]. Several studies have concluded that they offer a spectrum of possibilities to prepare new

materials including biocomposites [108,109]. The application of MOFs-based biocomposites

covers biocatalysis, DNA detection, sensing, drug delivery and immobilization [109]. It has been

shown that the textural properties (pore size and volume), crystal morphology and chemical

functionality of MOFs can be modulated to obtain specific performances for a variety of

applications [110,111]. MOFs properties can be tailored to encapsulate proteins and other

biological molecules preserving their functionalities [109]. These materials are also capable of

encapsulating bacteria and viruses in which case adsorption plays a fundamental role [108].

These findings open a broad spectrum of possibilities to employ MOFs for facing the

environmental and public health challenges caused by viruses, see Table 3.

The analysis and study of biological-inorganic matrixes obtained from MOFs are relevant topics

to improve and enhance the environmental and medical applications of this new type of

biomaterials. The organic functionalities of MOFs play an important role in the anchorage of

biomacromolecules for biocomposites synthesis. For instance, Doonan et al. [109] discussed and

analyzed the mechanisms of the incorporation of biological compounds on MOFs, which can be

performed via encapsulation, infiltration or bioconjugation (Figure 12). Note that MOFs

structures can host a wide variety of both inorganic and organic compounds including biological

macromolecules. Parameters like the composition, topology, porosity and surface functionalities

of MOFs are important and should be analyzed during the synthesis of biocomposites and to

perform the coating of living systems (i.e., biomimetic mineralization) [108].

However, it has been recognized that the incorporation of biomacromolecules on the MOFs pore

structures implies several technological challenges. Previous studies have indicated that

biomacromolecules encapsulated on MOFs can be released by changes in the medium

32

conditions, for example, pH [109]. On the other hand, MOFs can be used in vaccine

developments based on the fact that these materials can coat and work as exoskeletons to protect

living cells from aggressive environments [112]. Ricco et al. [108] have concluded that MOF can

be used to improve the cold chain with the aim of avoiding the degradation of drugs and vaccine.

It has been also suggested that hybrid biosynthetic materials can be prepared from MOFs to

improve the pharmacokinetics of viral nanoparticles thus affecting the immune response [108].

Vaccine design based on MOFs is a promising area that however still needs to be much largely

explored and studied to reach commercial applications.

Finally, MOFs-based materials have also been used to develop sensor for detecting Zika

[113,114], Dengue [113], human immune deficiency virus-1 (HIV-1) [115] and Japanese

encephalitis virus [116] with promising results.

Figure 12. Mechanisms for the incorporation of biological compounds on MOFs structures.

Reprinted from [108].

8. Clay and clay minerals

33

A variety of promising adsorbents obtained from clays and their composites has also been

proposed to remove rotaviruses and coronaviruses [105], see Table 3. Indeed, the diameter of

rotavirus and coronavirus particles are 60-80 and 60-220 nm [117], respectively, which is clearly

larger than the size of pores of different adsorbent particles. Hence, both viruses can be adsorbed

on the outer surface of adsorbents. The experimental results demonstrated that clay-based

adsorbents showed good (70-90 %) to excellent (> 90%) capability to remove bovine rotavirus

and bovine coronavirus [117]. Based on this investigation, it was suggested that the involved

interactions between the adsorbent surfaces and viruses is probably due to a non-specific protein

binding.

9- Viruses adsorption by carbohydrates and their derivatives

Several biological molecules, carbohydrates in particular, have shown effective antiviral

activities; these materials are also summarized in Table 3. Such activity is usually due to the

competition with the host cell for the interaction with viral capsid proteins, hence preventing the

first step of cell infections. Some of the most efficient agents in this context mimic the sugars

present at the cell surface, in particular heparan-sulfate proteoglycans that are responsible for the

initial viral attachment [118–120]. The chemical structure of these carbohydrates, their origins

and their antiviral properties are briefly described below.

9.1. Antiviral effect of sulfated polysaccharides

Various polysaccharides from plants, marine vegetables, algae and lichens have received

increasing attention due to their ability to scavenge free radicals, to activate immune systems, to

inhibit lipid peroxidation and to inhibit viral replication [121]. Consequently, these

polysaccharides have exhibited numerous biological activities including anticoagulant, antiviral,

antioxidative, anti-inflammatory, antiangiogenic, antithrombotic and anticancer effects [122–

127]. Sulfated polysaccharides (SPs) especially from sea algae such as fucoidans, carrageenans,

34

heparin, neem, laminarans and ulvansare are considered as the most interesting and attractive

carbohydrates showing antiviral properties [128–133].

Since 1978, Richards and coworkers [134] have recognized the inhibition of viruses by

polysaccharide fractions from marine algae. Recently, other studies have reported that several

plants and marine algae contain significant quantities of complex sulfated polysaccharides that

can exhibit antiviral activity against serious infectious diseases such as HIV [135], yellow fever

virus [136], dengue virus type 1 [136], dengue virus type 2 [137] and herpes simplex viruses

[133,138–140].

A number of hypotheses has been proposed to explain the antiviral mechanisms of sulfated

polysaccharides (see Figure 13) including direct interaction with the viral particle, alteration of

viruses’ adsorption or attachment to cell receptors, inhibition of the penetration of virus into the

host cell, the interference with different stages of viral replication [141–143] .

35

Figure 13. Antiviral action mechanisms of medicinal plant metabolites. Reprinted from [143].

On the other hand, numerous studies have reported efficient strategies, based on synthetic

pathways, enzymatic digestion, partial hydrolysis and methylation methods, to produce sulfated

derivatives of different polysaccharides such as dextran, pentosan, dermatan, carrageenan,

alginate, xylomannan and galactan [123,135,144]. Furthermore, it has been highlighted that the

presence of sulfated groups enhanced the antiviral properties, and is hence essential for viruses’

inactivation. More specifically, it has been noted that while the virucidal efficacy can increase

with the degree of sulfation and the specific position of the sulfate ester groups, it also depends

on the molecular weight, the constituent sugars, their conformation and dynamic stereochemistry

[132,145,146]. Generally, the results have indicated that the greater the degree of sulfation, the

higher the biological activity, an observation which could conduct to find a drug candidate with

higher potency and less cytotoxicity [141,147,148], since polysaccharides with low sulfation

36

degrees are in general inactive against viruses [145]. Some applications of these natural

compounds in virus inactivation have already been reported [121,137]. For example, Hidari et al.

[137] have found that dengue virus particles bounded exclusively to fucoidan via their envelope

glycoprotein thus indicating that sulfated polysaccharides could be developed as a potential

inhibitory agent. Kim et al. [121] reported that marine sulfated polysaccharides presented

numerous advantages such as relatively low production costs, broad spectrum of antiviral

properties, low cytotoxicity, safety, wide acceptability and novel modes of action over other

classes of antiviral drugs. Hence, they suggested the use of these sulfated polysaccharides as

promising decontamination agents in the near future.

9.2. Antiviral action of modified and sulfated cyclodextrins

Cyclodextrins (CDs) are natural cyclic oligosaccharides formed by α-(1-4)-linked glucose units

[149,150]. The most common CDs, referred as α-, β- and γ-CDs, have 6, 7 and 8

glucopyranoside moieities, respectively. These cyclic natural compounds have attracted a

considerable attention especially for their biological applications due to their ability to

encapsulate different compounds being, consequently, used as molecular carriers [151]. Thus,

CDs have found numerous applications in commercial and industrial fields including drug

delivery [151,152], gene delivery [153], bioimaging [154], photodynamic therapy [153], air

fresheners [153], cosmetics [153], food processing [155] and environmental depollution

[156,157]. As molecular carriers, CDs have been employed to enhance the antiviral activity of a

phosphodiester oligodeoxynucleotide [158]. This study showed that an important increase of the

antiviral activity (90 % inhibition) was obtained with only 7.5 mM oligonucleotide complexed to

a cyclodextrin derivative, the 6-deoxy-6-S-b-D-galactopyranosyl-6-thio-cyclomaltoheptaose, in

the 1:100 ratio. The authors suggested that the use of cyclodextrin derivatives as carrier for

phosphodiester oligonucleotides delivery could be an effective method for increasing the

37

therapeutic potential of these compounds against viral infections. On the other hand, De Clercq

[159] reported that the modified cyclodextrin sulfates acted, by themselves, as anti-HIV agents

since they interfered with the adsorption stage of HIV replicative cycle. It was also concluded

that the presence of sulfate groups was necessary to induce the anti-HIV activity as it is essential

for the inhibition of the virus-cell binding. CDs chemical modifications, like those reported for

the modified β-cyclodextrin sulfates (mCDS71 and mCDS11), is a promising approach to

achieve high oral bioavailability and absorption [160–162]. Further studies have also confirmed

the antiviral properties of sulfonated CDs against HIV [163,164]. However, their action was

found to be virus specific and reversible. Recently, Jones et al. [120] have prepared cyclodextrins

with mercaptoundecane sulfonic acids, to mimic heparan sulfates and obtained outstanding anti-

viral properties. They showed that the modified CDs, while being nontoxic and biocompatible,

possessed in vitro broad-spectrum virucidal properties at micromolar concentrations against

several viruses including herpes simplex virus (HSV), respiratory syncytial virus (RSV), dengue

virus, and Zika virus. Their results also indicate that modified CDs were effective ex vivo against

both laboratory and clinical strains of RSV and HSV-2 in respiratory and vaginal tissue culture

models, respectively. Additionally, they were also effective when administrated in mice before

intra vaginal HSV-2 inoculation. Finally, these modified CDs were successful in overcoming a

mutation resistance test that the available anti-HSV drug (acyclovir) failed.

10. Conclusion and Perspectives

This review covers the potential application of a number of adsorbents or inhibitors for the

treatment of water and air polluted by viruses and to the development of potential antivirals

treatment. Overall, the viruses’ properties and classification have been discussed, including the

available adsorbents that can be used for their removal or inactivation. Indeed, while a variety of

adsorbents can be used to remove different viruses present in the environment, their performance

38

is affected by both the structural parameters and their surface chemistry. It is clear from the

literature review that the surface charge of adsorbents is a paramount parameter for the effective

viral inactivation in both air and water, that can be tailored via chemical functionalization

[165,166]. Indeed, the electrostatic potential of adsorbent surface depends on the concentration

and type of functional groups that are exposed at the adsorbent/fluid interface [166]. The

adsorbent surface composition can be modified via the incorporation of a variety of doping

elements thus improving the surface interactions with viruses. Note that the identification of the

best chemical functionalization protocol to enhance the surface properties of a specific adsorbent

and, consequently, its corresponding antiviral activity is paramount to reduce the purification

costs. Also, the analysis of surface potential and antiviral properties of different adsorbents is a

relevant topic to be explored in forthcoming studies.

Globally, it appears that nanoparticles have a tremendous potential to develop effective and low-

cost sanitation systems for air and water purification. On the other hand, biological compounds

like polysaccharides and cyclodextrins may represent interesting alternative to develop novel

adsorbents for the removal of viruses from fluids. The production or extraction of these chemical

compounds, as well as their inclusion in everyday life objects (e.g., plastic surfaces, textiles,

hand gel) represents a most important challenge that the scientific community has to undertake to

fight against important public health threats.

As stated in this review, practical methods applied for virus removal include membrane

filtration, chemical disinfection with chlorine or ozone and ultraviolet disinfection [27,35].

However, these methods may face different economical and/or technical limitations. For

instance, the application of chemicals for water disinfection (e.g., chlorination and ozonation)

has been reduced in some countries due to the generation of toxic byproducts (e.g., haloacetic

acids, trihalomethane) from the degradation or transformation of the disinfectants [27,167].

Membrane technologies are effective for virus removal [27] but their main drawback is

39

associated with their operating costs, which can be very high and hence prohibitive for large

scale use in underdeveloped countries [11]. Previous studies have also reported that some viruses

(e.g., Norovirus) can resist the UV radiation thus limiting the efficacy of this process [168].

Adsorbents already available in the market for water disinfection include traditional filters with

activated carbons doped with silver [169], chemically modified polymers as ion exchange resins

[170] and even MOFs [171]. Overall, available commercial adsorbents may lack an effective

antiviral activity especially for new viruses besides relatively high production costs that are

mainly due to the specific compound used to confer antiviral properties of the adsorbent surface.

Indeed, in some cases they comprise high-added values compound which can be used for other

technological applications thus increasing their demand and, consequently, their market price.

Specific emphasis should then be placed on the development of efficient and low-cost

purification processes that will allow the large-scale treatment of fluids in developing or

underdeveloped countries to avoid the uncontrolled diffusion, or mutation, of dangerous viral

agents resulting in global threats. The production of self-sanitizing objects will be particularly

attractive and will require a considerable effort from the material science community in the

production of efficient, flexible, and miniaturized purifying agents. It is clear, as also shown by

the COVID-19 pandemic, that developing novel adsorbents with outstanding antiviral properties

will be a permanent and continuous necessity to face the presence of known and unknown

viruses in the environment.

CRediT author statement

Lotfi Sellaoui, Michael Badawi,Tetiana Tatarchuk: Conceptualization, Methodology

40

Lotfi Sellaoui, Michael Badawi, Tetiana Tatarchuk, Antonio Monari, , Sonia Jemli,

Guilherme Luiz Dotto,Adrian Bonilla-Petriciolet: Data curation, Writing- Original draft

preparation

Lotfi Sellaoui, Michael Badawi, Tetiana Tatarchuk, Antonio Monari, Sonia Jemli, Adrian

Bonilla-Petriciolet, Guilherme Luiz Dotto, Zhuqi Chen:Visualization, Investigation

Zhuqi Chen: Supervision

Lotfi Sellaoui, Michael Badawi, Antonio Monari, Adrian Bonilla-Petriciolet, Zhuqi Chen

:Writing- Reviewing and Editing,

Acknowledgements

This work was financially supported by the National Key R&D Program of China (No.

2018YFC1901403), the National Science Foundation of China (No. 21671072), the Fundamental

Research Funds for the Central Universities (No. 2019kfyRCPY058), and Chutian Scholar

Foundation from Hubei province.

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58

There is no conflict of interest.

This submission has not been published previously and not under consideration for publication

elsewhere. If it will be published, it will not be published elsewhere in the same form, in English

or in any other language, including electronically without the written consent of the copyright-

holder.

Highlights

-Type of viruses, their classification and physicochemical properties are reviewed

-A detailed review of different adsorbents for virus inactivation is reported

-Potential of biological materials to adsorb virus is discussed

- Perspectives of adsorption research for virus inactivation are reported

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