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II. Characteristics of Viruses Relevant for Subsurface Fate and Transport

II. Characteristics of Viruses Relevant for Subsurface Fate and Transport

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Table II

Basic Properties of Selected Viruses and Bacteriophages



Virus (strain)



Diameter

(nm)



Density

(g cm−3)



Shape



Envelope



Nucleic acid



Isoelectric point

(pHIEP)



References



Reovirus 3 (Dearing)

Poliovirus 1 (Mahoney)

Poliovirus 1 (LSc)

Poliovirus 2 (Sabin T2)

Echo 1 (5 strains)

Coxsackie A21



81

28–30

28–30

28–30

27

27



1.36

1.34

1.34

1.34

1.34

1.34



Human pathogens

Icosahedral, spikes

No

Icosahedral

No

No

Icosahedral

No

Icosahedral

Icosahedral

No

Icosahedral

No



ds-RNAa

ss-RNAb

ss-RNA

ss-RNA

ss-RNA

ss-RNA



3.9

8.2

6.6

4.5, 6.5c

5.0–6.4

4.8, 6.1c



Floyd and Sharp (1978)

Floyd and Sharp (1978)

Zerda (1982)

Murray and Parks (1980)

Zerda (1982)

Murray and Parks (1980)



T2

MS-2



60

24–26



n/a

1.422



Tailed

Icosahedral



Bacteriophages

No

No



ds-DNA

ss-RNA



4.2

3.5, 3.9c







24–26



1.439



Icosahedral



No



ss-RNA



5.3



φX174



25–27



1.43



Icosahedral, spikes



No



ss-DNA



6.6



PRD-1

R17



62

26



n/a

1.46



Icosahedral, spikes

Tailed or nontailed



No

No



ds-DNA

ss-RNA



3-4

3.9



PM2



60



n/a



Isometric, spikes



No



ds-DNA



7.3



rNorwalk Virus

SJC3



∼27 nm

8 × 900 nm



1.33–1.40

n/a



Icosahedral

Filamentous



No

No



None

ss-DNA



5

<2.5



Sharp et al. (1946)

Overby et al. (1966),

Zerda (1982), Penrod

et al. (1995)

Overby et al. (1966),

Ackermann and Dubow

(1987)

Ackermann and Dubow

(1987)

Loveland et al. (1996)

Ackermann and Dubow

(1987)

Ackermann and Dubow

(1987)

Redman et al. (1997)

Redman et al. (1997)



a



ds = double stranded.

ss = single stranded.

c

Values measured for two different conformational states of the same virus.

b



SUBSURFACE VIRUS FATE AND TRANSPORT



45



Table II summarizes some relevant data for viruses that are mentioned in this

manuscript, and four different viruses are depicted in Fig. 2 (see color insert). The

typical size for viruses is in the range of 20 to 100 nm in diameter (Powelson

and Gerba, 1995). There is considerable variability in the pHIEP among different

viruses.



III. VIRUS SORPTION

A. MECHANISMS

The mechanisms of virus sorption to solid surfaces have been summarized in

several review articles (Bitton, 1975; Duboise et al., 1979; Gerba, 1984; Gerba

and Bitton, 1984; Mix, 1974; Schijven and Hassanizadeh, 2000) and will only be

briefly discussed here.

Sorption of viruses has been studied with various types of viruses and sorbents

(Table III). Since virus particles fall into the size range of colloids, theories that

describe colloidal behavior have been applied to describe the behavior of viruses

(Gerba, 1984). Although viruses carry an electrical charge, a colloidal system in

its entirety remains electrically neutral. This phenomenon can be described by the

diffuse double-layer theory, as reviewed by Gerba (1984), in its relation to virus

sorption properties. Colloid stability is controlled by the balance between repulsive

double-layer interactions and attractive van der Waals forces, best described by the

Derjaguin–Landau–Verwey–Overbeek (DLVO) theory of colloid stability (Verwey

and Overbeek, 1948). Murray and Parks (1980) conducted sorption experiments

of poliovirus to a variety of metal oxides and found that free energies agreed with

potentials evaluated from the DLVO theory. Others have also used this theory to

explain their experimental observations (Loveland et al., 1996). Chattopadhyay

and Puls (1999) recently proposed that the total force leading to adhesion of virus

particles to solid surfaces can be divided into three groups: (1) electrostatic (EL) interactions; (2) Lifshitz–van der Waals electrodynamic forces (LW), which include

van der Waals–Keesom or orientation forces, van der Waals–Debye or induction

forces, and van der Waals–London or dispersion forces; and (3) polar forces or

acid–base interactions (AB). Both LW and AB forces depend on interfacial tensions, which are in turn determined by hydrophobicity of the sorbate and sorbent

surfaces. Thermodynamic calculations revealed a dominant effect of hydrophobicity of sorbates and sorbents on sorption (Chattopadhyay and Puls, 1999).

Virus sorption usually increases with increasing cation concentration in solution,

particularly in the presence of divalent cations (Bales et al., 1991; Bitton et al.,

1976; Drewry and Eliassen, 1968; Lipson and Stotzky, 1983; Moore et al., 1975).

The enhanced sorption is attributed to the decrease of the thickness of the electric



Table III

Virus Sorption to Soil and Aquifer Material Studied in Batch Systems

Sorbent



Resultsa



MS-2



Hydrophilic and hydrophobic

silica (pH 5 and 7)



Sorption conformed to linear Freundlich isotherm;

strong sorption to hydrophobic silica at pH 5

and 7; no sorption to hydrophilic silica at pH 7



Bales et al. (1991)



Poliovirus 1



Magnetite



Adsorption enhanced by presence of cations; no

effect of pH between pH 5 and 9, less sorption

at pH 4; sorption conformed to nonlinear

Freundlich isotherm; saturation-limited

behavior



Bitton et al. (1976)



φX174



5 soils (pH 6–7.2)



Sorption conformed to nonlinear Freundlich but

not Langmuir isotherm; no significant

correlation of K with pH, CEC, OC, and

specific surface area; amount of viruses sorbed

related to square root of time



Burge and Enkiri (1978a)



T2, MS-2, φX174



Clays (hectorite, saponite,

kaolinite, Norman clay)



Total free energy (δG) assumed to be the sum of

δGH (δG due to hydrophobic interactions) and

δGEL (δG due to electrostatic interactions);

hydrophobic interactions dominated during

sorption of the selected bacteriophages on the

selected clays



Chattopadhyay and Puls (1999)



Bacteriophages T1, T2, f2



9 soils (pH 4.7–6.3)



Sorption conformed to nonlinear Freundlich

isotherm; decreased sorption when pH

increased from 7 to 9; increased sorption with

increased cation concentration for some soils

only; increased sorption with increased CEC,

clay content, and OC.



Drewry and Eliassen (1968)



Poliovirus 1



Loamy sand soil



Sorption conformed to nonlinear Freundlich

isotherm.



Gerba and Lance (1978)



Virus



References



46



9 soils



Sorption is strain dependent; viruses grouped

according their sorption characteristics,

Group I, weakly sorbed, affected by pH, OC;

Group II, strongly sorbed, not affected by soil

characteristics; exception f2 which adsorbed

least to all of the soils



Gerba et al. (1981)



9 soils (pH 4.5–8.2)



Sorption is strain dependent, pH most significant

soil characteristic influencing sorption; strong

sorption when pH less than 5. Poliovirus 1 and

coliphage T4 sorbed better than all other

viruses. Echiovirus 1 and coliphage f2 sorbed

least.



Goyal and Gerba (1979)



Ottawa sand (pH 7)



Sorption of φX174 conformed to linear

Freundlich isotherm; no sorption of MS-2.



Jin et al. (1997)



Reovirus



Kaolinite (K), montmorillonite

(M) (pH 9.5)



More reovirus was adsorbed by M than by K.

Adsorption was essentially immediate and

correlated with CEC of the clays. The addition

of cations, especially divalent cations enhanced

virus adsorption. Constant partition-type

adsorption isotherm obtained.



Lipson and Stotzky (1983)



Reovirus, T1



Kaolinite (K) and

montmorillonite (M) (pH 7)



Reovirus type 3 and coliphage T1 did not share

common adsorption sites on K and M.

Compounds in the minimal essential medium

blocked T1 adsorption to K and M under some

experimental conditions. Results indicate there

was a specificity in adsorption sites for mixed

virus population.



Lipson and Stotzky (1984b)



Poliovirus 1



6 silicate minerals



Organic matter competes with virus sorption and

desorbs viruses, different sorption on different

silicates.



Lo and Sproul (1977)



Poliovirus 1; echovirus 1

isolates Farouk, V212,

V239, and V248;

coxsackievirus B3 and B4

isolates V216, V240;

rotavirus SA11;

bacteriophages MS-2,

φX174, T2, T4, f2

Poliovirus 1, 2, 3; echovirus

1–8, 11–13, 24–27, 29, 31,

and isolates; coxsackievirus

B1–B6, rotavirus SA11,

bacteriophages MS-2,

φX174, T2, T4, f2

MS-2, φX174

47



continues



Table III—continued

Sorbent



Resultsa



PRD-1



Quartz, ferric

oxyhydroxide-coated quartz



Attachment behavior changes at a pH value about

2.5–3.5 pH units above the pHIEP, below this

pH value the attachment is irreversible, above

this pH value attachment is reversible;

attachment described by DLVO potential

theory.



Loveland et al. (1996)



Poliovirus 1, bacteriophage

T2, T7, f2



Bentonite, kaolin, organic

particulates



T2, f2 more readily sorbed in presence of divalent

cations. Poliovirus and T7 sorb equally well to

organic and inorganic particulates; viruses

remain infective in sorbed state.



Moore et al. (1975)



Poliovirus 2



34 soils (pH 7)



Sorption conformed to nonlinear Freundlich

isotherm at low saturation, to Langmuir

isotherm at high concentrations;

saturation-limited behavior, most effective

sorbents were magnetite and hematite.



Moore et al. (1981)



Reovirus



30 soils, minerals, rocks (pH 7)



Adsorption increases with presence of divalent

cations and increasing available surface area;

adsorption decreases with presence of soluble

organic matter; adsorption inversely correlated

with capacity to adsorb cationic

polyelectrolytes and with electrophoretic

mobility.



Moore et al. (1982)



Poliovirus 1



Different oxides (pH 7)



Sorption conformed to nonlinear Freundlich

isotherm; adsorption and desorption points

coincide, no sorption hysteresis; application of

DLVO theory.



Murray and Parks (1980)



Virus



References



48



MS-2 sorption to both types of material

adequately described by Freundlich isotherm;

the amount of MS-2 sorption was controlled by

surface area and the shape of the activated

carbons used.

Sorption conformed to linear Freundlich

isotherm; sorption increased in the order MS-2,

PRD-1, poliovirus.

More T7 adsorbed to M than T1, but the same

amount sorbed to K. Adsorption confirmed to

equilibrium isotherm. Mechanisms involved

varied between the viruses and the clay

minerals.



Powell et al. (2000)



Activated carbons (granular

Calgon F-400, activated

carbon fiber composite

(ACFC)) (pH 7.4)



Poliovirus 1, MS-2, PRD-1



Sandy soil (pH 7.3)



T1 and T7



Kaolinite (K) and

montmorillonite (M)

(pH 7.1–7.4)



Poliovirus 2



Ottawa sand, montmorillonite,

3 soils



Sorption is consistent with pH-dependent charge

properties of virus and sorbent; there is a

critical pH region where sorption changes from

strong to weak; effect of electrolytes on

sorption was only significant at pH above the

critical region.



Taylor et al. (1981)



MS-2, φX174



Ottawa sand (pH 7.5)



Sorption of φX174 conformed to linear

Freundlich isotherm; no sorption of MS-2.



Thompson et al. (1998)



MS-2, φX174



Loamy sand, sandy loam

(pH 7.5)



Sorption conformed to nonlinear Freundlich

isotherm; different apparent sorption observed

in glass and polypropylene test tubes.



Thompson et al. (1998)



Poliovirus 1



Ottawa sand, montmorillonite

(pH 7.3)



Sorption to sand described by Langmuir isotherm;

saturation-limited behavior with low fractional

coverage f of sand particles (f = 0.01); sorption

to montmorillonite described by nonlinear

Freundlich isotherm.



Vilker et al. (1983)



49



MS-2



a



K, sorption coefficient; OC, organic carbon, CEC, cation-exchange capacity.



Powelson and Gerba (1994)



Schiffenbauer and Stotzky (1981)



50



JIN AND FLURY



double layer (Gerba, 1984). Solution pH determines the net charge of viruses and

sorbents and is therefore a dominant factor (Bales et al., 1991; Drewry and Eliassen,

1968; Goyal and Gerba, 1979). Hydrophobic effects may also play a major role.

Bales et al. (1991) showed that sorption of MS-2, which is a relatively hydrophobic

virus, was dominated by hydrophobic factors. They also demonstrated increased

sorption with increased temperature. This temperature effect might be due to the

endothermic unfolding of protein structures at the interface or due to increased

sorption rate at higher temperatures (Bales et al., 1991).

Although virus sorption has been studied extensively, no standard procedure or

systematic approach has been developed and followed. As a result, experimental

conditions differ from study to study, which makes it difficult to draw general

conclusions from the available data about the extent as well as the mechanisms

of virus sorption. Nevertheless, key variables influencing virus sorption have been

identified, which include pH and ionic strength of the solution, presence of compounds competing for sorption sites (e.g., organic materials), properties of the

virus (mainly isoelectric point and hydrophobicity), and properties of the sorbent.

Sorption is favored when viruses and sorbents have opposed electric charge, a

situation which usually occurs in natural porous media when the solution pH is

lower than the pHIEP of the virus. Increased ionic strength compresses the electric

double layer and results in increased virus sorption. Organic matter may provide

hydrophobic sorption sites for viruses, although organic matter in dissolved form

competes with viruses for the available sorption sites. A detailed review on how

different factors affect adsorption of viruses to soil can be found in Schijven and

Hassanizadeh (2000).



B. MODELING OF VIRUS SORPTION

1. Equilibrium

Sorption of viruses is usually determined in a batch experiment, where a virus

solution is mixed with a sorbent and shaken for a certain amount of time to let the

system equilibrate. The time to reach equilibrium is usually considered to be less

than 24 h. The equilibrium times used in sorption experiments range from 20 min

to 24 h.

Sorption data have usually been analyzed by the Langmuir or Freundlich

isotherm models (Table IV). The Langmuir and Freundlich isotherms are given by

Langmuir :



Smax K L C

1 + KLC



(1)



S = K Cn,



(2)



S=



Freundlich :



Table IV

Freundlich Sorption Isotherms for Viruses Reported in the Literature

Chemistry of background

electrolyte



Equilibrium time

and temperature



K and Kd value

(mL g−1)



20 min, 25◦ C

18 h, 26◦ C

18 h, 26◦ C

18 h, 26◦ C

18 h, 26◦ C

18 h, 26◦ C

1 h, 4◦ C



K = 553000, n = 0.736

K = 72.5, n = 1.058

K = 161, n = 1.101

K = 457, n = 0.806

K = 4.61, n = 1.092

K=0

K = 505, n = 1.2



Bitton et al. (1976)

Burge and Enkiri (1978b)



60 min, 24◦ C

60 min, 4◦ C

60 min, 4◦ C

60 min, 4◦ C

60 min, 4◦ C

3 h, 6–9◦ C

3 h, 6–9◦ C

3 h, 6–9◦ C

3 h, 6–9◦ C

3 h, 6–9◦ C

3 h, 6–9◦ C



φX174



Loamy sand



pH 7.5, Phosphate buffer salinea



3 h, 6–9◦ C



φX174



Sand loam



pH 7.5, Phosphate buffer salinea



3 h, 6–9◦ C



Kd = 580

Kd = 270

Kd = 0

Kd = 6.6

Kd = 8300

Kd = 0.74

Kd = 0

Kd = 0

Kd = 0.076

Kd = 0.44

Kd = 0.44b

K = 0.74, n = 0.88c

K = 2.9, n = 1.09b

K = 1.01, n = 1.16c

Kd = 6.5b

Kd = 11, n = 1.06c



Bales et al. (1991)



φX174

MS-2

MS-2

MS-2

MS-2

φX174



Hydrophilic silica

Hydrophilic silica

Hydrophilic silica

Hydrophilic silica

Hydrophobic silica

Ottawa sand

Ottawa sand

Ottawa sand

Loamy sand

Sandy loam

Ottawa sand



1610 mg L−1 CaCl2

pH 6.9, 0.03 M NaCl

pH 6.2, 0.02 M NaCl

pH 6.0, 0.02 M NaCl

pH 6.8, 0.02 M NaCl

pH 7.2, 0.02 M NaCl

pH 7, 1mM CaCl2, 1.25 mM

NaHCO3

Ca phosphate buffer, pH 5

Ca phosphate buffer, pH 5

Ca-free phosphate buffer, pH 7

Ca-free phosphate buffer, pH 5

Ca-free phosphate buffer, pH 5 and 7

pH 7.5, Phosphate buffer salinea

pH 7.5, Phosphate buffer salinea

pH 7.5, Phosphate buffer salinea

pH 7.5, Phosphate buffer salinea

pH 7.5, Phosphate buffer salinea

pH 7.5, Phosphate buffer salinea



Virus

Poliovirus 1

φX174



Poliovirus 1

MS-2



a



Sorbent

Magnetite

Clay loam

Silt loam

Silt loam

Silt loam

Loamy sand

Ottawa sand



0.1 M NaCl, 0.003 M KCl, 0.02 M Na2HPO4.

In glass tubes.

c

In polypropylene tubes.

b



References



Moore et al. (1981)



Jin et al. (1997)

Thompson et al. (1998)



52



JIN AND FLURY



where S and C are sorbed and solution concentrations, respectively; Smax is the

maximal sorbed concentration; and KL, K, and n are constants. In the Langmuir

isotherm, the sorbed concentration reaches the asymptotic value Smax when the

concentrations of dissolved chemicals or microbes are large (C

1). For small

concentrations (C

1), the Langmuir isotherm reduces to the linear Freundlich

isotherm,

S = K d C,



(3)



where Kd is usually denoted as the distribution coefficient.

Empirical laws such as the Langmuir and Freundlich isotherms do not yield any

information about the particular sorption mechanisms. The constants K, Kd, and

KL embrace all the possible sorption mechanisms. For example, the distribution

coefficient Kd may be written as (Schwarzenbach et al., 1993)

Kd =



Som f om + Smin A + Sie σie A + Srxn σrxn A

,

C



(4)



where Som, Smin, Sie, and Srxn are sorbed concentrations associated with organic

matter, mineral surfaces, electrostatic forces, and reversible chemical reactions,

respectively; fom is the fraction of organic matter; A is the surface area of minerals;

σ ie and σ rxn are the concentrations of charged and reactive sites on the solid surface.

For a charged, organic macromolecule such as a virus, all the mechanisms in Eq. (4)

play a role in the sorption process. Depending on the type of virus and sorbent and

the chemistry of the solution, some are more important than others. Given the large

variability in experimental conditions used to study virus sorption, it is therefore

not surprising that the Kd or K values reported vary considerably among various

studies (Table IV).

2. Kinetics

Kinetic models for virus sorption have almost exclusively been used in

connection with transport models. Basically two different approaches are used,

based on either first-order sorption kinetics or filtration theory. First-order kinetics

is formulated as

dS

= κ1 C − κ2 S,

dt



(5)



where κ 1 and κ 2 are the rate coefficients. This type of kinetics has often been

used to describe virus sorption (e.g., Sim and Chrysikopoulos, 1995). Grant et al.

(1993) proposed a compartment model that includes sorption and inactivation of

viruses. In this model, viruses can (i) inactivate in solution, (ii) adsorb reversibly

and irreversibly, (iii) inactivate after reversible and irreversible adsorption, (iv)

and transform from reversibly sorbed status to irreversibly sorbed status (Fig. 3).



SUBSURFACE VIRUS FATE AND TRANSPORT



53



Figure 3 Compartmental model for virus inactivation and sorption. Solid lines indicate an active

virus; dashed lines denote an inactive virus. Ellipses represent an irreversibly sorbed virus. Adapted

from Grant et al., 1993. Kinetic analysis of virus adsorption and inactivation in batch experiment. Water

Resour. Res. 29, 2067–2085. Copyright [1993] American Geophysical Union. Reproduced/modified

by permission of American Geophysical Union.



All sorption and inactivation reactions in this model are assumed to be of

first-order kinetics.

Other types of rate laws have been proposed for bacteria, and have recently

been applied to viruses (e.g., Chu et al., 2001; Sim and Chrysikopoulos, 2000).

Such rate laws include Langmuir-type and second-order kinetics (Bengtssen and

Lindqvist, 1995; Tan et al., 1994), expressed respectively as

∂S

= κ1 (Smax − S)C − κ2 S

∂t

∂S

= κ1 (Smax − S)C − κ2 C S.

∂t



(6)

(7)



3. Aggregation and Filtration

Viruses have often been considered to be of colloidal nature, and the concepts

used in colloid aggregation and filtration have been applied to describe virus retention and transport through porous media (Gerba, 1984; Loveland et al., 1996;

Murray and Parks, 1980). A colloid is considered to be a particle with a diameter

less than 2 to 10 μm. Colloids do not dissolve and remain suspended in waters

because their gravitational setting is less than 10−4 m s−1 (Stumm and Morgan,

1981). Colloids may aggregate when they contact each other in a solution under

favorable chemical conditions. The kinetics of colloid aggregation in monodisperse, static suspension due to collisions by Brownian motion can be represented

as a second-order process (Stumm and Morgan, 1981),

dN

= −k p N 2 ,

dt



(8)



54



JIN AND FLURY



where N is the number of particles in solution and kp is the rate coefficient for

colloid aggregation. According to von Smoluchowski (1917), the rate coefficient

kp can be expressed as

k p = α p 4Dπ d,



(9)



where D is the Brownian diffusion coefficient and d is the particle diameter. The collision efficiency factor α p describes the fraction of collisions that lead to permanent

aggregation. When the diffusion coefficient is expressed by the Einstein–Stokes

relation D = kT/(3πηd), then Eq. (8) can be written as

dN

4kT 2

= −α p

N ,

dt





(10)



where k is the Boltzmann constant, T is the absolute temperature, and η is the

dynamic viscosity. In a moving fluid, particles may have more chances to collide

and aggregation may increase. The rate of aggregation due to fluid motion caused

by a uniform velocity gradient dv/dz may be expressed as (Stumm and Morgan,

1981)

4 dv

dN

= − α0 d 3 N 2 ,

(11)

dt

3 dz

where the parameter α 0 is analogous to α p. If the volume of particles remains

constant during aggregation, Eq. (11) can be written as

4

dN

dv

= − α0 ϕ N ,

dt

π

dz



(12)



where



π 3

d N0

(13)

6

is the total volume of particles in suspension. The overall rate of aggregation may

then be given by adding collisions due to Brownian motion (Eq. 10) and due to

fluid motion (Eq. 12),

ϕ=



4kT 2 4

dv

dN

= −α p

N − α0 ϕ N .

dt



π

dz



(14)



The first term is more important than the second term for particles with a diameter

smaller than 1 μm (Stumm and Morgan, 1981).

Aggregation of colloids is closely related to filtration processes. The kinetic

equation for particle removal by filtration can be expressed as (Tien, 1989)

dC

= −λC,

(15)

dz

where λ is the filtration coefficient. The filtration coefficient is not constant because

the properties of the porous media that acts as a filter changes during proceeding



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