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Chapter 2. Fate and Transport of Viruses in Porous Media

Chapter 2. Fate and Transport of Viruses in Porous Media

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40



JIN AND FLURY

modeling of virus sorption, (ii) virus survival and factors affecting virus inactivation

in the natural environment, and (iii) mechanisms of virus transport in porous media

and available modeling approaches. Because viruses are surrounded by a protein

capsid and are expected to behave similarly to proteins, an overview on the mechanisms of protein sorption and denaturation is also provided. Factors such as solution

chemistry, virus properties, soil properties, temperature, association with solid particles, and water content have been found to influence virus sorption, survival, and

transport in porous media. A review of protein literature provides some insights as

to what mechanism might be involved in virus sorption that have so far not been

C 2002 Elsevier Science (USA).

studied. Some needs for future research are suggested.



I. INTRODUCTION

Viruses that are present in septic tanks, sewage sludges, wastewater, and other

sources can be transported into ground and surface waters. About 70% of the waterborne illness outbreaks in the United States has been associated with groundwater

(Craun, 1991; Herwaldt et al., 1992). In 1990, the U.S. Environmental Protection

Agency (USEPA) Science Advisory Board cited drinking-water contamination as

one of the highest ranking remaining environmental risks (USEPA, 1990). The

Science Advisory Board reported that microbiological contaminants (e.g., bacteria, protozoa, and viruses) are likely to be the greatest remaining health riskmanagement challenge for drinking-water suppliers. These risks are most likely

associated with groundwater. However, whereas stringent regulations to control

microbial contaminants apply to drinking-water systems using surface water, only

limited regulations apply to systems using groundwater (Macler and Merkle, 2000).

Although viruses are not the only pathogens known to contaminate groundwater,

they are much smaller in size than bacteria or protozoan cysts and are not filtered out

to the same extent in the porous soil matrix, thereby may move better through the

subsurface. Knowledge of the factors that influence the fate and transport of viruses

in soils and aquifers is critical to making accurate determinations of groundwater

vulnerability and to developing regulations that are protective of public health.

During passage through soil and aquifer systems, viruses are removed from the

water by attachment and inactivation processes, and both these processes depend

upon a number of factors (Table I). Natural soils and aquifers may serve as disinfection media. “Natural disinfection” is an essential component of the soil-aquifer

treatment process for removing viruses released from various sources in the subsurface. Determination of disinfection efficiency and groundwater vulnerability

requires accurate prediction of virus fate and transport in the subsurface. However,



Table I

Factors Influencing Virus Fate in the Subsurfacea

Factor



Influence on survival



Temperature



Viruses persist longer at low

temperatures.



Microbial

activity



Some viruses are inactivated more

readily in the presence of certain

microorganisms, while sorption to the

surface of bacteria can be protective.

Most viruses survive longer in moist

soils and even longer under saturated

conditions; unsaturated soil may

inactivate viruses at the air–water

interface.

Most enteric viruses are stable over a pH

range of 3–9; however, survival may

be prolonged at near-neutral

pH values

Certain cations may prolong survival

depending upon the type of virus.



Moisture content



pH



Salt species and

concentration



Virus association

with soil



Viral association with soil generally

increases survival, although

attachment to certain mineral surfaces

(e.g., oxides and hydroxides) may

cause inactivation.



Soil properties



Effects on survival are probably related

to the degree of virus sorption, either

prolonged or shortened depending on

the properties of soil particles.

Different virus types vary in their

susceptibility to inactivation by

physical, chemical, and biological

factors.

Organic matter may prolong survival by

competitively binding to air–water

interfaces where inactivation can

occur; organic matter may also retard

viral infectivity.



Virus type



Organic matter



Hydraulic

conditions



A moving air–water interface may

inactivate hydrophobic viruses.



Influence on migration

Viruses migrate farther when

inactivation is smaller; higher

temperature tends to increase sorption

to soils.

Unknown



Virus migration usually increases under

saturated flow conditions as compared

to unsaturated conditions; the

air–water interface can sorb viruses,

thereby decreasing migration.

Low pH typically increases virus

sorption to soils; high pH causes

desorption thereby facilitating greater

mobility.

Increasing ionic strength of the

surrounding medium will generally

increase attachment to soils thus

decrease mobility.

Viruses interacting with soil particles

are inhibited from migrating through

the soil matrix.



Greater migration in coarse-textured

soils; fine-textured soils, especially

clays, tend to sorb more viruses.

Virus sorption to soils is related to

physicochemical differences in capsid

surface structure and amino acid

sequence.

Soluble organic matter competes with

viruses for adsorption on soil particles

which may result in increased virus

migration; bonded organic matter

may provide hydrophobic binding

sites for viruses which may decrease

virus migration.

Virus migration generally increases at

higher hydraulic loads and flow rates.



a

Adapted and expanded from Yates and Yates (1988). Reprinted with permission from Crit. Rev. Environ.

Control 17, 307–344. Copyright CRC Press, Boca Raton, Florida.



42



JIN AND FLURY



quantitative information on the basic factors controlling virus fate is insufficient to

allow model predictions. Specifically, the use of models for regulatory purposes has

been questioned, particularly because uncertainties about input parameter values

may lead to large errors in model outputs (Yates, 1995; Yates and Jury, 1996).

The uncertainty of model parameters arises in part from insufficient knowledge of

virus sorption and inactivation characteristics during transport in porous media.

Regulatory agencies, such as the USEPA, have the task to protect drinkingwater resources from contamination by pathogenic organisms. Effective policy

making and the establishment of disinfection rules concerning viruses in drinking

water require a thorough understanding of the fate and transport of viruses in

subsurface waters. For instance, the question whether, and under what conditions,

viruses released from a septic tank system may pose a threat to a drinking-water

well need to be answered. The need to better understand the factors affecting and

limiting microbial contamination of groundwater sources has been reemphasized

recently (Macler and Merkle, 2000). The outstanding issues identified include the

hydrogeological properties affecting groundwater vulnerability to contamination

and the physical and chemical properties governing fate and transport of viruses

in the subsurface including the unsaturated zone, the capillary fringe, and the

saturated zone (Fig. 1).

Viruses are microorganisms that are composed of RNA or DNA that is surrounded by a protein capsid. Fate and transport of viruses in the environment are

largely determined by this protein coating. With respect to sorption and transport

processes, viruses and proteins may therefore be regarded as “macromolecules”



Figure 1 Schematic of virus transport from septic tank system to a drinking-water well, indicating

the pathways through the vadose zone, the capillary fringe, and the groundwater.



SUBSURFACE VIRUS FATE AND TRANSPORT



43



with similar characteristics. Protein adsorption at solid surfaces has been an active

area of research. This is motivated by the importance of protein adsorption for both

fundamental biochemical and biophysical processes and a variety of medical applications, including biomaterials, extracorporeal therapy, drug delivery, and solidphase diagnostics (Malmsten and Veide, 1996). Despite the similarities between

viruses and proteins, virus and protein sorption has been treated separately in the

literature, probably due to the isolation between the different disciplines engaged

in protein and virus research.

In this paper, we review the current state of knowledge on fate and transport

of viruses in porous media. We also present an overview of the mechanisms of

virus and protein sorption and transport and compare the different concepts used

to analyze virus and protein sorption.



II. CHARACTERISTICS OF VIRUSES RELEVANT

FOR SUBSURFACE FATE AND TRANSPORT

Viruses are obligate intracellular parasites that are incapable of replication outside of a host cell. Their structure consists of a protein capsid enclosing a nucleic

acid genome of RNA or DNA (Harrison, 1985). The capsid is made up of multiple

protein subunits, each of which is a single folded polypeptide chain. Viruses are

either enveloped or nonenveloped. A nonenveloped virus consists of a capsid and

associated nucleic acids, together termed the nucleocapsid. An enveloped virus

has a similar nucleocapsid, which is enclosed by an envelope consisting of both

glyco- and lipoproteins. Fate and transport of viruses in the environment are largely

determined by properties of the protein coating.

The most relevant properties of a virus with respect to subsurface fate and transport are morphological characteristics, including size, shape, and density, and the

physicochemical properties, including electrophoretic mobility, net charge, and hydrophobicity. The coating of viruses, whether enveloped or nonenveloped, contains

polar, nonpolar, and ionic regions (e.g., Mix, 1974). The charge distribution originating from the ionic regions is heterogeneous, with pH-dependent positive and

negative charges occurring simultaneously at different locations. Electrophoretic

mobility is a key parameter to characterize the charge of a virus. Often the electrophoretic mobility as a function of pH is not documented in the literature, but

rather the isoelectric point (pHIEP); i.e., the pH where the electrophoretic mobility

vanishes, is reported. Although the pHIEP alone does not provide detailed information about charge densities, it provides an important benchmark for charge reversal

relevant to an electric field and is as such a key characteristic for electrokinetic

phenomena.



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



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