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VIII. Indicators for Human Enteroviruses

VIII. Indicators for Human Enteroviruses

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SUBSURFACE VIRUS FATE AND TRANSPORT



87



PRD-1). In addition, some common disease-causing viruses (hepatitis A virus,

rotaviruses, and Norwalk virus) cannot as yet be detected practically, and techniques available for the recovery and identification of human enteric viruses often

have limited sensitivity. Use of “indicator” organisms to assess HEV behavior

in subsurface medium is necessary and has been practiced for almost a century.

Characteristics of coliphages and their suitability to serve as indicator have been

reviewed by Snowdon and Cliver (1989). An ideal indicator of viral contamination

of groundwater should possess the following particular properties (IAWPRC

Study Group on Health Related Water Microbiology, 1991; Snowdon and Cliver,

1989):

1.

2.

3.

4.

5.

6.

7.

8.

9.

10.



be applicable in all types of groundwater

be unable to reproduce in contaminated water

relate specifically to contamination by human feces

have a density in contaminated water that directly relates to the degree of

fecal pollution

enable rapid detection and unambiguous identification

be nonpathogenic to humans

be present whenever HEV are present, and in greater numbers

have physical properties similar to HEV

be similar to HEV in adsorption to soils and transport through groundwater

have a survival time as long as the most persistent HEV



The suitability of a particular virus as an indicator is evaluated based on relative

insensitivity to inactivation (Yates et al., 1985) and its ecological and morphological similarities to human pathogens (Havelaar et al., 1993). Coliphages, particularly RNA-phage, have been proposed as suitable indicators for HEV (Snowdon

and Cliver, 1989). Among the coliphages, MS-2 has been suggested to be the most

suitable indicator (Springthorpe et al., 1993; Yates et al., 1985).

From the hydrological point of view, a worst-case indicator for transport and

fate of HEV does not need to include all the criteria listed previously. We propose

that such an indicator should

1. be unable to reproduce in contaminated media (soil, water)

2. show similar or less sorption and retention than HEV in porous media under

identical conditions

3. be at least as resistant to inactivation under natural conditions as HEV

4. be nonpathogenic to humans and other animals (only if used as tracer in the

field)

We may call this type of indicator a transport indicator, to differentiate from

the pollution indicator that indicates viral pollution of groundwater.

Because of the extremely complex sorption and transport mechanisms of

viruses, recent studies have raised doubts regarding the applicability of any single



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indicator’s ability to mimic the behavior of HEV. MS-2 has been shown to be relatively easily inactivated in unsaturated systems and in the presence of metal oxides

(Chu et al., 2000; Jin et al., 2000a). Penrod et al. (1996) compared the deposition

kinetics of bacteriophages MS-2 and λ and found that even subtle differences in

viral surface structures could significantly influence the rate at which viruses were

removed from the water phase by infiltration. Taking a different approach, Redman

et al. (1997) used recombinant Norwalk virus (rNV) particles as a model system

to study the filtration behavior of Norwalk virus (NV), the human pathogen. The

biochemical procedure used to created the rNV particles is given in Redman et al.

(1997). The resulting rNV particles are morphologically and antigenically similar

to the native NV but lack the genetic material (i.e., RNA) so they are harmless

and cannot infect humans. Such rNV particles may be ideal to be used as a model

system for transport studies because they can be grown to high concentration, and

their noninfectious character implies that experiments at the field scale may be

possible (Redman et al. 1997). A comparison of the behavior between MS-2 and

rNV indicates that MS-2 is not a suitable surrogate for NV. Redman et al. (1997)

also pointed out that the rNV particle system is not well suited to simulate the

inactivation behavior of the real NV.

Considering the complex sorption and retention mechanisms of viruses, it is

unlikely that any single compound or microorganism will be able to adequately

represent the transport behavior of different HEV in porous media (Penrod et al.,

1996). Caution should be used when extrapolating results from studies conducted with indicator microorganisms or other types of colloidal particles to the

behavior of HEV, as such indicators are likely inadequate to represent human

pathogens.



IX. CONCLUDING REMARKS

There is evidence that large-scale virus transport occurs in the subsurface environment. The USEPA estimates that annually in the United States16 people are

at risk of death and 168,000 people are at risk of viral illness from consuming

groundwater contaminated with pathogenic viruses (USEPA, 2000). Development

of effective regulations to protect public health from microbial contamination relies on a thorough understanding of key processes governing virus survival and

transport in the natural environment.

Considerable knowledge has been accumulated from research conducted over

the last 20 to 30 years. The influence of the factors affecting virus sorption

and inactivation have been extensively studied and well documented. Solution

chemistry (pH and ionic strength), virus properties (isoelectric point and surface



SUBSURFACE VIRUS FATE AND TRANSPORT



89



characteristics), soil properties (organic matter content, CEC, presence of metal

oxides, etc.) have been found to affect virus sorption to various degrees, while

temperature, association with solid particles, and water content are among the

factors identified that affect virus survival. Laboratory and field experiments have

revealed many factors and processes that attenuate virus transport through porous

media.

As presented in this article, results from protein research provide some insights

as to what mechanisms might be involved in virus sorption that have so far not

been studied extensively. For example, the sorption mechanism seems to be affected largely by particle size, and there might be a transition between reversible

and irreversible sorption for particles in the size range of viruses. Such information is essential for identifying the appropriate models to describe virus sorption

behavior. Also lacking is information on reaction kinetics involved in virus sorption/desorption processes, especially under conditions that are closely related to

field conditions. Considering that one single virus can cause infection, the possible

slow desorption kinetics of viruses needs detailed investigation. Carefully designed

field scale studies are needed to investigate the extent that chemical and physical

heterogeneities of natural porous materials affect virus retention and transport. An

even more challenging task of future research is to effectively apply fundamental

theories from laboratory studies to the field. Some research needs are summarized

as follows.

r Examine virus sorption mechanisms using both macroscopic and microscopic

techniques and identify/develop appropriate models.

r Study kinetics of virus sorption/desorption, and develop quantitative descriptions

of these processes.

r Investigate the influence of physical and chemical heterogeneity on virus transport and retention in natural porous media.

r Elucidate mechanisms of virus inactivation during transport in unsaturated systems, and develop appropriate models to quantify these processes.

r Study the role and extent of colloids in facilitating virus transport behavior and

their effect on virus survival in natural media.

r Systematically compare the behavior of the commonly used model viruses with

that of the representative pathogens to identify more reliable surrogates for the

pathogens.

In summary, viruses and other pathogenic microorganisms may be one of the

greatest health risks and management challenges for our drinking water resources.

Viruses pose a public health threat at a very low level; e.g., the USEPA states a limit

of 2 virus particles per 107 L of water to achieve an annual infection risk of less than

10−4 (USEPA, 1994). Such a drinking-water limit can only be achieved through a

more thorough understanding of virus fate and transport in the subsurface.



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JIN AND FLURY

X. APPENDIX



Symbol



Description



a

a

aeff

A

ADE

AWI

C

C

Ctot

Ctot,in

d

D

DDisp

DLVO

fom

h0

K

Kd

KL

k

ka

kd

kp

k1 , . . . , k 8

L

N

N0

n

pHIEP

RSA

S

S

Sin

Smax

Smin

Sie

X1, . . . , Xn

Som

Srxn

TPB

t

v

U

Uin



Diameter of filter grain

Radius of filter grain

Effective radius of filter grain

Area of mineral surfaces per mass of solid

Advection–dispersion equation

Air–water interface

Concentration of dissolved chemical

Concentration of viable viruses in liquid phase

Total concentration of viable viruses

Total concentration of inactivated viruses

Diameter of particle

Brownian diffusion coefficient

Dispersion coefficient

Derjaguin–Landau–Verwey–Overbeek

Fraction of organic matter

Water-film thickness

Constant in Freundlich isotherm

Distribution coefficient

Constant in Langmuir isotherm

Boltzmann’s constant (1.3805 × 10−23 J K−1)

Attachment rate

Detachment rate

Rate coefficient in colloid aggregation

Ad- and desorption rate coefficients

Length of filter bed or space coordinate

Number of particles per unit suspension volume

Initial number of particles per unit suspension volume

Constant in Freundlich isotherm

isoelectric point

Random Sequential Adsorption

Concentration of sorbed chemical

Concentration of sorbed viable viruses

Concentration of sorbed inactivated viruses

Maximal concentration of sorbed chemical in Langmuir isotherm

Concentration of sorbed chemical associated with mineral surfaces

Concentration of sorbed chemical bonded by electrostatic forces

Various factors affecting virus inactivation

Concentration of sorbed chemical associated with organic matter

Concentration of sorbed chemical bonded by reversible reaction

Triple-phase boundary

Time

Pore water velocity

Concentration of viable viruses at air-water interface

Concentration of inactivated viruses at air-water interface



Dimension

[L]

[L]

[L]

[L2 M−1]

[ML−3]

[ML−3]

[ML−3]

[ML−3]

[L]

[L2 T−1]

[L2 T−1]

[−]

[L]

[L3 M−1]

[L3 M−1]

[L3 M−1]

[L3 M−1 T−1]

[T−1]

L3 T−1]

[T−1]

[L]

[L−3]

[L−3]

[−]

[−]

[MM−1]

[MM−1]

[MM−1]

[MM−1]

[ML−2]

[ML−2]

[Variable]

[MM−1]

[MM−1]

[T]

[LT−1]

[ML−3]

[ML−3]

continues



91



SUBSURFACE VIRUS FATE AND TRANSPORT

APPENDIX—continued

Symbol

z

α

α0

αp

β 1, . . . ,β n

βt

η

ηs



max



κi

λ

λ0

λl

λs

λu

φ

ρ

σ ie

σ rxn

θ

ϕ

ξ

ζ



Description

Spatial coordinate

Collision efficiency factor for spherical collector model

Collision efficiency factor for colloidal aggregation under uniform

gradient flow

Collision efficiency factor for colloidal aggregation in static solution

Coefficients assigned to variables X1, . . . , Xn

Coefficient assigned to time t

Dynamic viscosity

Single-collector efficiency

Porosity

Surface coverage

Jamming limit in RSA

Rate coefficients

Filtration coefficient

Initial filtration coefficient

First-order inactivation coefficients for the liquid phase

First-order inactivation coefficients for the solid phase

First-order inactivation coefficients for the air-water interface

Blocking factor in surface excusion models

Bulk density

Concentration of charged sites on solid surface

Concentration of reactive sites on solid surface

Volumetric water content

Total volume of particles per unit volume suspension

Effectiveness of particle removal

Volumetric air content



Dimension

[L]

[−]

[−]

[−]

[−]

[−]

[MT−1 L−1]

[−]

[−]

[−]

[−]

[Variable]

[L−1]

[L−1]

[T−1]

[T−1]

[T−1]

[Variable]

[ML−3]

[ML−2]

[ML−2]

[L3 L−3]

[L3 L−3]

[−]

[L3 L−3]



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