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VIII. Indicators for Human Enteroviruses
SUBSURFACE VIRUS FATE AND TRANSPORT
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,
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
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
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
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
JIN AND FLURY
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
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
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
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
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
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.
JIN AND FLURY
k1 , . . . , k 8
X1, . . . , Xn
Diameter of ﬁlter grain
Radius of ﬁlter grain
Effective radius of ﬁlter grain
Area of mineral surfaces per mass of solid
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
Fraction of organic matter
Constant in Freundlich isotherm
Constant in Langmuir isotherm
Boltzmann’s constant (1.3805 × 10−23 J K−1)
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
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
Pore water velocity
Concentration of viable viruses at air-water interface
Concentration of inactivated viruses at air-water interface
[L3 M−1 T−1]
SUBSURFACE VIRUS FATE AND TRANSPORT
β 1, . . . ,β n
Collision efﬁciency factor for spherical collector model
Collision efﬁciency factor for colloidal aggregation under uniform
Collision efﬁciency factor for colloidal aggregation in static solution
Coefﬁcients assigned to variables X1, . . . , Xn
Coefﬁcient assigned to time t
Jamming limit in RSA
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
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
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