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WATER RESOURCES RESEARCH, VOL. 42, W12S12, doi:10.1029/2005WR004805, 2006

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Full
ArticleTransport and straining of E. coli O157:H7 in saturated
porous media
Scott A. Bradford,1 Jirka Simunek,2 and Sharon L. Walker3
Received 13 December 2005; revised 9 May 2006; accepted 7 September 2006; published 18 November 2006.

[1] The transport and deposition behavior of pathogenic Escherichia coli O157:H7 wasstudied under unfavorable electrostatic conditions in saturated quartz sands of various
sizes (710, 360, 240, and 150 mm) and at several flow rates. At a given velocity, column
effluent breakthrough values for E. coli tended to decrease in magnitude, andconcentration curves became more asymmetric with decreasing sand size. In a given sand,experiments conducted at a higher velocity tended to produce higher effluent
concentrations, especially for finer (240 and 150 mm) textured sands. The shape of thedeposition profiles for E. coli was also highly dependent on the sand size and velocity.
Coarser-textured sands and higher flow rates were associated with less deposition andgradually decreasing concentrations with depth. Conversely, finer-textured sands andlower flow rates tended to produce greater deposition and nonmonotonic deposition
profiles that exhibited a peak in retained concentration. This deposition peak occurred
nearer to the column inlet for finer-textured sands and at low flow rates. Microscopic
observations of E. coli retention in these finer-textured sands (micromodel experiments)
clearly indicated that straining was the dominant mechanism of deposition. Batch
experiments also indicated minor amounts of E. coli attachment for the selected sands andsolution chemistry. A conceptual and numerical model was developed and successfully
used to describe the observed E. coli transport and deposition data. Our conceptual model
assumes that E. coli can aggregate when large numbers of monodispersed E. coli aredeposited at pore constrictions or straining sites. When the deposited E. coli reach acritical concentration at the straining site, the aggregated E. coli O157:H7 can be released
into aqueous solution as a result of hydrodynamic shearing forces.
Citation: Bradford, S. A., J. Simunek, and S. L. Walker (2006), Transport and straining of E. coli O157:H7 in saturated porous media,
Water Resour. Res., 42, W12S12, doi:10.1029/2005WR004805.

1. Introduction[2] Escherichia coli O157:H7 is a pathogenic bacteria
strain that can inhabit the intestines of animals and humans.
Gastrointestinal illness in infected individuals is characterized by severe cramping and bloody diarrhea due to the
production of toxins that can damage the lining of theintestine. In a small percentage of cases, infection can leadto a life-threatening complication known as hemolytic
uremic syndrome which involves the destruction of red
blood cells and acute kidney failure (Centers for Disease
Control and Prevention, Escherichia coli O157:H7, fact
sheet, http://www.cdc.gov/ncidod/dbmd/diseaseinfo/
escherichiacoli_g.htm). Surface and groundwater disease
outbreaks have been associated with E. coli O157:H7[Geldreich et al., 1992; U.S. Environmental Protection
Agency (USEPA), 2000; O’Connor, 2002] as well as other1
George E. Brown Jr. Salinity Laboratory, ARS, USDA, Riverside,
California, USA.
2
Department of Environmental Sciences, University of California,
Riverside, California, USA.
3
Department of Chemical and Environmental Engineering, University ofCalifornia, Riverside, California, USA.

Copyright 2006 by the American Geophysical Union.
0043-1397/06/2005WR004805$09.00

pathogenic bacteria. Water contamination by various strainsof E. coli is becoming common in rural areas of the UnitedStates, with up to 40% of tested wells found to be contaminated [USEPA, 1997]. This is a problem of serious concern
because of the low infectious dose for many pathogenic
bacteria [Loge et al., 2002]. Accurate knowledge of theprocesses that control the subsurface transport and survivalof E. coli O157:H7 is therefore needed to assess contamination potential and to develop efficient water treatment
techniques.
[3] Deposition of colloids in porous media has commonly
been assumed to be controlled by attachment (collision withand fixation to the porous media), and therefore describedusing first-order attachment (clean bed filtration) theory[Schijven and Hassanizadeh, 2000; Harvey and Harms,
2002; Jin and Flury, 2002; Ginn et al., 2002; de Jonge etal., 2004]. In this case, an exponential decrease in retained
concentration is predicted with transport distance. A growing body of literature, however, suggests that colloid deposition frequently does not agree with attachment theory
predictions [Camesano and Logan, 1998; Bolster et al.,
1999; Redman et al., 2001; Bradford et al., 2002; Tufenkji etal., 2003; Li et al., 2004; Tufenkji and Elimelech, 2005a,
2005b; Tong et al., 2005a, 2005b]. Deposition profiles formany types of colloids (latex microspheres, bacteria,

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viruses, protists) have been reported to follow a hyperexponential (power law) profile distribution [Albinger et al.,
1994; Baygents et al., 1998; Simoni et al., 1998; Bolster etal., 2000; DeFlaun et al., 1997; Zhang et al., 2001; Redman
et al., 2001; Bradford et al., 2002; Li et al., 2004; Bradford
and Bettahar, 2005], implying a decreasing rate of deposition with increasing transport distance. Conversely, deposition profiles have also been reported to exhibit a peak atsome distance down gradient from the source (nonmonotonic profile) [Tong et al., 2005a].
[4] Various competing explanations have been proposedin the literature to explain nonexponential deposition profiles. These theories can be broadly classified as chemicallyor physically based. Chemical explanations that have been
proposed include: porous media charge variability [Johnson
and Elimelech, 1995], heterogeneity in surface charge
characteristics of colloids [Bolster et al., 1999; Li et al.,2004], deposition of colloids in the secondary energy
minimum of the Derjaguin-Landau-Verwey-Overbeek(DLVO) potential energy distribution [Redman et al.,
2004; Hahn et al., 2004; Tufenkji and Elimelech, 2005b];
time-dependent deposition coefficients [Tan et al., 1994; Liuet al., 1995; Camesano et al., 1999]; and colloid detachment[Tufenkji et al., 2003]. Other researchers have proposed thatnonexponential deposition profiles may occur as a result ofphysical factors that are not included in filtration theory,
such as straining (deposition of colloids in smaller pores andat grain-grain junction) [Bradford et al., 2002, 2003, 2004;
Li et al., 2004; Tufenkji et al., 2004; Bradford and Bettahar,
2005; Foppen et al., 2005], soil surface roughness [Redman
et al., 2001; Kretzschmar et al., 1997], and hydrodynamic
drag [Li et al., 2005].
[5] Our ability to accurately predict the fate of pathogenic bacteria in the subsurface environment, such as
E. coli O157:H7, is currently limited by our incomplete
understanding of deposition mechanisms. The objectiveof this work is to systematically investigate the transportand deposition behavior of E. coli O157:H7 in several
sized sands and at various flow rates. Results from batch,micromodel, and column experiments are used to deduce
deposition mechanisms in these sands and the influenceof system hydrodynamics on these processes. Data analysis and interpretation was aided through numericalmodeling.

2. Materials and Methods
2.1. E. coli O157:H7[6] E. coli O157:H7/pGFP strain 72 (Pina Fratamico,
USDA-ARS-ERRC, Wyndmoor, PA) was used in the transport experiments. Green fluorescence in this bacteria is moststrongly manifested when grown under oxygen rich conditions. To maximize fluorescence, E. coli O157:H7 wasgrown on tryptic soy agar plates (Becton, Dickinson andCo., Sparks, MD) with ampicillin (50 mg mL1 final
concentration). Plates were inoculated 3 days in a row tomake sure that the final culture of bacteria was fully
activated. After 15– 18 hours of incubation, sterile water
was placed on the plates and the colonies were gently
harvested using a sterile glass rod to release the colonies
into solution. The harvested colonies were then combined ina tube, and the bacteria were washed twice with phosphate-

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buffered saline (PBS) solution (FisherBiotech, Fair Lawn,
NJ) by centrifugation at 2862  g for 10 min and thenresuspending in a 0.001 M NaBr solution. This 0.001 M
NaBr solution consisted of deionized water buffered to pH
6.73 using 5  105 M NaHCO3, and the solution electricalconductivity (EC) was 0.14 dS m1. This same 0.001 M
NaBr solution was also used as eluant for the experiments.
[7] An approximate cell concentration of the bacterial
stock was estimated using a calibration between opticaldensity at 550 nm and measured cell concentration. The
bacterial stock was then diluted to the desired concentrationsin the NaBr solution for use in the column studies. The actual
E. coli concentration in the influent solution was quantified
using the spread plating method [Clesceri et al., 1989] on
tryptic soy agar plates with ampicillin (50 mg mL1 final
concentration). Plates were incubated at 37°C overnight
and the concentrations were determined by enumeration.
Colonies were confirmed under UV light.
[8] The relative concentrations of E. coli O157:H7 inliquid samples were determined using a Turner Quantech
Fluorometer (Barnstead/Thermolyne, Dubuque, IA 520049910) equipped with excitation (490 nm: LE1095  13,
NB490) and emission (515 nm: LE1095  23, SC515)
filters. E. coli O157:H7 concentrations (average of triplicate
measurements) were determined using calibration curves
established between instrument response and standard solutions. The established calibration curves always had correlation coefficients very close to unity. This analytic
protocol was sensitive to concentrations over two ordersof magnitude below the initial concentration. Results fromthe fluorometer method discussed above were comparedwith the conventional spread plating technique in several
E. coli O157:H7 transport experiments. Reasonable agreement between the two methods was obtained, although thefluorometer method provided a better mass balance. It
should be noted that both spread plating and fluorometer
techniques for quantifying E. coli concentrations aredesigned for monodispersed cell suspensions, if significant
aggregation occurs then these methods may underestimate
cell concentrations.
[9] The electrophoretic mobility and zeta potential of
E. coli O157:H7 were measured in the 0.001 M NaBr
solution to be 0.21 mm cm V1 s1and 2.72 mV,
respectively, using a ZetaPals instrument (Brookhaven
Instruments Corporation, Holtsville, NY). The average sizeor effective diameter of E. coli O157:H7 was determined tobe 1.16 mm using a Horiba LA 930 laser scattering particle
size analyzer (Horiba Instruments, Irvine, CA 92614). This
instrument was also used to verify the uniformity of theE. coli O157:H7 size distribution; i.e., normal distribution
with a standard deviation of 0.31 mm. The hydrophobicityof E. coli O157:H7 was quantified by using the microbialadhesion to hydrocarbons (MATH) test [Pembrey et al.,1999]. MATH test results indicated that approximately 64%
of the cells partitioned into the hydrocarbon. Viability tests
were performed using the Live/Dead BacLight kit (L-7012,
Molecular Probles, Eugene, OR), and 100% of the cell were
determined to be viable.
2.2. Sand[10] Various sieve sizes of Ottawa aquifer sand (U.S.
Silica, Ottawa, IL) were used in the soil column experi-

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Table 1. Column Properties (Darcy Velocity, q; Porosity, e;Column Length, Lc; and Pulse Duration, To) and the Effluent (Meff),
Sand (Msand), and the Total (Mtotal) Mass Percentage Recovered for
the Experimental Systems
d50, mmq, cm min1eLc, cmTo, min

Meff

Msand

Mtotal

710
710
710
360
360
360
240
240
150
150
150

0.031
0.114
0.196
0.024
0.099
0.196
0.026
0.097
0.017
0.102
0.177

0.334
0.357
0.330
0.341
0.333
0.348
0.324
0.332
0.334
0.341
0.350

12.53
12.97
12.45
12.66
12.50
12.80
12.35
12.49
10.00
12.66
10.00

150.0
75.0
37.5
150.0
75.0
37.5
150.0
75.0
150.0
75.0
37.5

78.2
82.4
80.1
54.3
73.0
68.1
9.2
42.1
0.3
13.2
47.0

23.7
3.2
8.5
43.2
5.8
10.4
85.0
30.4
95.9
52.4
33.8

101.9
85.6
88.6
97.5
78.8
78.5
94.2
72.5
96.2
65.6
80.8

ments. These sands were designated by their median grain
size (d50) as: 710, 360, 240, and 150 mm. The uniformity
index (Ui = d60/d10 where x% of the mass was finer than dx)of the 710, 360, 240, and 150 mm sands was measured to be
1.21, 1.88, 3.06, and 2.25, respectively. Pore size distribution information for these Ottawa sands can be calculated
from capillary pressure – saturation curves presented by
Bradford and Abriola [2001]. Ottawa sands typically consisted of 99.8% SiO2 (quartz) and trace amounts of metaloxides, were spheroidal in shape, and had rough surfaces.
Quartz sands possess a net negative charge at a neutral pH[Redman et al., 2004].
2.3. Batch Experiments[11] Batch experiments were conducted by placing 10 gof Ottawa sand (710, 360, 240, and 150 mm) and 10 mL of aknown initial concentration of E. coli O157:H7 suspension
into a 20 mL glass scintillation vial with the temperature
kept at approximately 20°C. The suspension and sand wereallowed to equilibrate for 4 hours at 150 rpm using an
orbital shaker (Lab-Line, Melrose Park, IL). The initial andfinal concentrations of E. coli O157:H7 in the suspension
were determining using the fluorometer and/or spread plate
methods outlined above. A blank experiment (no sand) was
also run to quantify the potential for E. coli O157:H7
growth or death in the 0.001 M NaBr solution at 20°C.
2.4. Column Experiments[12] Column transport experiments were conducted toinvestigate the transport and deposition behavior of E. coli
O157:H7 under unfavorable attachment conditions. Specifically, buffered solutions (neutral pH) with low ionicstrength, quartz sands, and monodispersed cells were used.
Borosilicate glass Kontes Chromaflex chromatography columns (Kimble/Kontes, Vineland, NJ) (15 cm long and 4.8
cm inside diameter) or stainless steel soil columns (10 cmlong and 5.1 cm inside diameter) were used in the transport
studies. The chromatography columns were equipped with astandard flangeless end fitting at the column bottom and aflow adapter at the top. The flow adapter allowed thecolumn bed length to be adjusted, facilitating the tightsealing of the adapter at the soil surface. The manufacturer’s
bed support at the column inlet and outlet was replaced witha stainless steel wire screen (103 mm mesh spacing) sup-W12S12ported by a coarser polyethylene screen to uniformly
distribute the influent solution at the soil surface. The
stainless steel columns were equipped with standard fittingsand stainless steel wire screen at both of their ends. Tubing
to and from the columns, fittings, column O-rings, and flow
adapter were composed of chemically resistant materials
such as Teflon, viton, stainless steel and Kalrez.
[13] Bradford et al. [2002] provided details on our methods
for packing and cleaning the columns, and determining
porosity. Table 1 provides porosity (e) values and column
lengths for each experimental soil column. A Masterflex L/S
multihead drive pump (Barnant Company, Barrington, IL)
equipped with standard heads was used to pump the E. coli
O157:H7 suspension or eluant (0.001 M NaBr) solution
upward through the vertically oriented columns at a steadyrate. The average aqueous Darcy velocity (q) for the various
column experiments is also given in Table 1, and theexperimental temperature was approximately 20°C. Separate
column experiments were conducted at different flow rates
to better deduce the influence of hydrodynamics on E. coli
O157:H7 deposition. The suspension was pumped upward
to minimize any sedimentation that may occur as a result of
the difference in density between the E. coli O157:H7 andeluant. The E. coli suspension was pumped through thecolumns for approximately 2 pore volumes (PV), after whicha three-way valve was used to switch to the eluant for an
additional 4 PV. Effluent samples were collected in glass test
tubes over the course of each column experiment. E. coli
O157:H7 concentrations in the effluent samples were determined using the fluorometer method discussed above. The
maximum analytic error (twice the standard deviation)
associated with triplicate relative concentration measurements was 0.028, and typically values were around 0.008.
[14] Following completion of the transport experiments,
the deposition profile for E. coli O157:H7 retained in thesand was determined. The end fitting was removed and thesaturated porous medium was carefully excavated into 50 mL
Falcon tubes containing around 20 mL of 0.001 M NaBr
solution. Approximately 8 tubes were recovered from acolumn, with each tube containing around 50 g of sand.
The tubes were shaken for 15 min using an Eberbach shaker(Eberbach corporation, Ann Arbor, Michigan). The concentration of E. coli O157:H7 in the excess 0.001M NaBr
solution was then measured using the previously discussed
fluorometer method. The maximum analytic error (twice thestandard deviation) associated with triplicate concentration
measurements was 0.048, and typical values were around0.01. Liquid and sand filled tubes were placed in an oven(200°C) overnight to volatilize the remaining solution fromthe sand. The volume of solution and mass of sand in eachtube was determined from mass balance by measuring theweight of the empty tubes, liquid and sand filled tubes, andsand filled tubes.
[15] An E. coli O157:H7 number balance was conductedat the end of each soil column experiment using the effluent
concentration data and the final deposition profiles. The
calculated number of effluent and deposited E. coli
O157:H7 was normalized by the total number of injected
cells into a column. Table 1 presents the calculated effluent(Meff), sand (Msand) and the total (Mtotal = Msand +Meff) mass percentage recovered for the experimental
systems.

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Figure 1. (a) Effluent concentration curves and (b) deposition profiles for E. coli O157:H7 in the 710,
360, 240, and 150 mm Ottawa sands at a Darcy velocity of around 0.1 cm min1. In Figure 1a, relative
effluent concentrations (C/Ci) are plotted as a function of pore volumes, whereas in Figure 1b thenormalized concentration (number of colloids, Nc, divided by the total number added to the column, Ntc)
per gram of dry sand is plotted as a function of dimensionless distance (distance from the column inlet
divided by the column length).
2.5. Micromodel Experiments[16] Several transport experiments were conducted in a
specially designed micromodel [Bradford et al., 2005] tomicroscopically examine the deposition behavior of E. coli
O157:H7 in 150 mm sand. The micromodel consists of a
0.2 cm thick by 2.0 cm wide by 7 cm long glass chamber(inside dimensions), with a glass tube (0.5 cm inside
diameter) and septum assembly joined at both ends of thechamber. The tubing was connected to the chamber by aglass blower at an angle of about 45°, so that the micromodel could lay flat on a horizontal surface. During packing
the micromodel chamber was oriented vertically without the
top septum. The desired sands were then wet packed in thechamber. Hypodermic needles and Teflon tubing were used
to connect the inlet side of the chamber to a LabAlliancechromatography pump (State College, PA 16803) and areservoir on the outlet side of the chamber. To be consistent
with the column experiments conducted at a Darcy velocity
of around 0.1 cm min1, the E. coli O157:H7 suspension
was pumped at a steady rate of 0.04 mL min1 (Darcy
velocity of 0.1 cm min1) for about 60 min (around 2.5 porevolumes), followed by 0.001 M NaBr solution for an
additional 60 min. After completion of a transport experiment, the hypodermic needles were removed and the final
deposition behavior of the fluorescent E. coli O157:H7 was
microscopically examined at several locations distributed
along the micromodel using a Leica DM IRB epifluorescent
microscope (Leica Microsystems Inc., Bannockburn, IL
60015). Images were captured by connecting the microscope to a video monitor and computer system. Photographs(600 times magnification) were taken using various inten-

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Figure 2. (a– c) Several representative micromodel photos(magnified 600 times) of E. coli O157:H7 deposition in the
150 mm sand. Photos were taken at several locations
distributed along the micromodel. Grain surface roughness
and differences in mineralogy (light and dark sand grains)are apparent in these photos. Fluorescent E. coli appear as
bright particles in pore constrictions or on the solid surface.
sities of both UV and visible light so that sand grains andfluorescent bacteria could be visualized simultaneously.

3. Results and Discussion
3.1. Experiment[17] Batch experiments were conducted to determine themaximum potential for E. coli O157:H7 attachment to thevarious Ottawa sands under the selected experimental conditions (20°C, pH = 6.73, low ionic strength = 0.001 M,

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negatively charged bacteria = 2.72 mV, and negatively
charged quartz sand). A 4 hour equilibrium period was usedin the batch experiments to be consistent with the column
procedures, for which the average duration ranged from 2 to
7.5 hours depending on the water flow rate. Consistent withunfavorable attachment conditions, the initial and final
concentrations of E. coli O157:H7 were almost identical(within a few percent of the initial concentration). Thissuggests that the presence of any metal oxides on the quartz
sands had negligible influence on deposition. Similar results
were obtained for the blank batch experiments conducted in
the absence of sand, suggesting that the rates of bacteria
growth and/or death were not significant during theseexperimental conditions.
[18] Column transport experiments were conducted toinvestigate the transport and deposition behavior of E. coli
O157:H7 under unfavorable attachment conditions.
Figure 1a presents effluent concentration curves for E. coli
O157:H7 in the 710, 360, 240, and 150 mm sands at a Darcy
velocity of around 0.1 cm min1 (see Table 1 for values of q).
Here relative effluent concentrations (C/Ci) are plotted as afunction of pore volumes. The influent concentration wasmeasured to be 1.7  108 CFU mL1 using the spread plate
method. Figure 1a demonstrates a systematic trend of
decreasing peak effluent concentration with decreasing sandsize. Table 1 indicates that Meff ranged from 82 to 13% for
the experiments conducted at approximately 0.1 cm min1.
The effluent concentration curves for the finer-textured
sands also exhibit asymmetric shapes, that slowly increased
with continued addition of E. coli O157:H7 suspension.
This implies a blocking or filling of favorable deposition
sites.
[19] Figure 1b presents the deposition profiles for E. coli
O157:H7 in the 710, 360, 240, and 150 mm sands at the endof these column experiments. Here the normalized concentration (number of colloids, Nc, divided by the total number
added to the column, Ntc) per gram of dry sand is plotted asa function of dimensionless distance (distance from thecolumn inlet divided by the column length). Consistent
with the effluent curves, Table 1 indicates that the percent
recovery of E. coli O157:H7 in the sands increased withdecreasing sand size (3 – 52% for experiments conducted ataround 0.1 cm min1). The total percent recovery for E. coli
O157:H7 in the effluent and sands ranged from 86 to 66%(Table 1) at this velocity (0.1 cm min1). The shape of thedeposition curve was highly dependent on the sand size.
Deposition in the coarser-textured sands (710 and 360 mm)
was rather uniform with increasing depth. In contrast, thefiner-textured 240 and 150 mm sands exhibit an initial peaknear the column inlet and a second larger peak at dimensionless depths of 0.73 and 0.49, respectively. The second
deposition peak was also quite broad in the 240 and 150 mm
sands, ranging in dimensionless depth from around 0.2 to
1.0.
[20] The mechanisms of E. coli O157:H7 deposition
were further deduced by means of a micromodel experiment conducted in 150 mm sand at a Darcy velocity of
0.1 cm min1. Figure 2 presents several micromodel photosof E. coli O157:H7 deposition in the 150 mm sand.
Additional photos of E. coli O157:H7 deposition in this150 mm sand are presented by Bradford et al. [2006b]. Allof these photos demonstrate that E. coli O157:H7 can be

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Table 2. Fitted Values of Dispersivity (l), Attachment Coefficient (katt), and Detachment Coefficient (kdet) to the Effluent Concentration
Curves of E. coli O157:H7 in the Various Sands When the Darcy Velocity is Around 0.1 cm min1ad50, mml, cm

katt, min1

kdet, min1

2
reff

MSEeffr2sandMSEsand

710
360
240
150

0.486
0.365
0.531
0.088

4.64E-3
7.59E-3
20.7E-3
48.7E-3

0.32E-4
0.01E-4
0.01E-4
1.97E-4

0.98
0.99
0.97
0.91

21.2E-4
5.48E-4
12.4E-4
3.57E-4

0.18
0.00
0.41
0.24

2.86E-3
5.18E-3
15.5E-3
64.5E-3aAlso included in this table is the coefficient of linear regression and mean square error for observed and simulated effluent (reff2 and MSEeff) anddeposition (rsand2 and MSEsand) data. Read 4.64E-3 as 4.64  103.

deposited at grain junctions, small pores, and/or pore constrictions due to straining. The shape and surface roughnessof the sand grains are also apparent in this photo. The lightcolored sand grains are predominately made from quartz,
and the darker colored grains are believed to be associatedwith magnetite. Consistent with the batch experiments, aminimal amount of E. coli O157:H7 attachment wasobserved in the micromodel experiments.
[21] Attachment is not believed to be the dominantmechanism for E. coli O157:H7 deposition in the finertextured media due to the following reasons. First, micromodel observations of E. coli O157:H7 retention in the
150 mm sand did not support the hypothesis that attachment
was the controlling mechanism (see Figure 2). Second, theexperimental conditions were designed to minimize thepotential for E. coli O157:H7 attachment, specifically: thesuspension was monodispersed, the porous medium was
negatively charged, and the aqueous chemistry was selected
to have a low ionic strength and buffered to a neutral pH.
Third, the batch experiments suggest that a minimal amountof E. coli O157:H7 attachment occurred to the Ottawa sands.
The experimental protocol for determining the deposition
curves was also based upon the rapid release (15 min) of
E. coli O157:H7 into solution under batch conditions and is
not consistent with low desorption rates that are commonly
observed in similar column experiments; i.e., the equilibrium
concentration of colloids in solution is proportional to thedesorption rate [e.g., Schijven and Hassanizadeh, 2000].
Finally, the E. coli O157:H7 deposition profiles in the
240 and 150 mm sands were not consistent with a first-orderFigure 3. Effluent concentration curves for E. coli O157:H7 in the (a) 710, (b) 360, (c) 240, and(d) 150 mm Ottawa sands. The various experimental Darcy velocities are indicated in the figurelegends and Table 1. The corresponding final deposition profiles are presented in Figures 4a – 4d.
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attachment-detachment model simulation (see following
discussion and Table 2).
[22] Recent literature has attributed nonexponential deposition profiles to porous media charge variability [Johnson
and Elimelech, 1995], heterogeneity in surface charge characteristics of colloids [Bolster et al., 1999; Li et al., 2004],
and deposition of colloids in a secondary energy minimum[Redman et al., 2004; Tufenkji and Elimelech, 2005b].
Other potential explanations for nonexponential deposition
profiles include variability of the collector (grain) size andcell motility. We believe that these explanations are notconsistent with our experimental data for the following
reasons. First, solid surface charge heterogeneity andvariability in the collector size is expected to be uniformly
distributed throughout the sand depth, not at one particularlocation in the column. Second, the surface charge distribution characteristics for E. coli O157:H7 were the samefor the various sand sizes. If surface charge distribution
characteristics were controlling deposition, then a dependence on grain size would not be expected; i.e., only thedeposition magnitude would increase, not the shape of thedeposition curve. Third, deposition induced by attachment
in the secondary minimum of the potential energy curve
would not be expected to act preferentially in finer-textured
sands or with depth. Fourth, no appreciable cell motility
was observed in the Live/Dead cell analysis or in the
micromodel experiments, and advective flow is expected todominate over bacteria motility for the considered experimental conditions. Furthermore, cell motility is expected
to be independent of the sand size.
[23] Micromodel observations shown in Figure 2 support
our hypothesis that straining of E. coli O157:H7 is occurring in the 240 and 150 mm sands. Additional support forstraining is based on the ratio of E. coli O157:H7 diameter(de) to the median grain diameter (d50). The ratio of de/d50
was 0.005 and 0.007 for the 240 and 150 mm sands,
respectively. Bradford et al. [2003] reported that strainingof carboxyl latex microsphere occurred in these Ottawa
sands when de/d50 > 0.005. Furthermore, Bradford et al.
[2006a] found that particles larger than 1 mm were initiallyremoved by 240 and 150 mm sands due to mechanicalfiltration and/or straining. Larger particles were transported
in these sands with continued addition of suspension,
presumably due to filling of straining sites. The asymmetricshape of the effluent concentration curves for E. coli
O157:H7 in the 240 and 150 mm sands (Figure 1a) was
consistent with this hypothesis.
[24] To further explore the role of system hydrodynamics
on E. coli O157:H7 deposition additional experiments wereconducted at several Darcy velocities in the various sands.
Figures 3a – 3d present effluent concentration curves forE. coli O157:H7 in the 710, 360, 240, and 150 mm sand,respectively. The various Darcy velocities are indicated in
the figure legends and Table 1. Darcy velocity had aminimal influence on the breakthrough curves of the
710 and 360 mm sands. Conversely, increasing the Darcy
velocity tended to produce a significant increase in theeffluent concentration and Meff (Table 1) in the finertextured 240 and 150 mm sands.
[25] Figures 4a –4d present the corresponding deposition
profiles for E. coli O157:H7 in the 710, 360, 240, and
150 mm sands, respectively. The shape of the deposition

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profile is highly dependent on the size of the sand and theDarcy velocity. Deposition profiles in the coarsest-textured
710 mm sand are similar in shape at different Darcy
velocities. In contrast, deposition profiles in the finertextured 360, 240, and 150 mm sands show a strong
dependence on Darcy velocity. At higher Darcy velocities
and in coarser-textured sands a more uniform distribution
with depth is observed. The peak retained concentration islower in magnitude and occurs further down gradient (at agreater depth) at higher Darcy velocities and for larger sandsizes. These observations suggest that straining of E. coli
O157:H7 increases at lower velocities. This agrees withpredicted straining behavior presented by Cushing and
Lawler [1998]. Conversely, filtration theory predicts thatthe attachment coefficient will decrease with decreasing
pore water velocity [e.g., Logan et al., 1995]. We believethat hydrodynamic shear can diminish straining of E. coli
O157:H7 at higher velocities and/or slowly mobilize
strained bacteria down gradient (greater depth). Tong etal. [2005a] measured deposition curves for an adhesion
deficit bacterial strain and observed deposition curves thatwere qualitatively similar to that shown in Figure 1b for the
150 mm sand. These authors found that slow mobilizationof bacteria occurred mainly during bacteria injection. We
therefore hypothesize that collisions between bacteria insuspension and those already removed from suspension andbound in a straining site, or in small pore space, may also
play a role in bacteria removal and remobilization.
3.2. Theory and Model[26] The HYDRUS-1D computer code [Simunek et al.,2005] simulates water, heat, and multiple solute movement
in one-dimensional variably saturated porous media, andis coupled to a nonlinear least squares optimization
routine based upon the Marquardt-Levenberg algorithm[Marquardt, 1963] to facilitate the estimation of transportparameters from experimental data. HYDRUS-1D was
modified as described below to simulate the transport anddeposition of E. coli O157:H7 in the various sands.
Our conceptual model assumes that E. coli can occur as
monodispersed and aggregated species. Aggregation ishypothesized to occur when large numbers of monodispersed E. coli are deposited in straining sites as a result offlow induced collisions in small pore spaces (when hydrodynamic forces overcomes the electrostatic repulsion ofdeposited colloids). When the deposited E. coli reach acritical concentration in the straining site, the aggregatedE. coli can be released into aqueous solution as a result ofhydrodynamic shearing forces. The aggregated species canthen be transported and deposited down gradient at adifferent rate than the monodispersed E. coli.
[27] In the absence of biological growth or death, ageneralized form for the aqueous phase mass balance
equation for monodispersed E. coli O157:H7 (species 1)
is written as:@ ðqw C1 Þ
¼ rJ1  qw k1 Y1 C1 þ rb kdet 1 S1@tð1Þwhere t is time [T; T denotes time units], rb [M L3; M andL denote units of mass and length, respectively] is the soil
bulk density, C1 [Nc L3; Nc denotes number] is the liquid
phase concentration of species 1, S1 [Nc M1] is the solid

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Figure 4. Final deposition profiles for E. coli O157:H7 in the (a) 710, (b) 360, (c) 240, and (d) 150 mm
Ottawa sands. The various experimental Darcy velocities are indicated in the figure legends and Table 1.
The corresponding effluent concentration curves are presented in Figures 3a –3d.
phase concentration of species 1, qw is the volumetric watercontent (dimensionless), k1 [T1] is the first-order deposition coefficient, kdet1 [T1] is the first-order detachment
coefficient for species 1, J1 [Nc L2 T1] is the total solute
flux for species 1, and y 1 (dimensionless) is a dimensionless deposition function for species 1. The first term on theright hand side of equation (1) accounts for advective,
dispersive, and diffusive transport, whereas the second andthird terms describe colloid deposition to and detachmentfrom the solid phase.
[28] The solid phase mass balance equation for monodispersed E. coli O157:H7 (species 1) is given as:@ ðrb S1 Þ
¼ qw k1 Y1 C1  rb kdet 1 S1  rb k12 Fp@tgreater distance from solid surface where the hydrodynamic
shearing forces are greater. We hypothesis that a criticalvalue of S1 is reached, Scrit1, when E. coli can be released
into the aqueous phase as an aggregated species (Fp > 0).
[29] If we assume that monodispersed E. coli is released
as an aggregated species in the aqueous phase, then themass balance equations for aggregated E. coli O157:H7(species 2) in the aqueous and solid phases can be written ina manner analogous to equations (1) and (2) asð2ÞHere k12 [T1] is the first-order production coefficient toaccount for the release rate of aggregated E. coli O157:H7(species 2) into the aqueous phase, and Fp [Nc M1] is theaggregated species production function defined as the
maximum of (S1  Scrit1) and 0; i.e., max(S1  Scrit1, 0)
where Scrit1 [Nc M1] is the critical concentration of S1
when production starts. For values of S1 < Scrit1 no releaseof aggregated E. coli occurs and Fp = 0. As the small porespaces begin to fill with E. coli, the deposition occurs at a@ ðqw C2 Þ
¼ rJ2  qw k2 Y2 C2 þ rb kdet 2 S2 þ rb k12 Fp@tð3Þ@ ðrb S2 Þ
¼ qw k2 Y2 C2  rb kdet 2 S2@t

ð4ÞThe subscripts 1 and 2 on parameters in these equations areused to distinguish monodispersed (species 1) and aggregated (species 2) E. coli O157:H7. Here liquid and solid
phase concentrations of species 2 are written in terms of thenumber of monodispersed E. coli, so that consistent units
are applied to both species 1 and 2, and to achieve an
accurate mass balance.

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Figure 5. (a) Observed and simulated effluent concentration curves and (b) deposition profiles forE. coli O157:H7 in the 240 and 150 mm Ottawa sands at a Darcy velocity of around 0.1 cm min1 (seeTable 1 for values of q). The simulations in Figures 5a and 5b were based upon equations (1) – (5). The
simulation labeled ‘‘Attach’’ considered only attachment and detachment by setting values of k12 = 0 and
y 1 = 1, and model parameters are given in Table 2. The simulation labeled ‘‘2 Species’’ consideredstraining and both monodispersed and aggregated E. coli species, and model parameters are given in
Table 3.
[30] An alternative model formation for the aggregated
E. Coli (species 2) that is very similar to the above approachis to assume that the production term from species 1 to 2
(fourth term on the right hand side of equation (3)) occurs
on the solid phase (equation (4)) instead of the liquid phase(equation (3)). This model was not pursued in this work forthe following reasons. First, the existing model formulation
provided an adequate description of the experimental data
(see Figure 5 and the associated text below). Second, it was
only possible to distinguish aggregated and monodispersed
species of E. coli once they were released from solid phase;i.e., not when they were deposited in the pores. Finally,
HYDRUS is a continuum model that determines average
concentrations over a representative elementary pore volume, and therefore it can only simulate effective aggregation processes, not pore-scale details.

[31] To account for time and depth dependent deposition
behavior a generalized form for y 1 is utilized as
Y1 ¼




S1
d50 þ z b1
1  max
S1
d50

ð5Þ

where d50 [L] is the median grain size of the porous medium,b 1 (dimensionless) is a parameter that controls the shape ofthe spatial distribution of retained colloids for species 1 (i.e.,[Ncthe depth dependence of the deposition coefficient), Smax1
M1] is the maximum solid phase concentration of deposited
colloids for species 1, and z [L] is the down gradient distancefrom the porous medium inlet. A similar expression is used
for y 2. The first term on the right hand side of equation (5) isused to account for blocking of favorable attachment sites orfilling of straining sites (time dependent deposition)

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BRADFORD ET AL.: TRANSPORT AND STRAINING OF E. COLI O157:H7

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Table 3. Fitted Model Parameters (l, k1, and S1max and, When Necessary, k12, k2, kdet2, and Scrit1) for E. coli O157:H7 Transport in the
Various Sandsa
d50, mmq, cm min1l, cm

k1, min1

S1max, Nc Nic1 g1k12, min1

k2, min1

kdet2, min1

Scrit1, Nc Nic1 g1

r2

710b
710b
710b
360c
360b
360b
240c
240c
150c
150c
150c

0.031
0.114
0.196
0.024
0.099
0.196
0.026
0.097
0.017
0.102
0.177

0.214
0.486
0.160
0.703
0.365
0.199
1.000
0.531
0.088
0.088
0.371

0.002
0.004
0.012
0.023
0.007
0.021
0.831
0.175
0.255
0.853
1.260

1000.01000.01000.01000.01000.00.306
0.190
1000.01000.0
0.179
0.228

0.000
0.000
0.000
1.190
0.000
0.000
0.003
2.848
0.038
2.254
0.317

0.000
0.000
0.000
0.232
0.000
0.000
0.698
9.99
0.116
2.195
0.059

0.000
0.000
0.000
0.001
0.000
0.000
0.133
1.368
0.043
0.211
0.003

0.000
0.000
0.000
0.093
0.000
0.000
0.086
0.073
0.110
0.084
0.106

0.98
0.98
0.96
0.94
0.99
0.99
0.93
0.95
0.95
0.98
0.97

a

Also included in this table is the coefficient of linear regression r2. Values of b2 = 0.0, S2max = 1000.0, and kdet1 = 0.0 for all simulations.
Simulations employed b1 = 0.0.
c
Simulations employed b 1 = 0.432.
baccording to the Langmuirian approach [Deshpande andis large then thisShonnard, 1999]. When the value of Smax
1term goes to 1, and time dependent deposition behavior is
not considered. The second term on the right hand side ofequation (5) is used to described depth dependent deposition
behavior; i.e., decreasing deposition rates with depth. Whenb 1 goes to zero, then depth dependent deposition is notconsidered. Conversely, higher values of b1 indicate anincreasing depth dependence of the deposition coefficient,k1. Bradford et al. [2003] found that the value of b1 = 0.432
gave a good description of the spatial distribution of retained
colloids when significant straining occurred in these same
sands and for similar experimental conditions. In should be
noted, however, that the optimal value of b1 may also
dependent the sand size, the solution chemistry, andhydrodynamics of a system. Straining has only recently
been recognized as a potentially significant mechanism of
colloid deposition, and additional research is needed to
improve our understanding of this process under varioushydrologic and solution chemistry conditions, and to relatestraining model parameters to the collector efficiency of
conventional filtration theory.
3.3. Simulations[32] The model outlined above was solved numericallyand used to simulate the transport and deposition of E. coli
O157:H7 in the various sands. equations (1) – (5) reduce tothe well known first-order attachment-detachment model
when k12 = 0 and y 1 = 1. The E. coli O157:H7 transport
data shown in Figures 1a and 1b were simulated using thisfirst-order attachment-detachment model. Fitted values ofthe dispersivity (l), the attachment coefficient (katt) anddetachment coefficient (kdet) are provided in Table 2, as wellas the statistical parameters for the model fit to the data; i.e.,the coefficient of linear regression and mean square error for2
and MSEeff) and deposition (r2sand and MSEsand)effluent (reffdata. Table 2 indicates that the attachment-detachment
model provided a good description of effluent data forE. coli O157:H7. Conversely, this model does not provide
a satisfactory description of the E. coli O157:H7 depositionin these sands, especially in the finer-textured (240 and
150 mm) porous media (see r2sand and MSEsand in Table 2).
[33] Figure 5a presents the observed and simulated effluent concentration curves for E. coli O157:H7 in the 240 and
150 mm sands at a Darcy velocity of around 0.1 cm min1(see Table 1 for values of q). Two simulations are shown foreach data set. The first was the attachment/detachment
model, and the second was the 2 species straining modelthat accounted for production of an aggregated species. The
simulated curves for the 2 species model sums the contribution of monodispersed and aggregated E. coli concentrations together (both concentrations are written in terms ofmonodispersed E. coli). A summary of the fitted model
parameters and statistical parameters characterizing thegoodness of fit for the various model formulations isprovided in Tables 2 and 3. Figure 5b presents thecorresponding observed and simulated deposition profiles
for these same systems. The effluent concentrations and thedeposition profiles were reasonably described by the proposed 2 species straining model. Conversely, the attachment/detachment model does not accurately describe theexperimental deposition profiles. The improved descriptive
ability of the 2 species model can also be assessed bycomparing statistical measures of the goodness of fit. The
value of r2sand for the attachment/detachment and 2 species
straining model was 0.41 and 0.59, respectively, for the
240 mm sand, and 0.24 and 0.98 for the 150 mm sands.
We also calculated the Akaike information criterion (AIC)[Akaike, 1974] for these same data as a measure ofgoodness of fit that penalizes for adding fitting parameters;i.e., the model with the lowest value of AIC is preferred. The
value of AIC for the attachment/detachment and 2 species
straining model was 3.7 and 15.6, respectively, for the
240 mm sand, and 29.3 and 5.0 for the 150 mm sands.
Hence values of AIC also indicate that the 2 species
straining model provided a better description of the data
than the attachment/detachment model.
[34] In the 240 and 150 mm sands, the 2 species
model predicts breakthrough of a second peak for theaggregated E. coli (species 2) at later transport times andlower concentrations than for the monodispersed E. coli
(species 1). Additional experimental studies and improved
analytical sensitivity are necessary to fully verify thispredicted behavior in our experimental systems. Bacteriatransport data presented by Tong et al. [2005a], however,indicated that the peak concentration of nonmonotonic
deposition profiles moved down gradient with increasingtransport time (pore volumes). Harter et al. [2000] also
observed a second peak (at later times) in the breakthroughcurve for oocysts of Cryptosporidium.

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BRADFORD ET AL.: TRANSPORT AND STRAINING OF E. COLI O157:H7[35] Although we cannot prove our hypothesis of E. coli
aggregation, experimental evidence does support this line ofreasoning. For example, micromodel observations of E. coli
deposition shown in Figure 2 indicate that many cells can beretained in pore throats. Crist et al. [2005] also conducted
DLVO calculations that examined the potential for colloidcolloid interactions. These calculations indicate that attractive hydrophobic forces may dominate the total potential
interaction energies for colloids under conditions that otherwise (classical DLVO calculations) would produce repulsive conditions. Our MATH. tests for the E. coli O157:H7
indicate that 64% of the cells were hydrophobic, suggestingthat favorable hydrophobic interactions were certainly possible for our experimental conditions.
[36] Table 3 provides a summary of the fitted model andstatistical parameters for the 2 species model shown in
Figure 5, as well as for the other experimental systems. Hereof Scrit1 were normalized by the initial
the values of Smax
1number of bacteria in a unit volume of influent suspension,
Nic. Transport of E. coli in the 710 and 360 mm sands wasadequately described using the first-order attachment anddetachment model (k12 = 0, and y 1 = 1), with the one
exception of the experiment in the 360 mm sand at the lowest
velocity. In this case (low velocity and 360 mm sand),deviations between observed and simulated profiles suggest
an additional retention mechanism, such as straining, may be
involved in the cell deposition. An improved characterization of the transport behavior of E. coli in the 240 and
150 mm sands, however, required consideration of otherprocesses. To simulate straining behavior of monodispersed
E. coli O157:H7 we used b 1 = 0.432 and kdet1 = 0, whereas
y 2 = 1 for the second aggregated species was assumed. The
control the shape of the breakthroughvalues of k1 and Smax
1
curve for monodispersed E. coli O157:H7, whereas values ofk12, Scrit1, k2, and kdet2 control the shape and evolution of thedeposition profile and the second breakthrough curve. Systematic trends in model parameters were not obvious in
Table 3, suggesting the potential for nonunique parameter
estimates. Additional research is needed to fully assess
and/or measure the range of applicability for these 2 species
model parameters.

W12S12increasing depth. The experimental results of this study
indicate that nonmonotonic deposition profiles can also
occur as a result of straining. Differences in the shape ofthe nonmonotonic deposition profiles were demonstrated to
be a function of the sand size and the system hydrodynamics.
[39] A conceptual and mathematical modeling framework
was proposed to account for the observed E. coli O157:H7
transport and deposition. This model assumes that E. coli
O157:H7 aggregation occurs when large numbers of monodispersed E. coli O157:H7 are deposited in straining sites asa result of flow induced collisions in small pore spaces(when hydrodynamic forces overcome the electrostatic
repulsion of deposited colloids). When the deposited
E. coli O157:H7 reaches a critical concentration in thestraining site, the aggregated cells can be released intoaqueous solution as a result of hydrodynamic shearing forces.
The aggregated species can then be transported and deposited
down gradient at a different rate than the monodispersed
E. coli O157:H7. This conceptual model was numerically
implemented into the HYDRUS computer code and successfully used to describe the experimental data.
[40] Experimental evidence discussed above indicatesthat straining is likely to be an important mechanism of
E. coli O157:H7 deposition in the finer-textured sands
under unfavorable attachment conditions. Results also suggest that colloid-colloid interactions and system hydrodynamic influence straining processes. Additional research iswarranted to better quantify and model the influence of
these factors on straining deposition and mobilization, as
well as the potential influence of colloid chemistry andshape, cell membrane rigidity and motility, and solution
chemistry. This information is believed to be essential for
predicting the fate of colloids and colloid associated contaminants in natural subsurface environments.
[41] Acknowledgments. This research was supported by the 206
Manure and Byproduct Utilization Project of the USDA-ARS. Mentionof trade names and company names in this manuscript does not imply any
endorsement or preferential treatment by the USDA. We would also like toacknowledge the valuable assistance of Yadata F. Tadassa in the experimental aspects of this research.

References

4. Summary and Conclusions[37] The research presented herein indicates that straining
can play a significant role in the transport and deposition
behavior of E. coli O157:H7 in saturated sands underunfavorable attachment conditions. This finding was supported by micromodel observations of E. coli O157:H7
deposition at grain-grain junctions and in small pore spaces.
Batch experiments also indicated that little E. coli O157:H7
attachment occurred between the quartz sand for theselected solution chemistry.
[38] In column experiments, straining tended to increase
with decreasing sand size (increasingly smaller pores) andflow rate. Hydrodynamic shearing forces are believed todiminish colloid straining in these small pore spaces athigher flow rates. Most of the published research on colloid
straining has been conducted using latex microspheres[Bradford et al., 2002, 2003, 2004], or larger spherical
protozoan parasites [Bradford and Bettahar, 2005; Bradford
et al., 2006a]. In these cases, deposition profiles followed aninverse power law (hyperexponential) distribution with

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S. A. Bradford, George E. Brown Jr. Salinity Laboratory, ARS, USDA,
450 West Big Springs Road, Riverside, CA 92507-4617, USA. (sbradford @ussl.ars.usda.gov)
J. Simunek, Department of Environmental Sciences, University ofCalifornia, Riverside, CA 92521, USA.
S. L. Walker, Department of Chemical and Environmental Engineering,
University of California, Riverside, CA 92521, USA.

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