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Development of a Sulfate-Reducing Biological Process to Remove Heavy Metals from AcidMine DrainageAuthor(s): Vicki S. Steed, Makram T. Suidan, Munish Gupta, Takashi Miyahara, Carolyn M.Acheson, Gregory D. SaylesReviewed work(s):Source: Water Environment Research, Vol. 72, No. 5 (Sep. - Oct., 2000), pp. 530-535Published by: Water Environment FederationStable URL: http://www.jstor.org/stable/25045418 .Accessed: 23/01/2012 19:40
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Development of a Sulfate-Reducing
BiologicalProcess To Remove
HeavyMetals from Acid Mine Drainage
Vicki S. Steed, Makram T. Suidan, Munish Gupta, Takashi Miyahara, Carolyn M. Acheson,Gregory D. Sayles
ABSTRACT: The feasibility of using sulfate-reducing bacteria to
remove heavy metals from aqueous streams such as acid mine drainagewas evaluated using three anaerobic reactors: an upflow anaerobic
sludge blanket (UASB) reactor, a packed filter reactor, and a filter
reactor that was partially packed with floating plastic pall rings. The
packed filter reactors removed more than 99% of the influent metals.
The performance of the partially packed reactor was superior based on
effluent metal and sludge concentrations. Although the UASB reactor
reduced the concentration of dissolved iron, the effluent concentration of
total suspended solids remained greater than 18 g/L. This elevated solids
concentration indicated that the UASB reactor was not operating as an
effective clarifier, and, as a result, UASB reactor operation was
discontinued after 4 months. The packed filter reactors were operatedin parallel and received influent containing a combination of heavy
metals. By withdrawing sludge from the bottom of these reactors, the
accumulation of solids such as metal precipitates and biomass was
controlled. The effluent concentrations of most metals were low, often
less than drinking water standards, with the exception of manganese.
Water Environ. Res., 72, 530 (2000).
KEYWORDS: acid mine drainage, sulfate-reducing bacteria, anaerobic
reactors, metal sulfide precipitation.
IntroductionAcid mine drainage (AMD) is characterized by low pH (1.5 to
3.5) and large concentrations of sulfate and dissolved heavy metals
such as iron, manganese, aluminum, zinc, and copper. The ions
and concentrations present are site specific and vary considerably
depending on factors such as location and type of mine and, to a
large extent, the sampling site within the mine.
Typically, these metal bearing wastes have been treated by
chemical precipitation such as in situ addition of lime, calcium, or
sodium hydroxide or by sorption to materials such as ion-exchange
resins or the biomass-based sorbent Algasorb (Bio-Recovery Sys
tems, Inc., Las Cruces, New Mexico). Less costly technologies are
needed to remediate many sites that have been affected by metal
contaminated liquids and solids such as soils, sludges, and sedi
ments.
Bacterial sulfate reduction has been identified as a potentially
cost-effective means to remove metals from AMD (Dvorak et al.,
1992, and Kuyucak et al., 1991). Sulfate-reducing bacteria (SRB)can convert sulfate to sulfide using an organic carbon source as an
electron donor (for chemical reactions, see Table 1). This sulfide
reacts with many of the metal ions present. The low solubility of
metal sulfides under sulfate-reducing conditions results in a low
residual concentration of dissolved metal species (Hammack et al.,
1994). In addition, as the sulfate-reduction process mineralizes the
organic energy source, carbon dioxide is produced. Based on
chemical equilibria under sulfate-reducing conditions, pH and
alkalinityof the waste will increase. Furthermore, the carbonate
and hydroxide ions generated as the pH rises may also form metal
precipitates (Dvorak et al., 1992). The ability to reduce dissolved
metal concentrations and neutralize AMD acidity makes SRB
useful catalysts in treating AMD and other metal contaminated
materials.
To effectively treat metal contaminated wastes, an anaerobic
environment supporting sulfate reduction must be established for
metal precipitation, and clarification must be provided to remove
metal precipitates from the effluent. Because solids (metal precipitates and biomass) accumulate in the reactor and may eventually
clog it, a method of solids removal or cleaning is an importantconsideration in reactor selection. Two reactor types were evalu
ated in this study:an
upflow packed anaerobicfilter with
recycleand an upflow anaerobic sludge blanket (UASB) reactor. To clean
the UASB reactor, solids can be removed from the bottom of the
reactor. The same technique can be used for the filter reactor;
however, the presence of packing material complicates the process. Therefore, evaluation of reactor cleaning was another objective of the research. As a result, two configurations of the filter
reactor were evaluated: a reactor that was completely packed and
a reactor that was partially packed (60% by volume).
MethodologyThe reactors were constructed of plexiglass (1.07 m height, 170
mm diameter). Polypropylene pall rings (Glitsch Ballast Rings[Koch-Glitsch Mass Transfer Technology, Wichita, Kansas], 26
mm diameter) were used as the packing material in the filter
reactors. Pall rings were selected because of the large surface area
per unit volume, high porosity, and chemical resistance in the
corrosive environment of the sulfate-reducing system. Because the
packing was lighter than water, the packing material floated to the
top of the partially packed filter reactor leaving an open area at the
bottom. The reactors were kept completely mixed by recirculating
the effluent at a recycle ratio of 20:1. Because the influent was
acidic, recirculating the effluent moderated the pH and promotedmore efficient sulfate reduction. Figure 1 shows a schematic dia
gram of the filter reactors.
The reactors were seeded with a mixture of primary and anaer
obic digestor sludge obtained from the Mill Creek wastewater
treatment plant, Cincinnati, Ohio. Primary sludge was used be
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_Steedet al.
Table 1?Pertinent reactions and equilibria of SRB bio
logical process.9
Type Reaction
Sulfate
reducing
Acid/base
CHXOO- + SO2" + 3H+ -> 2CO? + 2H20+ HoS
2CH3COO 2S02+ 2HCO?
+ 3H+ -? 2C02HS" + H2S
CH3COO- + H20->
CH4 + HCO3
CH3COOH ^ H+ + CH3COO2HS07 ** 2S02~ + 2H+
HCO3<-> 2H+ + CO?
C02(g) + H20l20
<-> H+ + OhT
US <* H+ + HS" ^ 2H+ + S"
Metal
precipitation0 2M+n + nS-2 <^M2Sn
M+n + nOH~ *+M(OH)n
2M^n + nC03"2*?
M2 (C03)n
aTypical values for dissociation constants and thermodynamic
properties can be obtained from sources such as Lide (1991).bWhere M represents a generic metal ion, and n represents the
charge on a metal ?on.
cause of the long sewer lines in Cincinnati and the abundant
release of hydrogen sulfide from manholes located close to the
wastewater treatment plant. Also, primary sludge from the same
source had been used in previous experiments with SRB (Gupta et
al., 1996).
Acetic acid was selected as the carbon and energy source for
two reasons. Because acetic acid can be used to leach metals from
solids in thetoxicity
characteristic leachateprocedure (TCLP) test,
selecting acetic acid as the carbon and energy source for the SRB
biological process enhances the compatibility of this biological
process with other metal remediation efforts, such as the leachingof metals from mine tailings. The effectiveness of an aqueous
solution of acetic acid in leaching heavy metals from contaminated
soils needs to be verified. In addition, acetic acid is relatively
inexpensive.
Tables 2 and 3 show the composition of the feed. A synthetic
Gas Sampling Port
Effluent
Acid MineDrainage
Buffersolution
Sludge Withdrawal Port
Figure 1?Schematic diagram of the anaerobic filter reactor.
Table 2?Composition of reactor feed (iron-only feed).8
Components Concentration0
Acetic acid 3000Iron (ferrous) 1490Iron ferric) 840
Chloride 3480Hydrochloric acid 2.75c
Stock salt solution 32c
Vitamin solution 8C
Sulfate0 5200Sodium 5370Carbonate 870
Hydroxide 1630
aMetal concentrations are not based on a specific mine effluent
but are characteristic of types of effluent from hard rock mines.b
Inmg/L, except where noted.c
InmL/L.d
Sulfate was fed as sodium sulfate.
wastewater containing metals, sulfate, and acetate was fed to the
reactors. The concentration of metals in AMD can change drasti
cally from mine to mine and even along the depth of the water in
a pit as demonstrated at the Berkeley Pit in Butte, Montana (Davis,
1989). The combination and concentration of metals selected for
the synthetic wastewater used in this experiment was provided bythe U.S. Environmental Protection Agency as being characteristic
of mines in Montana and Colorado (Sayles, 1994). The concen
tration of acetic acid added was stoichiometrically calculated so
that the amount of sulfide produced from sulfate could precipitate
Table 3?Composition of reactor feed (metal mixture
feed).3
Components Concentration5
Acetic acid 3000Iron (ferric) 840
Zinc 650
Manganese 275
Copper 127Cadmium 2.3
Arsenic0 2.1
Lead 1.5
Chloride 2800Stock salt solution 24d
Vitamin solution 6d
Sulfate9 5000Sodium 7300Carbonate 700
Hydroxide 1700
aAll metals, except arsenic, were fed as their respective chloride
salts. Metal concentrations are not based on a specific mine
effluent but are characteristic of types of effluent from hard rock
mines.b
Inmg/L, except where noted.c
Arsenic was fed as arsenic trioxide.
d InmL/L.e
Sulfate was fed as sodium sulfate.
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Table 4? Stock salt solution.
Component Concentration8
Trace salt solution 33.1b
Magnesium chloride (MgCI2 6H20) 8.13
Sodium acid phosphate (NaH2P04 H20) 8.28
Potassium acid phosphate (KH2P04) 13.6Ammonium chloride (NH4CI) 30.33Calcium chloride (CaCI2 2H20) 5.88
aIn g/L, except where noted.
b InmL/L
all metals present in the wastewater. A solution containing essen
tial vitamins for the microorganisms and a stock salt solution
containing essential minerals were added to the metal solution (see
Tables 4, 5, and 6).
A pH set-point of 7.2 was selected for optimal SRB growth
(Barton, 1995). A buffer solution (containing sodium carbonate,
sodium hydroxide, and sodium sulfate) was fed to the reactors to
control pH. The concentration of sodium hydroxide in the buffer
solution was determined experimentally as the concentration nec
essary to achieve the desired pH set-point.The flow rates of the synthetic AMD and buffer solutions were
monitored using calibrated carboys. The solutions were fed to the
reactors using Cole-Parmer Masterflex pumps (Cole-Parmer In
strument Company, Vernon Hills, Illinois) operating at 2 r/min.
Power to the Masterflex pumps was channeled through electronic
Chrontrol timers (Lindberg Enterprises, Inc., San Diego, Califor
nia). These timers adjusted flows to obtain proper hydraulic resi
dence time. Both AMD and buffer flows were intermittent, cycling
every1 to 2 minutes. For the initial
comparisonof the UASB
reactor with the filter reactors, the combined flow rate of the
synthetic AMD and buffer was 2.0 L/d corresponding to a hydrau
lic detention time of 8.4 days.All reactors were operated at 30 ?C. The UASB reactor temper
ature was maintained by heating the recycle line and insulating the
reactor. The temperature of the filter reactors was maintained with
a Fisher Scientific (Pittsburgh, Pennsylvania) Isotemp WaterbathModel 28L-M.
All pH determinations were made on unfiltered samples imme
diately after collection using an Orion Model 720A pH meter
(Orion Research, Beverly, Massachusetts). All other effluent sam
ples (except total metals) were filtered with a 0.45-|xm MAGNA
Nylon membranefilter
(MSI, Westboro, Massachusetts)before
analysis. Whenever possible, measurements were determined on
Table 5?Stock trace salt solution.
Concentration,
Component g/L
Ammonium molybdate ((NH4)6Mo7024 4H20) 0.52
Sodium borate (Na2B407 10H2O) 1.15
Nickel chloride (NiCI2 6H20) 3.00
Manganese chloride (MnCI2 4H20) 4.74
Cobaltic chloride (CoCI2 H20) 2.86
Zinc chloride (ZnCI2)3.27
Copper(ll) chloride (CuCI2 2H20) 2.05
Table 6?Vitamin solution.
Component Concentration, g/L
p-Aminobenzoic acid 0.01
Biotin 0.003 9
Cyanocobalamin 0.000 2
Folie acid 0.003 9Nicotinic acid 0.01
d-Pantothenic acid 0.01
Pyridoxine hydrochloride 0.02
Riboflavin 0.01
Thiamine 0.01
Thiotic acid 0.01
the day samples were collected. Flow rate, pH, and temperaturewere monitored daily.
Samples for metal analysis were taken twice weekly. Metal
concentrations were analyzed using a PerkinElmer Atomic Ab
sorption Spectrophotometer Model 3100 with AS90 (flame) andHGA 600 and AS60 (furnace) according to the SW 846 method
(Office of Solid Waste, 1986). Total (unfiltered) and soluble (filtered) effluent samples were preserved with nitric acid (HN03)
(trace metal grade) before analysis. Sludge samples, diluted 1:200,
were also digested with HN03 before analysis.
Acetic and propionic acid concentrations were determined usinga Hewlett Packard (Palo Alto, California) Series 1050 LC diode
array detector with Bio Rad Aminex HPX-87H (300 X 7.8 mm
column). Chemical oxygen demand (COD) was determined usingHach (Loveland, Colorado) COD glass vials, a Hach COD ReactorModel 45600, and a Bausch & Lomb (Rochester, New York)
Spectronic70
spectrophotometer followingStandard Methods
(method 508 C; APHA et al., 1995). Total organic carbon (TOC)was determined using a TOC analyzer (Shimadzu TOC-5000
[Shimadzu Scientific Instruments, Inc., Columbia, Maryland]).Gas composition was determined using a Hewlett Packard 5890
Series II GC, TCD detector, HP 45/60 Molecular Sieve column,and HP 80/100 Hayesep Q column. Carbon dioxide, oxygen,nitrogen, and methane were measured and expressed as fractions
of the total sample. The above variables were analyzed weekly.
Sulfate concentration was determined using the gravimetric
method with drying of the residue as described in Standard Methods (method 4500-D; APHA et al., 1995). Dissolved sulfide con
centrations were determined using an Orion silver/silver sulfide
electrode onsamples prepared
with0.45-p-m
MAGNANylon
syringe filters (MSI) and mixed in equal portions with a sulfide
anti-oxidizing buffer (Orion). Sulfates and sulfides were analyzed
weekly.
Results and DiscussionThe reactors were evaluated in two comparisons. Initially, the
fully packed filter was compared to the UASB reactor using an
iron-only feed with an iron concentration of 32 mmol/L (see Table
2). The filter reactors reduced the effluent concentrations to 0.11
mg/L dissolved iron and 0.51 mg/L total suspended solids. Al
though the UASB reactor reduced the concentration of dissolved
metals to less than 0.25 mg/L, the concentration of total suspended
solids varied between 18 and 22 mg/L. No sludge granulation
occurred within the UASB reactor. Performance of this reactor
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1 I I I I I I I I I I s
Total fed s^
s' Total removed
^sin sludge 1
^/Remaining_ _
S^ In reactor
I Total removed in effluent~
J_I_I_L_. -L_U.. T 1.1.1.1.1.
Time, days
Figure 2?Idealized metal balance for the anaerobic filter.
indicated that it did not operate well as a clarifier, and, as a result,
UASB reactoroperation
was discontinued after 4 months.
During the comparison of the UASB and packed bed filter
reactors, solids accumulation in the filter reactor was controlled by
removing a fixed volume from the reactor every three hydraulic
retention times or 26 days. In time, performance of the reactors
deteriorated. The effluent COD, acetate, and dissolved metals
concentrations increased. Propionate was detected in the effluent,
indicating that the system was under stress. In addition, the total
effluent metal concentrations increased, indicating decreased per
formance of the filter reactors with respect to clarification.
Increasing the solids removal frequency did not improve reactor
performance. Both reactors were cleaned by removing the packing
material. The solids in the lower half of each reactor accumulated
tothe
extentthat the packing
wascompletely clogged. Approxi
mately 40% of the packing material was removed from one of the
reactors to provide a larger volume for the accumulation of solids.
In the second comparison, both filter reactors were restarted, and
hydraulic retention time was increased to 12.9 days (a decrease in
the combined flow rate to 1.3 L/d). The feed composition was
changed to include a combination of heavy metals (see Table 3).
Solids were withdrawn from the bottom of the reactors to remove
accumulating metal precipitates and biomass (sludge) in the reac
tor to avoid plugging of the reactor and allow continuous opera
tion. During the initial 3 to 4 weeks of operation, no sludge was
wasted from the reactors to allow for the accumulation of biomass.
After this initial phase, sludge was wasted based on a metal
balance for each reactor. It is interesting to note that neither reactorexhibited signs of inhibition resulting from exposure to oxygen
during cleaning.
Figure 2 shows an idealized metal balance for the anaerobic
filter reactor. One liter of sludge was wasted every week from each
of the reactors. The concentration of metals in the feed solution, in
the sludge, and in the unfiltered effluent was measured as previ
ously discussed. The total mass of metals remaining in each reactor
was calculated as the difference between total mass of metals fed
to the reactor and total mass of metals removed in the sludge and
effluent. If the total mass of metals removed in the sludge was less
than the total mass of metals fed to the reactor, then additional
sludge was wasted from the reactor to maintain a continually
constant mass of metals in the reactor. Performing a mass balance
for each reactor was necessary because the density of wasted
ECD
sludge varied; therefore, removing a constant volume of sludgewould not always equate to maintaining a constant mass of metals
within the reactor.
Figures 3 and 4 show the actual metal balance for the two most
prominent metals in the reactor feed and sludge. In Figures 5 and
6, the total mass of metals remaining in the completely packed and
partially packed filter reactors, respectively, is presented as a
function of time. As illustrated in these figures, the total mass of
metals increased in the beginning (during the period when no
sludge was wasted); however, over time, the rate of accumulation
slowed considerably.
As shown in Table 7, COD and acetic acid were reduced bymore than 95%. Based on the reactions given in Table 1, if the
reduction in COD and acetic acid was solely the result of SRB
activity, the sulfate concentration should be reduced to the same
level. (Acetate concentration was reduced from 50 to 0.83
mmol/L; therefore, sulfate concentration should have been reduced
from 52.1 to 2.9 mmol/L.) However, a sulfate residual of approx
imately 25% of the influent concentration (12 mmol/L) was
present.One possible explanation could be that methanogenesis was
responsible for the 9 mmol/L of acetate consumed that could not
be accounted for by sulfate reduction. If methanogenesis occurred,
methane should have been detected in the weekly gas samples.
However, the gas production was negligible, and the amount of
methane in the headspace was always less than 10% and frequentlybelow the detection limit. Another possible explanation could be
the presence of a consortium of bacteria, including non-SRB, that
used the acetic acid but not the sulfate. This is possible because the
reactor was seeded with sludge from a wastewater treatment plantrather than a pure culture of bacteria.
Based on the metal mass balance, the reactors are now operatingat
steadystate
with respectto
themass
of metals, except formanganese, remaining in the reactor. Stable operation was con
firmed by operating the reactors for more than three retention times
(40 days) at steady state, based on the metal mass balance with
respect to the mass of sludge in the reactor.
As shown in Tables 8 and 9, both filter reactors performed wellwith respect to the removal of metals, and the concentration of
soluble metals in the effluent, except manganese, was reduced to a
concentration less than drinking water standards. Both filter reac
tors, unlike the UASB reactor, worked well as clarifiers, and total
metal removal efficiencies exceeded 99%. However, the effluent
0 10 20 30 40 50 60 70 80 90 100 110 120 130
Time, days
Figure 3?Iron balance for the partially packed filter.
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Steed et al.
O 10 20 30 40 50 60 70 80 90 100 110 120 130
Time, days
Figure 4? Zinc balance for the partially packed filter.
total metal concentrations for iron, zinc, and manganese were
larger for the completely packed reactor than for the partially
packed reactor. Analysis of effluent total metal concentrations
using a Student t test with a 95% confidence interval confirmed
that the difference in iron and zinc concentrations was statistically
significant. However, there was no statistically significant differ
ence in soluble metal concentrations. This indicates that the par
tially packed reactor was a more effective clarifier than the com
pletely packed reactor.
One of the reasons for this observation may be the mechanism
of sludge accumulation. As shown in Table 10, analysis of total
solids indicated that the partially packed reactor produced a
slightly more compact sludge. The absence of packing in the
bottom part of the partially packed reactor may have producedmore dense sludge, which may have provided additional filtration
capability. Analysis of total solids using a Student t test with a 95%confidence interval indicated no statistically significant difference
between the two reactors. However, analysis found iron concen
trations to be significantly higher in the sludge in the partiallypacked reactor.
Conclusions
Compared to a UASB reactor, an upflow anaerobic filter reactor
was superior for treating water contaminated with heavy metals.
The filter reactor, unlike the UASB reactor, worked well as a
90 M . I I | I I I | I I I I |M . I | I IM | I I . I | , , I I |M I I |M I I , . I I |M I I | . , I , | I I I | IH
0 10 20 30 40 50 60 70 80 90 100 110 120 130
Time,days
Figure 5?Total metals remaining in the completelypacked filter.
120 M I I I |M I I | I I I I | I I I | I IM | I I I | I I I I | , I I I | , I I | I I I , | I , | I I I I | , I , , | ,||
0 10 20 30 40 50 60 70 80 90 100 110 120 130
Time, days
Figure 6?Total metals remaining in the partially packedfilter.
clarifier, and all metals, except manganese, were reduced to a
concentration close to drinking water standards. Sludge with
drawal from the bottom of the filter reactor can be used to remove
accumulating metal precipitates and biomass, and therefore, the
reactor can be operated continuously. Sludge levels can be con
trolled in the filter reactors using a mass balance for metals that
compares feed to effluents, including sludge withdrawal and liquideffluent. Among the two configurations of filter reactors, the par
tially packed reactor was more effective because it produced an
effluent with smaller metal concentrations.
AcknowledgmentsCredits. The U.S. Environmental Protection Agency (U.S.
EPA) through its Office of Research and Development funded and
managed the research described here under Cooperative Agreement CR-821029 to Makram Suidan. This paper has not been
subjected to an agency review and therefore does not necessarily
reflect the views of the U.S. EPA. No official endorsement should
be inferred.
Authors. Vicki Steed is a researcher with Battelle Memorial
Institute, Columbus, Ohio. At the time the research was performed,she was a research assistant at the University of Cincinnati, Cin
cinnati, Ohio. Makram Suidan is Professor of Environmental En
gineering, Department of Civil and Environmental Engineering,
University of Cincinnati. Munish Gupta is with Parsons Engineer
ing Sciences, Atlanta, Georgia. At the time the research was
performed, he was a research associate at the University of Cin
Table 7?Comparison of filtered liquid effluent concen
trations for the two filter reactors to influent.
Concentration, mg/L
Completely PartiallyComponent Influent packed packed
Chemical
oxygendemand 3500 85.2 ? 23.1 83.7 ? 22.6
Acetic acid 3000 46.9 ? 26.7 14.9?
2.7Sulfate 5000 1148 ?364 1155 ?317Sulfide 0 156.7 ? 20.2 180.0 ? 18.7
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Table 8? Comparison of total liquid effluent metal con
centrations for the two filter reactors to influent.
Concentration, mg/L
Component InfluentCompletely
packed
Partiallypacked
Iron
Zinc
Manganese
CopperTotal
840650275127
1894
1.28 ?0.36
0.927 ? 0.229
8.06 ? 1.77
0.036 ? 0.021
10.32 ? 1.49
0.343 ?0.18
0.205 ?0.176
6.99 ? 1.13
0.024 ?0.018
7.60 ? 1.94
cinnati. Takashi Miyahara is assistant professor, Department of
Civil Engineering, Tohoku University, Sendai, Japan. At the time
the research was performed, he was a visiting scientist at the
University of Cincinnati. Carolyn Acheson and Gregory D. Saylesare with the U.S. EPA National Risk
ManagementResearch Lab
oratory, in Cincinnati. Correspondence should be addressed to
Makram T. Suidan, Department of Civil and Environmental En
gineering, University of Cincinnati, Cincinnati, OH 45221-0071.
Submitted for publication November 18, 1997; revised manu
script submitted September 7, 1999; accepted for publication April
27, 2000.
The deadline to submit Discussions of this paper is January 15,
2001.
Table 9?Comparison of effluent metal concentrationsfrom the partially packed filter reactor to drinking water
standards (Pontius, 1996).
Concentration, mg/L
Component Total Soluble
Maximum
contaminant
level
Iron
Zinc
Manganese
Copper
0.343 ?0.18
0.205 ?0.176
6.99 ? 1.13
0.024 ? 0.018
0.097 ? 0.073
0.025 ? 0.023
6.66 ? 1.68
0.017 ?0.015
0.30
5.00
0.05
1.30
Table 10? Comparison of sludge concentrations for thetwo filter reactors.
Concentration, g/L
Completely PartiallyComponent packed packed
Total solids 24.2 ? 5.2 27.8 ? 10.6
Iron 5.07 ?0.87 5.76 ?1.24
Zinc 3.49 ? 0.71 3.54 ? 0.62
Manganese 0.96 ? 0.22 0.98 ? 0.22
Copper 0.61 ?0.10 0.61 ?0.17
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