Journal of Environmental Quality 31:1782-1788 (2002)
© 2002 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
TECHNICAL REPORTS
Atmospheric Pollutants and Trace Gases
Hydrogen Sulfide Effects on Ammonia Removal by a Biofilter Seeded with Earthworm Casts
E. Y. Leea,
K. S. Cho*,a,
H. D. Hanb and
H.W. Ryub,c
a National Subsurface Environmental Research Laboratory, Ewha Womans University, 11-1 Daehyun-dong, Seodaemun-gu, Seoul 120-750, Korea
b Dep. of Chemical and Environmental Engineering, Soongsil University, 1-1 Sangdo-dong, Dongjak-gu, Seoul 156-743, Korea
c Research Institute of Biological and Environmental Technology, Biosanit Co., 600-16 Shinsa-dong, Kangnam-gu, Seoul 135-120, Korea
* Corresponding author (kscho{at}ewha.ac.kr)
Received for publication October 17, 2001.
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ABSTRACT
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Ammonia (NH3) removal efficiencies were evaluated when hydrogen sulfide (H2S) and NH3 in binary mixture gases were supplied to a ceramic biofilter seeded with earthworm (Lumbricus terrestris) casts. The effect of inlet H2S concentration and space velocity (SV) on the removal of NH3 was investigated after the acclimation of the biofilter with NH3 gas. When NH3 was singly supplied to the biofilter, NH3 removal was maintained at almost 100% until inlet NH3 concentration was increased up to 600 µL L-1 and SV up to 330 h-1, at which the elimination capacity of NH3 was 148 g N m-3 h-1. When H2S was supplied simultaneously, however, the accumulation of toxic sulfide ions showed dual effects on NH3 removal efficiencies. First, no effects were observed at inlet H2S loading below 60 g S m-3 h-1; however, inhibition by H2S at higher loading was observed above 60 g S m-3 h-1. The point at which loading achieved a maximum of more than 99% NH3 removal efficiency was 139 g N m-3 h-1, when inlet H2S concentration was held under 100 µL L-1, but it dropped to 76 and 30 g N m-3 h-1 when the inlet H2S concentration increased to 220 and 460 µL L-1, respectively. The critical points of inlet H2S loading that guaranteed over 99% NH3 removal were determined as 100, 100, 60, and 40 g S m-3 h-1 at inlet NH3 concentrations of 100, 200, 400, and 600 µL L-1, respectively. Inlet NH3 loading had synergic effects of increasing the inhibition of inlet H2S loading on the NH3 removability of the biofilter.
Abbreviations: SV, space velocity
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INTRODUCTION
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AMMONIA AND HYDROGEN sulfide are colorless air pollutants with repellent odor and corrosive characteristics. They are simultaneously emitted from food processing plants, composting plants, wastewater treatment plants, and night soil treatment plants (Eikum and Storhang, 1998; Ryer-Power, 1991; Yang and Allen, 1994). The traditional treatment of these malodorous gases is based on physical and/or chemical processes, such as activated carbon adsorption, incineration, catalytic oxidation, wet scrubbing, and thermal oxidation, all of which are expensive and produce secondary pollutants as well (Wani et al., 1997). As a technology for controlling odors, biofiltration has several advantages over traditional air pollution control technologies: low capital and operating costs, less energy requirements, no need of additional chemicals or fuels, the absence of residual products requiring further treatment or disposal, and, above all, public acceptance as an "environmentally friendly" process (Cho et al., 1992, 2000; Wani et al., 1997). Another advantage of biofiltration is its ability to deal with several contaminants simultaneously (Wani et al., 1997).
Because various kinds of malodorous gases are simultaneously emitted from odor sources, the effect of mixed gas on the removal efficiency of each gas cannot be ignored (Lipski et al., 1994; Williams, 1995). In most biofilters designed for the treatment of malodorous gases containing NH3 and H2S, which are mainly produced from sewage treatment plants and night soil treatment plants (where H2S concentration is greater than NH3), NH3 is neutralized chemically with SO2-4 (the oxidation product of H2S), and the residual NH3 is biologically removed by NH3–oxidizing bacteria (Cho et al., 1992; Kim et al., 2000b). Gas mixtures of NH3 and H2S are removed by biofilters packed with co-immobilized cells (Nitrosomonas europea for NH3 and Thiobacillus thioparus CH11 for H2S; Arthrobacter oxydans CH8 for NH3 and Pseudomonas putida CH11 for H2S) (Chung et al., 2000, 2001). A three-phase fluidized-bed bioreactor including Thiobacillus sp. IW was treated to remove NH3 and H2S simultaneously (Kim et al., 2000b). In results from previous studies, the effects of NH3 on the removal efficiencies of H2S by sulfur oxidizing bacteria (e.g., Pseudomonas, Thiobacillus sp.) were summarized as follows. At low concentration of NH3, H2S removal efficiency was as high as 99% with operating time. The reason may be that the ample supply of nitrogen promotes the metabolic activity of Thiobacillus, and because of the neutralization reaction between NH+4(aq) and SO2-4 (Chung et al., 2000). In the case of a higher concentration of NH3, the poor H2S removal efficiency might be attributed to the acidification of the biofilter (Chung et al., 2001).
On the other hand, the main component of odor produced from the composting plant and feedstuff plant was NH3, and a relatively low concentration of H2S was produced simultaneously. Therefore, the scope of this research was to evaluate the effect of H2S presence on the NH3 removal efficiency of the biofilters used to treat the high NH3 concentration, and to compare it with the condition where only NH3 gas was supplied. The operational parameters, such as the inlet NH3 and H2S concentration and space velocity (SV, volumetric gas flow rate per unit of the packing volume of ceramics), which were the factors determining the inlet loading, were also evaluated.
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MATERIALS AND METHODS
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Earthworm Casts and Porous Ceramics
Earthworm casts and porous ceramics were used as an inoculum source and packing materials for a NH3 removal biofilter, respectively. Earthworm casts were sampled from a sewage treatment plant located in Seoul, Korea. In the plant, the earthworms were sustained in anaerobically digested sludges.
Porous ceramics were supplied from SsangYong Co. Ltd, Daejon, Korea. After crushing, particles ranging in size from 7 to 11 mm were selected by sieving as packing materials (mean particle size was 9.0 mm). The physical properties of the ceramics are shown in Table 1.
Removal of Ammonia and/or Hydrogen Sulfide from the Biofilter Inoculated with Earthworm Casts
Figure 1
shows a schematic diagram of the laboratory-scale biofilter used in this study. The biofilter was constructed from a pyrex column with an internal diameter of 46 mm and a height of 300 mm. The column was packed with the porous ceramics prepared as follows: 50 g wet of the earthworm casts were added into a 500-mL flask containing 200 mL of mineral salts medium. The mineral salts medium was composed of 0.7 g of KH2PO4, 34.0 g of Na2HPO4·12H2O, 0.1 g of MgSO4·7H2O, 0.5 g of NaHCO3, 0.05 g of CaCl2·12H2O, and 0.001 g of Fe-EDTA. After the earthworm cast solution was shaken at 250 rpm for 30 min, the supernatant was centrifuged at 8000 rpm for 20 min, and then the precipitates were suspended with 40 mL of the mineral salt medium. The suspension was mixed with 75 g of dry porous ceramics. Another column, which contained raw porous ceramic without inoculation of earthworm cast, was used for a control experiment to demonstrate adsorption capacity. The details of packing conditions of the ceramics in the biofilter are summarized in Table 2. Sixty microliters per liter of NH3 gas was supplied into the biofilter at 56 h-1 of SV, and inlet and outlet gas concentrations were regularly measured by gas chromatography. When the outlet gas concentration reached nearly zero, the inlet gas concentration was increased to a desired higher level. After the gas supply was started, 50 mL of sterile water was splashed to the top of the biofilter every day to maintain moisture content at more than 70%. The moisture content in outlet gas of the biofilter was measured by a thermo hydro recorder (Cole-Parmer, Vernon Hills, IL). One hundred milliliters of sterile mineral salt medium was sprayed on the biofilter manually every week to supplement the minerals.
After the acclimation of NH3–degrading microorganisms in the ceramic biofilter, the removal capacity of NH3 was investigated by changing both the inlet NH3 concentration (100–660 µL L-1) and SV (55–330 h-1). The effect of mixed gases of NH3 and H2S on the removal efficiency of NH3 was also investigated. The experimental conditions such as inlet H2S concentration, inlet NH3 concentration, and SV are summarized in Table 3. A total of 80 conditions were used: the concentrations of NH3 and H2S were varied from 100 to 600 µL L-1 and 0 to 460 µL L-1, respectively, and the SV also varied in a similar manner anywhere from 55 to 330 h-1 for each condition. In every experimental condition, the outlet concentration of each gas from the biofilter was measured every 30 min until a constant level of outlet gas concentrations was detected.
Ammonia and H2S gases were supplied from concentrated standard gas cylinders containing 50 000 µL L-1 NH3 and 100000 µL L-1 H2S, respectively (balanced gas N2; Hana Gas Co., Busan, Korea). The odorous gases diluted with air in the mixing chamber were supplied into the glass biofilter. In this study, the elimination efficiency and elimination capacity were calculated according to the following formulae:
where 
is elimination efficiency (%); Cin is inlet concentration of gas (µL L-1); and Cout is outlet concentration of gas (µL L-1), and:
where EC is elimination capacity (g m-3 h-1); SV is space velocity (h-1); and 
is the conversion coefficient (m3 µL L-1 g N-1 [or g S-1]).
Analysis
The inlet and outlet NH3 gases were absorbed in 5 mM H2SO4 solution for 10 min. The concentration of NH+4 ion in the solution was analyzed by ion chromatography (Waters, Milford, MA) with an IC Pak Cation M/D column (3.9-mm diameter x 150-mm length; Waters). The inlet and outlet H2S gas concentrations were analyzed by gas chromatography (5890 Plus II; Hewlett-Packard, Palo Alto, CA) equipped with flame photometric detector and HP-1 capillary column (0.25-mm diameter x 3000-mm length; Hewlett-Packard). The temperature of the oven, injector, and detector were fixed at 35, 100, and 200°C, respectively.
Microscopic determination of the ceramic samples, after appropriate treatment, was performed with scanning electron microscopy (JSM-35CF; JEOL, Tokyo, Japan) as described by Cho et al. (2000).
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RESULTS AND DISCUSSION
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Acclimation of Ammonia-Degrading Microorganisms
The biofilter was acclimated by increasing the average NH3 concentration gradually from 60 to 590 µL L-1 to establish steady state conditions as indicated by outlet NH3 concentrations remaining constant with time. When 60 to 590 µL L-1 of NH3 was supplied at SV of 56 h-1, the removal characteristics for NH3 of the biofilter inoculated with earthworm casts were shown in Fig. 2 . The biofilter exhibited short-lived peaks after every step change in inlet NH3 concentration. In the outlet gas, 1 to 20 µL L-1 of NH3 gas was detected just after an increase of the inlet concentration, presumably due to the quick increase in inlet load. The biofilter then performed at low removal for a few days before microorganisms began to re-acclimate, after which the removal efficiency gradually improved. After several days of fluctuation of the outlet gas, less than 0.1 µL L-1 of NH3 gas was detected with time in the outlet. Thereafter, increasing the inlet NH3 concentration to 168 µL L-1 increased the load. After complete removal was observed, the load was increased again by changing the inlet NH3 concentration from 168 to 328 and 590 µL L-1. On the other hand, physical adsorption of NH3 on the ceramic also was measured. When 100 µL L-1 of NH3 was supplied at 56 h-1 to the same ceramics filter without inoculation, breakthrough time at which the concentration in the outlet stream reached the breakthrough point (98% of the inlet concentration) was 61 h. Ammonia adsorption capacity on the ceramic was negligible (0.53 g kg-1). This result indicates that NH3 removal is associated with biological reaction caused by microorganisms originating from earthworm casts, not physico–chemical removal reaction with the carrier material.
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Fig. 2. Time course of NH3 concentration on the biofilter inoculated with earthworm casts during acclimation period. The symbol • denotes inlet NH3 concentration (µL L-1), the solid line denotes average inlet NH3 concentration (µL L-1), and the symbol  denotes outlet NH3 concentration (µL L-1).
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Scanning electron micrographs showed that many rod-type bacteria with a length of 1 µm attached to the surface of the porous ceramics sampled from the biofilter (Fig. 3)
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Fig. 3. Scanning electron micrograph of (a) raw porous ceramics and (b) NH3–degrading bacteria immobilized on porous ceramics.
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Effect of Hydrogen Sulfide on Ammonia Removal by the Ceramic Biofilter
When NH3 single gas ranging from 100 to 600 µL L-1 at SV from 55 to 330 h-1 was supplied to the ceramic biofilter, NH3 was completely removed. Outlet NH3 concentration was less than 0.1 µL L-1 (detectable limit concentration) at all experimental conditions. The maximum loading of NH3 was 148 g N m-3 h-1 and NH3 removal capacity was 148 g N m-3 h-1, showing complete removal of NH3 under these conditions. The NH3 elimination capacity obtained from this study was relatively high compared with those of other biofilters (Table 4). The differences in physical properties of packing materials such as porosity, mean pore diameter, and maximum water content contribute to the differences in mass transfer capacity of odorous gas, resulting in a different removal capacity of each packing material (Hirai et al., 2001a).
As a result of an analysis with ion chromatography of the drain samples after the biofilter was washed with distilled water, ammonium ion, nitrates, and nitrites were detected. Although the concentration of ammonium ion was negligible (less than 50 ± 20 mg L-1), the concentrations of nitrite and nitrate were in the range of 3.5 ± 0.7 and 5.5 ± 1.3 g L-1, respectively. The nitrification is the most sensitive process to saline concentrations so that the activity of nitrifying bacteria fell sharply with increasing salt concentration (Glass and Silverstein, 1999; Instrasungkha et al., 1999; Panswad and Ana, 1999; Campos et al., 2002). Campos et al. (2002) found the inhibitory behavior of nitrifying bacteria for NO-3, reaching inhibition of 100% at concentrations around 250 mM (44.6 g NaNO3 L-1). However, the efficiency was maintained at nearly 100% up to a salt concentration around 525 mM, when nitrifying organisms adapted for high saline concentrations in the case of continuous operation, indicating that the adapted nitrifying organisms were less sensitive to high saline concentrations. The nitrate and nitrite in the biofilter used in this study were not accumulated to the inhibiting level to nitrifying bacteria because of the frequent washing of the biofilter with distilled water. Moreover, the nitrifying bacteria immobilized on the biofilter may be adapted to relatively high saline concentrations during long-term operation.
Ammonia removal efficiencies of the biofilter at various SV conditions were investigated when the changes of the inlet NH3 gas at concentrations from 100 to 600 µL L-1 and the H2S gas from 50 to 460 µL L-1 were performed (Fig. 4)
. When inlet H2S gas in the range of 50 to 100 µL L-1 was simultaneously supplied with NH3 (100–600 µL L-1) to the biofilter, outlet NH3 concentration remained below 0.1 µL L-1, indicating H2S gas lower than 100 µL L-1 did not affect NH3 removability of the ceramic biofilter.
When 220 µL L-1 of H2S gas was supplied simultaneously with NH3 to the biofilter, NH3 removability was significant depending on the inlet NH3 concentration and SV. In the case of the inlet NH3 concentration below 200 µL L-1, 100% NH3 removal efficiencies were obtained at all SV conditions (Fig. 4a,b). However, at inlet NH3 concentration of 400 µL L-1, NH3 removal efficiency decreased with increasing SV (Fig. 4c). At an inlet NH3 concentration of 600 µL L-1, NH3 removal efficiency was 100% when SV was below 55 h-1, but it decreased to 88% at SV of 330 h-1, respectively (Fig. 4d).
When 460 µL L-1 of H2S gas was supplied simultaneously with NH3 to the biofilter, NH3 removability was remarkably inhibited by the coexistence of H2S. Ammonia removal efficiency was 100% until SV increased to 110 h-1, while it decreased to 84% at SV of 330 h-1 in the case of inlet NH3 gas concentration of 100 µL L-1 (Fig. 4a). At inlet NH3 concentration of 200 µL L-1, 100% NH3 removal efficiencies were obtained when SV was below 110 h-1. However, it decreased to 72% at SV of 330 h-1 (Fig. 4b). At inlet NH3 concentration of 400 µL L-1, NH3 removal efficiencies decreased from 100 to 69% at SV from 55 to 330 h-1 (Fig. 4c). When inlet NH3 concentration and inlet H2S concentration increased to 600 and 460 µL L-1, NH3 removal efficiencies sharply dropped with increasing SV (Fig. 4d). On the other hand, H2S gas supplied simultaneously with NH3 was adsorbed a little by the biofilter in the first period of operation, and was not removed later. Chung et al. (2001) had reported that adequate H2S concentration (60 µL L-1) favored the metabolism of NH3 by A. oxydans CH8 compared with the H2S-free inlet. In addition, excess H2S concentration (120 µL L-1) decreased NH3 removal efficiency.
To evaluate the effect of the presence of H2S on the NH3 removal capacity of the biofilter inoculated with earthworm casts, the NH3 removal capacity was calculated from the inlet and outlet NH3 gas concentrations as a function of the inlet loading of NH3 at various inlet H2S concentrations (Fig. 5)
. When low concentration of H2S (less than 100 µL L-1) was supplied simultaneously with NH3 to the biofilter, NH3 gas was not detected in the outlet and maximum NH3 removal capacity was determined to be 139 g N m-3 h-1 (the maximum loading of NH3 was 139 g N m-3 h-1). When high concentration of H2S (greater than 220 µL L-1) was supplied simultaneously with NH3 to the biofilter, NH3 removal capacity decreased. When inlet NH3 loading was 137 g N m-3 h-1, NH3 removal capacities decreased to 120 and 69 g N m-3 h-1 at inlet H2S concentrations of 220 and 460 µL L-1, respectively. In particular, the decreasing tendency of NH3 removal capacity was evident at 460 µL L-1 of inlet H2S concentration. Ammonia removal capacities increased linearly until inlet NH3 loading was increased to 91 g N m-3 h-1. However, NH3 removal capacities remained at 70 g N m-3 h-1 after inlet NH3 loading was more than 91 g N m-3 h-1. This result indicated that the critical point of NH3 removal capacity of the ceramic biofilter was 70 g N m-3 h-1 when 460 µL L-1 of H2S were supplied simultaneously with NH3.
The maximum NH3 loading achieving more than 99% of NH3 removal efficiency was 139 g N m-3 h-1 when inlet H2S concentration was under 100 µL L-1, but it dropped to 76 and 30 g N m-3 h-1 when inlet H2S concentration increased to 220 and 460 µL L-1, respectively.
Although some researchers have studied the simultaneous removal of H2S and NH3, their research did not provide a clear explanation regarding the inhibition effect of H2S on NH3 removal (Chung et al., 2000, 2001; Kim et al., 2000b). Kim et al. (2000b) observed that NH3 removal efficiency was always lower when a stoichiometrically excessive amount of NH3 compared with H2S entered the bioreactor, but did not clearly describe the inhibition effect of H2S. Chung et al. (2000)( 2001) explained the inhibition effect of H2S on the NH3 removal by inlet H2S concentration. Inlet gas concentration plays an important role in the design of a scale-up biofilter when constant packing material volume and space velocity are used. However, the removal capacities or efficiencies in terms of inlet loading should be considered, because inlet concentration differs according to the different SV conditions and scale of the biofilter.
Thus, the relationship between inlet H2S loading and NH3 removal efficiency was shown in Fig. 6
to evaluate the effect of inlet H2S loading on the NH3 removal efficiency. Ammonia removal efficiencies decreased when increasing the inlet H2S loading to a constant level under all experimental conditions. When inlet NH3 concentration was 100 µL L-1, 100% removal of NH3 was obtained at inlet H2S loading of 100 g S m-3 h-1. Ammonia removal efficiencies were 97% and 85% at inlet H2S loadings of 130 and 200 g S m-3 h-1, respectively. These inhibition effects on the NH3 removal efficiencies increased when increasing the inlet NH3 concentration. For example, when inlet H2S loading was 200 g S m-3 h-1, NH3 removal efficiencies were 84, 72, 69, and 50% at inlet NH3 concentration of 100, 200, 400, and 600 µL L-1, respectively. Ammonia removal efficiencies decreased significantly with the increase of inlet NH3 concentration at constant inlet H2S loading.
On the other hand, the critical points of inlet H2S loading that guaranteed more than 99% NH3 removal were determined as 100, 100, 60, and 40 g S m-3 h-1 at inlet NH3 concentrations of 100, 200, 400, and 600 µL L-1, respectively.
Effects of both the inlet H2S loading and inlet NH3 loading on the NH3 removal efficiencies were investigated by regression of experimental data obtained with the mixed gases of NH3 and H2S (Fig. 7)
. Within the operation conditions of this research, the range of inlet H2S loading that did not affect NH3 removal efficiencies, irrespective of inlet NH3 loading, was less than 60 g S m-3 h-1. The ranges of inlet H2S loading that did not affect NH3 removal efficiencies at low inlet NH3 loading were wider than that of high inlet NH3 loading. For example, inlet H2S loading that did not affect NH3 removal efficiencies was 60 g S m-3 h-1 at inlet NH3 loading of 140 g N m-3 h-1, while it was 120 g S m-3 h-1 at inlet NH3 loading of 20 g N m-3 h-1. That is to say, inlet H2S loading had a significant effect on NH3 removal efficiencies at high inlet NH3 loading compared with low inlet NH3 loading. Also clear was the inhibition effect of H2S on the NH3 removal of the biofilter. Inlet NH3 loading also had synergic effects of increasing the inhibition of inlet H2S loading on the NH3 removability of the biofilter.
The reduction in the NH3 removal in mixed gases (H2S and NH3) compared with the NH3 removal in single NH3 gas may be caused by two possibilities, the high concentration of H2S and the accumulation of NO-3 on the biofilter, which may block the nitrification of NH3–oxidizing bacteria (Julitte et al., 1993; Joye and Hollibaugh, 1995; Chung et al., 2000). The addition of 60 and 100 µM hydrogen sulfide (HS-) reduced nitrification by 50 and 100%, respectively (Joye and Hollibaugh, 1995), and therefore caused the reduction in NH3 removal efficiency (Chung et al., 2001). A sulfide concentration of 0.5 mg L-1 had a considerable negative effect on the nitrification activity (Æsøy et al., 1998). Furthermore, the accumulated NO-3, the oxidation product of ammonia, caused the decrease of pH and inhibited the oxidation activity of NH3–oxidizing bacteria.
We conclude that the presence of H2S had no significant effects on the NH3 removal by the biofilter when inlet H2S loading was below 60 g S m-3 h-1. The effects of both the inlet NH3 loading and the inlet H2S loading on the NH3 removal efficiencies were evaluated quantitatively. Results obtained in this research should provide important information in the design and operation of a biofilter for malodorous gases containing high concentrations of NH3 gas.
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ACKNOWLEDGMENTS
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Funding for this research was provided by Grant no. 96-0601-06-01-3 from the Korea Science and Engineering Foundation and the National Research Laboratory Program of the Korean Ministry of Science and Technology.
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NOTES
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E.Y. Lee, present address: Dep. of Environmental Engineering, University of Suwon, Suwon P.O. Box 77, Suwon 440-600, Korea.
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ABSTRACT
INTRODUCTION
, 100; 
, 220; 
, 460 µL L-1.
