Article pubs.acs.org/est
Monitoring Tc Dynamics in a Bioreduced Sediment: An Investigation with Gamma Camera Imaging of 99mTc-Pertechnetate and 99mTcDTPA Nicholas T. Vandehey,* James P. O’Neil, Aaron J. Slowey, Rostyslav Boutchko, Jennifer L. Druhan, William W. Moses, and Peter S. Nico Lawrence Berkeley National Laboratory, 1 Cyclotron Road, Berkeley, California, USA S Supporting Information *
ABSTRACT: We demonstrate the utility of nuclear medical imaging technologies and a readily available radiotracer, [99mTc]TcO4−, for the noninvasive monitoring of Fe(II) production in acetate-stimulated sediments from Old Rifle, CO, USA. Microcosms consisting of sediment in artificial groundwater media amended with acetate were probed by repeated injection of radiotracer over three weeks. Gamma camera imaging was used to noninvasively quantify the rate and extent of [99mTc]TcO4− partitioning from solution to sediment. Aqueous Fe(II) and sediment-associated Fe(II) were also measured and correlated with the observed tracer behavior. For each injection of tracer, curves of 99mTc concentration in solution vs time were fitted to an analytic function that accounts for both the observed rate of sedimentation as well as the rate of 99mTc association with the sediment. The rate and extent of 99mTc association with the biostimulated sediment correlated well with the production of Fe(II), and a mechanism of [99mTc]TcO4− reduction via reaction with surface-bound Fe(II) to form an immobile Tc(IV) species was inferred. After three weeks of bioreduction, a subset of microcosms was aerated in order to reoxidize the Fe(II) to Fe(III), which also destroyed the affinity of the [99mTc]TcO4− for the sediments. However, within 3 days postoxidation, the rate of Tc(VII) reduction was faster than immediately before oxidation implying a rapid return to more extensive bioreduction. Furthermore, aeration soon after a tracer injection showed that sediment-bound Tc(IV) is rapidly resolubilized to Tc(VII). In contrast to the [99mTc]TcO4−, a second commercially available tracer, 99mTc-DTPA (diethylenetriaminepentaacetic acid), had minimal association with sediment in both controls and biostimulated sediments. These experiments show the promise of [99mTc]TcO4− and 99mTc-DTPA as noninvasive imaging probes for a redox-sensitive radiotracer and a conservative flow tracer, respectively.
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INTRODUCTION The use of medical radiotracer imaging techniques for studying bioremediation of environmental toxins is gaining interest bridging the fields of environmental research and medical imaging.1−3 Radiotracers have been used in environmental sciences for many years over a wide range of applications due to their ability to probe specific chemical processes.4,5 The recent use of nuclear medical imaging tools (i.e., gamma camera, single photon emission computed tomography [SPECT], or positron emission tomography [PET]) is driven by their ability to dynamically measure the 3D distribution of radiotracers inside sediment systems, with better than 1 cm resolution and picomolar sensitivity. These tools hold the potential for noninvasive, real-time monitoring of both physical and chemical properties of porous sediment, which is important in understanding the feedback pathways that couple chemically and microbially induced physical changes in pore structure and flow paths within porous media,6 a key question for many areas of subsurface sciences. Specifically, the ability to simultaneously measure hydrological properties using a conservative tracer while © 2012 American Chemical Society
measuring the location and extent of reducing microenvironments using a redox-sensitive radiotracer represents a significant new tool for understanding of the relationship between chemical transformations and the associated porosity and permeability evolution during reactive transport. For example, the production of Fe(II) through microbial reduction of iron oxides for bioremediation of metal contaminants7,8 can also lead to substantial changes in flow field permeability due to biomass growth, production of methane, and precipitation of iron, carbonates, and sulfides.6 The relative contribution of Fe(II) to this flow field evolution and the coupled influence of permeability change on iron reduction in the system has been indirectly inferred through electrodic potentials9 but has never been directly quantified. With the goal of developing methods for Fe(II) detection and evaluation of a potential conservative radiotracer, we used Received: Revised: Accepted: Published: 12583
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gamma camera imaging to measure 99mTc-pertechnetate (TcO4−) and 99mTc-DTPA (diethylenetriaminepentaacetic acid) interactions with sediment before and after microbial stimulations with acetate. It is expected that [99mTc]TcO4− would rapidly associated with solid phase via reductive precipitation upon the onset of Fe(III) bioreduction and the accumulation of surface Fe(II): TcO−4(aq) + 3Fe(II)aqueous + mH 2O
Twenty-two microcosms were prepared anaerobically in a glovebox filled with a 5% CO2/95% N2 mixture. Each microcosm consisted of 15 g dry sediment (∼10 mL) in 110 mL AGW, contained in a thick-walled 100 mL glass serum vial, crimp-sealed with a butyl-rubber stopper. A reference vial filled with only 110 mL AGW (no sediment) was used as a 99mTc concentration standard, which is needed for image normalization. Throughout the course of the experiment, all vials remained intact, sealed, and stored at room temperature until analyzed for sediment-bound Fe(II/III). Nineteen microcosm vials were amended with sodium acetate to an acetate ion concentration of 6 mM, whereas the other three microcosms served only as controls. Reoxidation Experiments. Initial reoxidation experiments were aimed at investigating the oxidation of Fe(II) to Fe(III) in oxygen-saturated water and observing the subsequent recovery to reducing conditions as conducted on seven vials starting 22 days after acetate amendment. Our prior 99mTc-pertechnetate studies suggested amended vials were in highly reducing conditions at this time. A second set of reoxidation experiments was conducted on two vials investigating the oxidation of Tc(IV) back to Tc(VII) in oxygen-saturated water with realtime imaging during the oxidation. Prior to beginning the first reoxidation imaging sequence, the vials were aerated between 2 and 2.5 h; allowed to sit overnight; and then, 2 h before injection of radiotracer, sparged with 5% CO2/95% N2 for 1.5 h. The aeration was realized by pumping air into the base of the vials via 19G x 5″ needles coupled to an aquarium pump. 19G needles served as air vents. Aeration provided agitation to the sediment causing partial resuspension. For the secondary reoxidation experiments, the three vials in their reduced state were imaged with [99mTc]TcVIIO4− as described above, aerated for 50 min, and then immediately imaged again. Vials were not sparged of oxygen following the secondary aeration. 99m Tc Radiotracers. Medical-grade 99mTc radiotracers of >95% radiochemical purity were obtained from Cardinal Health (Richmond, CA. 99mTc-pertechnetate (TcVIIO4−) was supplied as the sodium salt in saline solution at a concentration of >20 mCi/mL (740 MBq/mL). 99mTc-DTPA (diethylenetriaminepentaacetic acid) was synthesized by Cardinal Health using a radiopharmaceutical labeling kit supplied by DraxImage20 (Quebec, Canada) reacting DTPA with a reduced form of 99m Tc(III−V).21 The product was supplied in a sterile saline solution at a concentration of >20 mCi/mL containing 5 days postamendment). Again in supporting batch experiment controls, it was shown that 99mTc-DTPA showed less than 3% association with filterable FeS colloids in solution, yet no appreciable filterable precipitates with either Fe(II), or S2− in solution (Supporting Information). Microcosm Responses to Oxygenation. The transient increase in dissolved oxygen with the first reoxidation experiment is evident in Figure 3 (right) showing that in the
aerated 99mTc-pertechnetate microcosms Tc(VII) was minimally reduced at day zero. However, within one day following this aeration, reducing conditions returned, and end points (Aend) were similar to those just before reoxidation within only two days. Also, the initial slope of β versus time (Figure 3) is greater following oxygenation than following acetate amendment, with Tc(VII) to Tc(IV) reduction rates (β reaching 0.0084 min−1 within five days postoxygenation, which is up to 40% faster than the maximum rate following the initial amendment. Acid soluble Fe(II)solid concentration 16 days following reoxidation was 5.8 ± 2.3 μmol/g dry sediment, 15% higher than 19 days postamendment. The microcosm imaged with 99mTc-DTPA following aeration showed no change in signal due to aeration. Three time-activity curves for experiments following the secondary reoxidation are given in Figure 5. These data show 12586
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Figure 4. (Left) Time course of iron concentration measurements. Error bars are standard error of the mean across microcosms. (Right) Proportional relationship of Fe(II)solid measurements to mean coefficient values on days 0, 7, 15, and 19. Y axes and data correspond by color. Ellipses represent standard error of the mean.
that 30−50% of the Tc(IV) bound to the sediment at t = 3.5 h was driven back into solution within 50 min of aeration.
able association with amended sediment. Finally, with oxygen saturation of the microcosms, we were able to investigate the reoxidation dynamics of both iron and technetium, with data suggesting that rapid, large swings in Fe(II)/Fe(III) concentrations took place and that oxidation of sediment-bound Tc(IV) to soluble Tc(VII) in oxygenated microcosms occurred over the time scale of a few hours. Quantification of Tc(VII) Reduction Rate. The methods presented here share many similarities with those of Lear et al.22 Microcosms were prepared in a similar fashion and shaking of vials occurred regularly over the first few hours following 99m Tc injection to ensure good contact between the sediment and the radioactive solution. Our protocol, however, provided dynamic imaging of the microcosm vials with high temporal resolution, allowing for quantification of the rate of Tc(VII) reduction (inferred from the rate of removal of 99mTc(VII) from solution). Furthermore, by having many samples and staggering the timing of augmentation and imaging, we were able to observe the rise of Fe(II) at one day intervals despite needing to wait two days between imaging studies for the 99mTc signal to decay. Assuming first-order sedimentation26 and Fe(II)- Tc(VII) reaction kinetics, we applied nonlinear curve fitting of measured 99mTc concentration to a series of timeshifted dual exponentially decaying functions, a technique similar to analyses of medical images acquired with multiple radiotracer injections.27,28 This model (eq 1) provided a very good description of the data, with R2 > 0.98 across all fits where Tc(VII) reduction occurred. Variations of the model were tested that allowed for additional degrees of freedom in the fit, but none provided a significantly better fit. The fitting of data to a mathematical model provided a number of indices of reaction rate and Fe(II)solid content that are more valuable than the final concentration alone (Aend). When plotted versus time, the fit parameters β, a, and b (Figure 3) all show trends similar to Fe(II) measures but with less variability. Average measures of solid phase Fe(II)solid measurements at days 0, 7, 15, and 19 were compared to average values of imaged-derived values using Deming Regression analysis.29
Figure 5. Time-activity curves for three secondary reoxidation experiments showing sediment-bound Tc(IV) being oxidized to soluble Tc(VII) following aeration. The vials were aerated for 50 min between imaging experiments. Data was not collected during the aeration period.
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DISCUSSION These experiments provide a significant extension of earlier work done using 99mTc labeled radiopharmaceuticals for studies of environmental remediation, presenting both new experimental methods and results relevant to technetium bioremediation chemistry. We have expanded upon prior experiments, using 99mTc-pertechnetate as a probe for the presence of reduced iron while also developing a mathematical model for quantitatively measuring the rate of reduction from Tc(VII) to Tc(IV). The results of data fitting to the model revealed a linear relationship of terms in this model to measured Fe(II)solid. 99m Tc-DTPA was evaluated as a conservative hydrologic flow tracer, with results showing great promise due to its minimal interaction with nonamended sediments and nearly undetect12587
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disturbed by the brief exposure to oxygenated water and can return rapidly to Fe(II) production as soon as O2 is depleted. Second, the amorphous Fe(III) solids produced during the rapid oxidation of Fe(II) are likely more easily reduced and bioavailable than the solid Fe(III) initially present in the system. Third, the increase in rate of Fe(II) build up after reoxidation could be due to competition with oxidized manganese in pristine sediment, but not in reoxygenated sediment, as others have suggested previously upon observation of the same effect.10,38 In the secondary reoxidation experiments, we allowed 99m Tc(VII) to be reduced to 99mTc(IV) on reduced sediment. The 99mTc was then remobilized back into solution after oxygenation via aeration, with 30−50% of the sediment-bound 99m Tc remobilizing over about 4 h (Figure 5). This was considerably faster than previously published time periods of two days39 and 15 days36 to reach 50% remobilization. The time-activity curves also show that most oxidation occurred during the aeration period, but reoxidation continues after aeration is terminated. As elevated nitrate concentrations have been measured at nuclear waste sites40,41 and can provide different reoxidation dynamics,36,37,39 it would be of interest to future work to conduct dynamic 99mTc imaging experiments that directly compare redox cycling with nitrate and dissolved oxygen. In conclusion, we have performed experiments quantifying radiotracer-sediment interactions at the laboratory scale, but with implications applicable to much larger bioremediation systems. In our microcosms we have shown that 99mTc-DTPA can be used as a conservative tracer, as it predominately remains in solution in both reducing and nonreducing conditions. Our measurements also show that 99m Tcpertechnetate is more rapidly removed from solution as Fe(III) is progressively reduced to Fe(II), with modeled parameters proportional to Fe(II)solid concentration. Furthermore, analogous in both scale and duration to human medical research studies, it is reasonable to believe that applications using these radiotracers could be scaled up to longitudinally study larger bioremediation experiments, such as a sediment column. In such an experiment, 99mTc-pertechnetate and 99mTc-DTPA would be the perfect complement to each other, as successive imaging experiments would provide 3D images of the tracers representing both Fe(II) concentration and water flow, respectively. Finally, in considering a much larger scale, the micro- and mesoscale imaging techniques presented and proposed here will help provide a better understanding of the redox chemistry associated with oxidation events often associated with field-scale bioremediation efforts.
Among the image-derived parameters, the best predictors of solid phase Fe(II) were a and b, with r2 = 0.99 and r2 = 0.95, respectively (Figure 4). Whereas reaction rates (β) did not track linearly with Fe(II)solid, the measured rates of up to 0.006 min−1 postamendment and 0.0084 min−1 postreoxidation are very similar to those published previously (0.006 min−1, 17 days post 10 mM lactate amendment10). Whereas our model was developed to describe the data from our acquisition protocol, it is also expected to be robust across a variety of similar acquisition protocols. Specifically, we expect the parameters that describe physical rates (α and β) to be independent of protocol timing, whereas other parameters (a, b, c, Aend) would change if the protocol were modified (e.g., different number of shaking instances or time between shakes). We also expect that experiments utilizing different reactive tracers would have different reaction rates (β) but similar sedimentation rates (α) unless particle size changed as could occur during sediment aggregation. These estimates of the rate of sedimentation and reduction could also provide valuable a priori information for optimizing the design of further experiments.30,31 99m Tc-DTPA as a Conservative Tracer. The data presented here show that 99mTc-DTPA acts as a mostly conservative radiotracer in our microcosm vials, with only slight absorption in control microcosms (∼7%) and even less following amendment (∼2%). Our hypothesized mechanism for the changing 99mTc-DTPA behavior is that the DTPA complex has some small amount of unsatisfied chelation ability that caused association with the sediment in the control microcosms. Upon iron reduction, these sites are satisfied with aqueous Fe minimizing sediment interaction. Important for the dual use of the two tracers, 99mTc-DTPA associates much less under reduced conditions where TcO4− is immobilized creating a stark contrast between the behavior of the two radiotracers. With information confirmed from this experiment in hand, flow-through column experiments have also been performed with 99mTc-DTPA,32 where it did not accumulate along the a column’s flowpath neither prior to nor following biostimulation (Supporting Information). These results are similar to various reports showing that Gd-DTPA moved conservatively through both a bank filtration system33 and an artificial aquifer.34 This is in contrast to Jurisson et al.,35 however, who reported 25−66% sorption of 99mTc-DTPA to surface soils, a difference likely related to the high organic matter content in the soils tested relative to the subsurface sediment used in our experiments. Reoxidation Experiments. Reoxidation experiments showed both the oxidation of Fe(II) → Fe(III) and Tc(IV) → Tc(VII) by increasing dissolved oxygen in solution. Immediately following the first aeration sequence, microcosms showed little to no 99mTc reduction over the 3.5 h experiment, suggesting that Fe(II) was nearly completely oxidized to Fe(III) after 10 h of residence in high dissolved-oxygen water. This rate of reoxidation was considerably faster than a previous report measuring only 61% return to Fe(III) after one day of aeration36 suggesting a high variability in the rate of oxidation dependent on experimental conditions. Similar measurements have also been made in a flow-through column, with nearly 30 days needed for Fe(II) concentrations to drop to baseline.37 Following the first aeration, reducing conditions were restored faster than they originally evolved after acetate amendment. There are several potential reasons for this. First, the Fe(III) reducing microbial community that has established itself since augmentation is likely not greatly
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ASSOCIATED CONTENT
S Supporting Information *
Details on the sampling and scanning schedule, a more detailed description of the sorption of on iron sulfide experiments, and images of both tracers in a flow-through bioreductive column. This material is available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. 12588
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Notes
(10) Fredrickson, J. K.; Zachara, J. M.; Kennedy, D. W.; Kukkadapu, R. K.; McKinley, J. P.; Heald, S. M.; Liu, C.; Plymale, A. E. Reduction of TcO4− by sediment-associated biogenic Fe(II). Cosmochim. Acta 2004, 68, 3171−3187. (11) Zachara, J. M.; Serne, J.; Freshley, M.; Mann, F.; Anderson, F.; Wood, M.; Jones, T.; Myers, D. Geochemical processes controlling migration of tank wastes in Hanford’s vadose zone. Vadose Zone J. 2007, 6, 985. (12) Wildung, R. E.; McFadden, K. M.; Garland, T. R. Technetium sources and behavior in the environment. J. Environ. Qual. 1979, 8, 156. (13) Istok, J.; Senko, J.; Krumholz, L.; Watson, D.; Bogle, M.; Peacock, A.; Chang, Y. J.; White, D. In situ bioreduction of technetium and uranium in a nitrate-contaminated aquifer. Environ. Sci. Technol. 2004, 38, 468−475. (14) Anger, H. O. A new instrument for mapping gamma-ray emitters. Biology and Medicine Quarterly Report; University of California Radiation Laboratory: Berkeley, CA, 1957, 3653. (15) Cherry, S. R.; Sorenson, J. A.; Phelps, M. E. In Physics in Nuclear Medicine; 3rd ed.; Saunders: Philadelphia, PA, 2003; pp 1−6. (16) Anderson, R. T.; Vrionis, H. A.; Ortiz-Bernad, I.; Resch, C. T.; Long, P. E.; Dayvault, R.; Karp, K.; Marutzky, S.; Metzler, D. R.; Peacock, A.; White, D. C.; Lowe, M.; Lovley, D. R. Stimulating the in situ activity of geobacter species to remove uranium from the groundwater of a uranium-contaminated aquifer. Appl. Environ. Microbiol. 2003, 69, 5884−5891. (17) Hartmann, G. L.; Arp, S.; Hempill, H. Waste minimization opportunities at the U.S. Uranium Mill Tailings Remedial Action (UMTRA) Project, Rifle, Colorado, site; Jacobs Engineering Group, Inc.: Albuquerque, NM, 1993. (18) Final site observational work plan for the UMTRA project Old Rif le site GJO-99−88-TAR; U.S. Department of Energy: Grand Junction, CO, 1999. (19) Li, L.; Steefel, C. I.; Williams, K. H.; Wilkins, M. J.; Hubbard, S. S. Mineral transformation and biomass accumulation associated with uranium bioremediation at Rifle, Colorado. Environ. Sci. Technol. 2009, 43, 5429−5435. (20) DTPA: Kit for Preparation of Technetium Tc 99m Pentetate Injection. http://www.draximage.com/Draximage/content/share/ data/rte/File/216184_Insert_DTPA_2011OC04_clean.pdf (Accessed June 4, 2012). (21) Környei, J.; Zolle, I. In Technetium-99m Pharmaceuticals; Ilse Zolle, Ed.; Springer: Berlin, 2007; pp 297−303. (22) Zolle, I. In Technetium-99m Pharmaceuticals; Ilse Zolle, Ed.; Springer: Berlin, 2007; pp 77−93. (23) Heron, G.; Crouzet, C.; Bourg, A. C.; Christensen, T. H. Speciation of Fe(II) and Fe(III) in Contaminated Aquifer Sediments Using Chemical Extraction Techniques. Environ. Sci. Technol. 1994, 28, 1698−705. (24) Stookey, L. L. Ferrozinea new spectrophotometric reagent for iron. Anal. Chem. 1970, 42, 779−781. (25) Coleman, T. F.; Li, Y. An interior trust region approach for nonlinear minimization subject to bounds. SIAM J. Control Optim. 1996, 6, 418. (26) Newman, K. A.; Morel, F. M. M.; Stolzenbach, K. D. Settling and coagulation characteristics of fluorescent particles determined by flow cytometry and fluorometry. Environ. Sci. Technol. 1990, 24, 506− 513. (27) Vandehey, N. T.; Moirano, J. M.; Converse, A. K.; Holden, J. E.; Mukherjee, J.; Murali, D.; Nickles, R. J.; Davidson, R. J.; Schneider, M. L.; Christian, B. T. High-affinity dopamine D2/D3 PET radioligands 18F-fallypride and 11C-FLB457: A comparison of kinetics in extrastriatal regions using a multiple-injection protocol. J. Cereb. Blood Flow Metab. 2010, 30, 994−1007. (28) Morris, E. D.; Christian, B. T.; Yoder, K. K.; Muzic Jr., R. F. In Imaging in Biological Research, Part A; Enzymology, Imaging in Biological Research, Part A Conn., P., Ed.; Academic Press: San Diego, CA., 2004; Vol. 385, pp 184−213.
DISCLAIMER. This document was prepared as an account of work sponsored by the United States Government. While this document is believed to contain correct information, neither the United States Government nor any agency thereof, nor the Regents of the University of California, nor any of their employees, makes any warranty, express or implied, or assumes any legal responsibility for the accuracy, completeness, or usefulness of any information, apparatus, product, or process disclosed, or represents that its use would not infringe privately owned rights. Reference herein to any specific commercial product, process, or service by its trade name, trademark, manufacturer, or otherwise, does not necessarily constitute or imply its endorsement, recommendation, or favoring by the United States Government or any agency thereof, or the Regents of the University of California. The views and opinions of authors expressed herein do not necessarily state or reflect those of the United States Government or any agency thereof or the Regents of the University of California. The authors declare no competing financial interest.
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ACKNOWLEDGMENTS We would like to thank Dr. Kenneth Williams and the researchers at the IFRC for their collaborations and making their sediment available to us to study and Dr. Christina Leggett for valuable discussions and help in preparing this manuscript. This work was conducted as part of the Subsurface Science Scientific Focus Area and the Radiotracer Imaging Technologies for Plant, Microbial and Environmental Systems Scientific Focus Area supported by the Director, Office of Science, Office of Biological and Environmental Research, Biological Systems Science Division of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231.
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