State indicators for monitoring the anaerobic digestion process

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    Monitoring and control are important strategies for achieving

    ideal indicator should reflect the current process status and

    be straightforward to measure. Moreover, its response to the

    process imbalances should be significant compared to back-

    groundfluctuations.Thecommonindicators for themonitoring

    Biogas production is the most commonly monitored indi-

    1994). The low biogas production results not only fromprocess

    inhibition but also from low reactor loading. pH is relatively

    straightforward to measure and is often the only online liquid

    stated measured parameter. A pH decrease can indicate an

    accumulation of VFA. In a reactor with low buffering capacity,

    * Corresponding author. Tel.: 45 45251429; fax: 45 45932850.

    Avai lab le a t iencedi rec t .com


    wat e r r e s e a r c h 4 4 ( 2 0 1 0 ) 5 9 7 3e5 9 8 0E-mail address: (I. Angelidaki).a better process stability and higher conversion efficiencies in

    anaerobic digesters. Monitoring is a requirement for process

    control. The lack of suitable process indicators results in the

    limited control and optimization of anaerobic digestion. An

    cator, since it indicates the overall process performance and

    can be measured by a number of robust online sensors.

    However, it can poorly indicate an imbalanced state and often

    decreaseswhen the process is already damaged (Moletta et al.,digesters effectively.

    2010 Elsevier Ltd. All rights reserved.

    1. Introduction of the biogas process are gas production, biogas composition,pH, alkalinity and volatile fatty acids (VFA) (Hawkes et al., 1993).Received 24 February 2010

    Received in revised form

    6 June 2010

    Accepted 14 July 2010

    Available online 23 July 2010


    Anaerobic digestion


    Volatile fatty acids

    Dissolved hydrogen

    Biogas0043-1354/$ e see front matter 2010 Elsevdoi:10.1016/j.watres.2010.07.043a b s t r a c t

    Anaerobic process state indicators were used to monitor a manure digester exposed to

    different types of disturbances, in order to find the most proper indicator(s) for monitoring

    the biogas process. Online indicators tested were biogas production, pH, volatile fatty acids

    (VFA), and dissolved hydrogen. Offline indicators tested were methane and hydrogen

    content in the biogas. A CSTR reactor with 7.2 L working volume was operated at a varying

    hydraulic loading rate (HRT 10e20 days) for 200 days. During this period, the reactor was

    overloaded with extra organic matter such as glucose, lipid, gelatine, and bio-fibers, in

    order to create dynamic changes in the process state. Biogas production increased in

    response to the increase in organic load with a slight decrease in methane content. pH was

    relatively stable and did not show clear response to hydraulic load changes. However, pH

    changes were observed in response to extra organic load. Individual VFA concentrations

    were an effective indicator, with propionate persistent for the longest time after intro-

    duction of the disturbance. Dissolved hydrogen was very sensitive to the addition of easily

    degradable organics. However, it responded also to other disturbances such as slight air

    exposure which had no impact on process performance. A combination of acetate,

    propionate and biogas production is an effective combination to monitor this type ofAdvanced Water Management Centrec Laboratory of environmental biotechnniversity of Queensland, St Lucia, QLD 4067, Australia

    rench National Institute for Agronomic Research, Avenue des Etangs, 11100 Narbonne, FranceDepartment of Environmental Engineering, Technical University ofb , The UKanokwan Boe , Damien John Batstone , Jean-Phillippe Steyer , Irini Angelidaki *aState indicators for monitoringprocess

    a a,b

    journa l homepage : www.ier Ltd. All rights reservedthe anaerobic digestion

    a,c a,

    ev ier . com/ loca te /wat res.

  • pHcanbeauseful indicator.However, thepHresponsehas low

    sensitivity in a well-buffered system (Bjornsson et al., 2000).

    Biogas composition is a traditional parameter where low

    methane percent (i.e. high carbon dioxide content) could

    indicate inadequate process performance. However, the

    carbondioxide content is dependent on pH and, consequently,

    fluctuation of pH can affect the gas composition without

    decreasing methane production (Hansson et al., 2002).

    Hydrogen content of biogas is a very sensitive indicator and is

    connected to the imbalance between microbial groups in the

    digestion process (Molina et al., 2009; Steyer et al., 2002). The

    hydrogen content in biogas can easily be measured online

    using a semiconductor sensor (Hornsten et al., 1991). However,

    dissolved hydrogen may be more appropriate than gaseous

    hydrogen, as it is not delayed by liquidegas transfer and could

    2. Material and methods

    The experiment was carried out in a 9-L CSTR reactor with

    a 7.2 L working volume. Cattle manure (3%TS, 2%VS) was used

    as substrate for the reactor. The reactor was operated at 55 Cat a varying hydraulic loading (10e20 days HRT) for 200 days

    and was fed four times per day using a peristaltic pump

    (Watson Marlow) controlled by a timer and relay.

    To compare the indicators responses, hydraulic and

    organic load disturbances were introduced. For hydraulic

    disturbances, the feed volume was increased by increasing

    the feed duration. For organic overload, different organic

    compounds, besides the daily manure feed, were added into

    the reactor as summarised in Table 1. Rapeseed oil and gela-


    8 Mixed with feed and fed 4 times

    wat e r r e s e a r c h 4 4 ( 2 0 1 0 ) 5 9 7 3e5 9 8 05974better correlate to the VFA concentration (Pauss and Guiot,

    1993). Dissolved hydrogen increases together with VFA accu-

    mulation during sudden increase of organic load (Bjornsson

    et al., 2001b). VFA is widely suggested as process indicator,

    since it is the main pre-methanogenic intermediate (Jacobi

    et al., 2009; Molina et al., 2009). VFA accumulation in anaer-

    obic reactors indicates process imbalance (Ahring et al., 1995).

    Moreover, individual VFA concentrations give specific infor-

    mation for process diagnosis (Ahring et al., 1995; Cobb andHill,

    1991). Total VFA concentration can be measured online by

    titration (Feitkenhauer et al., 2002), or indirectly where light

    spectroscopy is correlated to total VFA concentrations, by

    using near infrared spectroscopy (NIR) (Holm-Nielsen et al.,

    2008; Jacobi et al., 2009). However, to measure individual VFA,

    online monitoring is more complex. The online monitoring of

    individual VFAhas beenbased on sample filtration followed by

    analysis in a gas chromatograph (Pind et al., 2003), or using

    headspace extraction followed by analysis in a gas chromato-

    graph (Boe et al., 2007).

    Many of the studies cited above assessed only a limited

    number of indicators, and often in processes operating under

    unstressed state. Moreover, lack of an online sensor for indi-

    vidual VFA limits the evaluation of this important indicator.

    The aim of this study is to assess the suitability of different

    anaerobic process indicators. A range of indicators, including

    biogas production, pH, individual VFA, dissolved hydrogen,

    and gas phasemethane and hydrogen contentwere compared

    under different types of disturbances.

    Table 1 e Summary of extra organic load added to the reac

    Day Amount added (g/day)

    Lipid Glucose Gelatine

    77 85 e e

    112 157 e e

    126 e 25 e

    137 e 50 e

    142 e e 25

    161 e 50 e

    168 e 100 e

    185e187 4 e e188e196 4 40 etine were used to represent lipid and protein, respectively.

    Glucose was used to represent easily degradable carbohydrate

    while bio-fiber containing arabinoxylans (Ispaghula Husk,

    Vi-Siblin; Edwards et al., 2003) was used to represent slowly

    degradable carbohydrate.

    During operation, the responses of different process indi-

    cators were measured. Online indicators were biogas

    production, pH, volatile fatty acids (VFA), and dissolved

    hydrogen. Offline indicators were percent methane and

    hydrogen in the biogas. Biogas production was measured by

    an automated displacement gas metering system with

    a 100 mL reversible cycle and registration (Angelidaki et al.,

    1992). The water used in gas meter was acidified to pH 3 by

    HCl added NaCl to prevent CO2 dissolution. Gas production

    data was recorded automatically every 6 h. pH was measured

    online by a mini CHEM-pH Process Monitor (TPS Pty Ltd.,

    Australia). The meter was calibrated against pH 4.00 and pH

    6.88 buffers every second week. The pH was recorded auto-

    matically every 10 min. Individual VFA concentrations were

    measured by an online VFA monitoring system based on ex-

    situ VFA extraction (Boe et al., 2007). The reactor had a liquid

    circulation loop from which a 40 mL liquid sample was

    pumped into an extraction chamber, acidified, added with

    salt, and was heated in order to extract the VFA into gas phase

    before injecting into a gas chromatograph (GC) for analysis.

    The signal output from the GC was then sent to data pro-

    cessing system for integration. The VFA concentrations were

    analysed and recorded automatically every 6 h.

    during experiment.

    Method of addition


    e Added once, directly into the reactor

    e Mixed with feed and fed 4 times

    e Added once, directly into the reactor

    e Added once, directly into the reactor

    e Added once, directly into the reactor

    e Added once, directly into the reactor

    e Added once, directly into the reactor8 Mixed with feed and fed 4 times

  • Bjornsson et al. (2001a). The system applied a liquid-to-gas

    wat e r r e s e a r c h 4 4 ( 2 0 1 0 ) 5 9 7 3e5 9 8 0 5975membraneextractionforextractingdissolvedhydrogenfromthe

    liquid content. Thedissolvedhydrogendiffused throughaTeflon

    membrane immersed in the reactor. The diffused hydrogenwas

    then oxidized at the surface of a Palladium-Metal Oxide semi-

    conductor (Pd-MOS) sensor. The picoammeter converted the

    resultingoxidationcurrent toasignal.Thesignaloutput fromthe

    picoammeter was then recorded in the data processing system.

    The results from hydrogen sensors were presented here as

    relative numbers of signal outputs compared to the initial signal,

    since it was found unreliable to calibrate absolute concentration

    of dissolved hydrogen inmanure against water.

    Gas phase methane and carbon dioxide were measured

    offlinebyagaschromatograph(Mikrolab, Arhus)equippedwith

    thermal conductivity detector and a glass column 20m 3mmID packed with Poropack Q (10/80). The temperature of the

    injector, the detector and the oven was isothermal at 55 C.Heliumwas used as a carrier gas with the flow rate 40mL/min.

    Gas phase hydrogen was measured by a gas chromatograph

    (Mikrolab, Arhus) equippedwith thermal conductivity detector

    and a packed column 4.5 m 3 mm ID Molsieve 5A 10/80. Theinjector and detector temperature was 90 C. The temperatureprogramwas isothermal at 80 C.Nitrogenwasusedas a carriergas with the flow rate 20 mL/min.

    Online data processing was done by a programmable logic

    control (PLC) system (Versamax PLC, GE Fanuc Automation

    Europe S.A, Luxembourg), with a PC interface. All calculations,

    including peak area calculation of the GC were managed

    within the PLC. The interface and data logging on the PLCwere

    using GE Cimplicity HMI 6.1 (HMI, GE Fanuc Automation

    Europe S.A, Luxembourg).

    3. Results

    All the measured indicators showed response to the changes

    in hydraulic and organic load. During the start-up period (day

    0e20), very high VFA concentrations, up to 70 mM, were

    observed. Biogas production and VFA levels increased while

    pH changed by 0.5e1 unit. Acetate and butyrate were themost

    dominant VFA. After day 20, acetate and butyrate decreased

    relatively quickly while propionate was the most persistent.

    3.1. Response to lipid additionDuring day 122e128, the dissolved hydrogen was measured

    by an online hydrogen micro-sensor (Unisense A/S, Aarhus,

    Denmark). The sensor principle is based on hydrogen diffusion

    from the liquid through a sensor tip silicone membrane, to the

    platinum anode which is polarized against an internal refer-

    ence. The flow of electrons from the oxidizing anode to the

    internal referencereflects linearly thehydrogenpartialpressure

    around the sensor tip and is in the pico-amp range. A picoam-

    meter converted the resulting oxidation current to a signal. The

    signal output from the picoammeter was then recorded in the

    data processing system (Unisense A/S, Aarhus, Denmark).

    During day 157e200, the dissolved hydrogen was measured

    by the online hydrogen measuring system developed byTwo lipid additions were introduced by adding 85 g and 157 g

    of rapeseed oil directly into the reactor at day 77 and day 110,respectively (Fig. 1). No increase in biogas production and only

    a small increase of VFA were observed after the first addition.

    While after the second one a drop of both biogas production

    and methane percent, but no clear response in both pH and

    VFA were observed. After the second addition, most of the oil

    came out undigested with the effluent from the top of reactor

    and biogas production returned slowly to normal levels.

    3.2. Response to glucose addition

    Four glucose additions were introduced by adding 25, 50, 50

    and 100 g of glucose directly into the reactor at day 126, 137,

    161 and 168, respectively. The results from the first two

    additions are shown in Fig. 2, and the results from the last two

    additions are shown in Fig. 3.

    At approximately 1 day after the 25 g glucose was added,

    biogas production increased shortly (Fig. 2a), pH droppedwhile

    dissolved hydrogen increased (Fig. 2b), and VFA concentration

    increased slightly while methane percent did not show signifi-

    cant response (Fig. 2c and d). Hydrogen content in biogas

    increased slightly during the same period that dissolved

    hydrogen increased. However, the values were very low and

    fluctuated. At day 123, dissolved hydrogen showed some

    response fewminutesafter the reactorwasopened to repair the

    effluent tube.Additionof 50g glucoseat day 137 showedsimilar

    response to theaddition of 25 g glucose, however,with stronger

    response of VFA, where butyrate, iso-valerate and valerate

    increased slightly at both day 137 and 161. At day 161, the dis-

    solved hydrogen increased sharply, along with a pH drop,

    a slight increase in hydrogen content and a slight decrease in

    biogas methane content (Fig. 3b and d).

    After the addition of 100 g glucose, biogas production

    increased while methane content decreased (Fig. 3a and d).

    Acetate and butyrate increased significantly and followed by

    an increase of iso-butyrate, iso-valerate, valerate and propio-

    nate concentrations (Fig. 3c). pH values dropped and dissolved

    hydrogen increased sharply (Fig. 3b). Dissolved hydrogen

    dropped back very quickly, while pH slowly increased over

    severalhours.VFAtook longer time todecreaseback tonormal.

    Also, the gas phase hydrogen content increased slightly.

    3.3. Response to protein addition

    Proteinwasaddedatday 142byadding25g gelatinedirectly into

    the reactor (Fig. 2). Only biogas production and acetate concen-

    tration slightly increased while the rest of VFA and pH did not

    show significant response. There was no data of dissolved

    hydrogen and biogas composition available during this period.

    3.4. Response to continuous addition of extraorganic load

    The reactor was daily fed with extra organic load, mixed with

    the manure in the influent flask, during day 185e196. The

    results are shown in Fig. 3. From day 185, the feed (manure)

    was supplemented with 8 g bio-fiber and 4 g rapeseed oil per

    day. Acetate started to increase and pH began to drop while

    small response of dissolved hydrogen was noticed. From day188, the feedwas also supplementedwith 40 g glucose per day.

    At this point, the rest of VFA started to increase. A strong

  • wat e r r e s e a r c h 4 4 ( 2 0 1 0 ) 5 9 7 3e5 9 8 05976response of dissolved hydrogen was observed, as well as a pH

    decrease. Biogas production increased significantly while the

    methane content decreased slightly. As the process was

    continued to be fed with extra organic load, the dissolved

    hydrogen and acetate concentration were the first to decrease

    followed by butyrate and iso-butyrate. The rest of VFA started

    to decrease shortly after extra organic load was ceased except

    for propionate which continued increasing. The pH increased

    slightly after removal of extra organic load, but did not reach

    the previous level. Dissolved hydrogen decreased back to the

    normal level.

    4. Discussion

    4.1. Reactor response to extra organic load

    The reactor responded quickly to the addition of glucose

    because glucose is easily degradable. Dissolved hydrogen, VFA

    and biogas production levels were all good indicators of

    response to this stimulus. After the first lipid addition, no

    increase in biogas production and only small increase in VFA

    were observed, which could be explained by the slow degra-

    dation of lipid. A similar observation was previously reported

    by Bjornsson et al. (2001b), where the lipid addition gave low

    production of VFA and they suggested that this was due to

    hydrolysis being the rate-limiting step for lipid digestion. After

    the second addition with doubling the amount of lipid, the

    drop in biogas production with small increase of VFA

    Fig. 1 e Reactor resultssuggested that the process was probably inhibited by long-

    chain fatty acids (LCFA) from the oil. LCFA is known to be

    inhibitory to all groups of microorganisms (Angelidaki and

    Ahring, 1992; Rinzema et al., 1994). In this case, acidogens

    were also inhibited and concentration of VFA alone was not

    a suitable indicator for this disturbance. Moreover, the fact

    that the reactor slowly recovered after the undigested oil

    washed out with the effluent suggested that the reactor was

    recovered due to dilution of LCFA by the new feed, rather than

    adaptation of microorganisms, agreeing with observations by

    Pereira et al. (2003) and Rinzema et al. (1994). The addition of

    protein at day 142 did not disturb the process as seen that only

    acetate increased slightly and the biogas increased.

    4.2. Analysis of indicators

    The criteria used for comparing the process indicators in this

    paper were their responses during different disturbances, in

    relating to their baselines under normal operation. From the

    experiment, it was noticed that acetate exhibited faster

    dynamics and fluctuated more than propionate. Acetate

    increased very fast after the increase of hydraulic or organic

    load. However, it decreased again few days later while organic

    load was still high. This could be due to fast growth rates of

    aceticlastic methanogens compared to propionate degraders,

    or a larger population of aceticlasts. Propionate degraders are

    having growth rates around 0.49 day1, while aceticlasticmethanogens around 0.6 day1 (Angelidaki et al., 1999). Buty-rate responded also very quickly to an overload. However,

    during day 1e120.

  • wat e r r e s e a r c h 4 4 ( 2 0 1 0 ) 5 9 7 3e5 9 8 0 5977butyrate accumulation seemed to depend on the substrate

    composition and not all disturbances could increase butyrate.

    Butyrate accumulatedmostly during the period of adding high

    concentrationofglucose, forexample,by100gofglucoseatday

    168. However, only a slight increase in butyrate was observed

    during additions of 50 g glucose at day 137 and 161, and no

    butyrate accumulation was observed during the addition of

    25 g glucose at day 125. Valerate showed similar responses

    as butyrate, however, with much lower concentration level.

    Iso-butyrate and iso-valerate showed similar responses as

    butyrate and valerate, respectively. However, the iso-formwas

    more persistent in the reactor than the normal-form. During

    continuousoverload,propionate remained in thereactormuch

    longer than other VFA. Moreover, while acetate and butyrate

    started to decrease after the reactor had been exposed to

    organicoverload for sometime,propionatekeptaccumulating.

    This could be due to the fact that propionate degradation is the

    Fig. 2 e Reactor results dmost thermodynamic unfavourable among other VFA degra-

    dation,whichmade propionate degraders the slowest growing

    and most sensitive compared to acetate and butyrate

    degraders which could faster increase their degradation rate

    (Ozturk, 1991). In this case, propionate would be a better

    parameter to indicate process stress. This observation was

    similar to the study of Nielsen et al. (2007) where they sug-

    gested that propionate was the best indicator to describe the

    normalizing of the process.

    Dissolved hydrogen had strong response specially when

    adding glucose to the feed. This is consistent with hydrogen

    beingamajorproduct fromglucosedegradation (Batstoneetal.,

    2002). However, it responded also to other disturbances such as

    slight air exposure which had no impact on process perfor-

    mance. This ismore likely a semiconductor response to change

    in redox. In principle, the increase of both VFA and dissolved

    hydrogen in the reactor couldbe linkeddirectly to the increased

    uring day 120e147.

  • wat e r r e s e a r c h 4 4 ( 2 0 1 0 ) 5 9 7 3e5 9 8 05978activities of acidogens. Thedecrease of acetate could reflect the

    increased activity of aceticlastic methanogens. Similarly, the

    rapid decrease inhydrogen could be due to increased activity of

    hydrogenotrophic methanogens. Fig. 4 shows the dynamics of

    dissolved hydrogen in the reactor during continuous overload.

    The fast response of hydrogen was clearly observed as oscilla-

    tions following the feed interval of four times per day. It was

    noticed that the peak of dissolved hydrogen was reached

    around 30min after each feed, corresponding to small pH drop.

    Moreover, thedissolvedhydrogendecreasedagainwithin a few

    hours, while pHwas still increasing.

    The decrease of pH corresponded to the VFA accumulation

    during overload. However, the level of pH change was not

    significant enough to indicate the state of the process in this

    case due to the high buffer capacity in manure digester. The

    response of pH also corresponded to the dissolved hydrogen

    during sudden overload but not during gradual overload. This

    Fig. 3 e Reactor results dcould be explained by the pH response as being the result of

    overall ion interactions in the solution, while dissolved

    hydrogen measurements are not compensated by these

    interactions. Thus, during sudden overload of particular

    substrate such as glucose, where hydrogen production was

    high, the dissolved hydrogen response could be correlated to

    the pH. Moreover, it was noticed that after removal of

    continuous organic addition, the pH was not back to the

    previous level due to VFA accumulation. Dissolved hydrogen

    dropped rapidly to normal level.

    Biogas production responded very quickly to the change in

    organic load. However, it could not indicate the imbalanced

    state of the reactor. During continuous overload the biogas

    production was increasing along with the VFA concentration.

    The overload was then removed due to high VFA concentra-

    tion. If only the biogas production was used as indicator of the

    process status, the imbalance would not had been discovered

    uring day 155e200.

  • dissolved hydrogen but with very small change whichmade it


    wat e r r e s e a r c h 4 4 ( 2 0 1 0 ) 5 9 7 3e5 9 8 0 5979and one would had continued with the same loading which

    may have led to process failure.

    4.3. Suitability of indicators

    Several indicators showed interesting responses to the

    increase of organic load. The parameters that had the fastest

    response were dissolved hydrogen, pH and acetate, followed

    by butyrate (in case of glucose), propionate (in case of high

    overload), and biogas, respectively. The response time of

    biogas composition was quite slow probably due to large

    headspace volume of the reactor. However, none of these

    indicators showed response to all perturbations. Thus, the

    combination of different indicators might be necessary to

    cover all imbalance situations. As propionate was the most

    persistent in the reactor, it could be an important indicator to

    determine the degree of process imbalance. On the other

    hand, although biogas production could not indicate process

    imbalance, it is main product of interest reflecting overall

    process performance. Thus, the combination of acetate/

    propionate and biogas production is an effective group of

    indicators of both performance, and process balance. This is

    in contrast to traditional indicators, which aremainly pH, and

    either acetate only, or a combination of all organic acids.

    However, it should be remarked that the indicators suggested

    here were tested in a manure digester which had very high

    buffering capacity. For the processwith low buffering capacity

    such as sludge digester or high-rate anaerobic digester, the pH

    could still be a useful indicator.

    Other important factors to be considered when choosing

    Fig. 4 e Dynamics of dissolved hydrthe state indicator for the full-scale application are reliability

    and robustness of the online meters. Gas production and pH

    are easy to measure and most of the anaerobic wastewater

    treatment plants have gas and pH meters as standard

    instruments (Spanjers and van Lier, 2006). However, the liquid

    phase parameters such as individual VFA are still measured

    through manual analysis. The individual VFA online moni-

    toring used in this experiment (Boe et al., 2007) is under

    further development of the industrial prototype to improve

    the robustness for operation in full-scale plants.

    5. Conclusions

    Dissolved hydrogen was sensitive to organic overload, espe-

    cially when glucose was present in the feed. However, it alsodifficult to indicate the status of the process based on pH

    value. Acetate and propionate were very sensitive to organic

    overload. Propionate was the most persistent parameter

    which was effective indicator of stress status of the process

    while acetate decreased faster and was more fluctuated. The

    sensitivity of gas phase composition in this study was quite

    low, probably due to large headspace volume of the reactor,

    and slow gaseliquid dynamics. Biogas productionwas still the

    important parameter for indicating overall reactor perfor-

    mance although it could not indicate the stress status of the

    reactor. A monitoring of both individual VFA such as acetate,

    propionate and biogas productionwould allow combination of

    process state and performance.


    This work was supported by the Ph.D. scholarship from the

    Institute of Environment and Resources, Technical University

    of Denmark. The work of J.P. Steyer was supported by the

    European Communitys Human Potential Programme under

    contract MEIF-CT-2005-009500 (CONTROL-AD4H2) and both

    are greatly acknowledged.

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    State indicators for monitoring the anaerobic digestion processIntroductionMaterial and methodsResultsResponse to lipid additionResponse to glucose additionResponse to protein additionResponse to continuous addition of extra organic load

    DiscussionReactor response to extra organic loadAnalysis of indicatorsSuitability of indicators



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