short term effects of copper, sulfadiazine and difloxacin on the anaerobic digestion of pig manure...
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Waste Management 32 (2012) 131–136
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Waste Management
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Short term effects of copper, sulfadiazine and difloxacin on the anaerobicdigestion of pig manure at low organic loading rates
Jianbin Guo a, Anne Ostermann b, Jan Siemens b, Renjie Dong c, Joachim Clemens d,⇑a College of Water Conservancy and Civil Engineering, China Agricultural University, P.O. Box 184, Beijing 100083, PR Chinab Institute of Crop Science and Resource Conservation, University of Bonn, Nussallee 13, 53115 Bonn, Germanyc College of Engineering, China Agricultural University, P.O. Box 184, Beijing 100083, PR Chinad Institute of Crop Science and Resource Conservation, University of Bonn, Karlrobert-Kreiten-Straße 13, 53115 Bonn, Germany
a r t i c l e i n f o a b s t r a c t
Article history:Received 21 December 2010Accepted 29 July 2011Available online 24 August 2011
Keywords:Anaerobic digestionCopperAntibioticsPig manure
0956-053X/$ - see front matter � 2011 Elsevier Ltd. Adoi:10.1016/j.wasman.2011.07.031
⇑ Corresponding author. Tel.: +49 228 732150; fax:E-mail addresses: [email protected] (J. G
Ostermann), [email protected] (J. Siemens), [email protected] (J. Clemens).
Antibiotics of inorganic and organic origin in pig manure can inhibit the anaerobic process in biogasplants. The influence of three frequently used antibiotics, copper dosed as CuSO4, sulfadiazine (SDZ),and difloxacin (DIF), on the anaerobic digestion process of pig manure was studied in semi-continuousexperiments. Biogas production recovered after every Cu dosage up to a sum of 12.94 g Cu kg�1 organicdry matter (ODM), probably due to Cu precipitation following the formation of sulphide from sulphate.Complete inhibition was found at the very high Cu concentration of 19.40 g Cu kg�1 ODM. Inhibitoryeffect of SDZ and DIF was observed at concentrations as high as 2.70 g kg�1 ODM and 0.54 g kg�1
ODM, respectively. It seems very unlikely that the antibiotics tested would inhibit the anaerobic processin a full-scale biogas plant.
� 2011 Elsevier Ltd. All rights reserved.
1. Introduction
Most of the biogas plants in China are operated with animalmanure to reduce the biological oxygen demand and to producebiogas (Zhang et al., 2009). The biogas process may be influencedby trace elements or pharmaceuticals such as antibiotics as re-viewed by Chen et al. (2008).
Trace elements and antibiotics are widely used as feed additivesin pig farming, either to improve the growth performance or toprevent infection (Lallai et al., 2002; Lillie et al., 1977). After inges-tion by animals, some of these compounds are excreted with themanure and may inhibit the biogas process when the manure isused as substrate in a biogas plant.
Previous studies have shown that medication according to reg-ulations or excessive dosages of feed additives may lead to their al-most complete excretion via feces or urine (Bolan et al., 2003;Jjemba, 2002; Nicholson et al., 2003). The concentrations of copper(Cu) in pig feed samples in Beijing and Fuxin, China, were found torange from 6.9 to 395 mg kg�1 dry matter (DM), while the Cu con-centrations in the pig faeces varied from 50 to 2017 mg kg�1 DM(Li et al., 2007). However, in a study in the UK, the concentrationsof Cu were found to range from only 5 to 217 mg kg�1 DM in feedsamples and 160–780 mg kg�1 DM in faeces (Nicholson et al.,1999). In addition to being a feed additive, Cu in form of CuSO4
ll rights reserved.
+49 228 732489.uo), [email protected] ([email protected] (R. Dong),
solution is occasionally used as a footbath or disinfectant to pre-vent the spread of infectious diseases on pig farms.
With regard to the negative effects of Cu on the anaerobic diges-tion process, results reported in the literature vary considerablybecause of the complex mechanisms occurring during anaerobicdigestion, e.g. precipitation, adsorption and acclimation. In batchstudies, severe Cu inhibition concentration on anaerobic digestionof sewage sludge has been found in the range of 2–90 mg Cu L�1
dosed in the form of CuCl2 (Ahring and Westermann, 1985; Hickeyet al., 1989; Jin et al., 1998; Karri et al., 2006; Lin, 1992) and 200–800 mg Cu L�1 dosed in form of CuSO4 (Hobson and Shaw, 1976;Wong and Cheung, 1995). Ahring and Westermann (1983) haveperformed experiments on sewage sludge with semi-continuoussystems. They reported complete inhibition of methane productionat a Cu (dosed as CuCl2) concentration of 300 mg L�1 under ther-mophilic conditions. Zayed and Winter (2000) performed experi-ments on whey solution in an anaerobic fixed-bed reactor andbiogas process was inhibited completely at 18.9 mg Cu L�1 (dosedas CuCl2).
Unfortunately, these studies did not report the organic dry mat-ter concentration, rendering it difficult to compare the results be-cause the solids concentration in an anaerobic digester buffersmetal toxicity to microorganisms (Hickey et al., 1989). The essen-tial mechanism is that the negatively charged organic matter maybind cations and reduce their toxic potential (Jia et al., 1996).
In comparison to German biogas plants with 8–12% DM (Wei-land, 2000), the DM concentration in Chinese biogas plants is lowerand this may increase the negative effect of Cu.
1
22 3
4
5
6
Fig. 1. Schematic diagram of the completely stirred tank reactor. (1) Stirrer; (2)Water jacket to keep the digestion temperature at 38 �C; (3) Digestion tank; (4)Inlet for feeding; (5) Biogas outlet; (6) Outlet for effluent.
132 J. Guo et al. / Waste Management 32 (2012) 131–136
In addition to Cu, organic antibiotics may inhibit biogas forma-tion (Loftin et al., 2005). For the six most frequently used antibiot-ics (chlortetracycline, tylosin, erythromycin, chloramphenicol,bacitracin and virginiamycin), a study by Poels et al. (1984) foundno inhibitory effect when they were used at concentrations com-mon in practice. In another study in sequencing batch reactors,only penicillin and tetracycline inhibited the anaerobic digestionprocess, by 35% and 25% respectively, when they were applied atthe highest permissible dose in the feed (Massé et al., 2000). Fedlerand Day (1985) reported a reduction in the methane production of20% because of chlortetracycline (CTC) inhibition when this antibi-otic was fed to pigs. However, no inhibition was found when CTCwas fed directly into the digester.
Sulphonamides, a group of the most prescribed antibiotics, arebroadly used veterinary pharmaceuticals in animal husbandry(Sarmah et al., 2006). Mohring et al. (2009) studied the degradationand elimination of various sulphonamides during anaerobic diges-tion through 34 day batch experiments. Sulfadiazine (SDZ) wasnearly degraded after 2 weeks and its metabolite was confirmedand methane production was not tested.
Dozens of fluoroquinolones used in veterinary medicine world-wide have been synthesized and reported in recent decades (Smith,1986; Sárközy, 2001). This class of antibiotics has been bannedfrom use in pigs by US Food and Drug Administration (US FDA,2002, cited by Campagnolo et al., 2002). In China they are still inuse and no information is available on their effect on anaerobicdigestion.
The microbial processes in batch digesters are different to thosein full scale biogas plants which are semi-continuous systems, fed atleast once daily. In batch digesters, the microbial processes of acido-genesis, acetogenesis and methanogenesis occur simultaneouslyonce methanogenic conditions are established. Hydrolysing organ-isms will produce organic acids that are simultaneously consumedby acetogens and methanogens. Rather, a batch process will gothrough phases because methanogens take longer to establish apopulation that balances the activity of the faster growing acido-gens, whereas in a biogas plant all processes take place simulta-neously making extrapolations from batch experiments to fullscale biogas plants difficult. However, only few studies are per-formed in semi-continuous system (Hilpert et al., 1984; Poelset al., 1984; Sankvist et al., 1984; Varel and Hashimoto, 1981;Winterhalder, 1985).
According to our knowledge on anaerobic digestion of animalmanure, no study exists where the effect of Cu (dosed as CuSO4),SDZ and DIF were studied in semi-continuous digesters that en-abled the bacteria to acclimate to the increasing antibiotic concen-tration and represent a realistic biogas system. Such studies are ofimportance to simulate realistically the influence of pharmaceuti-cals on the biogas process.
The objectives of the present work were to evaluate the effect ofCuSO4, both growth promoter and disinfectant, and the two antibi-otics SDZ and DIF on biogas formation at low organic loading ratethat is typical for Chinese biogas plants.
2. Materials and methods
Cupric sulphate (CuSO4), SDZ and DIF were used as potentialinhibitors. Pig manure was anaerobically digested in semi-contin-uous digesters and their biogas production was compared with acontrol treatment without addition of an additive (2 replicatesper treatment).
2.1. Additives, feedstock and inocula
The water solubility of SDZ and DIF is 13–77 mg L�1 (Wehrhan,2006) and 27 mg L�1 (pH 7, 25 �C) (calculated using Advanced
Chemistry Development (ACD/Labs) Software V8.14 for Solaris(�1994–2008 ACD/Labs)). Thus both antibiotics have low watersolubility. We decided not to add the antibiotics as solid powderbecause the rate and completeness of the dissolution of this pow-der can hardly be controlled. For the present experiment, the anti-biotics were therefore dissolved in methanol and stored at �20 �Cin the dark before they were added to the digesters. The CuSO4 wasdosed as solid powder.
Pig manure was collected from the Frankenforst UniversityExperimental Farm, Bonn, Germany (DM was 5.5%, the organicdry matter (ODM) 72.0% of DM, NH4–N 1.3 g L�1 and electric con-ductivity (EC) 7.7 mS cm�1). The liquid manure had higher concen-trations of ODM than animal manure in China (DM: 2.7%, ODM:68.7% of DM, NH4–N: 1.2 g L�1, EC: 12.3 mS cm�1). To simulate Chi-nese manure conditions, the manure from the experimental farmwas diluted accordingly. As German biogas plants are not run onpig slurry alone, sewage sludge was used as an inoculum. To startthe biogas process, the digesters were inoculated with sewagesludge (DM: 1.2%, ODM: 62.8% of DM, NH4–N: 0.5 g L�1, Cu:<5 mg Cu kg�1 DM) from the wastewater treatment plant in Bonn,Germany.
2.2. Digester
Eight completely stirred tank reactors (Fig. 1) with a volume of10 L (diameter 19 cm, height 37.5 cm) and an effective slurry vol-ume of 8 L were used. Each digester was sealed by a Plexiglascap with a stirrer in the middle of the cap and a biogas outlet con-nected to a gas bag. Stirring was conducted automatically for 30 severy 5 min at a speed of 70 rpm throughout the entire experimen-tal period. Two ports were fitted at the top and bottom of the di-gester walls for feeding and withdrawing liquid samples,respectively.
2.3. Experimental design
The digesters were started with 6 L slurry and 2 L sewagesludge. For the start-up period, all digesters were fed only withpig slurry daily. The slurry was prepared once for the whole periodand stored at 4 �C. The digesters were operated at a hydraulic
Table 1Dosage (mg L�1) of the antibiotics and methanol used in Phases 1–5 of the experiment.
Phase Additiveconcentration(mg Cu L�1)
Additive dosage (mg) Methanol dosage (mL) Additiveconcentration(mg L�1)
Additive dosage (mL) Additional methanoldosage (mL)
Dosage at thebeginning of eachphase
Daily Dosage at thebeginning of eachphase
Daily Dosage at thebeginning of eachphase
Daily Dosage at thebeginning of eachphase
Daily
Control Treatment SDZ1 – - - 8 0.32 1 8 0.32 - –2 – – – 32 1.6 5 32 1.6 – –3 – – – 40 3.2 10 40 3.2 – –4 – – – 320 16.0 50 320 16.0 – –5 – – – 1000 56.0 175 1000 56.0 – –
Treatment CuSO4 Treatment DIF1 40 800 32 8 0.3 0.1 8 0.32 – –2 120 1600 96 32 1.6 0.5 32 1.6 – –3 240 2400 192 40 3.2 1 40 3.2 – –4 360 2400 288 320 16.0 10 240 11 80 55 720 7200 576 1000 56.0 28 480 30 520 26
Concentration of SDZ stock solution was 1 g L�1.Concentration of DIF stock solution was 0.1 g L�1 for phase 1–3 and 0.3 g L�1 for Phase 4–5.
Table 2Calculated biogas production derived from the methanol added to the control digester at each phase.
Phase Daily methanoladdition
Total amount of methanoladded in each phase (mL)
Duration for eachphase (day)
Theoretical biogas yield ineach phase (L)
Analysedbiogas yield (L)
Proportion of methanolconverted to biogas (%)c
g/(gODM.d) mL Methanolbiogas yielda
Manurebiogas yieldb
1 0.04 0.32 13.76 18 7.61 29.52 19.33 �133.92 0.21 1.6 44.80 8 24.79 13.12 27.49 58.03 0.43 3.2 65.60 8 36.30 13.12 36.53 64.54 2.14 16.0 432.00 7 239.05 11.48 101.49 37.75 7.47 56.0 1672.00 12 925.19 19.68 2.56 �1.9
a Theoretical methanol biogas yield can be calculated by this equation: Total amount (mL) of methanol added in each phase � 0.79/32 � 22.414. Where 0.79 is density ofmethanol (g ml�1); 32 is molar mass of methanol (g mol�1); 22.414 is molar volume of gas (L mol�1) at standard condition (T = 273 K and 1013 mbar).
b Manure biogas yield = 1.64L d�1 � Duration for each phase (before day 14 of the experiment, the average biogas yield of control fermenters is 1.64 L d�1).c Proportion of biogas yield from methanol (%) = (Analysed biogas yield �manure biogas yield)/theoretical methanol biogas yield � 100.
J. Guo et al. / Waste Management 32 (2012) 131–136 133
retention time (HRT) of 25 days (semi-continuous feedings;320 mL of influent per day) and an organic loading rate of 0.8 gODM L�1 d�1 at 38 �C. After 14 days, the biogas process had stabi-lised and dosing of the additives started. The additives were ap-plied in increasing dosages together with pig manure. Asmethanol was applied to the substrate with SDZ and DIF, puremethanol in equivalent amounts was also added to the controland the Cu treatment. All treatments were carried out in duplicate.For the whole study, the variability of the duplicates in biogas pro-duction was less than 5%.
Digesters received the next higher dosage as soon as biogas pro-duction had stabilized or had no severe inhibition (Phase 4 of treat-ment SDZ and DIF) for 5 days. At the beginning of a new phase witha higher concentration, the additive was applied in a high dosage toincrease the concentration of the whole digester volume to thenew target concentration. This can be considered a form of ‘shockloading’. The shock volumes and loads instantaneously elevate theconcentration of methanol and the inhibitors to the next intendedconcentration level that is subsequently maintained by a propor-tionate daily dose. The detailed dosage operation is shown inTable 1.
2.4. Monitoring
Biogas production was monitored by drum type gas meter (Rit-ter Apparatebau, Germany). The quality of biogas was analysed
with an infra-red sensor (GA94, Analytics System and ComponentGmbH). The pH and total inorganic carbon content were deter-mined during the experiments (pH340/ION, WTW).
3. Results and discussion
Biogas production stabilised after 14 days at 1.64 L d�1 at a pHof around 7.1 in the substrate. The biogas production at that timecorresponded to 0.28 L biogas g�1 ODM fed.
3.1. Effect of methanol on anaerobic digestion
Before methanol addition the average biogas yield was1.64 L d�1 but after every addition of methanol, there was a dis-tinct peak in biogas production (Fig. 3 control). To determine thebiogas yield of methanol, it was assumed that the yield of1.64 L d�1 remained constant for the whole experiment. On thisbasis, the biogas yield from methanol was computed theoretically.At the lowest methanol addition there was a theoretical inhibitionof biogas production of 47.9% ((theoretical biogas yield-analysedbiogas yield)/theoretical biogas yield) (Table 2). This indicates thatthe bacteria needed some time to acclimate to the new substratemethanol. At 0.21 and 0.43 g methanol g�1 ODM d�1, the potentialinhibition from methanol alleviated and the biogas yield of meth-anol increased from 58% of the theoretical gas yield in phase 2 to64.5% in phase 3. During phase 4 (2.14 g methanol g�1 ODM d�1),
Met
hane
pro
duct
ion
L d
-1
0
5
10
15
20
25
30
Time (days)0 5 10 15 20 25 30 35 40 45 50 55 60 65 70
Bio
gas
prod
uctio
n L
d-1
0
5
10
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30
Phase 1 2 3 4 5
Fig. 3. Biogas and methane production (L d�1) in the CuSO4 treatment: (d) Control;(s) CuSO4.
Time (days)0 5 10 15 20 25 30 35 40 45 50 55 60 65 70
pH V
alue
6.8
7.0
7.2
7.4
7.6
7.8
8.0
8.2
8.4
Phase 1 2 3 4 5
Fig. 2. pH value in the digester for each treatment: (d) Control; (s) CuSO4; (.)SDZ; (4) DIF.
Met
hane
pro
duct
ion
L d
-1
0
5
10
15
20
25
30
35
Time (days)0 5 10 15 20 25 30 35 40 45 50 55 60 65 70
Bio
gas
prod
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n L
d-1
0
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35
Phase 1 2 3 4 5
Fig. 4. Biogas and methane production (L d�1) in the SDZ treatment: (d) Control;(s) SDZ.
134 J. Guo et al. / Waste Management 32 (2012) 131–136
the theoretical gas yield of methanol decreased to 37.7%. Biogasproduction stopped completely in phase 5 with a methanol dosageof 7.47 g methanol g�1 ODM d�1.
Corresponding to the decreased biogas yield in phase 4, pH de-creased from 7.2 to 7.0 (Fig. 2). This result can be confirmed byFlorencio et al. (1995) who found the production of organic acids
was likely to be strongly stimulated at higher methanol concentra-tions. At low methanol concentrations, direct methanogenesis isthe predominant mineralisation route for methanol under meso-philic conditions (Weijma and Stams, 2001).This may explainwhy there was a distinct peak in biogas production in Phases 1–4.
3.2. Effect of CuSO4 on anaerobic digestion
At a Cu concentration of 6.46 g Cu kg�1 ODM (phase 2), biogasformation on the first and second days was reduced by 50.5% and60.3%, respectively (Fig. 3). On the third day, biogas productionwas higher than in the control and thereafter it stabilised at1.61 L d�1, i.e. similar to the control. In phase 3 (12.94 g Cu kg�1
ODM), a similar effect was observed. In phase 4, with a Cu concen-tration of 19.40 g kg�1 ODM, corresponding to an initial Cu concen-tration of 360 mg L�1, biogas and methane production broke downwithin three days and did not recover again.
In contrast with the batch digester, our stepwise feeding in thesemi-continuous digester enabled the bacteria to acclimate to theincreasing Cu concentration. Ahring and Westermann (1983) haveever also ascribed the biogas production recovery from Cu to thebacteria acclimation. Moreover, Cu may have been precipitatedwith the correspondingly applied SO2�
4 -S applied, but this SO2�4
would have had to be reduced to S2� first. CuS would then haveprecipitated, as its solubility product is very low (Ksp = 6.3 � 10�36)(Dean, 1999).
Table 3Average biogas yield (L) of each phase for all used additives.
Treatment Phase 1 Phase 2 Phase 3 Phase 4 Phase 5
Control 19.33 27.49 36.53 101.49 2.56CuSO4 17.31 26.59 35.66 9.20 1.48SDZ 15.74 26.22 36.01 91.43 2.44DIF 18.16 27.44 36.48 92.32 2.60
Met
ahne
pro
duct
ion
L d
-1
0
5
10
15
20
25
30
Time (days)0 5 10 15 20 25 30 35 40 45 50 55 60 65 70
Bio
gas
prod
uctio
n L
d-1
0
5
10
15
20
25
30
35
Phase 1 2 3 4 5
Fig. 5. Biogas and methane production (L d�1) in the DIF treatment: (d) Control;(s) DIF.
J. Guo et al. / Waste Management 32 (2012) 131–136 135
In the study on anaerobic digestion of sewage sludge, Ahringand Westermann (1983) found that the biogas production de-creased slightly when Cu (dosed as CuCl2) concentration was upto 100 mg L�1, and the gas production increased to its former levelagain after 4–6 days because of the bacteria acclimation. However,in our study, the biogas production recovered from Cu (dosed asCuSO4) inhibition to its former level within only 2 days in phase2 and 3. Lawrence and McCarty (1965) reported that Cu was re-moved from municipal sludge via CuS after CuSO4 addition mostlikely because of the slow reduction of sulphate to sulphide. Thisagrees with findings by Karri et al. (2006), who studied Cu2+ toxic-ity for sulphate reducing bacteria (SRB) with acetate as electrondonor and reported a maximum rate of sulfide production occurredbetween 7.3 and 32 h. The sulphide formation from sulphate maycontribute to the shorter gas recovery time in present study.
Inhibitory concentrations should relate to free Cu content, butthis is difficult to determine in animal slurry. In biogas plants, con-siderable amount of metals are precipitated in form of sulphides.
When CuSO4 is dissolved, SO2�4 is reduced to sulphide and may
subsequently precipitate Cu2+. Theoretically, all Cu applied in theform of CuSO4 can be inactivated by the SO2�
4 it contains, as indi-cated earlier. However, the SO2�
4 reduction may take up to two daysand thus the Cu2+ is potentially active and toxic within the firstdays, whereas no toxic effect of Cu2+ will be observed later. Whenother Cu-salts are used as additives, the toxic effect of Cu may per-sist for a longer time, especially if the HS� and S2� concentrationsare low.
3.3. Effect of antibiotics on anaerobic digestion
At the start of phase 3 for SDZ, biogas production was lower onthe first day compared with the control (Fig. 4). However, on thesecond day in phase 3, biogas production in the SDZ treatmentwas higher than in the control. No obvious difference betweenSDZ treatment and control was observed on the overall biogas pro-duction in this phase, 36.01 and 36.53 L, respectively (Table 3). Asimilar trend was observed for DIF in phase 3 (Fig. 5). In phase 4,the biogas process was inhibited by 9.9% and 9.0% caused by SDZand DIF (Table 3), respectively, when their concentrations reached2.70 g SDZ kg�1 ODM and 0.54 g DIF kg�1 ODM. This SDZ concen-tration is much higher than that in normal pig manure of 3.5–11.3 mg SDZ kg�1DM measured by Hamscher et al. (2005). Accord-ing to the study of Sukul et al. (2009), if all the DIF (normal use) fedto pigs are excreted, the highest DIF concentration in manurewould be 0.05–0.09 g kg�1DM. Therefore, it’s very unlikely thatthe antibiotics tested would inhibit the anaerobic process in afull-scale biogas plant.
4. Conclusions
The antibiotics, SDZ and DIF, inhibit the biogas process by 9.9%and 9.0%, respectively, at very high concentrations of 2.70 g SDZkg�1 ODM and 0.54 g DIF kg�1 ODM.
Biogas production can recover from one or two days of Cu inhi-bition when CuSO4 is applied, even at very high concentrations (upto 12.94 g Cu kg�1 ODM). This is most likely because Cu is precip-itated in form of Cu–sulphide. When other Cu-salts are applied atlow HS� and S2� concentrations, the biogas process may be inhib-ited at lower Cu concentrations.
The biogas process is rather resilient to addition of methanol atrates of up to 2.14 g g�1 ODM d�1.
Acknowledgements
This study was supported by Sino-German project (BMBF:0330847D, MOST: 2009DFA32710). The authors thank CarstenHafermann for his patient technical help. Many thanks to UrsulaKotowski for information on the testing of our samples.
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