effect of antibiotics on psychrophilic anaerobic digestion of swine manure slurry in sequencing...

E�ect of antibiotics on psychrophilic anaerobic digestion of swinemanure slurry in sequencing batch reactors q

D.I. Mass�e a,*, D. Lu a, L. Masse a, R.L. Droste b

a Dairy and Swine Research and Development Centre, Agriculture and Agri-Food Canada, P.O. Box 90, Route 108 East, Lennoxville, Quebec,

Canada J1M 1Z3b Department of Civil Engineering, University of Ottawa, Ottawa, Ontario, Canada K1N 6N5

Received 28 July 1999; received in revised form 28 February 2000; accepted 19 March 2000

Abstract

The e�ect of antibiotics on the psychrophilic anaerobic digestion (PAD) of swine manure slurry in sequencing batch reactors

(SBRs) was investigated. Six antibiotics, tylosin, lyncomycin, tetracycline, sulphamethazine, penicillin and carbadox, were indi-

vidually added to the pig diet at their maximum prescribed level. Manure slurries collected from pigs receiving control and

medicated diets were individually fed to pairs of SBRs at organic loading rates (OLRs) ranging from 2.2 to 3.5 g total chemical

oxygen demand (TCOD) per litre of bioreactor initial sludge volume per day. Three mixtures of slurries from pigs fed on in-

dividual antibiotics were also tested at OLRs varying between 2.5 and 3.2 g TCOD/l/d. The presence of penicillin and tetracycline

in manure slurries reduced methane production by 35% and 25%, respectively. However, the slurries from pigs receiving the other

antibiotics and the slurry mixtures did not signi®cantly a�ect �P > 0:05� methane production. In addition, the presence of in-

dividual and combined antibiotics did not have noticeable adverse e�ects on process stability and treatment e�ciency. Total and

soluble COD (TCOD and SCOD) reduction, total and volatile solids (TS and VS) removal, pH and volatile fatty acid (VFA)

concentrations in experimental units were not statistically di�erent �P > 0:05� than in the controls. In all bioreactors, the TCOD,

SCOD, TS and VS removal exceeded 62%, 76%, 65% and 75%, respectively. Crown Copyright Ó 2000 Published by Elsevier

Science Ltd. All rights reserved.

Keywords: Antibiotics; Psychrophilic; Anaerobic digestion; Biogas; Pig diets; Feed additives; Growth promoters

1. Introduction

Variation in environmental conditions may a�ect thestability and performance of an anaerobic bioreactor.Factors such as the type and concentration of antibi-otics fed to the animals, animal diet, and digester op-erating conditions, including temperature, hydraulicretention time (HRT) and hydraulic ¯ow regimes, mayhave an impact on the anaerobic micro¯ora. Antibac-terial compounds such as antibiotics are used as feedadditives in swine diets to enhance production orcontrol diseases. The fraction of antibiotics excretedwith the pig slurry may produce a toxic substance thatcould cause inhibition or failure of the anaerobic di-gestion process.

Waste from cattle fed lasalocid and salinomycin hadminimal e�ects on methane production in anaerobicdigesters operated under thermophilic conditions (Vareland Hashimoto, 1982). However, manure slurry fromcattle fed monensin totally inhibited methane produc-tion in mesophilic and thermophilic bioreactors (Vareland Hashimoto, 1981). It required nearly 40 days for themicroorganisms to recover and produce methane again.The authors did not determine if the recovery in meth-ane production was due to microorganism acclimationor to chemical inactivation of monensin. Fischer et al.(1981) reported that when lyncomycin was added toswine diet for the control of dysentery at a rate of 40 mg/kg of feed, a pilot scale digester failed twice and couldnot be revived.

Poels et al. (1984) investigated the e�ect of six anti-biotics (chlortetracycline (CTC), tylosin, erythromycin,chloramphenicol, bacitracin and virginiamycin) on theanaerobic digestion of swine manure slurry in 1.5 l fer-menters operated at 30±33°C. The antibiotics were

Bioresource Technology 75 (2000) 205±211

q Contribution no. 648.* Corresponding author. Fax: +1-819-564-5507.

E-mail address: [email protected] (D.I. MasseÂ).

0960-8524/00/$ - see front matter Crown Copyright Ó 2000 Published by Elsevier Science Ltd. All rights reserved.

PII: S 0 9 6 0 - 8 5 2 4 ( 0 0 ) 0 0 0 4 6 - 8

directly added to the pig manure slurry in concentra-tions equivalent to the veterinary prescribed dose indrinking water (Poels et al., 1984). It was assumed thatall the antibiotics passed through the animal and wasexcreted with the manure. The experiments were alsocarried out with higher concentrations of antibiotics.The digesters received an organic loading rate (OLR) of2±4 g chemical oxygen demand (COD)/l/d at an HRT of20 days. Results showed that at concentrations normallyused in practice, the antibiotics had no inhibitory e�ecton the methane fermentation process. However, athigher concentrations, the antibiotics bacitracin andvirginiamycin severely reduced biogas production and,consequently, caused an increase in volatile fatty acid(VFA) and COD concentrations in the fermenters.Sankvist et al. (1984) reported that in a semi-continuous¯ow thermophilic fermenter with an HRT of 5±7 days,methane production was reduced by 50% after six con-secutive days of adding oxytetracycline at a rate of 100mg/l of manure. Fedler and Day (1985) showed thatmanure from pigs fed 100 mg CTC/kg of feed reducedmethane production by about 20%. However, whenCTC was added directly into the fermenter, there was noreduction in methane production. Sankvist et al. (1984)suggested that the antibiotic itself may not inhibit bac-terial activity but some metabolites produced in thegastrointestinal tract of the swine may do so. Therefore,to evaluate the e�ect of an antibiotic on the anaerobicdigestion process, the antibiotic should be fed to theanimal rather than be added directly to the manureslurry. This method would also simulate the actualpractices on commercial farm operations.

Tylosin, lyncomycin, tetracycline, sulphamethazine,penicillin and carbadox are the most commonly usedantibiotics in pig diets in Canada. There is a lack ofinformation on the e�ect of these antibiotics on theanaerobic digestion process at low temperature. Al-though some of these antibiotics have been previouslystudied by other researchers, tested concentrations werelower than those fed to pigs on Canadian commercialfarm operations. In addition, none of the studies werecarried out at temperatures of 20°C and lower. Psychr-ophilic anaerobic digestion (PAD) in sequencing batchreactors (SBRs) as developed at Agriculture and Agri-Food Canada is a promising technology for the treat-ment of swine manure slurry (Mass�e et al., 1996, 1997).The system can e�ectively reduce manure odour andorganic pollutant concentrations. It can remove between85% and 95% of manure soluble COD (SCOD). How-ever, before this technology can be recommended for thetreatment of swine manure slurry on commercial farmoperations, the e�ect of adding antibiotics to animaldiets must be investigated. Therefore, the main objectiveof this study was to examine the e�ect of dietary anti-biotics on the stability and treatment e�ciency of PADin SBRs.

2. Methods

2.1. Diet preparation

One diet without antibiotic (control) and six medi-cated diets each containing one of the antibiotics listedin Table 1 were prepared. The control and medicateddiets were made of 50% ground corn, 25% ground bar-ley, 17% soybean meal, 1.3% limestone, 1.8% dicalciumphosphate, 1.25% lignosol, 0.4% iodized salt, 0.5% swinepremix, 0.5% swine vitamin P, 0.1% hydrochloride and2.0% stabilized fat. The antibiotic doses (Table 1) werebased on the recommendation of the Compendium ofMedicating Ingredients Brochures (Agriculture Canada,1990).

2.2. Slurry collection

Sixteen growing±®nishing barrows or gilts weighingabout 30 kg were used to supply manure. Pairs of pigsplaced in individual pens were fed one of the diets for aperiod of two weeks. Feces and urine collected every dayduring the second week were mixed thoroughly at theend of the week, placed in 3.5 l polypropylene contain-ers, and stored in a freezer at )15°C to prevent biolog-ical activities. Samples were taken during the mixingoperation and analysed for chemical and physicalproperties. The day before feeding, the containers wereremoved from the freezer, thawed at room temperature,and diluted with tap water at a ratio of 2:1 (slurry:wa-ter). Dilution was used to adjust the characteristics ofthe manure slurry to a level that is more representativeof manure characteristics in commercial swineoperations.

2.3. Laboratory set-up

The antibiotic experiments were conducted in eightSBRs that had been used for the treatment of swinemanure for more than a year (Mass�e et al., 1997). TheSBRs were located in a controlled temperature roommaintained at 20°C. Each SBR had a volume of 40 l andan initial sludge volume of 9 l. Biogas production wasmonitored with wet tip gas meters. To avoid sludgecompaction in the digesters, the mixed-liquor was mixed

Table 1

Antibiotics used in pig diets (administered in feed)

Antibiotic Concentration in diet

(mg/kg, d.m. basis)

Carbadox 55

Tylosin 110

Penicillin 16

Tetracycline 550

Sulphamethazine 110

Lyncomycin 220

206 D.I. Mass�e et al. / Bioresource Technology 75 (2000) 205±211

every morning for ®ve minutes by recirculating thebiogas. Duplicate SBRs were used for the control andeach antibiotic experiment. All reactors were operatedunder the same conditions.

2.4. Experimental design

The experiments were divided into three runs (Table2). In the ®rst two runs, slurries containing individualantibiotics and the control slurry were simultaneouslyfed to four pairs of digesters. In the third run, manureslurries used in test runs 1 and 2 were mixed and thee�ects of the mixtures were evaluated. In addition,the OLRs (g COD/l/d) used during the feeding period ofthe experimental runs are presented in Table 2. AllOLRs are based on the initial volume of sludge in thereactor. The SBR operating cycle included a two-weekfeeding period followed by a two-week reaction period.The bioreactors were fed once a week during the two-week feeding period. The settling and idling periodswere included in the react period. The settling periodprovides quiescent conditions, which result in the for-mation of a thick sludge blanket at the bottom of thereactor and of a supernatant layer above it. During theidling period the treated manure is removed. The ®rsttwo runs were repeated for two cycles. In the third run,the reactors were only operated for one cycle.

2.5. Analytical procedures

A full cycle lasted four weeks. During each cycle, a100 ml sample of mixed-liquor was collected once aweek from each SBR. In order to obtain uniform sam-ples, the SBRs were mixed for 10 min before samplecollection. Mixing was not provided at the end of thetreatment cycle when 100 ml samples were taken fromboth the supernatant and the settled sludge layers.Samples were analysed weekly for pH and SCOD. Total

COD (TCOD), alkalinity (Alk), total solids (TS), vola-tile solids (VS), total suspended solids (TSS), volatilesuspended solids (VSS), ammonia and total Kjeldahlnitrogen (TKN) were determined at the beginning andend of each cycle. Gas composition was analysedweekly. VFAs were analysed at the beginning and themiddle of each week. The analytical methods were car-ried out according to APHA (1992).

2.6. Statistical model

Data from each run were analysed according to a oneway factorial design with repeated measures on the cy-cles. DunnettÕs multiple comparison procedure was usedto compare each treatment to the control.

yijk � l� si � dij � ck � �sc�ik � eijk;

where si is the e�ect of treatment i, i � 1; 2; 3; 4; dij therandom e�ect associated with the jth repetition intreatment i, j � 1; 2; ck the e�ect of cycle k, k � 1; 2;�sc�ik the interaction cycle � treatment; and eijk is therandom error associated with the jth repetition intreatment i at cycle k.

3. Results and discussion

3.1. Characteristics of swine manure slurries

The composition of the swine manure used in testruns 1 and 2 is given in Table 3. The manure com-position for test run 3 is provided in Table 4. Theswine manure slurries had a high pollutant content.Solids content varied between 9% and 14.5% andTCOD ranged from 129 000 to 205 000 mg/l. TheVFAs ranged from 8000 to 14 000 mg/l. The concen-trations of ammonia and total nitrogen were also high;they varied between 4600±5200 and 5900±9200 mg/l,

Table 2

Experimental designa

Test run # Digesters Antibiotics tested Number of cycles OLR (g COD/l/d)

1 5±6 Carbadox 2 2.4

7±8 Control 1 2 2.3

9±10 Tylosin 2 2.2

11±12 Penicillin 2 3.0

2 5±6 Tetracycline 2 3.5

7±8 Control 1 2 2.3

9±10 Sulphamethazine 2 3.3

11±12 Lyncomycin 2 3.3

3 5±6 Mixture 1 1 2.6

7±8 Control 2 1 2.5

9±10 Mixture 2 1 3.2

11±12 Mixture 3 1 2.9

a Mixture 1: Tylosin + Carbadox + Sulphamethazine; mixture 2: Tetracycline + Penicillin + Lyncomycin; mixture 3: all six antibiotics; controls 1 and 2

were collected from di�erent pairs of pigs.

D.I. Mass�e et al. / Bioresource Technology 75 (2000) 205±211 207

respectively. Variations in manure slurry characteristicsmay be due to di�erences in pig metabolism (seevariations between controls in Tables 3 and 4) and tothe presence of antibiotics. It was not possible toquantify the contributions of antibiotics from indi-vidual animals.

3.2. Biogas production

Speci®c methane production values (1 CH4/g TCODand 1 CH4/g VS fed to the bioreactors) for the biore-actors fed with the control manure and with manurefrom pigs receiving one of the antibiotics are presentedin Tables 5 and 6. The speci®c methane production wasnot signi®cantly di�erent �P < 0:05� in bioreactors fedwith swine manure slurry containing tylosin, lyncomy-cin, sulphamethazine, or carbadox than in the controls.Bioreactors fed with manure containing penicillin ortetracycline experienced a signi®cant �P < 0:05� de-crease of 35% and 25%, respectively, in methane pro-duction with respect to the control. For all antibioticsbut one, methane production was higher in Cycle 2 thanin Cycle 1. This increase is probably due to microor-

ganism acclimation to the high COD and solids contentof the swine manure slurries.

The speci®c methane production from bioreactors feda mixture of slurries containing individual antibioticswas not signi®cantly di�erent from the control (Table 7).The slurry mixtures containing penicillin and tetracy-cline had less e�ect on biogas production than the slurrycontaining only penicillin or tetracycline. One possibleexplanation is that the concentrations of penicillin andtetracycline were reduced by dilution when they weremixed with swine manure slurries containing other an-tibiotics.

In all reactors, the biogas was of good quality: itsmethane content ranged from 73% to 76%. The biore-actors fed with manure slurries containing antibioticshad about the same concentration of methane in theirbiogas as the bioreactors fed with control manure slurry.

3.3. Process stability

The patterns of acetic acid, propionic acid, andSCOD concentrations in bioreactors during test run 1are shown in Figs. 1±3, respectively. Similar patterns

Table 3

Characteristics of raw swine manure slurries used in test runs 1 and 2a

Parameter Control Carbadox Tylosin Sulphamethazine Tetracycline Penicillin Lyncomycin

TCOD 139180.0 142610.0 129090.0 196810.0 205270.0 177730.0 194044.0

SCOD 38240.0 41890.0 37680.0 52830.0 48420.0 40560.0 48337.0

Acetic 9110.0 8080.0 8060.0 10780.0 8110.0 6030.0 5179.0

Propionic 2510.0 3790.0 2420.0 1960.0 2110.0 2100.0 1651.0

Butyric 3080.0 1680.0 2490.0 2430.0 3060.0 1700.0 1451.0

ALK (as CaCO3) 16840.0 15390.0 14110.0 14730.0 15230.0 16450.0 15447.0

pH 7.16 6.69 6.90 6.64 6.68 6.77 6.73

TS 93780.0 97270.0 94150.0 126090.0 127780.0 121870.0 144340.0

VS 74120.0 75010.0 75480.0 101330.0 103620.0 97170.0 116602.0

TSS 80770.0 86960.0 82884.0 107900.0 105900.0 105690.0 127116.0

VSS 67910.0 73980.0 70150.0 89830.0 88800.0 87630.0 106496.0

TKN 7760.0 5940.0 6160.0 7790.0 7700.0 8030.0 9172.0

NH3±N 4950.0 4640.0 3990.0 4950.0 4640.0 4780.0 5200.0

a All concentrations are in mg/l except pH.

Table 4

Characteristics of raw swine manure slurries used in test run 3a

Parameter Control Mixture 1 Mixture 2 Mixture 3

TCOD 159320.0 166190.0 183170.0 146690.0

SCOD 46130.0 54430.0 57950.0 50660.0

Acetic 6910.0 8490.0 9910.0 9040.0

Propionic 2050.1 2630.0 2900.0 2690.0

Butyric 5630.0 3470.0 3000.0 2960.0

ALK (as CaCO3) 13919.0 17250.0 18460.0 16710.0

pH 6.47 6.59 6.48 6.57

TS 111060.0 105840.0 131330.0 118590.0

VS 90770.0 83940.0 105800.0 94870.0

TKN 7260.0 7470.0 8530.0 7570.0

NH3±N 4350.0 4890.0 5250.0 4930.0

a All concentrations are in mg/l except for pH.


were obtained during test runs 2 and 3. Soluble COD,acetic acid and propionic acid concentrations increasedsharply during the ®ll period and decreased rapidlyduring the react period. The acetic and propionic acids

were almost completely utilized during treatment: at theend of the cycles, they were reduced by over 96% (Tables5±7). Butyric acid was detected at concentrations below200 mg/l during most of the experimental runs, and it

Table 6

Adjusted mean and P-value for methane production rate and treatment e�ciency in test run 2

Cycle Control Lyncomycin Sulphamethazine Tetracycline P

l CH4/gTCOD 1 0.358 0.284 0.318 0.318 0.102

2 0.384 0.303 0.331 0.290 0.053

l CH4/g VS 1 0.191 0.182 0.168 0.160 0.182

2 0.205 0.171 0.170 0.146a 0.048

TCOD % reduction 1 77.01 80.24 80.86 82.24 0.204

2 76.76 76.64 78.50 80.67 0.218

SCOD % reduction 1 83.11 84.66 88.03 86.98 0.083

2 82.71 82.68 87.12 85.09 0.123

TS % reduction 1 65.55 74.19a 69.32 70.76 0.064

2 67.26 72.90 69.19 71.33 0.174

VS % reduction 1 75.21 81.71 78.21 79.07 0.093

2 76.08 80.36 77.55 79.23 0.197

Total VFA% reduction 1 99.34 97.19 100.00 100.00 0.517

2 100.00 96.82 100.00 99.45 0.510

a Di�erent from the control at P < 0:05 according to DunnettÕs test.

Table 5


Cycle Control Carbadox Penicillin Tylosin P

l CH4/g TCOD 1 0.139 0.149 0.110a 0.154 0.027

2 0.243 0.226 0.156a 0.244 0.030

l CH4/g VS 1 0.260 0.283 0.201a 0.264 0.028

2 0.457 0.429 0.286a 0.417 0.032

TCOD % reduction 1 88.93 87.09 81.00 91.40 0.109

2 80.17 82.24 82.09 79.15 0.441

SCOD % reduction 1 83.32 84.69 83.96 86.18 0.739

2 82.26 85.88 82.33 82.99 0.617

TS % reduction 1 82.35 84.84 73.66a 85.68 0.021

2 65.83 69.12 70.44 68.75 0.673

VS % reduction 1 88.69 89.94 82.74 91.30 0.053

2 75.62 77.15 79.15 78.39 0.677

Total VFA % reduction 1 97.79 97.92 96.65 98.89 0.691

2 99.13 99.14 99.07 99.15 0.999

a Di�erent from the control at P < 0:05 according to DunnettÕs test.

Table 7


Cycle Control Mixture 1 Mixture 2 Mixture 3 P

l CH4/g TCOD 1 0.216 0.179 0.201 0.240 0.191

l CH4/g VS 1 0.378 0.355 0.348 0.370 0.844

TCOD % reduction 1 63.19 62.44 66.67 66.72 0.550

SCOD % reduction 1 81.10 79.96 82.99 76.12 0.119

TS % reduction 1 71.63 67.50 72.00 70.27 0.190

VS % reduction 1 75.67 71.00 72.83 76.24 0.050

Total VFA % reduction 1 99.66 99.86 99.86 99.69 0.856


was not detectable at the end of the treatment cycle inany reactors.

The utilization of manure slurries from pigs fed a dietcontaining an antibiotic did not have a signi®cant e�ecton SCOD or VFA reduction during treatment (Tables

5±7). The SCOD concentrations at the end of thetreatment cycle were always much lower than those inthe raw swine manure slurries. The SCOD removal inthe bioreactors fed manure containing penicillin or tet-racycline was similar to that in the controls. Therefore,the reduction in methane production observed withpenicillin and tetracycline was probably due to a de-crease in the hydrolysis rate.

The antibiotics did not seem to have an e�ect on pH.At the end of the treatment cycle, the pH in the biore-actors fed slurries containing antibiotics was similar tothe pH in the control bioreactors (Table 8). The NH3±Nand TKN concentrations in the supernatant at the endof a cycle were also similar in all SBRs (Table 8). TheNH3±N concentrations ranged from 4300 to 4700 mg/l,and TKN from 5900 to 6300 mg/l. The bioreactorsperformed well under these very high concentrations ofNH3±N and TKN. Previous studies reported that NH3±N concentrations varying between 1700 and 3000 mg/lcan be inhibitory or even toxic for the methanogenicbacteria (Kroeker et al., 1979; Melbinger and Donnel-lon, 1971; McCarty, 1964; Henze and Harremoes,1983). In this study, inhibition by ammonia-N was notobserved.

The SBRs: (a) were not a�ected by high concentra-tions of ammonia nitrogen, (b) did not experience ac-cumulation of VFAs at the end of the react period, (c)had a high concentration of methane in their biogas, and(d) maintained an adequate pH. These conditions indi-cated that the bioreactors fed manure slurries containingantibiotics remained very stable. Therefore, the inhibi-tion of methane production observed in this study whenmanure containing penicillin or tetracycline was fed tothe SBRs should not be critical for the stability andoperation of farm scale bioreactors.

3.4. Treatment e�ciency

The presence of antibiotics in the pig diet did notseem to have a negative e�ect on treatment e�ciency.Total COD, SCOD, TS and VS removals exceeded 62%,76%, 65% and 75%, respectively, and were similar in allbioreactors (Tables 5±7).

Fig. 1. Acetic acid accumulation in test run 1.

Fig. 2. Propionic acid accumulation in test run 1.

Fig. 3. Soluble COD accumulation in test run 1.

Table 8

Ammonia and pH in SBRs

Antibiotics

tested

pH Max. ammonia

conc. (mg/l)

Max. TKN

conc. (mg/l)

Control 7.75 4750.0 6300.0

Carbadox 7.75 4340.0 5900.0

Tylosin 7.72 4350.0 5650.0

Penicillin 7.77 4730.0 6230.0

Tetracycline 7.66 4470.0 6150.0

Sulphameth-

azine

7.67 4450.0 6040.0

Lyncomycin 7.69 4690.0 6304.0


Although methane production was 35±25% lower indigesters fed with penicillin or tetracycline, the treat-ment e�ciency was not a�ected. The explanation forthis is probably the large contribution of physical re-moval in the reduction of solids. The manure slurry fedto the bioreactors had very high TCOD and solidscontent. The particulate COD comprised over two-thirds of total in¯uent COD. At the end of a cycle, theSBR system provides quiescent settling conditions,which allow for the removal of a large fraction of TCODand solids. Based on the methane production and theCOD equivalent of methane, about two-thirds of totalCOD and VS were removed biologically, while one thirdwas accomplished by physical separation. Ng (1989)also observed that 50±60% of COD reduction in SBRstreating diluted piggery wastewater was due to physicalremoval. The larger contribution of physical removal inthe Ng study can probably be explained by the lowHRTs, which ranged from 3 to 15 days.

4. Conclusions

The individual or combined e�ects of carbadox,tylosin, penicillin, tetracycline, sulphamethazine andlyncomycin on PAD of swine manure slurry inintermittently fed SBRs were examined in this study.Only penicillin and tetracycline had an inhibitory e�ecton methane production when applied at the maximumallowable dose in feed. However, the observed inhibitionshould not be critical for farm scale operation becausethe reactors exhibited patterns of recovery or acclima-tion as time progressed. Except for tetracycline, thespeci®c methane production rate (l CH4/g of COD fed)increased from Cycle 1 to Cycle 2, indicating that acc-limation was taking place.

The high CH4 production and high SCOD and VFAremoval obtained in this study indicated that the anti-biotics did not have any observable negative e�ects onprocess stability. In addition, manure treatment was nota�ected by high concentrations of ammonia nitrogen.The pH remained within the optimal range for biomass

growth. The biogas contained between 73% and 76% ofmethane, and TCOD, SCOD, TS and VS removal ex-ceeded 62%, 76%, 65% and 75%, respectively, in allbioreactors.

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