Bioresource Technology 100 (2009) 6217–6222

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Bioresource Technology

journal homepage: www.elsevier .com/locate /bior tech

Effect of low power ultrasonic radiation on anaerobic biodegradabilityof sewage sludge

Chang Liu a, Bo Xiao a, Alain Dauta b, Guifen Peng a, Shiming Liu a, Zhiquan Hu a,*

a School of Environmental Science and Engineering, Huazhong University of Science and Technology, Wuhan 430074, Chinab Equipe InterBio/EcoLab – Laboratoire d’écologie fonctionnelle, UMR 5245 (CNRS-UPS-INPT), Toulouse cedex 31055, France

a r t i c l e i n f o

Article history:Received 30 April 2009Received in revised form 29 June 2009Accepted 1 July 2009Available online 3 August 2009

Keywords:Sewage sludgeUltrasonic radiationAnaerobic biodegradability

0960-8524/$ - see front matter � 2009 Elsevier Ltd. Adoi:10.1016/j.biortech.2009.07.001

* Corresponding author. Tel./fax: +86 02787557464E-mail address: zhiquanhu@yahoo.com.cn (Z. Hu).

a b s t r a c t

The effect of low power ultrasonic radiation on anaerobic biodegradability of sewage sludge was inves-tigated. For this purpose, soluble substances and variation of microbial system of sewage sludge sub-jected to low power ultrasonic radiation were tested. The well known hydromechanical shear forcesand heating effect of low frequency ultrasound plays a major role in the sludge pre treatment process.More, the increase of soluble substance may partly result from the destruction of microbial cell by excessultrasonic pretreatment, which will inhibit the anaerobic process. By orthogonal tests, the optimalparameters were found to be an exposure time of 15 min, ultrasonic intensity of 0.35 W/cm2 and ultra-sonic power density of 0.25 W/ml. Under the optimal condition, anaerobic biodegradability of sewagesludge (R(vss/ss) %) was increased by 67.6%. Consequently, it can be concluded that low power ultrasonicpretreatment is a valid method for improving anaerobic biodegradability of sewage sludge.

� 2009 Elsevier Ltd. All rights reserved.

1. Introduction

The development of industrialization and urbanization has re-sulted in an enormous increase in the amount of wastewater inChina. The increasing environmental awareness and its subsequentregulations have led to the enhancement of wastewater disposalrate in China (MEPPRC and NDRC, 2007). According to state envi-ronmental protection ‘‘11th five-year” plan, the objective for2010 is to dispose of at least 70% of municipal wastewater(MEPPRC and NDRC, 2007). Sewage sludge is an inevitable by-product in the process of wastewater treatment. The yield of sew-age sludge is equivalent to about 0.3–0.5% of treated wastewater interms of volume. The treatment of increasing volumes of wastewa-ter will generate more and more sewage sludge; this sewagesludge must be treated to avoid important secondary environmen-tal consequences.

Traditional methods of sewage sludge disposal mainly includelandfill, sea dumping and soil application (Young and Patrick,2002; Sánchez-Monedero et al., 2004). But these methods willcause secondary environmental pollution (Kim et al., 2005; Singhand Agrawal, 2008). Anaerobic digestion of sewage sludge is a kindof environmentally sound technology. As we know, organic mattercan be transformed into biogas in anaerobic conditions. Mean-while, it also reduces the ultimate sludge quantity, destroys mostof the pathogens present in the sludge, and eliminates unpleasant

ll rights reserved.

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smell problems (Buhr and Andrews, 1977; Zábranská et al., 2000).As an energy source, biogas can be used for heating and electricityproduction (Angelidaki and Ahring, 1997).

Many researchers have been dedicated to the improvement ofdigestion efficiency. It has been found that ultrasonic pretreatmentis valid in enhancing anaerobic biodegradability of sludge. Theirwork mainly focused on two technical directions. One is highpower ultrasonic disruption for accelerating hydrolysis of sludge,which is considered as the rate-limiting step in anaerobic process(Pavlostasthis and Gosset, 1985; Park et al., 2005). Under highpower ultrasonic radiation, disruption of sludge occurs with thephenomena of floc disintegration and cell lysis (Zhang et al.,2007), thus releasing and solubilizing intracellular material intothe water phase and transforming refractory organic material intobiodegradable species. Moreover, treated sewage sludge can bedecomposed more drastically with inoculation. Tiehm et al.(2001) reported that the hydromechanical shear forces producedby ultrasonic cavitation, which occurs only under sufficient ultra-sonic intensity, was the predominant factor in sludge disintegra-tion. Likewise, Nickel and Neis (2007) found that cavitationunder high acoustic intensities was needed to disintegrate biolog-ical cells in sewage sludge, which enhanced the biodegradability ofthe sludge. But the high power ultrasonic results in high energyconsumption, which hinders the development of the technology(Müller, 2001).

Consequently, the other technical direction, low power ultra-sonic, is extensively studied with regards to its activation functionon sludge. Chu et al. (2001) reported that an insufficient ultrasound

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dose did not directly release insoluble substances into the suspen-sion, but allowed the organics to be more easily attacked by thehydrolyzed enzyme. Many researchers have shown that low powerultrasonic exposure can promote the activity of enzymes, cellgrowth and cell membrane permeability (Barton et al., 1996; Liuet al., 2003; Pitt and Ross, 2003). Normally, a significant increaseof biological activity could be obtained only in a very narrow rangeof ultrasonic power (Schläfer et al., 2002; Zhang et al., 2008; Xieet al., 2009). Schläfer et al. (2002) found that either very low powerultrasonic or too high level of ultrasonic led to decrease of biolog-ical activity and degradation rate down to the standard value with-out ultrasonic intake. Although the exact mechanism of low powerultrasonic on the biodegradability of sludge is not clear, it is postu-lated to be related to soluble substances and to the variation of themicrobial system of sewage sludge according to related researches(Chu et al., 2002; Zhang et al., 2007; Li et al., 2009). However, veryfew studies have reported on such consideration. Furthermore, theinformation on how this would affect biodegradability is presentlyunknown.

In this study, the disposal mechanism of low power ultrasonicwas discussed. The increase of soluble substances and the variationof microbial system were both considered in conditions of differentultrasonic power densities, with the aim to determine why signif-icant promotion of biodegradability normally appears in conditionof appropriate ultrasonic dosage. Different ultrasonic power densi-ties, ultrasonic intensities, and exposure times of pretreatmentwere investigated for the optimization of ultrasonic treatment pro-cess. The influencing degree of different ultrasonic parameters forsludge biodegradability improvement was also investigated.

2. Methods

2.1. The samples

In this study, sludge was taken from the thickening tank of amunicipal wastewater treatment plant in Wuhan City, China. Theplant adopts Anerobic–Anoxic–Oxic process. The collected samplewas transported to a laboratory within 60 min following sampling.

2.2. Ultrasonic irradiation facility and parameters

The low power ultrasonic radiation was performed on thesludge in an ultrasonic cleaner (KQ-100DB, Kunshan Inc., China)that produced a 40 kHz ultrasound at its bottom. Bath capacity of

Table 2The orthogonal test factors and levels.

Level Exposure time(min)

Ultrasonic intensity (W/cm2)

Ultrasonic power density(W/ml)

1 10 0.25 0.252 15 0.3 0.23 20 0.35 0.1

Table 1Characteristics of sludge sample taken from thickening tank of the municipalwastewater treatment plant.

Parameter Average value

Water content (%) 98.85TCOD (mg/l) 8179SCOD (mg/l) 139SS (mg/l) 11620VSS (mg/l) 6094pH 7.25Organic content (%) 53.38

the sonicator is 2 l. Its power can be changed from 40 to 100 W.By adjusting sludge volume and power, we could achieve a givenultrasonic power density for the samples. The ultrasonic intensitywas calculated by dividing power with the bottom area(10 cm � 20 cm).

2.3. Experimental procedures

First, the variation of soluble substances reflected by SCOD andmicrobial systems reflected by sludge floc size and microbial col-ony number during the ultrasonic process was analyzed. We choserelative high ultrasonic intensity (0.5 W/cm2) and different ultra-sonic power density (0.1 W/ml, 1000 ml; 0.2 W/ml, 500 ml; and0.4 W/ml, 250 ml) for three groups of sludge samples with expo-sure duration from 5 to 60 min, respectively. The temperature ofsludge samples was not controlled during ultrasonic pretreatment.

Then, the ultrasonic parameters including ultrasonic powerdensity, ultrasonic intensity, and exposure time were optimizedthrough single-factor experiments. Seven sludge samples were irra-diated with different ultrasonic intensities from 0.2 to 0.5 W/cm2

with interval of 0.05 W/cm2, ultrasonic power density of 0.2 W/ml, and exposure time of 20 min. Then, all the samples were testedfor mesophilic anaerobic digestion over a period of 8 days. Subse-quently, biodegradability of sludge of all the samples was exam-ined to confirm the optimal ultrasonic intensity. Another sevensludge samples were treated with different ultrasonic power den-sities from 0.05 to 0.5 W/ml, ultrasonic intensity of 0.35 W/cm2,and exposure time of 20 min. The same operation as above wasrepeated to confirm the optimal ultrasonic power density. Theoptimal exposure time was confirmed by seven digested sludgesamples, pretreated with different exposure times from 5 to50 min, ultrasonic power density of 0.2 W/ml, and ultrasonicintensity of 0.35 W/cm2.

In order to investigated joint effect of the three parameters onsludge biodegradability and further confirm the optimal parame-ters, an orthogonal test (Xie et al., 2008) was arranged as shownin Table 2. In the orthogonal test, nine sludge samples were ex-posed to the ultrasonic with different ultrasonic exposure times,ultrasonic intensities, and ultrasonic power densities (see Table3). One sample without exposure was as a control. The biodegrad-ability of sludge of each sample was determined to evaluate theoptimal ultrasonic parameters.

All the treated sludge samples were carried out for a mesophilicanaerobic digestion over a period of 8 days. Seventy milliliters of

Table 3Results of orthogonal test.

No. Exposuretime (A)

Ultrasonicintensity (B)

Ultrasonic powerdensity (C)

R(VSS/SS)

(%)

Control 3.921 1 1 1 5.742 1 2 2 5.523 1 3 3 4.174 2 1 2 4.945 2 2 3 6.036 2 3 1 6.577 3 1 3 5.868 3 2 1 6.099 3 3 2 6.10k1 5.14 5.51 6.13k2 5.85 5.88 5.52k3 6.01 5.61 5.35Range 0.87 0.37 0.78Remarkable

parametersA > C > B

Optimalcondition

A2B3C1

0

10

20

30

40

50

60

0 10 20 30 40 50 60Time (min)

SCO

D/T

CO

D (

%)

0.1W/ml

0.2W/ml

0.4W/ml

Fig. 1. Effect of different ultrasonic power density at constant ultrasonic intensityof 0.5 W/cm2 on SCOD/TCOD (%) (no temperature control).

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each well mixed sludge sample were put into 100 ml flask. Thenwe filled free space of each flask with pure N2 to guarantee anaer-obic condition. The temperature of each flask was kept at 35 �Cwith a water bath.

2.4. Analytical procedures

The sludge sample was analyzed for water content, total chem-ical oxygen demand (TCOD), soluble chemical oxygen demand(SCOD), suspended solids (SS), volatile suspended solids (VSS)and pH (Table 1). All the chemical reagents were AR and from var-ious commercial sources. COD, VSS and SS were determinedaccording to standard methods (APHA et al., 1995). The sampleswere centrifuged at 4000 rpm/min for 20 min, and then the super-natant was removed for SCOD analysis. Extracellular polymericsubstance (EPS), an important material to combine the biomass,was considered to play a key role for colloidal stability of sludgefloc (Keiding and Nielsen, 1997). Hundred milliliters of sludgewas put into the water bath at 70 �C for 15 min, then the sludgemixture was centrifuged at 4000 rpm/min for 20 min. The superna-tant was removed for EPS analysis.

An electron microscope (BX60, OLYMPUS, Japan) was used toobserve the structure of sludge floc with 1000 times magnification.Each sludge sample (original sludge; 0.1 W/ml, 0.5 W/cm2, 60 min;0.2 W/ml, 0.5 W/cm2, 60 min; and 0.4 W/ml, 0.5 W/cm2, 60 min)was diluted to 10�4 parts of the original concentration with sterilewater. Then all the diluted samples were cultured with bacteriaculture medium for 2 days. Conoly number on each culture med-ium was investigated to reflect microbial colony variation of trea-ted sludge with different ultrasonic parameters. The bacteriaculture medium consisted of 0.75 g beef extract, 1.5 g peptone,0.75 g NaCl, 3 g agar, and 150 ml distilled water, with pH 7.6. Gramstain was used to distinguish between gram-positive bacteria (G+)and gram-negative bacteria (G�).

In order to avoid inaccurate results induced by inhomogeneoussampling, we chose VSS/SS ratio to reflect variation of organic sub-stance. The biodegradability of sludge was evaluated with the fol-lowing formula, in which (VSS/SS)0 is the ratio of VSS/SS inuntreated sludge sample:

RðVSS=SSÞ ¼ðVSS=SSÞ0 � VSS=SS

ðVSS=SSÞ0� 100% ð1Þ

3. Results and discussions

3.1. Effect of low power ultrasonic on the characteristics of sludge

We investigated the effect of low power ultrasonic radiation onsewage sludge from two aspects, (i) the increase of soluble sub-stance and (ii) the variation of microbial system, both are closelyrelated to the anaerobic biodegradability of sludge.

Fig. 2. Effect of different ultrasonic power density at constant ultrasonic intensityof 0.5 W/cm2 on sludge temperature.

3.1.1. Effect of low power ultrasonic on soluble substanceThe percentage of SCOD/TCOD was measured to evaluate the re-

lease of soluble organics from sludge flocs during ultrasonic pre-treatment (Chu et al., 2001). The percentage for sludge treatedwith EPS extracting procedure was 28.4%. If SCOD/TCOD of soni-cated sludge is higher than the value, it implies that EPS went intosupernatant, EPS layer for combining sludge floc was fully de-stroyed. Fig. 1 presents the percentage of SCOD/TCOD in conditionsof different ultrasonic pretreatment time and power density. Thepercentage for the raw sludge was 1.7% without ultrasound. Witha power density of 0.1 W/ml, the percentage increased smoothlyto 37.9% after 60 min of ultrasonic pretreatment. The percentageranged from 26.9% to 30.8% during the period of 40–50 min, when

it was estimated that the EPS layer for combining sludge floc wasfully destroyed. Under the power density of 0.2 W/ml, the percent-age increased rapidly to 42.9% for 40 min of ultrasonic pretreat-ment. Afterwards, the percentage approached a plateau value of43.2–47.1% until 60 min. The EPS layer was fully destroyed after20 min, with the relevant percentage of 31.53%. Under the pre-treatment time of 20 min, the percentage promptly reached41.2% with a power density of 0.4 W/ml. Thereafter, the percentagereached a plateau value of 43.32–52.21% for the next 40 min. With20-min pretreatment time, the percentage under power density of0.4 W/ml was obvious higher than that under power density of0.2 W/ml. So we thought the EPS layer and sludge floc will be de-stroyed more quickly under power density of 0.4 W/ml (0.5 W/cm2, 400 ml sludge). It can be concluded that higher power densityinduces (i) a more rapid increase of SCOD/TCOD percentage (ii) ashorter time for destroying sludge floc. Nevertheless, it seems thata plateau exists using a pretreatment of higher power density.Slight increase of the percentage appears during the period ofplateau.

As shown in Fig. 2, the increase of sludge temperature is signif-icant. For heat treatment is also a pretreatment method for sludge:this phenomena must be taken into account. Under differentpower densities, after 40 min of ultrasonic exposure, the sludgetemperature all reaches 60 �C, but do not increase either. From this

Fig. 3. Effect of different temperature on SCOD/TCOD (%) with no ultrasonication(20, 40 and 60-min water bathing time for each temperature).

Fig. 5. Effect of different ultrasonic power density at constant ultrasonic intensityof 0.5 W/cm2 (60-min ultrasonication) on microbial colony distribution (10�4 partsof original sludge concentration).

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observation, different temperature of water bath ranging from 40to 60 �C were used for investigating heating effect induced byultrasonic on SCOD/TCOD of sludge. Under 40 �C water bath(Fig. 3), the percentage approached a plateau value of 3.7–3.8%during 20–60 min treatment. With the same treatment time, thepercentage ranged from 11.4% to 14.2% under 50 �C water bath,and 17.3–24.1 under 60 �C water bath. The percentage increase

Fig. 4. Images for sludge floc under different ultrasonic power density at constant ultras0.1, 0.2 and 0.4 W/ml ultrasonic, the corner marks: 1, 2 and 3 stand for exposure time o

seems to be more related to the temperature than to the waterbath time. However, higher ultrasonic power density induces morerapid increase of sludge temperature. Compared to the first set ofvalues (Fig. 1), it is clear that the increase of the percentage in-duced by heating effect cannot be neglected. However, the heatingeffect seems not to be the predominant factor in the increase of

onic intensity of 0.5 W/cm2 ((a) for raw sludge; (b–d) represents sludge exposed tof 20, 40, 60 min, respectively, images with �1000 magnification).

Fig. 6. Effects of various parameter levels on the R(VSS/SS).

C. Liu et al. / Bioresource Technology 100 (2009) 6217–6222 6221

soluble substance. For more rapid increase of temperature underhigher power density (Fig. 2) and effect of temperature on SCOD/TCOD (Fig. 3), we concluded that the increase of the percentagebenefited more from the heating effect under higher powerdensity.

3.1.2. Effect of low power ultrasonic on microbial systemThe microorganisms in sewage sludge plays a role mainly in the

form of floc (Marcos von, 2007). The structure of the sludge floc,the microbial colony number and the distribution of G+ and G�

were investigated to evaluate microbial system variation createdby ultrasonic radiation (Kavindra and Jitendra, 2008), especiallyunder different power densities.

There was a obvious change of the structure of sludge afterultrasonic treatment (Fig. 4). The sludge floc is decomposed intosmaller size particles. The floc size decreased with the extensionof radiation time under the power density of 0.1 W/ml (Fig. 4b1–b3). A slight change of the floc size was observed after 20 min un-der higher power density (0.2 and 0.4 W/ml). Main decompositionof sludge took place in the first 20-min ultrasonic time under high-er power density. So we think higher power density induced amore rapid and drastic decomposition of sludge.

Besides the decomposition of sludge floc, the impact of lowpower ultrasonic on the microbial colony was estimated (Fig. 5).The microbial colony number evenly decreased with increasingultrasonic power density, apparently linked to the decrease ofthe colony number of G�. The phenomena can be explained withthinner cell wall of G� than that of G+, which is more easily to bedestroyed.

The percentage of SCOD/TCOD after ultrasonic pretreatmentwas greatly improved (Fig. 1), suggesting that a large amount ofthe insoluble sludge substances is transferred into soluble sub-stances: a way to enhance the hydrolysis rate. However, afterultrasonic pretreatment, the increase in SCOD may result fromthe destruction of sludge structure and microbial cells whichwould inhibit the anaerobic process. With the aim of enhancinganaerobic biodegradability of sludge, the next step was to optimizethe parameters of ultrasonic treatment.

3.2. Optimizing ultrasonic parameters for enhancing anaerobicbiodegradability

The results of single-factor experiments optimizing ultrasonicintensity, ultrasonic power density and exposure time are pre-sented in Fig. 6. The R(VSS/SS) value of raw sludge was 3.83 afteranaerobic digestion for 8 days. The value of R(VSS/SS) reached thepeak of 5.5% when the intensity was 0.3 W/cm2 and decreasedwith lower and upper intensities. The corresponding ultrasonicpower density to the highest R(VSS/SS) value of 5.23% was 0.2 W/ml. With an optimal exposure time of 15 min, the R(VSS/SS) value

came to be 5.64%. From this analysis, the biodegradability ofsludge can be improved significantly with relatively low ultra-sonic intensity, low ultrasonic power density and short irradia-tion time. Lack or excess of ultrasonic dosage is detrimental tothe biodegradability of sludge. All the results may arise fromthe co-effect of ultrasonic pretreatment on soluble substanceand microbial system.

Subsequently, all of the 10 orthogonal tests (including a testwithout ultrasonic irradiation as a control) were conducted simul-taneously under the conditions given in Tables 2 and 3, R(VSS/SS)

was considered as an index for parameters optimization. Basedon the analytical data obtained in Table 3, the highest R(VSS/SS)

was achieved with exposure time of 15 min, ultrasonic intensityof 0.35 W/cm2 and ultrasonic power density of 0.25 W/ml. TheR(VSS/SS) under the optimal condition was increased by 67.6% com-pared to the value of control. The results (Table 3) allowed to rankthe parameters as follows: exposure time > ultrasonic power den-sity > ultrasonic intensity. Exposure time and ultrasonic powerdensity are both important ultrasonic parameters influencingbiodegradability.

4. Conclusions

According to our results, the heating effect produced in the pro-cess of low power ultrasonic radiation has some effect on the in-crease of soluble substances. Moreover, the effect becomesobvious with the increase of ultrasonic power density. The increaseof soluble substances will induce the modification of microbial sys-tem, which will affect the biodegradability of sludge. So that, theoptimization of each ultrasonic parameter is essential. The optimi-zation to reach the best effect leads to a set of conditions as: expo-sure time of 15 min, ultrasonic intensity of 0.35 W/cm2 andultrasonic power density of 0.25 W/ml, taking into account therank of each parameter as exposure time > ultrasonic power den-sity > ultrasonic intensity.

With the optimal condition, R(vss/ss) of sewage sludge can be im-proved by 67.6%. Consequently, low power ultrasonic appears to bea valid method for improving anaerobic biodegradability of sewagesludge.

Acknowledgements

The work was financially supported by the Opening Project ofState Key Laboratory of Freshwater Ecology and Biotechnology ofChinese Academy of Sciences (Grant No. 2008FB006), and HUSTBrain Gain Fund (Grant No. 0124261002), China. We are gratefulto Prof. S. WEST (Wales, UK) for the English reviewing of the man-uscript. We would also like to thank two Anonymous reviewers fortheir helpful comments and suggestions.

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