Lactic acid fermentation of food waste for swine feed

Bioresource Technology 97 (2006) 1858–1864

Lactic acid fermentation of food waste for swine feed

S.Y. Yang a, K.S. Ji b, Y.H. Baik b, W.S. Kwak b,¤, T.A. McCaskey c

a Life Sciences Research Center, Dan Biotech, Chunan, Chung-Nam 330-834, Republic of Koreab Animal Science, School of Life Resource and Environmental Sciences, College of Natural Sciences, Konkuk University,

Danwol-dong 322, Chung-Ju, Chung-Buk 380-701, Republic of Koreac Department of Animal Sciences, Auburn University, Auburn, AL 36830, USA

Received 4 May 2005; received in revised form 13 August 2005; accepted 26 August 2005Available online 27 October 2005

Abstract

This study was conducted to determine the eVects of lactic acid bacteria (LAB, Lactobacillus salivarius) inoculation on the microbial,physical and chemical properties of food waste mixture (FWM) stored at ambient temperature (25 °C) for 10 and 30 days. A complete pigdiet including restaurant food waste, bakery by-product, barley and wheat bran, and broiler poultry litter was amended with LAB at thelevels of 0.1%, 0.2%, 0.5% and 1.0% and fermented anaerobically. These treatments were compared with intact FWM before storage andnon-anaerobically stored FWM.

Non-anaerobic storage of FWM showed microbial putrefaction with the loss (P < 0.05) of water and water soluble carbohydrate(WSC) and increases (P < 0.005) in protein and Wber. Anaerobic fermentation of FWM with or without LAB seemed eVective in both 10-and 30-day-storage. The addition of LAB inoculants to FWM showed a linear trend (P < 0.05) toward an increase in the number of totaland lactic acid bacteria and toward the nutritional improvement with WSC increased and Wber decreased. Long-term (30 days) storageresulted in consistent reduction (P < 0.05) in numbers of total and lactic acid bacteria and pH and showed little change in chemical com-ponents, compared with short-term (10 days) storage. On the basis of these results, LAB inoculation improved fermentative characteris-tics of FWM. Among anaerobic treatments, further WSC increase and NDF reduction did not occur (P > 0.05) when LAB-added levelswere over 0.2%. Based on these observations the optimum level of LAB addition to FWM was 0.2%.© 2005 Elsevier Ltd. All rights reserved.

Abbreviations: FWM, food waste mixture; LAB, lactic acid bacteria; DM, dry matter; CP, crude protein; NDF, neutral detergent Wber; ADF, acid deter-gent Wber; WSC, water soluble carbohydrate

Keywords: Food waste; Lactic acid bacteria; Fermentation; Pig; Feed

1. Introduction

Food wastes derived from restaurant and householdsare principally putricible wastes that must be managed tocontrol vermin, odor, disease and other sanitary issuesassociated with modern cities. In Korea, some food wastesare used as fertilizer or as feed ingredients for animal pro-duction. The huge production (about 4.5 million metrictons annually) of food wastes has led to intensive researchin the Weld of waste recycling in Korea and the exploration

* Corresponding author. Tel.: +82 043 840 3521; fax: +82 043 851 8675.E-mail address: [email protected] (W.S. Kwak).

0960-8524/$ - see front matter © 2005 Elsevier Ltd. All rights reserved.doi:10.1016/j.biortech.2005.08.020

for bioengineering to transform food wastes into usefulproducts. Bioconversion processes involving microbialmetabolic processes oVer opportunities to transform foodwastes into recycled products. Not only can the putrefac-tion of the wastes be stopped by processing the waste, butalso the waste can be preserved and transformed into eco-nomically useful products.

Lactic acid fermentation process, typical of the silagetechnique applied to forages, has been investigated byseveral workers (Jalil et al., 2001; Kherrati et al., 1998; Shiraiet al., 2001). Food wastes have not been studied extensivelyto determine what type of processes might be applied toconvert the wastes to useful products. Recently we developed

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S.Y. Yang et al. / Bioresource Technology 97 (2006) 1858–1864 1859

a method based on a biotechnological transformation/preservation process to convert food wastes into a feedingredient for swine.

Lactic acid starter bacteria are commonly used as inocu-lants by food fermentation industries to produce a variety offermented foods. The fermentative process not only creates adiVerent food product but also adds other attributes to thefood such as preservation of the food and amends the foodwith desirable microbes. Also, the addition of microbialinoculants with or without enzymes has been reported toimprove ensiling characteristics of alfalfa (Kung et al., 1991;Shockey and Borger, 1991; Sheperd et al., 1995), wheatforage (Froetschel et al., 1991), grass–legume forage (Stokes,1992), corn forage (Kung et al., 1993) and wet brewers grains(Schneider et al., 1995). Because food wastes are typicallywet and contain high levels of fermentable carbohydrate, thelactic fermentation process appears to be the method ofchoice for processing food wastes into animal feed.

A study was conducted to determine the eVects of a lac-tic acid bacterium (Lactobacillus salivarius) inoculant toFWM on the microbial, physical and chemical properties ofthe FWM anaerobically fermented at ambient temperature(25 °C) for 10 and 30 days.

2. Methods

2.1. Manufacture of food waste mixture (FWM)

Fresh food waste (79% moisture) collected from severaloriental restaurants in Seoul, Korea was used in this experi-ment. The food waste was composed primarily of cookedrice, meat and vegetables. For pre-treatment, the foodwaste was ground and screened for foreign materialremoval with a screening grinder (Deplus Engineering Inc.,Korea). Food waste (225 kg lots) was mixed 112.5 kg ofbakery by-product, 87.5 kg of barley bran, 50 kg of wheatbran and 25 kg of broiler poultry litter which had beendeep-stack processed as described in Kwak and Park(2003). The ratio of the ingredients was 16.1:34.8:26.8:15.2:7.1 on a DM basis. An aerobic microbial culture wasadded at the level of 0.3% on a DM basis to hydrolyzestarch to simple carbohydrates in the FWM. The aerobicmicrobial culture developed by Sakai and Kubota (1989)was composed primarily of Bacillus spp. Bakery by-prod-uct, barley bran and wheat bran were used as sources ofenergy and as water absorbents and broiler poultry litter assource of readily available N and minerals for fermentativemicrobes. Bakery by-product was a dried mixture of vari-ous bakery and bread by-products. The chemical composi-tion of the Wnal mixture was as follows: DM 53.9%, crudeprotein 16.1%, neutral detergent Wber 26.5%, and aciddetergent Wber 13.7%.

The mixture was heated at 80 °C for 30 min using a 1 toncapacity vacuum drier (Deplus Engineering Inc., Korea) tomeet the processing regulation of food waste as pig feed inKorea (KFMR, 2001). Following the heat process the mix-ture was cured for 18 h inside a plywood box (90 cm

long£ 90 cm wide£ 130 cm high) with the upper surfaceopen and the metal bottom perforated to facilitate free airmovement.

In order to determine the eVect of lactic acid bacteriaaddition on the storage of FWM, the manufactured FWMwas treated as follows; intact FWM before storage (BS),non-anaerobic storage (NAN), anaerobic storage (AN),and anaerobic storage with lactic acid bacteria cultureadded at the level of 0.1% (ANL0.1), 0.2% (ANL0.2), 0.5%(ANL0.5), and 1.0% (ANL1.0) on a wet basis. A lactic acidbacteria (LAB) was inoculated at levels of 0.1%, 0.2%, 0.5%,and 1.0% (wet basis) into 15 kg aliquots of the FWM andmixed in a small scale mixer (Atika, Italia). The inoculatedmixtures were sealed in double-lined plastic bags within2 kg capacity plastic containers and fermented for 10 and30 days at ambient temperature (25 °C) under anaerobiccondition. For the non-anaerobic storage, the intact mix-ture was left over on the laboratory table at ambient tem-perature (25 °C) for 10 and 30 days.

2.2. Preparation of LAB culture

An acid and bile tolerant Lactobacillus culture that wasisolated from fresh piglet feces was used as the inoculantfor the food waste. This was done to improve the opportu-nity that the lactic culture might serve as a probiotic culturein the gut of the pigs fed the lactic acid-fermented foodwaste. Selection for acid and bile tolerance also might helpensure that the culture would adapt to the gut environmentof the pig. To screen for acid and bile tolerance, MRS(Difco) agar acidiWed to pH 2.0, amended with 1% oxgallwas used to isolate Lactobacillus from piglet feces. The pre-dominant lactic acid bacteria isolated from the feces wasL. salivarius. The culture was identiWed based on morpho-logical and biochemical characteristics provided by Bergey’sManual (Krieg, 1984). Carbohydrate utilization patternsof the isolate were determined with the API CH50 kit (Bio-Merieux, France).

The L. salivarius culture was maintained on MRS agarheld at 4 °C. Prior to inoculation of the food waste, the cul-ture was grown on MRS broth at 37 °C for 48 h to producecell mass which was harvested by centrifugation at 5000g.The centrifugate had a viable lactobacilli count of 1.2£108 cfu/ml, and this was used as starter (inoculum) for theFWM. The starter was added to the FWM at 0%, 0.1%,0.2%, 0.5%, and 1.0% (v/w). The inoculated FWM was heldat 25 °C and analyzed at 0, 10 and 30 days after fermenta-tion. The lactobacillus bacterial count was determined bythe pour plate procedure on MRS agar inoculated at 37 °Cfor 48–72 h.

2.3. Physical and microbial analysis

Physical properties of the FWM fermented 10 and 30days under diVerent conditions were observed for fungalgrowth, for putrefactive appearance and for alcoholic andacidic odors. Three trained evaluators observed the treated

1860 S.Y. Yang et al. / Bioresource Technology 97 (2006) 1858–1864

FWM subjectively by a casual observation method used inour laboratory.

Five grams of each sample were homogenized with495 ml of sterile physiological saline (0.85% NaCl) toachieve a 1:100 dilution of the FWM. Additional dilutionswere achieved using 9 ml aliquots of sterile saline. The totalbacterial count (aerobes and facultative anaerobes) wasdetermined on plate count agar incubated at 30 °C for 48 h.LAB were determined on MRS agar incubated at 37 °C for24 h. Yeasts were determined on yeast-malt extract agar(Difco Laboratories, USA) incubated at 37 °C for 48 h. Col-ony counts of yeast and Bacillus spp. were determined byselective counting characteristic colonies on the agar plates.

2.4. Chemical analysis

Dry matter was determined by drying samples at 65 °Cfor 48 h to constant weight. Crude protein was analyzed bythe Kjeltec System (Tecator, Denmark) using AOAC meth-ods (1990). Neutral detergent Wber (NDF) and acid deter-gent Wber (ADF) were determined according to the methodof Van Soest et al. (1991). pH was measured using a pHmeter (HI9321, Hanna Instrument, Portugal). Water solu-ble carbohydrate was determined by the method of Duboiset al. (1956).

2.5. Statistical analysis

All data were analyzed by the general linear model pro-cedure of SAS (SAS Institute Inc., 1990). Means were com-pared by general contrast including BS vs NAN; BS vs ANtreatments; and NAN vs AN treatments (SAS InstituteInc., 1990). Among AN treatments, linear, quadratic andcubic trends were tested by polynomial contrasts (SAS

Institute Inc., 1990). Comparison of means among ANtreatments was made using LSD test (SAS Institute Inc.,1990). Comparison of means between 10- and 30-day treat-ments was made using student-t test (SAS Institute Inc.,1990).

3. Results and discussion

3.1. Physical parameters of fermented FWM

Physical parameters of the fermented FWM for swinefeed were analyzed subjectively by trained evaluators(Table not presented). Both the 10- and 30-day observationpatterns for fungal growth and for alcoholic and acidicodors were the same. The non-anaerobically (NAN) storedFWM was putreWed and had signiWcant fungal growth. Theanaerobically (AN) stored waste did not putrefy and fer-mentation was evident by an acidic odor of the FWM.Yeast fermentation was evident by an alcoholic odor of theFWM, and this appeared to diminish as the lactic starterinoculum addition to the FWM was increased.

3.2. Microbial parameters

Microbial population and pH changes in the FWM heldfor 10 and 30 days are shown in Table 1, Fig. 1. The pH ofanaerobically stored FWM dropped from pH 5.98 to pH4.5 at the 10-day storage period and to pH 4.4 at the 30-daystorage period, whereas the pH of aerobically stored FWMincreased from 5.98 to 6.51 for a 0.5 pH unit increase. Thelower (P < 0.005) pH of the fermented FWM is attributedto the anaerobic storage of the FWM which encourages thegrowth of acid-producing bacteria that convert fermentableFWM carbohydrate to lactic acid. A fast pH decline by

Table 1Microbial population (Log10 cfu/g1) and pH of diVerently treated food waste mixtures for swine feed depending upon the 10- and 30-day storage perioda,b

a Colony-forming unit per gram of wet samples.b BS D before storage; NAN D non-anaerobic storage; AN D anaerobic storage; ANL D anaerobic storage with lactic acid bacteria added at the level of

0.1% for ANL0.1, 0.2% for ANL0.2, 0.5% for ANL0.5, and 1.0% for ANL1.0.c UC D uncountable due to the over-growth of molds.d BS diVers from NAN (P < 0.005).e BS diVers from AN, ANL0.1, ANL0.2 ANL0.5 and ANL1.0 (P < 0.005).f NAN diVers from AN, ANL0.1, ANL0.2 ANL0.5 and ANL1.0 (P < 0.005).g Among AN treatments, polynomial contrasts showed a linear trend (P < 0.05).h Among AN treatments, polynomial contrasts showed a cubic trend (P < 0.05).

Item BS NANc AN ANL0.1 ANL0.2 ANL0.5 ANL1.0 SE

0-day vs 10-day storageTotal bacteriad,e,f,g 7.49 UC 9.17 9.13 9.42 9.15 9.64 0.20Lactic acid bacteriad,e,f,g 7.40 UC 9.16 9.12 9.41 9.14 9.63 0.26Bacillus spp. 6.39 7.01 6.36 5.86 6.81 6.01 6.65 0.35Yeastd,f,h 6.29 8.91 6.15 5.83 6.08 6.18 5.97 0.13pHd,e,f 5.98 6.41 4.58 4.55 4.60 4.55 4.54 0.02

0-day vs 30-day storageTotal bacteriad,e,g 7.49 9.08 8.38 8.67 8.47 8.58 8.99 0.21Lactic acid bacteriad,e,g 7.40 9.02 8.35 8.65 8.45 8.57 8.89 0.27Bacillus spp.d,f,h 6.39 8.41 6.32 6.03 6.32 5.92 6.52 0.36Yeastd,f,h 6.29 8.59 6.02 6.22 6.13 5.82 6.25 0.19pHd,e,f 5.98 6.51 4.45 4.43 4.43 4.42 4.43 0.03


LAB inoculation to silages was observed in other research(Schneider et al., 1995; Sheperd et al., 1995). A pH of 4–5 isdesired for fermented feed ingredients because below pH 4feed intake is decreased and over pH 5 microbial spoilage islikely to occur (Lee et al., 2004).

Total bacteria and lactic acid bacteria counts increased(P < 0.05) during anaerobic storage of the FWM. The addi-tion of lactic acid bacteria inoculum to FWM showed atrend toward an increase in the number of total and lacticacid bacteria relating to the inoculum level. Compared withthe AN treatment (LAB not added), LAB counts increased(P < 0.05) when LAB was added at 0.2% and 1.0% levels for10 days storage and when LAB was added at the 1.0% levelfor 30 days storage.

Yeast and Bacillus spp. counts were higher (P < 0.005)for aerobically stored FWM than for anaerobically storedFWM. In addition, the concentration of water-soluble car-bohydrates was increased (P < 0.005) by additional levelsof LAB (Table 2). According to a general theoreticalscheme suggested for lactic acid fermentation, insolublecomplex organic polymer components (such as protein,fats and carbohydrates) are Wrst hydrolyzed into smallersoluble compounds by extracellular enzymes and the lowpH. In the next stage, the soluble sugars are converted intolactic acid by LAB (Wang et al., 2003). Lactobacilli gener-ally have a higher tolerance to low pH than lactococci andother lactic acid bacteria (Ohmomo et al., 2002). The mini-mum pH for the growth of most lactobacilli is about pH 4

Fig. 1. EVects of the 10-day vs 30-day storage on chemical composition (% of dry matter) of diVerently processed food waste mixture for swine feed[NAN D non-anaerobic treatment; AN D anaerobic fermentation; ANL D anaerobic fermentation with lactic acid bacteria added at the level of 0.1% forANL0.1, 0.2% for ANL0.2, 0.5% for ANL0.5, and 1.0% for ANL1.0; Means with diVerent letters within the same treatment diVer (P < 0.05)].

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(Wang et al., 2001). If a LAB strain could survive at aboutpH 3.5 and maintain a high concentration of living cells, itwould competitively inhibit the growth of other microbesand thereby contribute to the preservation of the FWM. L.salivarius, which was used as the inoculum for the FWM,showed high acid tolerance. The culture tolerated pH 2.5for 3 h without appreciable loss of viability (Shin et al.,2002).

Yeast populations were higher (P < 0.005) in aerobicallystored FWM than in anaerobically stored FWM and thepopulations were not aVected by storage time. Among ANtreatments, polynomial contrasts of yeast counts showed acubic trend (P < 0.05) at both of the storage periods. Yeastcan attain more energy from soluble carbohydrates duringaerobic growth (respiration) than during anaerobic growth(fermentation). Yeast can metabolize the lactic acid and tol-erate the low pH of the fermented FWM. During aerobicstorage, an increase in DM and CP and a decrease in water-soluble carbohydrates was the result of proliWc yeastgrowth (Table 2, Fig. 2).

3.3. Chemical parameters

Chemical composition of the treated FWM held for 10and 30 days are presented in Table 2. The FWM held for 10days under non-anaerobic storage (NAN) showed micro-bial putrefaction with the loss (P < 0.005) of water andWSC and an increase (P < 0.005) in protein and Wber, bothNDF and ADF Wber.

Compared to FWM before storage (BS), anaerobic stor-age of FWM with or without LAB addition resulted in adecrease (P < 0.005) in DM level, an increase (P < 0.005) inWSC (45%–100%) and ADF levels, with little change(P > 0.05) in CP and NDF levels. The increased level ofWSC indicated that the rate of carbohydrate breakdown

into WSC exceeded that of WSC conversion into microbialbiomass or other metabolites. Among anaerobic treat-ments, as the added levels of LAB increased, WSC wasincreased linearly (P < 0.01), whereas NDF and ADF werelinearly (P < 0.01) and quadratically (P < 0.05) decreased,and DM and CP were not aVected (P > 0.05). Comparedwith the AN treatment (LAB not added), WSC in theFWM increased (P < 0.05) when LAB was added at the lev-els between 0.2% and 1.0% for both of the storage periodsand NDF decreased (P < 0.05) when LAB was added at0.2% and 0.5% levels. Increased WSC content was alsoobserved when wet brewers grains inoculated with LABwas fermented for 6 days (Schneider et al., 1995). Althoughmicrobial inoculation to forage and by-product silage didnot aVect NDF and ADF contents in other studies (Kunget al., 1991, 1993; Stokes, 1992; Schneider et al., 1995), itsinoculation to FWM in our study showed a slight butsigniWcant decline in Wber contents.

Anaerobic storage of FWM with or without LAB addi-tion resulted in lower (P < 0.005) levels of DM, CP and Wber(NDF and ADF) and higher (P < 0.005) levels of WSCcompared to the levels in non-anaerobically treated FWM.

When the FWM treatments were stored for long-term(30 days), the pattern of change in chemical compositiondepending upon treatments was identical to the short-term(10 days) storage with the exception of ADF, in which therewas no diVerence detected between non-anaerobic andanaerobic treatments and also among anaerobic treatments.Long-term (30 days) non-anaerobic storage induced higher(P < 0.05) DM, CP and NDF contents and lower (P < 0.05)ADF content in FWM, however, the anaerobic treatmentsshowed little change in chemical components, comparedwith short-term (10 days) storage. In general, among ANtreatments, further WSC increase and NDF reduction didnot occur (P > 0.05) when LAB-added levels were over 0.2%.

Table 2Chemical composition (% of dry matter) of diVerently treated food waste mixtures for swine feed depending upon the 10- and 30-day storage perioda

a BS D before storage; NAN D non-anaerobic storage; AN D anaerobic storage; ANL D anaerobic storage with lactic acid bacteria added at the level of0.1% for ANL0.1, 0.2% for ANL0.2, 0.5% for ANL0.5, and 1.0% for ANL1.0.

b BS diVers from NAN (P < 0.005).c BS diVers from AN, ANL0.1, ANL0.2 ANL0.5 and ANL1.0 (P < 0.005).d NAN diVers from AN, ANL0.1, ANL0.2 ANL0.5 and ANL1.0 (P < 0.005).e Among AN treatments, polynomial contrasts showed a linear trend (P < 0.01).f Among AN treatments, polynomial contrasts showed a quadratic trend (P < 0.05).

Item BS NAN AN ANL0.1 ANL0.2 ANL0.5 ANL1.0 SE

0-day vs 10-day storageDry matterb,c,d 61.8 73.5 60.8 60.7 60.9 60.8 60.5 0.21Water soluble carbohydrateb,c,d,e 5.14 0.78 7.43 7.86 9.37 9.57 10.30 0.57Crude proteinb,d 15.9 19.8 16.1 16.1 16.1 16.2 16.1 0.21Neutral detergent Wberb,d,e,f 25.5 33.4 28.1 26.2 26.8 26.3 27.2 0.52Acid detergent Wberb,c,d,e 14.7 19.2 19.0 18.6 17.0 17.5 15.9 0.36

0-day vs 30-day storageDry matterb,c,d 61.8 80.4 59.9 59.9 60.6 60.5 60.1 0.35Water soluble carbohydrateb,c,d,e,f 5.14 1.39 7.07 8.37 10.44 10.88 10.37 0.49Crude proteinb,d 15.9 20.3 16.1 16.0 16.1 16.0 16.2 0.16Neutral detergent Wberb,d,e,f 25.5 37.9 30.2 28.6 26.9 27.6 28.2 0.94Acid detergent Wberb,c 14.7 17.9 17.4 17.8 17.2 16.8 16.7 0.60


4. Conclusion

Our results indicated that non-anaerobic storage ofFWM resulted in microbial putrefaction. Anaerobic treat-ment of FWM was an eVective storage method. Themicrobial inoculant was beneWcial in stimulating micro-bial fermentation and in improving fermentative charac-teristics, that is, consistently higher WSC content andlower NDF content in FWM. These results indicated thatLAB inoculants induced signiWcant breakdown of Wber(NDF) into soluble carbohydrate. Food waste mixturecould be more eVectively utilized for short-term (10 days)anaerobic storage showing more microbial population,compared with long-term (30 days) storage. No furtherWSC increase and NDF decrease at LAB-added levels

over 0.2% indicated that the optimum level of LAB addi-tion to FWM was 0.2% on a wet basis. Improved micro-bial and chemical characteristics of LAB addition toFWM needs to be further proved by an in vivo animalfeeding study.

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Fig. 2. EVects of the 10-day vs 30-day storage on microbial population and pH of diVerently treated food waste mixture for swine feed [NAN D non-anaer-obic treatment; AN D anaerobic fermentation; ANL D anaerobic fermentation with lactic acid bacteria added at the level of 0.1% for ANL0.1, 0.2% forANL0.2, 0.5% for ANL0.5, and 1.0% for ANL1.0; Means with diVerent letters within the same treatment diVer (P < 0.05)].

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Lactic acid fermentation of food waste for swine feed