anaerobic digestion of organic solid poultry slaughterhouse waste – a review

Review paper

Anaerobic digestion of organic solid poultryslaughterhouse waste – a review

E. Salminen 1, J. Rintala *

Department of Biological and Environmental Science, University of Jyv€aaskyl€aa, P.O. Box 35, FIN-40351 Jyv€aaskyl€aa, Finland

Accepted 23 October 2001

Abstract

This work reviews the potential of anaerobic digestion for material recovery and energy production from poultry slaughtering by-

products and wastes. First, we describe and quantify organic solid by-products and wastes produced in poultry farming and poultry

slaughterhouses and discuss their recovery and disposal options. Then we review certain fundamental aspects of anaerobic digestion

considered important for the digestion of solid slaughterhouse wastes. Finally, we present an overview of the future potential and

current experience of the anaerobic digestion treatment of these materials. � 2002 Elsevier Science Ltd. All rights reserved.

Keywords: Anaerobic digestion; Ammonia; Inhibition; Long-chain fatty acids; Nutrients recovery; Renewable energy; Solid poultry slaughterhouse

waste

1. Introduction

In the past decades, the consumption of poultry inFinland and in many other countries has been on theincrease, reaching about 10 kg per capita in Finland in1999 and even more elsewhere (Finnish Food and DrinkIndustries’ Federation, 1999, Fig. 1).

As a result of the growing poultry industry, poultryslaughterhouses are producing increasing amounts oforganic solid by-products and wastes. On the otherhand, legislation on the recovery of organic materialsfor animal feed is becoming tighter (Commission of theEuropean Communities, 2000) and more restrictive oftheir landfilling (Commission of the European Com-munities, 1999). In this regard, anaerobic digestion is apromising alternative for the treatment of these mate-rials, as the process combines material recovery andenergy production (DeBaere, 2000; Hulshoff Pol et al.,1997).

Little literature is available on the characteristics andquantification of organic solid by-products and wastesfrom poultry slaughterhouses, though such informationis needed to evaluate treatment options for these mate-

rials. Bull et al. (1982), Cooper and Russel (1992), andJohns (1995) have reviewed the characteristics andtreatment of wastewater in slaughterhouses, whereasTritt and Schuchardt (1992) present the most recentsummary on the characteristics and treatment of solidwaste and wastewater streams from cattle and pigslaughtering.

The objective of the present study was to review rel-evant information necessary to determine the applica-bility of anaerobic digestion to energy production andmaterial recovery from poultry slaughterhouse wastes.Accordingly, we will describe and quantify organic solidby-products and wastes produced in poultry farmingand poultry slaughterhouses and discuss their recoveryand disposal options. We will also review certain aspectsof anaerobic digestion considered essential in digestingsolid slaughterhouse wastes. In addition, we present anoverview of experience with anaerobic digestion treat-ment of these materials.

2. Quantities and characteristics of organic solid by-

products and wastes from poultry farming and slaughter-

ing

In this section, we quantify and characterise organicsolid by-products and wastes produced in broiler farm-ing and slaughtering (Table 1). Broiler was chosen as anexample because of its importance among all poultry

Bioresource Technology 83 (2002) 13–26

*Corresponding author. Tel.: +358-14-260-1211; fax: +358-14-260-

2321.

E-mail address: [email protected] (J. Rintala).1 Present address: SCC Viatek Ltd., Piispanm€aaentie 5, P.O. Box 3,

FIN-02241 Espoo, Finland.

0960-8524/02/$ - see front matter � 2002 Elsevier Science Ltd. All rights reserved.

PII: S0960-8524 (01 )00199-7

products. The slaughtering of broilers does not essen-tially differ from the slaughtering of other poultry spe-cies, though the amount of by-products and wastes doesdepend on the species. Organic solid waste may be de-fined as organic biodegradable waste with moisturecontent below 85–90% (Mata-Alvarez et al., 2000).

Litter, i.e., excreta and peat or wood chip, is pro-duced at about 2 kg/broiler in deep litter broiler growingfacilities where the birds are allowed to roam freely(Saksala, T., personal communication), and it may varyconsiderably in its characteristics (Table 1) dependingon how long it remains on the ground (Webb andHawkes, 1985a). Its nitrogen content generally increases

with increasing poultry manure deposits, but uric acidmay degrade to ammonia and then volatilise from thelitter (Webb and Hawkes, 1985a). In comparison, cagedpoultry produce only manure (Table 1).

Broilers are grown for 5–6 weeks to a weight of about1.8–1.9 kg before they are slaughtered. Their naturaldeath rate is about 2–3%, being highest during the first 2weeks of their growth with bodies averaging in weightabout 10–15 g/broiler (Saksala, T., personal communi-cation). Breeding produces waste which contains peat,eggshells, stillborn, unborn, and dead birds. In slaugh-terhouses the excreta from vehicles, crates, and cages areusually washed into the sewer.

In the past few decades, poultry slaughtering hasmarkedly changed as the industry has sought to improveits processing efficiency. Today broilers are often pro-cessed in highly automated purpose-designed plants,which typically slaughter and process tens of thousandsof birds per day. In these plants, broilers are removedfrom crates and cages, hung from shackles (Papinaho,1996), electrically stunned, and then bled (Fig. 2). Bloodaccounts for about 2% of the live weight of a broiler,about 40 g/broiler (Rinne, K., personal communica-tion), whereas dried blood contains about 95% protein(Table 1) (Cooper and Russel, 1992). After bleeding andto ease feather removal, broilers are scalded by im-mersing them in hot water (Fig. 2) (Papinaho, 1996).Feather removal may be performed by rubbing thescalded carcass with rotating rubber fingers and usingpressurised water jets (Fig. 2) (Papinaho, 1996). Feathercontributes about 10% to the broiler’s live weight(Rinne, K., personal communication), while driedfeather contains 85–99% proteins (Table 1) (Papado-poulos, 1985). Subsequent evisceration produces, inpercentage of live weight, head (ca. 6.9%), feet (ca. 4.4%)and viscera (ca. 10%) (Rinne, K., personal communi-

Table 1

Quantities and characteristics of organic solid wastes produced in poultry (broiler) farming and poultry slaughterhouses

TS

(%)

VS

(% of TS)

Kjeldahl-N

(% of TS)

Protein

(% of TS)

Lipids

(% of TS)

Methane potential

(m3=kg VSadded)

Methane potential

(m3=kg wet weight)

Carcass 37c Na Na Na Na Na 0.20–0.25b ;c

Litter 52–81h 61–65h 3.2–5.7h Na Na 0.14–0.22h 0.10–0.15h

Manure 20–47d ; i 60–76d;i 4.6–6.7d;i Na 1.5–2.1e 0.2–0.3d ;f 0.04–0.06d;f

Feather 24.3g 96.7g 15g 91g 1–10a 0.2g 0.05g

Blood 22g 91g 7.6g 48g 2g 0.5g 0.10g

Offal, feet, and head 39g 95g 5.3g 32g 54g 0.7–0.9g 0.3g

Trimmings and bone 22.4g 68g 68.6g 51g 22g 0.6–0.7g 0.15–0.17g

Na: not available.a Bourne (1993).b Chen (1999).c Chen and Shyu (1998).dHuang and Shih (1981).eMackie et al. (1991).f Safley et al. (1987).g Salminen et al. (submitted).hWebb and Hawkes (1985a).iWebb and Hawkes (1985b).

Fig. 1. Pork, beef, and poultry consumption. (a) In Finland from 1985

to 1999. (b) Per capita in different countries in 1997 (Finnish Food and

Drink Industries’ Federation, 2000).

14 E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 13–26

cation, Table 1, Fig. 2). After slaughtering, the broilerweighs an average of 1.4 kg (Rinne, K., personal com-munication), and the carcasses are chilled upon evis-ceration to control microbial growth. Furtherprocessing produces trimmings and bones in varyingamounts, depending on practices and processes and thedegree of processing, about 140 g in live weight (Rinne,K., personal communication). Poultry slaughterhousesproduce also a variety of spoiled meat and condemnedmaterials, and their wastewater treatment yields wastessuch as screenings, fat from grease traps, settlings, excessactivated sludge, and flotation tailings (Bull et al., 1982;Johns, 1995).

Poultry by-products and wastes may contain several100 different species of micro-organisms in contami-nated feather, feet, intestinal contents, and processingequipment, including potential pathogens such as Sal-monella sp., Staphylococcus sp., and Clostridium sp.(Chen, 1992). Compared to many other countries,Finnish meat products contain considerably lesspathogens (Ministry of Agriculture and Forestry, 2000).For example, in 1997, positive Salmonella samples inbroiler and turkey meat in slaughtered flock and meatfrom cutting plants rated 0.6% and 3.1%, respectively(Ministry of Agriculture and Forestry, 2000). In com-parison, in the US, about 30% of chicken products arecontaminated with live Salmonella, and 60–80% ofchickens are contaminated with Campylobacter, many

strains of which are resistant to common antibiotics(Haapapuro et al., 1997).

In addition, animals may accumulate various metals,drugs, and other chemicals added in their feed for nu-tritional and pharmaceutical purposes (Haapapuro et al.,1997). Veterinary drugs and other chemical contami-nants are also present in poultry in varying concentra-tions; e.g., zinc and copper concentrations in poultryfeeds in England and Wales range from 28–4030 to5–234 mg/kg TS, respectively, whereas zinc and copperconcentrations in poultry manure were ca. 400 and ca.80 mg/kg TS, respectively (Nicholson et al., 1999).Poultry litter in Israel has been shown to contain vary-ing levels of testosterone (up to 700 ng/g) and esterogen(up to 500 ng/g), which can interfere with reproduction(Shore et al., 1993).

3. Recovery and disposal of organic solid by-products and

wastes produced in poultry farming and poultry slaugh-

terhouses

This section reviews the current recovery and disposalpractices and requirements for organic solid wastesproduced in poultry farming and poultry slaughter-houses (Fig. 3). Council Directive 90/667/EEC (Com-mission of the European Communities, 1990) specifiesthe animal and public health requirements for the

Fig. 2. Organic solid materials (per broiler) produced in broiler farming and slaughtering (Papinaho, 1996; Rinne, K., personal communication;

Saksala, T., personal communication; adapted from Shai, 1992; Ty€oopp€oonen, P., personal communication).

E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 13–26 15

disposal and processing of animal waste to destroy po-tential pathogens present in the waste. Animal wastemay be defined as carcasses or parts of animals, in-cluding products of animal origin not intended for directhuman consumption (Commission of the EuropeanCommunities, 1990). Animal waste is classified either ashigh-risk material, if it is suspected to present serioushealth risks to people or animals, or as low-risk mate-rial, if it does not. High-risk material includes animalsdied on the farm, stillborn and unborn animals, andspoiled and condemned materials. The Commission iscurrently working on a new Directive for health rulesconcerning animal by-products not intended for humanconsumption (Commission of the European Communi-ties, 2000; Rantaj€aarvi, P., personal communication).

3.1. Rendering

Rendering refers to various heating processes toseparate fat from meat (Swan, 1992). Rendering at 133�C for a minimum of 20 min at 3 bars (Commission ofthe European Communities, 1990) or an alternative heattreatment (Commission of the European Communities,1992) is needed for high-risk materials intended for an-imal feed or as an intermediate product for the manu-facture of organic fertiliser or other derived products.Rendering produces meat-bone-meal, which may beused in animal feed or as fertiliser or be further pro-cessed via anaerobic digestion or composting. In addi-tion, rendering produces fat, which may be used foranimal feed, in chemical industry products, or burned asfuel.

3.2. Use for animal feed

As rich sources of protein and vitamins, slaughter-house by-products are preserved with formic acid andused as animal feed either as such or together with

regular feed, e.g. in Finland, for fur animals or for petfood production (Pulsa, 1996). As one among the big-gest fur animal producers in the world, Finland uses anannual 370 million kg of fur animal feed, more than halfof which is by-products from the meat and fish industry(Pulsa, 1996). Poorly degradable in its natural state,feather is not suitable for animal feed, but pre-treatedfeather is sometimes used in animal feed (El Boushy andvan der Poel, 1990; Onifade et al., 1998; Papadopoulos,1985). Legislation, however, is becoming stringent aboutthe use of slaughter by-products for animal feed to re-duce the risk of disease transmission via the feed and thefood chain (Commission of the European Communities,2000; Rantaj€aarvi, P., personal communication).

3.3. Incineration

Incineration refers to technologies of thermal de-struction, apparently among the most effective methodsfor destroying potentially infectious agents (Ritter andChinside, 1995). Air-dried poultry litter is a provencombustible solid fuel with a gross calorific value ofabout 13.5 GJ per tonne, about half that of coal(Dagnall, 1993), whereas materials having a high mois-ture content have little or no energy value. In incinera-tion, the air emission, process conditions, and thedisposal of solid and liquid residues need to be strictlycontrolled. The Commission of the European Commu-nities is currently preparing a new Directive on wasteincineration.

3.4. Burial and controlled landfilling

Burial of dead birds on the farm is strictly controlledto avoid groundwater contamination. As the operation,monitoring, and control of landfilling have also becomemore tightly regulated under Directive 1999/31/EC(Commission of the European Communities, 1999),

Fig. 3. Current recovery and disposal of organic solid by-products and wastes produced in the poultry farming and slaughterhouses in Finland and

the option of anaerobic digestion for the recovery of these materials (� � �) (Lahtinen, M., personal communication).


landfills must prevent or reduce as much as possibletheir adverse effects on the local environment, particu-larly the pollution of surface water, groundwater, soiland air, as well as on the global environment, includingthe greenhouse effect. All these measures increase thecosts of landfilling. Furthermore, legislation is restrict-ing landfilling of organic wastes but allowing biologi-cally treated material to be used as landfill cover(Commission of the European Communities, 1999).

3.5. Composting

Composting, an aerobic biological process to de-compose organic material, is carried out in either win-drows or reactors. It is a common method to treatpoultry slaughterhouse wastes, including screenings,flotation tailings, grease trap residues, manure, litter,and sometimes also feather. Composting reducespathogens, and composted material may be used as soilconditioner or fertiliser (DeBertoldi et al., 1983; Senesi,1989). However, wastes with a high moisture and lowfibre content need considerable amounts of moisture-sorbing and structural support to compost well (Trittand Schuchardt, 1992). In addition, emission to air,water, and land may present a problem, especially inwindrow composting, and this may also reduce the ni-trogen (fertilising) content in the compost (Tritt andSchuchardt, 1992).

3.6. Anaerobic digestion

Anaerobic digestion is a biological process in whichorganic matter is degraded to methane under anaerobicconditions. Methane can then be used for energy to re-place fossil fuels and thereby to reduce carbon dioxideemissions. Anaerobic digestion reduces pathogens andodours, requires little land space for treatment, and maytreat wet and pasty wastes (Braber, 1995; Shih, 1987,1993). In addition, any releases to air, water, and landfrom the process can be well controlled (reviewed byBraber, 1995; Shih, 1987, 1993). Most of the nutrients

also remain in the treated material and can be recoveredfor agriculture or feed use (Salminen et al., 2001a; Shih,1987, 1993; Sundradjat, 1990; Vermeulen et al., 1992).The pros and cons of anaerobic digestion treatment ofpoultry slaughterhouse wastes are reviewed in detail inthe following section.

4. Some fundamental aspects of anaerobic digestion ofsolid slaughterhouse wastes

In this section, we will briefly describe the metabolicpathways of anaerobic degradation of solid slaughter-house waste. The effects of long-chain fatty acids(LCFAs) and ammonia on the degradation process willbe discussed in detail because the compounds are im-portant in the anaerobic digestion of solid poultryslaughterhouse waste. Attention will also be paid to theanaerobic degradation of feather and, briefly, to the fateof pathogenic microorganisms in anaerobic digestion.

4.1. Degradation pathways

A diversity of micro-organisms are involved in themany steps of anaerobic degradation of complex sub-strates, such as solid poultry slaughterhouse waste (Fig.4), any of which may be rate-limiting, depending on thewaste being treated as well as process conditions andoperation (reviewed by Pavlostathis and Giraldo-Go-mez, 1991). Solid slaughterhouse waste contains highamounts of different proteins and lipids. Fermentativebacteria, particularly the proteolytic Clostridium species,hydrolyse proteins to polypeptides and amino acids,while lipids are hydrolysed via b-oxidation to long-chainfatty acids (LCFAs) and glycerol (Koster, 1989; McIn-erney, 1988; Zinder, 1984) and polycarbohydrates tosugars and alcohols (Koster, 1989; Pavlostathis andGiraldo-Gomez, 1991; Zinder, 1984, Fig. 4). After that,fermentative bacteria convert the intermediates to vol-atile fatty acids (VFAs), hydrogen (H2), and carbondioxide (CO2) (Koster, 1989; McInerney, 1988; Zinder,

Fig. 4. Degradation pathways in anaerobic degradation (previously reviewed by Koster, 1989; Pavlostathis and Giraldo-Gomez, 1991; Zinder, 1984).


1984). Ammonia and sulphide are the by-products ofamino acid fermentation (Koster, 1989; McInerney,1988; Zinder, 1984). Hydrogen-producing acetogenicbacteria metabolise LCFAs, VFAs with three or morecarbons, and neutral compounds larger than methanolto acetate, H2, and CO2 (Fig. 4). As these reactions re-quire an H2 partial pressure of ca. 10�3 atm, they areobligately linked with micro-organisms consuming H2,methanogens, and some acetogenic bacteria (Dolfing,1988; Zinder, 1984). Methanogens ultimately convertacetate, H2 and, CO2 to methane and CO2 (Fig. 4)(Vogels et al., 1988; Zinder, 1984). In the presence ofhigh concentrations of sulphate, H2 consuming aceto-genic bacteria and sulphate reducing bacteria competewith methanogens for H2 (Widdel, 1988; Zinder, 1984).

4.2. Effects of long-chain fatty acids on anaerobicdigestion

LCFA degradation may be the limiting step in theanaerobic degradation of solid slaughterhouse wastes(Broughton et al., 1998) because of the slow growth ofLCFA-consuming bacteria (maximum growth rateusually below 1 d�1) (Angelidaki and Ahring, 1995, re-viewed by Hwu, 1997) and because the breakdown ofLCFAs requires low (ca. 10�3 atm) H2 partial pressure(Novak and Carlson, 1970). On the other hand, theeasily accumulating LCFAs may cause problems in an-aerobic digestion of solid slaughterhouse waste(Broughton et al., 1998, Salminen et al., 2000) becausethey are toxic to anaerobic micro-organisms, particu-larly acetogens and methanogens (Angelidaki and Ah-ring, 1992; Galbraith et al., 1971; Hanaki et al., 1981;Hwu et al., 1996; Koster and Cramer, 1987; Rinzemaet al., 1994; Roy et al., 1985). An additional problem istheir tendency to form floating scum (Salminen et al.,2001b), for floating LCFAs may affect their bioavail-ability and toxicity and cause common obstacles such asfouled gas collection pipes and scum overflow (Hobsonand Wheatley, 1988; Pagilla et al., 1997).

LCFAs are surface-active compounds and in aqueoussystems behave like synthetic surfactants. The unionisedform of LCFAs adsorbs initially to the microbial cellsurface and is then taken up into the cell. Subsequently,acyl-CoA synthetase activates LCFAs, which are thendegraded with a sequential removal of two-carbon unitswith acetate as end-product, i.e., via b-oxidation (Fig. 4)(reviewed by Hwu, 1997). Adsorption is also a mecha-nism of inhibition (Galbraith et al., 1971; Hwu et al.,1998). Both LCFA adsorption and inhibition depend onthe concentration (Hwu et al., 1998), though the al-lowable concentration of LCFAs in digesters cannot bereliably determined as the inhibition also depends onseveral other factors. The inhibition is dependent on thetype of bacteria present, and Gram-positive microor-ganisms and methanogens are more vulnerable to

LCFAs than Gram-negative microorganisms (Nieman,1954; Roy et al., 1985). The inhibition depends, fur-thermore, on the specific surface area of sludge withsuspended sludge being more vulnerable than granularsludge (Hwu et al., 1996). The carbon chain length andsaturation of LCFAs, too, affect the inhibition (Gal-braith et al., 1971; Komatsu et al., 1991; Koster andCramer, 1987; Rinzema, 1988), saturated LCFAs with12–14 carbon atoms and unsaturated LCFAs with 18carbon atoms being the most inhibitory (Nieman, 1954;Rinzema, 1988). In addition, LCFA toxicity to metha-nogens is synergistic, i.e., it increases in the presence ofanother LCFA (Koster and Cramer, 1987). On the otherhand, various substances, including albumin, starch, bileacids, and cholesterol, may reduce the toxicity ofLCFAs due to the formation of complexes or competi-tive adsorption at the cell wall (Nieman, 1954). Ben-tonite and calcium are also substances that may preventLCFA inhibition, bentonite because of its flocculatingcapability or cations of bentonite such as calcium (An-gelidaki et al., 1990) and calcium from other sourcesbecause of such ions combined ability to form precipi-tates and increase surface tension (Galbraith et al., 1971;Hanaki et al., 1981; Koster, 1989; Roy et al., 1985).

4.3. Effects of ammonia on anaerobic digestion

Ammonia produced in protein degradation maycause problems in anaerobic digestion of solid slaugh-terhouse waste, as unionised ammonia inhibits anaero-bic microorganisms, particularly methanogens(Angelidaki and Ahring, 1993; DeBaere et al., 1984;Hansen et al., 1998; Hashimoto, 1986; McCarty andMcKinney, 1961; Melbinger and Donnellon, 1971; Wi-egant and Zeeman, 1986). Unionised ammonia is toxicbecause, unlike ammonia ions, it can readily diffuseacross the cell membrane (Kadam and Boone, 1996).

Reportedly, unionised ammonia inhibits methano-genesis at initial concentrations of ca. 0.1–1.1 g N/l(Angelidaki and Ahring, 1993; DeBaere et al., 1984;Hansen et al., 1998; Hashimoto, 1986; McCarty andMcKinney, 1961; Melbinger and Donnellon, 1971; Wi-egant and Zeeman, 1986). Methanogens may adapt toammonia concentrations several times the initialthreshold level, i.e., the level beyond which methaneproduction is possible only after a certain period ofadaptation (Koster and Lettinga, 1988; Parkin et al.,1983). Angelidaki and Ahring (1993) postulated thatadaptation results from the growth of new methanogensrather than metabolic changes in the methanogens al-ready present, as proposed by Koster (1986). Ammoniais unlikely to cause a bactericidal effect, as dilutingconsiderably accelerated the recovery from inhibition ofa failed digester (Parkin et al., 1983). Recently, Hansenet al. (1999) found that even a small amount of sulphide(23mg S�

2 =l) may increase ammonia inhibition (4.6 gN/l),


whereas activated carbon (2.5% w/w) or FeCl2 (4.4 mM)could relieve inhibition by reduction of sulphide con-centration via adsorption onto activated carbon orprecipitation as ferrous sulphide.

Air stripping may be used to remove ammonia frommaterials to be digested (Liao et al., 1995), or ammoniamay be recovered from an anaerobic digester in insol-uble form as struvite by adding stoichiometric amountsof magnesium and orthophosphate (Kim, 1995; Maek-awa et al., 1995). Addition of phosphorite ore was foundto prevent ammonia inhibition in the anaerobic diges-tion of poultry manure, supposedly by either immobi-lizing methanogens on the mineral grains, whichincreases the buffering capacity of the medium, or byexchanging ammonium ions for cations such as K, Ca,Mg (Krylova et al., 1997).

4.4. Anaerobic degradation of poultry feather

Poultry feather is a challenge to anaerobic digestionbecause it degrades poorly under anaerobic conditions(reviewed by Bourne, 1993). Feather consists mainly ofkeratin, a fibrous protein, and it is the tight packing ofthe protein chain into a supercoiled polypeptide chainwith a high degree of cross-linking by cystine disulphidebonds, which is mainly responsible for its poor degra-dability (reviewed by Bourne, 1993). Friedrich andAntranikian (1996) isolated an anaerobic bacterium,thermophilic Fervidobacterium pennavorans, that is ca-pable of degrading native feather, and Williams andShih (1989) isolated and characterised a feather-degrading bacterium, Bacillus licheniformis, from adigester treating manure and poultry feather (Williamset al., 1990). The latter bacterium, though isolated froman anaerobic habitat, grew maximally under aerobiccondition, but its cell number declined slowly underanaerobic condition. Besides, the bacterium could de-grade only autoclaved feather.

Various pre-treatments have been shown to improvethe nutritive value of feather for animal feed (El Boushyand van der Poel, 1990; Onifade et al., 1998; Papado-poulos, 1985). Several pre-treatments to increase themethane yield of feather were tested (Salminen et al.,submitted). Combined thermal (120 �C, 5 min) and en-zymatic (commercial alkaline endopeptidase, 2–10 g/l)treatments increased its methane yield in the range of37–51%, whereas thermal (70–120 �C, 5 min–1 h),chemical (NaOH 2–10 g/l, 2–24 h), and enzymatictreatments were less effective in yielding methane, in-creasing in the range of 5–32%.

4.5. Fate of pathogenic microorganisms in anaerobicdigestion

Pathogenic bacteria, parasites, and viruses may con-stitute a serious risk to animals and public health if

untreated poultry slaughterhouse waste is to be recov-ered for agriculture or animal feed (Marchaim et al.,1991; Shih, 1987, 1993). Anaerobic digestion has beenshown to destroy pathogens, thermophilic being usuallymore effective than mesophilic digestion (Shih, 1987). Acomplete eradication of fecal coliforms and salmonellaewas observed in a thermophilic digester (50 �C), whereasa comparable mesophilic digester (35 �C) destroyedthem only partially (reviewed by Shih, 1987, 1993). Theoocysts of Eimeria tenella, a pathogenic protozoancausing chicken coccidiosis, were inactivated 99.9% in athermophilic digester and 90–99% in a mesophilic di-gester, whereas thermophilic and mesophilic conditionsreduced the counts of excreta-born fungal spores by 99–100% and 94–98%, respectively (reviewed by Shih, 1987,1993). Viruses may tolerate the conditions in an anaer-obic digester considerably better than bacteria (reviewedby Turner and Burton, 1997), yet thermophilic treat-ment (at 55 �C) with an appropriate holding time maydestroy many of the viruses present in wastes. Anaerobictreatment at 50 �C has been shown to destroy Marek’sdisease virus (Shih, 1993). Besides temperature, the de-struction of pathogens in anaerobic digestion dependsalso on several other factors. For example, increasingthe hydraulic retention time (HRT) may increase bac-terial and viral destruction (Kun et al., 1989). A two-phase anaerobic digestion reduced the number ofpathogens even more than the conventional one-phasedigestion (Kun et al., 1989). However, unstable perfor-mance or incomplete anaerobic digestion may, in fact,lower the ability of the process to reduce pathogens(Marchaim et al., 1991). To ensure the microbial safetyof the digested material, sanitation, typically at 70 �C for1 h, or sterilisation of high-risk materials, at 133 �C and3 bars for 20 min, is usually required (Ling, 1997).

5. Experiences with anaerobic digestion of solid slaugh-

terhouse wastes

Recent advances in anaerobic digestion technologieshave made it possible to treat an increasing diversity ofwastes. Assuming that operation conditions are care-fully optimised and economic viability can be achieved,anaerobic digestion competes well with other treatmentsof solid slaughterhouse waste (Banks, 1994; Tritt andSchuchardt, 1992). In this section, we review experienceswith treating solid slaughterhouse waste, including alsoslaughterhouse waste other than those from poultryslaughterhouse. This is because there is limited infor-mation available about the anaerobic digestion ofpoultry slaughterhouse waste and because we considerthat information about the treatment of slaughterhousewaste other than from poultry slaughterhouse may beuseful in the design and operation of poultry slaugh-terhouse waste digesters. On the other hand, over the


past decades a large number of studies have been con-ducted on the anaerobic digestion of poultry excreta(e.g. Webb and Hawkes, 1985a, 1995b). A comprehen-sive review of the subject is not presented in this paper.

5.1. Experiences with full-scale

The number of full-scale anaerobic digesters treatingonly solid slaughterhouse waste is still limited (Table 2)and to our knowledge, no full-scale anaerobic digestertreats solid poultry slaughterhouse wastes alone. In theUK in the year 1999 seven digesters treated solidslaughterhouse wastes, such as cattle paunch wastes,blood, and settlement tank solids, the largest of them40–50 t of waste/d (Banks and Wang, 1999). Banks(1994) described the performance of a 105 m3 digestertreating cattle and lamb paunch contents, blood, andprocess wastewaters with an organic loading of 0.36 kgCOD/m3 d and an HRT of 43 days: the process pro-duced methane 0.18 m3=kg CODadded. Fluctuations andan overload of blood in the feed, however, destabilisedthe process, evidently creating ammonia inhibition(Banks, 1994).

Shih (1993) described two well-functioning, full-scalepoultry manure digesters, one in Beijing and one inShanghai, treating waste from 50 000 hens. Safley et al.(1987) reported on the sustainable operation of a 587 m3

digester treating manure from 70 000 caged layers (seeTable 2). Over the past decades, there has been a num-ber of full-scale applications of the anaerobic digestionof poultry excreta.

5.2. Experiences with laboratory-scale

The anaerobic degradation and methane yield ofdifferent poultry slaughterhouse by-products and wasteswere recently investigated in batch assays (Salminenet al., submitted). Poultry offal showed a high methaneyield, 0.7–0.9 m3 of methane/kg VSadded (Table 1), but itsproduction was considerably delayed due most likely toinhibition by LCFAs. Poultry blood, meat and bonetrimmings produced 0.5–0.7 m3 of methane/kg VSadded,respectively, while feather showed the lowest methaneyield of 0.21 m3 of methane/kg VSadded. Up to 0.67 m3 ofmethane/kg VSadded was produced from a solid poultryslaughterhouse waste mixture (bone and trimmings,blood, offal, and feather mixed in an approximate ratioas generated in the slaughterhouse: 42%, 16%, 32%, and10% by weight, respectively) in batch assays (Salminenet al., 2000).

Continuous anaerobic digestion of solid poultryslaughterhouse waste was found technically possible(Salminen and Rintala, submitted). The process wasmanageable with a loading of 0.8 kg VS/m3 d and an

Table 2

Anaerobic digestion of solid slaughterhouse wastes and poultry manure and litter, influent feed characteristics, process conditions, and methane yield

Reactor Substrate T (�C) HRT (d) Loading rate Methane yield References

CSTR, 105 m3 Cattle and lamb paunch

contents, blood, and

process wastewaters

Na 43 0.36 kg COD/m3 d 0.18 m3=kg COD Banks (1994)

CSTR, 2 l Solid slaughterhouse

waste

35 50 0.8 kg VS/ m3 d 0.52–0.55 m3=kg VS Salminen et al.

(2000)

Two phases, (1)

HFR, 4 l (2) CSTR,

1 l with zeolite

as immobilisation

matrix, 20 g/l

Cattle blood and rumen

paunch contents

35 (1) solids 2–30,

liquid 2 (2) 2–10

3.6 kg TS/m3 d 0.27 m3=kg TS Banks and Wang

(1999)

CSTR, batch, 12 l Sheep tallow 35, 55 Na 5–20 g/l tallow

(2.84 g COD/g)

Na Broughton et al.

(1998)

Two phases, (1) LB,

3 or 10 l (2) UASB,

2.35 or 3 l

Poultry mortalities 35, 55 Na (1) 2279 g (2)

<2 kg COD/m3 d

0.201 m3=kg wet

weight

Chen and Shyu

(1998)

Two phase, LB and

UASB

Poultry mortalities Na Na Na 0.254 m3=kg wet

weight

Chen (1999)

CSTR, 5 l Poultry litter 35 12–29 0.3–4.2 kg VS/m3 d 0.14–0.22 m3=kg VS Webb and Hawkes

(1985a,b)

CSTR, 15 m3 Poultry manure 35 22–24 1.63 kg VS/m3 d 0.22 m3=kg VS Safley et al. (1987)

CSTR, 5 l Poultry litter 35 12–29 0.7–4.2 kg VS/m3 d 0.14–0.22 m3=kg VS Webb and Hawkes

(1985a)

CSTR, 15 m3 Poultry manure 50 4 7.5 kg VS/m3 d 0.29 m3=kg VS Steinberger and

Shih (1984)

CSTR, 5 l Poultry manure 34 40 2.26 kg VS/m3 d 0.20 m3=kg VS Pechan et al. (1987)

CSTR, 5 l Poultry manure 35 14–29 Na 0.24–0.26 m3=kg VS Webb and Hawkes

(1985b)

HFR: hydraulic flush reactor, CSTR: continuously stirred tank reactor, LB: leach bed, UASB: upflow anaerobic sludge blanket, Na: not available.


HRT of 50 days and showed a methane yield of 0.55 m3

of methane/kg VSadded (Table 2). However, both HRTand loading were highly significant for the performanceof the process. At a loading of 1.0–2.1 kg VS/m3 d and aHRT of 12.5–25 days, the process appeared inhibited, asindicated by the accumulation of LCFAs and the de-clined methane yield (Salminen and Rintala, submitted).Accumulated LCFAs were proposed to be the mainfactor affecting the recovery of the process from inhi-bition (Salminen et al., submitted). Furthermore, thesimulation model showed that the degradation patternsof solid poultry slaughterhouse waste involved compli-cated feedback connections, suggesting that the inhibi-tion of propionate degradation by LCFAs and theinhibition of hydrolysis by a high propionate concen-tration constituted the rate-limiting step in the degra-dation of the waste in batch assays (Salminen et al.,2000).

Webb and Hawkes (1985a) described a practicabletreatment of poultry litter in mesophilic digesters (Table2). Anaerobic treatment of poultry manure has beenproven feasible as well (Table 2) (Barik et al., 1991;Webb and Hawkes, 1985b), though ammonia inhibitionmay cause difficulties in the process (Hunik et al., 1990;Krylova et al., 1997; Pechan et al., 1987; Webb andHawkes, 1985b).

A complete degradation of up to 20 g/l of sheep tal-low was shown in batch digesters under mesophilicconditions in ca. 90 days of incubation (Broughton et al.,1998). Under thermophilic conditions, though, and witha substrate concentration of 5 and 10 g/l, methaneproduction was delayed by 43 and 48 days, respectively,and 20 g/l of tallow showed no methane productionwithin 90 days of incubation. In these studies, LCFAsand VFAs accumulated considerably but were finallydegraded to biogas, except in the thermophilic studywith a tallow concentration of 20 g/l.

Banks and Wang (1999) investigated the treatmentof cattle blood and rumen paunch contents in a two-phase process with uncoupled solids and liquid reten-tion times. Compared to a single stage process, thetwo-phase process allowed a higher overall loading,3.6 kg TS/m3 d, with acceptable performance (Table 2).In the first phase of the process, hydrolysis was ap-parently enhanced owing to the hydraulic flush, whichprevented the accumulation of intermediates, the po-tential inhibitors of hydrolysis (Banks and Wang,1999).

Chen and Shyu (1998) investigated the anaerobictreatment of poultry mortalities in a combined UASBreactor and a leach bed. An 86% TS reduction and amethane yield of ca. 0.20 m3=kg of wet weight of mor-talities were achieved in 118 days (Chen and Shyu,1998). Chen (1999) showed a methane yield of 0.25 m3/kg of wet weight of mortalities in a process in whichthree leach beds were connected to one UASB in an

alternating fashion. The degradation of one batch ofmortalities took about 62 days.

5.3. Co-digestion

Co-digestion of wastes with varying characteristics isone way to dilute toxicants and to supply missing nu-trients and a suitable moisture content (reviewed byMata-Alvarez et al., 2000). However, transport costs andvarious policies of waste producers may limit the use ofthis process (reviewed by Mata-Alvarez et al., 2000).

A mesophilic laboratory-scale digester, treatingpoultry slaughterhouse waste together with waste from afood packing plant and inoculated with mesophilic di-gested sewage sludge could handle loads up to 4.6 g VS/ld with an HRT of 18 days and produce methane up to0.33 m3/kg VSadded (Table 3). On the other hand, undersimilar conditions, digesters inoculated with mesophilicand thermophilic granular sludge failed apparently be-cause of inhibition by ammonia and/or LCFAs (Salmi-nen and Rintala, 1999).

Co-digestion of manure and industrial organicwastes, including slaughterhouse waste, takes place inDenmark in a number of anaerobic digestion plants(Danish Institute of Agricultural and Fisheries Eco-nomics, 1999). Manure and slaughterhouse waste, in-cluding blood, fat, stomach, and visceral contents, andresidues from a rendering plant, are also being treated ina plant in Sweden (Ling, 1997) (Table 3).

Rosenwinkel and Meyer (1999) showed a successfultreatment of slaughterhouse waste, hog, and cowstomach contents with sewage sludge in a pilot-scale,mesophilic digester at a loading of 2.9 kg TS/m3 d andan HRT of 17 days with a methane production of 0.23m3=kg TSadded. In another study, methane production ina sewage sludge digester treating flotation tailings waspossible at a loading of 1.5 kg TS/m3 d and an HRT of15 days with a methane production of 0.32m3=kg TSadded (Table 3). Brinkman (1999) described astable, thermophilic treatment of kitchen waste slurriesand flotation sludges from slaughterhouse wastes in alaboratory-scale digester at a loading of less than 3.5 kgCOD/m3 d with an HRT of 32 days, but shock loads of5–7.5 kg COD/m3 d caused an accumulation of LCFAsand VFAs.

5.4. Slaughterhouse wastewaters

Anaerobic treatment of slaughterhouse wastewater isfar more common than the treatment of solid slaugh-terhouse waste. In 1968 in Leeds, the UK, an anaerobicplant was built to treat slaughterhouse wastewater(Black et al., 1974). Treatment of slaughterhousewastewater in high-rate anaerobic treatment processeshas been proven feasible in several investigations (e.g.Borja and Banks, 1994; Borja et al., 1995a,b,c,d, 1998;


Pozo del et al., 2000; Harper et al., 1987, 1990;Macaulay et al., 1987; Sayed and De Zeeuw, 1988;Sayed et al., 1984, 1987; Tritt, 1992). A few full-scaleplants operate in slaughterhouses in the Netherlands,Belgium, and New Zealand (reviewed by Johns, 1995),and anaerobic lagoons or covered anaerobic ponds areused to treat slaughterhouse wastewater in warm cli-mates and where land cost is low as in Australia andNew Zealand (reviewed by Cooper and Russel, 1992).

6. Applications of digested material

The recovery of anaerobically digested slaughter-house waste for agriculture conserves and recycles nu-trients and may reduce waste discharge and the use ofchemical fertilisers, but the safety of the material mustbe carefully evaluated before use (Marchaim et al., 1991;Shih, 1987, 1993). Anaerobic digestion reduces patho-gens and minimises odour, and nutrients remain mostlyin the digested material (Shih, 1987, 1993). On the otherhand, a major part of organic nitrogen is mineralisedinto ammonia, and any excess liquid rich in ammoniacan be either spread as slurry on farmland or treated in awastewater plant.

In a study by Salminen et al. (2001a), anaerobicallydigested solid poultry slaughterhouse waste was shownrich in nitrogen (ca. 20% N of TS) but potentially phy-totoxic. Fertilised with the material, carrots grew in 27-dplant growth assays almost as well as with a commercialmineral fertiliser used as reference (Salminen et al.,2001a), but the growth of Chinese cabbage was inhib-ited. In further 5-d phytotoxicity assays, probably or-ganic acids present in the digested material inhibited thegermination and root growth of ryegrass and Chinesecabbage. Organic acids are potential inhibitors of rootgrowth and may cause ion loss in roots (De Vlees-chauwer et al., 1981; Lee, 1977; Lynch, 1977, 1980;Manios et al., 1989; Marambe et al., 1993). The union-ised and ionised forms of ammonia, too, may affectplant growth (Hill et al., 1997; Sundradjat, 1990; Tiquiaand Tam, 1998; Wong et al., 1983).

Aerobic post-treatment of anaerobically digestedmaterial may greatly reduce its phytotoxicity, as inhib-itory compounds present in the material, including or-ganic acids and ammonia, may be readily degradedaerobically or volatilised during the treatment, as foundin a study of anaerobically digested solid poultryslaughterhouse waste (Salminen et al., 2001a). In addi-tion, aerobic post-treatment of digested materials mayenhance the physical and chemical properties of thematerial as well, though it may also result in a lossof nitrogen due to ammonia volatilisation (Marchaimet al., 1991; Sundradjat, 1990; Vermeulen et al., 1992).

Anaerobically digested materials may sometimes beused in animal feed, though legislation is restricting thisT

able

3

Anaerobic

co-digestionofsolidslaughterhouse

waste,

influentfeed

characteristics,andprocess

conditions

Reactor

Substrate

T(�C)

HRT(d)

Organic

loadingrate

Methane

References

CSTR,2m

3(1)Hogstomach

contents

(25vol%

,

67%

ofloading)co-treatm

entin

sewage

digester,(2)flotationtailings(25vol%

,

43%

ofloading)co-treatm

entin

municipaldigester

37

(1)17,(2)15

(1)2.9

kgTS/m

3d,

(2)1.5

kgTS/m

3d

(1)0.23m

3=k

gTS,

(2)0.32m

3=k

gTS

Rosenwinkel

and

Meyer

(1999)

CSTR,2�3700m

3Co-digestionofmanure,slaughterhouse

waste,

andcarcasses

Na

25

2.5

kgVS/m

3d

Na

Ling(1997)

CSTR,3l

Poultry

slaughterhouse

wastes,

andfoodpackingplantwastes

35

18

4.6

kgVS/m

3d

0.33m

3=k

gVS

Salm

inen

and

Rintala

(1999)

CSTR:continuouslystirredtankreactor,Na:notavailable.


practise. Studies of dried anaerobically digested poultrymanure used as a feed supplement for growing chicksshowed that 90–95% of the phosphorus in the material isusable, and no toxicity or negative effects were discov-ered when up to 10% of the material was added in ani-mal feed (Shih, 1993).

Blood and other high nitrogen-containing fractionsmay be used to produce VFA and ammonia, as pro-posed by Banks (1994). Because of ammonia’s highbuffering capacity, considerable amounts of VFA couldbe produced from blood before the pH dropped to alevel inhibitive of VFA production. Ammonia had to befirst precipitated and VFA extracted with solvents be-fore distillation (purification) could take place (Banks,1994).

7. Economics

Lack of economic sustainability has so far limited thefull-scale implementation of anaerobic digestion of solidwastes (Braber, 1995). The cost of anaerobic digestiondepends greatly on local circumstances, including con-struction and labour costs, treatment capacity, possi-bilities of energy recovery, energy prices, and taxes aswell as energy purchase tariffs, land price, markets, andprices of digested material. On the other hand, thequality of the digested material determines to a greatextent its marketability and price, while the local statusand cost of alternative technologies must be consideredas well. Though capital investment may be somewhathigher in an anaerobic digestion plant than in a com-posting plant (reviewed by Mata-Alvarez et al., 2000),anaerobic digestion offers the added potential for re-covering energy. Unlike in many other countries, elec-tricity is fairly inexpensive in Finland; nevertheless, theincreasing cost of landfilling and the energy tax on fossilfuels should encourage the exploitation of renewableenergy sources, thus making anaerobic digestion ahighly competitive alternative for the treatment of theabove wastes.

8. Final considerations

Anaerobic digestion technology is practicable for thetreatment of organic solid slaughterhouse waste tocombine material recovery and energy production. As-suming that the operation conditions can be optimisedand the process made economically sustainable, anaer-obic digestion is fully competitive with other treatmentoptions for the above wastes. However, since only ahandful of full-scale plants exist so far, the constructionand successful operation of full-scale demonstrationplants is essential for gaining confidence and experiencefor any comparison of treatment processes.

Acknowledgements

We thank the Academy of Finland for its financialsupport (Grant No. 38044).

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