Anaerobic digestion of organic solid poultry slaughterhouse waste – a review
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Anaerobic digestion of organic solid poultryslaughterhouse waste a review
E. Salminen 1, J. Rintala *
Department of Biological and Environmental Science, University of Jyvaaskylaa, P.O. Box 35, FIN-40351 Jyvaaskylaa, Finland
Accepted 23 October 2001
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
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 landlling (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; Hulsho Pol et al.,1997).
Little literature is available on the characteristics andquantication 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-
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) 1326
*Corresponding author. Tel.: +358-14-260-1211; fax: +358-14-260-
E-mail address: firstname.lastname@example.org. (J. Rintala).1 Present address: SCC Viatek Ltd., Piispanmaaentie 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 dier 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-ned as organic biodegradable waste with moisturecontent below 8590% (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 56 weeks to a weight of about1.81.9 kg before they are slaughtered. Their naturaldeath rate is about 23%, being highest during the rst 2weeks of their growth with bodies averaging in weightabout 1015 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 eciency. 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 ngers and usingpressurised water jets (Fig. 2) (Papinaho, 1996). Feathercontributes about 10% to the broilers live weight(Rinne, K., personal communication), while driedfeather contains 8599% 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-
Quantities and characteristics of organic solid wastes produced in poultry (broiler) farming and poultry slaughterhouses
(% of TS)
(% of TS)
(% of TS)
(% of TS)
(m3=kg wet weight)
Carcass 37c Na Na Na Na Na 0.200.25b ;c
Litter 5281h 6165h 3.25.7h Na Na 0.140.22h 0.100.15h
Manure 2047d ; i 6076d;i 4.66.7d;i Na 1.52.1e 0.20.3d ;f 0.040.06d;f
Feather 24.3g 96.7g 15g 91g 110a 0.2g 0.05g
Blood 22g 91g 7.6g 48g 2g 0.5g 0.10g
Oal, feet, and head 39g 95g 5.3g 32g 54g 0.70.9g 0.3g
Trimmings and bone 22.4g 68g 68.6g 51g 22g 0.60.7g 0.150.17g
Na: not available.a Bourne (1993).b Chen (1999).c Chen and Shyu (1998).dHuang and Shih (1981).eMackie et al. (1991).f Saey 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 dierent countries in 1997 (Finnish Food and
Drink Industries Federation, 2000).
14 E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 1326
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 otation tailings (Bull et al., 1982;Johns, 1995).
Poultry by-products and wastes may contain several100 dierent 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 ock 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 6080% 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 284030 to5234 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-
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) speciesthe 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; Tyooppoonen, P., personal communication).
E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 1326 15
disposal and processing of animal waste to destroy po-tential pathogens present in the waste. Animal wastemay be dened 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 classied 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; Rantajaarvi, P., personal communication).
Rendering refers to various heating processes toseparate fat from meat (Swan, 1992). Rendering at 133C 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 sh 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; Rantajaarvi, P., personal communication).
Incineration refers to technologies of thermal de-struction, apparently among the most eective methodsfor destroying potentially infectious agents (Ritter andChinside, 1995). Air-dried poultry litter is a provencombustible solid fuel with a gross caloric 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 landlling
Burial of dead birds on the farm is strictly controlledto avoid groundwater contamination. As the operation,monitoring, and control of landlling 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).
16 E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 1326
landlls must prevent or reduce as much as possibletheir adverse eects on the local environment, particu-larly the pollution of surface water, groundwater, soiland air, as well as on the global environment, includingthe greenhouse eect. All these measures increase thecosts of landlling. Furthermore, legislation is restrict-ing landlling of organic wastes but allowing biologi-cally treated material to be used as landll cover(Commission of the European Communities, 1999).
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,otation 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 lowbre 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 briey describe the metabolicpathways of anaerobic degradation of solid slaughter-house waste. The eects 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, briey, 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 dierent 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).
E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 1326 17
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 (Dolng,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. Eects 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 d1) (Angelidaki and Ahring, 1995, re-viewed by Hwu, 1997) and because the breakdown ofLCFAs requires low (ca. 103 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 oating scum (Salminen et al.,2001b), for oating LCFAs may aect their bioavail-ability and toxicity and cause common obstacles such asfouled gas collection pipes and scum overow (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 specic surface area of sludge withsuspended sludge being more vulnerable than granularsludge (Hwu et al., 1996). The carbon chain length andsaturation of LCFAs, too, aect the inhibition (Gal-braith et al., 1971; Komatsu et al., 1991; Koster andCramer, 1987; Rinzema, 1988), saturated LCFAs with1214 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 occulatingcapability 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. Eects 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 diuseacross the cell membrane (Kadam and Boone, 1996).
Reportedly, unionised ammonia inhibits methano-genesis at initial concentrations of ca. 0.11.1 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 eect, 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 S2 =l) may increase ammonia inhibition (4.6 gN/l),
18 E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 1326
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 buering 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 brous 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, 210 g/l)treatments increased its methane yield in the range of3751%, whereas thermal (70120 C, 5 min1 h),chemical (NaOH 210 g/l, 224 h), and enzymatictreatments were less eective in yielding methane, in-creasing in the range of 532%.
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 eective 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 9099% in a mesophilic di-gester, whereas thermophilic and mesophilic conditionsreduced the counts of excreta-born fungal spores by 99100% and 9498%, 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 Mareksdisease 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-
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
E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 1326 19
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 them4050 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. Saey 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 ofdierent poultry slaughterhouse by-products and wasteswere recently investigated in batch assays (Salminenet al., submitted). Poultry oal showed a high methaneyield, 0.70.9 m3 of methane/kg VSadded (Table 1), but itsproduction was considerably delayed due most likely toinhibition by LCFAs. Poultry blood, meat and bonetrimmings produced 0.50.7 m3 of methane/kg VSadded,respectively, while feather showed the lowest methaneyield of 0.21 m3 of methane/kg VSadded. Up to 0.67 m
3 ofmethane/kg VSadded was produced from a solid poultryslaughterhouse waste mixture (bone and trimmings,blood, oal, 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
Anaerobic digestion of solid slaughterhouse wastes and poultry manure and litter, inuent 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
Na 43 0.36 kg COD/m3 d 0.18 m3=kg COD Banks (1994)
CSTR, 2 l Solid slaughterhouse
35 50 0.8 kg VS/ m3 d 0.520.55 m3=kg VS Salminen et al.(2000)
Two phases, (1)
HFR, 4 l (2) CSTR,
1 l with zeolite
matrix, 20 g/l
Cattle blood and rumen
35 (1) solids 230,
liquid 2 (2) 210
3.6 kg TS/m3 d 0.27 m3=kg TS Banks and Wang
CSTR, batch, 12 l Sheep tallow 35, 55 Na 520 g/l tallow
(2.84 g COD/g)
Na Broughton et al.
Two phases, (1) LB,
3 or 10 l (2) UASB,
2.35 or 3 l
Poultry mortalities 35, 55 Na (1) 2279 g (2)
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 signicant for the performanceof the process. At a loading of 1.02.1 kg VS/m3 d and aHRT of 12.525 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 aecting 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 diculties 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 nallydegraded 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 rst phase of the process, hydrolysis was ap-parently enhanced owing to the hydraulic ush, 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.
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 otation 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 otation 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 of57.5 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;
E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 1326 21
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 aectplant 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
22 E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 1326
practise. Studies of dried anaerobically digested poultrymanure used as a feed supplement for growing chicksshowed that 9095% of the phosphorus in the material isusable, and no toxicity or negative eects 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 ammonias highbuering capacity, considerable amounts of VFA couldbe produced from blood before the pH dropped to alevel inhibitive of VFA production. Ammonia had to berst precipitated and VFA extracted with solvents be-fore distillation (purication) could take place (Banks,1994).
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 taris, 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 oers the added potential for re-covering energy. Unlike in many other countries, elec-tricity is fairly inexpensive in Finland; nevertheless, theincreasing cost of landlling 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 condence and experiencefor any comparison of treatment processes.
We thank the Academy of Finland for its nancialsupport (Grant No. 38044).
Angelidaki, I., Ahring, B.K., 1992. Eect of free long-chain fatty acids
on thermophilic anaerobic digestion. Appl. Microbiol. Biotechnol.
Angelidaki, I., Ahring, B.K., 1993. Thermophilic anaerobic digestion
of livestock waste: eect of ammonia. Appl. Microbiol. Biotechnol.
Angelidaki, I., Ahring, B.K., 1995. Establishment and characteriza-
tion of an anaerobic thermophilic (55 C) enrichment culturedegrading long-chain fatty acids. Appl. Environ. Microbiol. 61,
Angelidaki, I., Petersen, S.P., Ahring, B.K., 1990. Eects of lipids on
thermophilic anaerobic digestion and reduction of lipid inhibition
upon addition of bentonite. Appl. Microbiol. Biotechnol. 33, 469
Banks, C.J., 1994. Anaerobic digestion of solid and high nitrogen
content fractions of slaughterhouse wastes. Environmentally
Responsible Food Processing, AlChE Symp. Ser. 90, 4855.
Banks, C.J., Wang, Z., 1999. Development of a two phase anaerobic
digester for the treatment of mixed abattoir wastes. Water Sci.
Technol. 40 (1), 6776.
Barik, S., Forgacs, T., Isbister, J., 1991. Bioconversion of chicken
wastes to value-added products. Bioresour. Technol. 36, 229234.
Black, M.G., Brown, J.M., Kaye, E., 1974. Operational experiences
with an abattoir waste digestion plant at Leeds. Water Pollut.
Control 7 (5), 532537.
Borja, R., Banks, C.J., 1994. Performance and kinetics of an upow
anaerobic sludge planket (UASB) reactor treating slaughterhouse
wastewater. J. Environ. Sci. Health A 29, 20632085.
Borja, R., Banks, C.J., Maartin, A., 1995a. Inuence of the organicvolumetric loading rate on soluble chemical oxygen demand
removal in a down-ow xed bed reactor treating abattoir
wastewater. J. Chem Tech. Biotechnol. 64, 361366.
Borja, R., Banks, C.J., Wang, Z., 1995b. Performance of a hybrid
anaerobic reactor, combining a sludge blanket and a lter, treating
slaughterhouse wastewater. Appl. Microbiol. Biotechnol. 43, 351
Borja, R., Banks, C.J., Wang, Z., 1995c. Kinetic evaluation of an
anaerobic uidised-bed reactor treating slaughterhouse wastewater.
Bioresour. Technol. 52, 163167.
Borja, R., Banks, C.J., Wang, Z., 1995d. Eect of organic loading rate
on anaerobic treatment of slaughterhouse wastewater in a uidised-
bed reactor. Bioresour. Technol. 52, 157162.
Borja, R., Banks, C.J., Wang, Z., Mancha, A., 1998. Anaerobic
digestion of slaughterhouse wastewater using a combination sludge
blanket and lter arrangement in a single reactor. Bioresour.
Technol. 65, 125133.
Bourne, T.F., 1993. Biodegradation of keratins and phenolic com-
pounds. Ph.D. Thesis, Georgia Institute of Technology.
Braber, K., 1995. Anaerobic digestion of municipal solid waste: a
modern waste disposal option on the verge of breakthrough.
Biomass Bioenergy 9, 365376.
Brinkman, J., 1999. Anaerobic digestion of mixed waste slurries from
kitchens, slaughterhouses and meat processing industries. In:
Mata-Alvarez, J., Tilche, A., Cecchi, F. (Eds.), Proceedings of
the Second International Symposium on Anaerobic Digestion of
Solid Wastes, Barcelona, vol. 1, pp. 190195.
Broughton, M.J., Thiele, J.H., Birch, E.J., Cohen, A., 1998. Anaerobic
batch digestion of sheep tallow. Water Res. 32, 14231428.
E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 1326 23
Bull, M.A., Sterritt, R.M., Lester, J.N., 1982. The treatment of
wastewater from the meat industry: a review. Environ. Technol.
Lett. 3, 117126.
Chen, T.C., 1992. Poultry meat microbiology. In: Hui, Y.H. (Ed.),
Encyclopedia Food Science Technol., vol. 4, pp. 21402145.
Chen, T.-H., 1999. Anaerobic treatment of poultry mortalities. In:
Mata-Alvarez, J., Tilche, A., Cecchi, F. (Eds.), Proceedings of the
Second International Symposium on Anaerobic Digestion of Solid
Wastes, Barcelona, vol. 2, pp. 6972.
Chen, T.-H., Shyu, W.-H., 1998. Chemical characterization of anaer-
obic digestion treatment of poultry mortalities. Bioresour. Technol.
Commission of the European Communities, 1990. Council Directive
90/667/EEC. Ocial journal, No. L 363, 27.12.1990, p. 51.
Commission of the European Communities, 1992. Commission
Decision 92/562/EEC. Ocial journal, No. L 359, 9.12.1992,
Commission of the European Communities, 1999. Council Directive
1999/31/EC. Ocial Journal, No. L 182, 16.7.1999, pp. 19.
Commission of the European Communities, 2000. White paper on
food safety (presented by the Commission). Ocial Journal, No. C
076, 11.3.1997, pp. 14.
Cooper, R.N., Russel, J.M., 1992. Meat industry processing wastes:
characteristics and treatment. In: Hui, Y.H. (Ed.), Encyclopedia
Food Science Technology, vol. 3, pp. 16831690.
Dagnall, S.P., 1993. Poultry litter as a fuel in the UK. CADDET
Renewable Energy Newsletter 7, 2830.
Danish Institute of Agricultural and Fisheries Economics, 1999.
Centralised biogas plants integrated energy production, waste
treatment and nutrient redistribution facilities.
DeBaere, L.A., Devocht, M., van Assche, P., 1984. Inuence of high
NaCl and NH4Cl salt levels on methanogenic associations. Water
Res. 18, 543548.
DeBaere, L., 2000. Anaerobic digestion of solid waste: state-of the art.
Water Sci. Technol. 41 (3), 283290.
DeBertoldi, M., Vallini, G., Pera, A., 1983. The biology of compo-
sting: a review. Waste Manag. Res. 1, 157176.
De Vleeschauwer, D., Verdonck, O., Van Assche, P., 1981. Phytotox-
icity of refuse compost. BioCycle 22, 4446.
Dolng, J., 1988. Acetogenesis. In: Zehnder, J.B. (Ed.), Biology of
Anaerobic Microorganisms. Wiley, New York, pp. 417468.
El Boushy, A.R., van der Poel, A.F.B., 1990. Feather meal a
biological waste: its processing and utilization as a feedstu for
poultry. Biol. Wastes 32, 3974.
Finnish Food and Drink Industries Federation, 1999. In: Haar-
ukkapaloja elintarviketeollisuudesta (in Finnish).
Friedrich, A.B., Antranikian, G., 1996. Keratin degradation by
Fervidobacterium pennavorans, a novel thermophilic anaerobic
species of the order Thermotogales. Appl. Environ. Microbiol. 62,
Galbraith, H., Miller, T.B., Paton, A.M., Thompson, J.K., 1971.
Antibacterial activity of long chain fatty acids and the reversal with
calcium, magnesium, ergocalciferol and cholesterol. J. Appl.
Bacteriol. 34, 803813.
Haapapuro, E.R., Barnard, N.D., Simon, M., 1997. Review-Animal
waste used as livestock feed: danger to human health. Prev. Med.
Hanaki, K., Matsuo, T., Nagase, M., 1981. Mechanism of inhibition
caused by long-chain fatty acids in anaerobic digestion process.
Biotechnol. Bioeng. 23, 15911610.
Hansen, K.H., Angelidaki, I., Ahring, B.K., 1998. Anaerobic digestion
of swine manure: inhibition by ammonia. Water Res. 32, 512.
Hansen, K.H., Angelidaki, I., Ahring, B.K., 1999. Improving therm-
ophilic anaerobic digestion of swine manure. Water Res. 33, 1805
Hashimoto, A.G., 1986. Ammonia inhibition of methanogenesis from
cattle wastes. Agric. Wastes 17, 241261.
Harper, S.R., Ross, C.C., Valentine, G.E., 1987. Feasibility of packed-
bed anaerobic treatment of poultry processing wastewater. In: Bell,
J.M. (Ed.), Proceedings of the Fortysecond Industrial Waste
Conference, West Lafayette, Indiana, pp. 657671.
Harper, S.R., Ross, C.C., Valentine, G.E., Pohland, F.G., 1990.
Pretreatment of poultry processing wastewater in a pilot-scale
anaerobic lter. Water Sci. Technol. 22 (9), 916.
Hill, D.T., Payne, V.W.E., Rogers, J.W., Kown, S.R., 1997. Ammonia
eects on the biomass production of ve constructed wetland plant
species. Bioresour. Technol. 62, 109113.
Hobson, P.N., Wheatley, A.D., 1988. Anaerobic Digestion: Modern
Theory and Practice. Elsevier, London.
Huang, J.J.H., Shih, J.C.H., 1981. The potential of biological methane
generation from chicken manure. Biotechnol. Bioeng. 23, 2307
Hulsho Pol, L.H., Euler, H., Eitner, A., Gronganz, D., 1997. GTZ
sectorial project, promotion of anaerobic technology for the
treatment of municipal and industrial sewage and wastes. In:
Proceedings of the 8th International Conference on Anaerobic
Digestion, Sendai, vol. 2, pp. 285292.
Hunik, J.H., Hamelers, H.V.M., Koster, I.W., 1990. Growth-rate
inhibition of acetoclastic methanogens by ammonia and pH in
poultry manure digestion. Biol. Wastes 32, 285297.
Hwu, C.-S., 1997. Enhancing anaerobic treatment of wastewaters
containing oleic acid. Ph.D. Thesis, Wageningen Agricultural
Hwu, C.-S., Donlon, B., Lettinga, G., 1996. Comparative toxicity of
long-chain fatty acid to anaerobic sludges from various origins.
Water Sci. Technol. 34 (56), 351358.
Hwu, C.-S., Tseng, S.-K., Yuan, C.-Y., Kulik, Z., Lettinga, G., 1998.
Biosorption of long-chain fatty acids in UASB treatment process.
Water Res. 32, 15711579.
Johns, M.R., 1995. Developments in wastewater treatment in the meat
processing industry: a review. Bioresour. Technol. 54, 203216.
Kadam, P.C., Boone, D.R., 1996. Inuence of pH on ammonia
accumulation and toxicity in halophilic, methylotrophic methano-
gens. Appl. Environ. Microbiol. 62, 44864492.
Kim, S.-H., 1995. The removal of high strength ammonia in
anaerobically treated egg and chicken processing wastewater by
precipitation. J. KSEE 17, 615623.
Komatsu, T., Hanaki, K., Matsuo, T., 1991. Prevention of lipid
inhibition in anaerobic processes by introducing a two-phase
system. Water Sci. Technol. 23 (79), 11891200.
Koster, I.W., 1986. Characteristics of the pH-inuenced adaptation of
methanogenic sludge to ammonium toxicity. J. Chem. Technol.
Biotechnol. 36, 445455.
Koster, I.W., 1989. Toxicity in anaerobic digestion with emphasis on
the eect of ammonia, sulde and long-chain fatty acids on
methanogenesis. Ph.D. Thesis, Wageningen Agricultural Univer-
Koster, I.W., Cramer, A., 1987. Inhibition of methanogenesis from
acetate in granular sludge by long-chain fatty acids. Appl. Environ.
Microbiol. 53, 403409.
Koster, I.W., Lettinga, G., 1988. Anaerobic digestion at extreme
ammonia concentrations. Biol. Wastes 25, 5159.
Krylova, N.I., Khabiboulline, R.E., Naumova, R.P., Nagel, M.A.,
1997. The inuence of ammonium and methods for removal during
the anaerobic treatment of poultry manure. J. Chem. Technol.
Biotechnol. 70, 99105.
Kun, M.L., Brunner, J.B.F., Atal, E.E., 1989. Destruction of enteric
bacteria and viruses during two-phase digestion. J. Water Pollut.
Control Fed. 61, 14211429.
Lee, R.B., 1977. Eects of organic acids on the loss of ions from barley
roots. J. Exp. Botany 28, 1729.
Liao, P.H., Chen, A., Lo, K.V., 1995. Removal of nitrogen from swine
manure wastewater by ammonia stripping. Bioresour. Technol. 54,
24 E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 1326
Ling, D.T., 1997. A concept for processing carcass together with
energy production. In: Proceedings of the 8th International
Conference on Anaerobic Digestion, Sendai, vol. 3, pp. 436439.
Lynch, J.M., 1977. Phytotoxicity of acetic acid produced in the
anaerobic decomposition of wheat straw. J. Appl. Bacteriol. 42,
Lynch, J.M., 1980. Eects of organic acids on the germination of seeds
and growth of seedlings. Plant Cell Environ. 3, 255259.
Macaulay, M.N., Stebor, T.W., Berndt, C.L., 1987. Anaerobic contact
pretreatment of slaughterhouse wastewater. In: Bell, J.M. (Ed.),
Proceedings of the Fortysecond Industrial Waste Conference, West
Mackie, R.I., White, B.A., Bryant, M.P., 1991. Lipid metabolism in
anaerobic ecosystems. Crit. Rev. Microbiol. 17, 449478.
Maekawa, T., Liao, C.-M., Feng, X.-D., 1995. Nitrogen and
phosphorus removal from swine wastewater using intermittent
aeration batch reactor followed by ammonium crystallization
process. Water Res. 29, 26432650.
Manios, V.I., Tsikalas, P.E., Siminis, H.I., 1989. Phytotoxicity of olive
tree leaf compost in relation to the organic acid concentration.
Biol. Wastes 27, 307317.
Marambe, B., Nagaoka, T., Ando, T., 1993. Identication and
biological activity of germination-inhibiting long-chain fatty acids
in animal-waste composts. Plant Cell Physiol. 34, 605612.
Marchaim,U., Levanon,D., Danai, O.,Musaphy, S., 1991. A suggested
solution for slaughterhouse wastes: uses of the residual materials
after anaerobic digestion. Bioresour. Technol. 37, 127134.
Mata-Alvarez, J., Macee, S., Llabrees, P., 2000. Anaerobic digestion of
organic solid wastes. An overview of research achievements and
perspectives. Bioresour. Technol. 74, 316.
McCarty, P.L., McKinney, R.E., 1961. Salt toxicity in anaerobic
digestion. J. Water Pollut. Control Fed. 33, 399415.
McInerney, M.J., 1988. Anaerobic hydrolysis and fermentation of fats
and proteins. In: Zehnder, J.B. (Ed.), Biology of Anaerobic
Microorganisms. Wiley, New York, pp. 373415.
Melbinger, N.R., Donnellon, J., 1971. Toxic eects of ammonia
nitrogen in high-rate digestion. J. Water Pollut. Control Fed. 43,
Ministry of Agriculture and Forestry, 2000. Control of foodstus of
animal origin. Veterinary and food department.
Nieman, C., 1954. Inuence of trace amounts of fatty acids on the
growth of microorganisms. Bact. Rev. 18, 147163.
Nicholson, F.A., Chambers, B.J., Williams, J.R., Unwin, R.J., 1999.
Heavy metal contents of livestock feeds and animal manures in
England and Wales. Bioresour. Technol. 70, 2331.
Novak, J.T., Carlson, D.A., 1970. The kinetics of anaerobic long chain
fatty acid degradation. J. Water Pollut. Control Fed. 42, 19321943.
Onifade, A.A., Al-Sane, N.A., Al-Musallam, A.A., Al-Zarban, S.,
1998. A review: Potentials for biotechnological applications of
keratin-degrading microorganisms and their enzymes for nutri-
tional improvement of feathers and other keratins as livestock feed
resource. Bioresour. Technol. 66, 111.
Pagilla, K.R., Crany, K.C., Kido, W.H., 1997. Causes and eects of
foaming in anaerobic sludge digesters. In: Proceedings of the 8th
International Conference on Anaerobic Digestion, Sendai, vol. 2,
Papadopoulos, M.C., 1985. Processed chicken feathers as feedstu for
poultry and swine. A review. Agric. Wastes 14, 275290.
Papinaho, P.A., 1996. Physiological and processing factors aecting
broiler Musculus pectoralis shear vales and tenderness. Ph.D.
Thesis, Department of Food Technology, University of Helsinki.
Parkin, G.F., Speece, R.E., Yang, C.H.J., Kocher, W.M., 1983.
Responce of methane fermentation systems to industrial toxicants.
J. Water Pollut. Control Fed. 55, 4453.
Pavlostathis, S.G., Giraldo-Gomez, E., 1991. Kinetics of anaerobic
treatment: a critical review. Crit. Rev. Environ. Control 21, 411
Pechan, Z., Knappova, O., Petrovicova, B., Adamec, O., 1987.
Anaerobic digestion of poultry manure at high ammonium
nitrogen concentrations. Biol. Wastes 20, 117131.
Pozo del, R., Diez, V., Beltraan, S., 2000. Anaerobic pre-treatment of
slaughterhouse wastewater using xed-lm reactors. Bioresour.
Technol. 71, 143149.
Pulsa, A., 1996. Turkistarhat tarvitsevat laadukasta teurasjaatettaa.
Lihalehti 3, 3841, in Finnish.
Rinzema, A., 1988. Anaerobic treatment of wastewater with high
concentrations of lipids or sulfate. Ph.D. Thesis, Wageningen
Rinzema, A., Boone, M., van Knippenberg, K., Lettinga, G., 1994.
Bactericidal eect of long chain fatty acids in anaerobic digestion.
Water Environ. Res. 66, 4049.
Ritter, W.F., Chinside, A.E.M., 1995. Impact of dead bird disposal
pits on groundwater quality on the Delmarva Peninsula. Bioresour.
Technol. 53, 105111.
Rosenwinkel, K.-H., Meyer, H., 1999. Anaerobic treatment of
slaughterhouse residues in municipal digesters. Water Sci. Technol.
40 (1), 101111.
Roy, F., Albagnac, G., Samain, E., 1985. Inuence of calcium
addition on growth of highly puried syntrophic cultures degrad-
ing long-chain fatty acids. Appl. Environ. Microbiol. 49, 702
Saey Jr., L.M., Vetter, R.L., Smith, D., 1987. Operating a full-scale
poultry manure anaerobic digester. Biol. Wastes 19, 7990.
Salminen, E.A., Rintala, J.A., 1999. Anaerobic digestion of poultry
slaughtering wastes. Environ. Technol. 20, 2128.
Salminen, E., Rintala, J., Lokshina, L.Ya., Vavilin, V.A., 2000.
Anaerobic batch degradation of solid poultry slaughterhouse
waste. Water Sci. Technol. 41 (3), 3341.
Salminen, E., Rintala, J., Haarkoonen, J., Kuitunen, M., Hoogmander,
H., Oikari, A., 2001a. Anaerobically digested solid poultry
slaughterhouse wastes to be used as fertiliser on agricultural soil.
Bioresour. Technol. 78, 8188.
Salminen, E., Einola, J., Rintala, J., 2001b. Characterisation and
anaerobic batch degradation of materials accumulating in anaer-
obic digesters treating poultry slaughterhouse waste. Environ.
Technol. 22, 577585.
Salminen, E., Rintala, J., Semi-continuous anaerobic digestion of solid
poultry slaughterhouse waste: eect of hydraulic retention time and
loading. Water Res. (submitted).
Salminen, E., Einola, J., Rintala, J., The methane production of
poultry slaughtering residues and eects of pre-treatments on the
methane production of poultry feather. J. Chem. Technol.
Sayed, S., De Zeeuw, W., 1988. The performance of a continuously
operated occulent sludge UASB reactor with slaughterhouse
wastewater. Biol. Wastes 24, 199212.
Sayed, S., De Zeeuw, W., Lettinga, G., 1984. Anaerobic treatment of
slaughterhouse waste using a occulant sludge UASB reactor.
Agric. Wastes 11, 197226.
Sayed, S., Van Campen, L., Lettinga, G., 1987. Anaerobic treatment of
slaughterhouse waste using a granular sludge UASB reactor. Biol.
Wastes 21, 1128.
Senesi, N., 1989. Composted materials as organic fertilizers. Sci. Total
Environ. 81/82, 521542.
Shai, B., 1992. Poultry processing and product technology. In: Hui,
Y.H. (Ed.), Encyclopedia Food Science Technology, vol. 4, pp.
Shih, J.C.H., 1987. Ecological benets of anaerobic digestion. Poultry
Sci. 66, 946950.
Shih, J.C.H., 1993. Recent development in poultry waste digestion and
feather utilization a review. Poultry Sci. 72, 16171620.
Shore, L.S., Harel-Markowitz, E., Gurevich, M., Shemesh, M., 1993.
Factors aecting the concentration of testosterone in poultry litter.
J. Environ. Sci. Health A 28 (8), 17371749.
E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 1326 25
Steinberger, S.C., Shih, J.C.H., 1984. The construction and operation of
a low-cost poultry waste digester. Biotechnol. Bioeng. 26, 537543.
Sudradjat, R., 1990. Transformations and uses of digested solid
organic residues. Ph.D. Thesis, Rijksuniversiteit Gent.
Swan, J.E., 1992. Animal by-product processing. In: Hui, Y.H. (Ed.),
Encyclopedia Food Science Technology, vol. 4, pp. 4249.
Tiquia, S.M., Tam, N.F.Y., 1998. Elimination of phytotoxicity during
co-composting of spent pig-manure sawdust litter and pig sludge.
Bioresour. Technol. 65, 4349.
Tritt, W.P., 1992. The anaerobic treatment of slaughterhouse waste-
water in xed-bed reactors. Bioresour. Technol. 41, 201207.
Tritt, W.P., Schuchardt, F., 1992. Materials ow and possibilities of
treating liquid and solid wastes from slaughterhouses in Germany.
A review. Bioresour. Technol. 41, 235245.
Turner, C., Burton, C.H., 1997. The inactivation of viruses in pig
slurries: a review. Bioresour. Technol. 61, 920.
Vermeulen, J., Huysmans, A., Crespo, M., van Lierde, A., de Rycke,
A., Verstraete, W., 1992. Processing of biowaste by anaerobic
composting to plant growth substrates. In: Proceedings of the
International Symposium on Anaerobic Digestion of Solid Waste,
Venice, pp. 147157.
Vogels, G.D., Keltjens, J.T., Van der Drift, C., 1988. Biochemistry of
methane production. In: Zehnder, J.B. (Ed.), Biology of Anaerobic
Microorganisms. Wiley, New York, pp. 707770.
Webb, A.R., Hawkes, F.R., 1985a. Laboratory scale anaerobic
digestion of poultry litter: gas yield-loading rate relationship.
Agric. Wastes 13, 3149.
Webb, A.R., Hawkes, F.R., 1985b. The anaerobic digestion of poultry
manure: variation of gas yield with inuent concentration and
ammoniumnitrogen levels. Agric. Wastes 14, 135156.
Widdel, F., 1988. Microbiology and ecology of sulfate- and sulfur-
reducing bacteria. In: Zehnder, J.B. (Ed.), Biology of Anaerobic
Microorganisms. Wiley, New York, pp. 469585.
Wiegant, W.M., Zeeman, G., 1986. The mechanism of ammonia
inhibition in the thermophilic digestion of livestock wastes. Agric.
Wastes 16, 243253.
Williams, C.M., Shih, J.C.H., 1989. Enumeration of some microbial
groups on thermophilic poultry waste digesters and enrichment of a
feather-degrading culture. J. Appl. Bacteriol. 67, 2535.
Williams, C.M., Richter, C.S., MacKenzie Jr., J.M., Shih, J.C.H.,
1990. Isolation, identication, and characterization of a feather-
degrading bacterium. Appl. Environ. Microbiol. 56, 15091515.
Wong, M.H., Cheung, Y.H., Cheung, C.L., 1983. The eect of
ammonia and ethylene oxide in animal manure and sewage sludge
on the seed germination and root elongation of Brassica parachin-
ensis. Environ. Pollut. A 30, 109123.
Zinder, S.H., 1984. Microbiology of anaerobic conversion of organic
wastes to methane: recent developments. ASM News 50, 294298.
26 E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 1326