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Bioresource Technology 83 (2002) 1326

Review paper

Anaerobic digestion of organic solid poultry slaughterhouse waste a review

E. Salminen 1, J. Rintala
Accepted 23 October 2001

Department of Biological and Environmental Science, University of Jyv askyl a, P.O. Box 35, FIN-40351 Jyv askyl a, Finland

Abstract This work reviews the potential of anaerobic digestion for material recovery and energy production from poultry slaughtering byproducts 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 in Finland and in many other countries has been on the increase, reaching about 10 kg per capita in Finland in 1999 and even more elsewhere (Finnish Food and Drink Industries Federation, 1999, Fig. 1). As a result of the growing poultry industry, poultry slaughterhouses are producing increasing amounts of organic solid by-products and wastes. On the other hand, legislation on the recovery of organic materials for animal feed is becoming tighter (Commission of the European Communities, 2000) and more restrictive of their landlling (Commission of the European Communities, 1999). In this regard, anaerobic digestion is a promising alternative for the treatment of these materials, as the process combines material recovery and energy production (DeBaere, 2000; Hulsho Pol et al., 1997). Little literature is available on the characteristics and quantication of organic solid by-products and wastes from poultry slaughterhouses, though such information is needed to evaluate treatment options for these mateCorresponding author. Tel.: +358-14-260-1211; fax: +358-14-2602321. E-mail address: jukka.rintala@cc.jyu. (J. Rintala). 1 Present address: SCC Viatek Ltd., Piispanm aentie 5, P.O. Box 3, FIN-02241 Espoo, Finland.

rials. Bull et al. (1982), Cooper and Russel (1992), and Johns (1995) have reviewed the characteristics and treatment of wastewater in slaughterhouses, whereas Tritt and Schuchardt (1992) present the most recent summary on the characteristics and treatment of solid waste and wastewater streams from cattle and pig slaughtering. The objective of the present study was to review relevant information necessary to determine the applicability of anaerobic digestion to energy production and material recovery from poultry slaughterhouse wastes. Accordingly, we will describe and quantify organic solid by-products and wastes produced in poultry farming and poultry slaughterhouses and discuss their recovery and disposal options. We will also review certain aspects of anaerobic digestion considered essential in digesting solid slaughterhouse wastes. In addition, we present an overview of experience with anaerobic digestion treatment of these materials.

2. Quantities and characteristics of organic solid byproducts and wastes from poultry farming and slaughtering In this section, we quantify and characterise organic solid by-products and wastes produced in broiler farming and slaughtering (Table 1). Broiler was chosen as an example because of its importance among all poultry

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E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 1326

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).

products. The slaughtering of broilers does not essentially dier from the slaughtering of other poultry species, though the amount of by-products and wastes does depend on the species. Organic solid waste may be dened as organic biodegradable waste with moisture content below 8590% (Mata-Alvarez et al., 2000). Litter, i.e., excreta and peat or wood chip, is produced at about 2 kg/broiler in deep litter broiler growing facilities where the birds are allowed to roam freely (Saksala, T., personal communication), and it may vary considerably in its characteristics (Table 1) depending on how long it remains on the ground (Webb and Hawkes, 1985a). Its nitrogen content generally increases

with increasing poultry manure deposits, but uric acid may degrade to ammonia and then volatilise from the litter (Webb and Hawkes, 1985a). In comparison, caged poultry produce only manure (Table 1). Broilers are grown for 56 weeks to a weight of about 1.81.9 kg before they are slaughtered. Their natural death rate is about 23%, being highest during the rst 2 weeks of their growth with bodies averaging in weight about 1015 g/broiler (Saksala, T., personal communication). Breeding produces waste which contains peat, eggshells, stillborn, unborn, and dead birds. In slaughterhouses the excreta from vehicles, crates, and cages are usually washed into the sewer. In the past few decades, poultry slaughtering has markedly changed as the industry has sought to improve its processing eciency. Today broilers are often processed in highly automated purpose-designed plants, which typically slaughter and process tens of thousands of birds per day. In these plants, broilers are removed from crates and cages, hung from shackles (Papinaho, 1996), electrically stunned, and then bled (Fig. 2). Blood accounts for about 2% of the live weight of a broiler, about 40 g/broiler (Rinne, K., personal communication), whereas dried blood contains about 95% protein (Table 1) (Cooper and Russel, 1992). After bleeding and to ease feather removal, broilers are scalded by immersing them in hot water (Fig. 2) (Papinaho, 1996). Feather removal may be performed by rubbing the scalded carcass with rotating rubber ngers and using pressurised water jets (Fig. 2) (Papinaho, 1996). Feather contributes about 10% to the broilers live weight (Rinne, K., personal communication), while dried feather contains 8599% proteins (Table 1) (Papadopoulos, 1985). Subsequent evisceration produces, in percentage 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 (%) Carcass Litter Manure Feather Blood Oal, feet, and head Trimmings and bone 37c 5281h 2047d ; i 24.3g 22g 39g 22.4g VS (% of TS) Na 6165h 6076d;i 96.7g 91g 95g 68g Kjeldahl-N (% of TS) Na 3.25.7h 4.66.7d;i 15g 7.6g 5.3g 68.6g Protein (% of TS) Na Na Na 91g 48g 32g 51g Lipids (% of TS) Na Na 1.52.1e 110a 2g 54g 22g Methane potential (m3 =kg VSadded ) Na 0.140.22h 0.20.3d ; f 0.2g 0.5g 0.70.9g 0.60.7g Methane potential (m3 =kg wet weight) 0.200.25b ; c 0.100.15h 0.040.06d;f 0.05g 0.10g 0.3g 0.150.17g

Na: not available. a Bourne (1993). b Chen (1999). c Chen and Shyu (1998). d Huang and Shih (1981). e Mackie et al. (1991). f Saey et al. (1987). g Salminen et al. (submitted). h Webb and Hawkes (1985a). i Webb and Hawkes (1985b).

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Fig. 2. Organic solid materials (per broiler) produced in broiler farming and slaughtering (Papinaho, 1996; Rinne, K., personal communication; ppo nen, P., personal communication). Saksala, T., personal communication; adapted from Shai, 1992; Tyo

cation, Table 1, Fig. 2). After slaughtering, the broiler weighs an average of 1.4 kg (Rinne, K., personal communication), and the carcasses are chilled upon evisceration to control microbial growth. Further processing produces trimmings and bones in varying amounts, depending on practices and processes and the degree of processing, about 140 g in live weight (Rinne, K., personal communication). Poultry slaughterhouses produce also a variety of spoiled meat and condemned materials, and their wastewater treatment yields wastes such as screenings, fat from grease traps, settlings, excess activated sludge, and otation tailings (Bull et al., 1982; Johns, 1995). Poultry by-products and wastes may contain several 100 dierent species of micro-organisms in contaminated feather, feet, intestinal contents, and processing equipment, including potential pathogens such as Salmonella sp., Staphylococcus sp., and Clostridium sp. (Chen, 1992). Compared to many other countries, Finnish meat products contain considerably less pathogens (Ministry of Agriculture and Forestry, 2000). For example, in 1997, positive Salmonella samples in broiler and turkey meat in slaughtered ock and meat from cutting plants rated 0.6% and 3.1%, respectively (Ministry of Agriculture and Forestry, 2000). In comparison, in the US, about 30% of chicken products are contaminated with live Salmonella, and 6080% of chickens 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 nutritional and pharmaceutical purposes (Haapapuro et al., 1997). Veterinary drugs and other chemical contaminants are also present in poultry in varying concentrations; e.g., zinc and copper concentrations in poultry feeds in England and Wales range from 284030 to 5234 mg/kg TS, respectively, whereas zinc and copper concentrations 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 varying 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 slaughterhouses This section reviews the current recovery and disposal practices and requirements for organic solid wastes produced in poultry farming and poultry slaughterhouses (Fig. 3). Council Directive 90/667/EEC (Commission of the European Communities, 1990) species the animal and public health requirements for the


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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).

disposal and processing of animal waste to destroy potential pathogens present in the waste. Animal waste may be dened as carcasses or parts of animals, including products of animal origin not intended for direct human consumption (Commission of the European Communities, 1990). Animal waste is classied either as high-risk material, if it is suspected to present serious health risks to people or animals, or as low-risk material, if it does not. High-risk material includes animals died on the farm, stillborn and unborn animals, and spoiled and condemned materials. The Commission is currently working on a new Directive for health rules concerning animal by-products not intended for human consumption (Commission of the European Communities, 2000; Rantaj arvi, P., personal communication). 3.1. Rendering Rendering refers to various heating processes to separate fat from meat (Swan, 1992). Rendering at 133 C for a minimum of 20 min at 3 bars (Commission of the European Communities, 1990) or an alternative heat treatment (Commission of the European Communities, 1992) is needed for high-risk materials intended for animal feed or as an intermediate product for the manufacture of organic fertiliser or other derived products. Rendering produces meat-bone-meal, which may be used in animal feed or as fertiliser or be further processed via anaerobic digestion or composting. In addition, rendering produces fat, which may be used for animal feed, in chemical industry products, or burned as fuel. 3.2. Use for animal feed As rich sources of protein and vitamins, slaughterhouse by-products are preserved with formic acid and used as animal feed either as such or together with

regular feed, e.g. in Finland, for fur animals or for pet food production (Pulsa, 1996). As one among the biggest fur animal producers in the world, Finland uses an annual 370 million kg of fur animal feed, more than half of 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-treated feather is sometimes used in animal feed (El Boushy and van der Poel, 1990; Onifade et al., 1998; Papadopoulos, 1985). Legislation, however, is becoming stringent about the use of slaughter by-products for animal feed to reduce the risk of disease transmission via the feed and the food chain (Commission of the European Communities, 2000; Rantaj arvi, P., personal communication). 3.3. Incineration Incineration refers to technologies of thermal destruction, apparently among the most eective methods for destroying potentially infectious agents (Ritter and Chinside, 1995). Air-dried poultry litter is a proven combustible solid fuel with a gross caloric value of about 13.5 GJ per tonne, about half that of coal (Dagnall, 1993), whereas materials having a high moisture content have little or no energy value. In incineration, the air emission, process conditions, and the disposal of solid and liquid residues need to be strictly controlled. The Commission of the European Communities is currently preparing a new Directive on waste incineration. 3.4. Burial and controlled landlling Burial of dead birds on the farm is strictly controlled to avoid groundwater contamination. As the operation, monitoring, and control of landlling have also become more tightly regulated under Directive 1999/31/EC (Commission of the European Communities, 1999),

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landlls must prevent or reduce as much as possible their adverse eects on the local environment, particularly the pollution of surface water, groundwater, soil and air, as well as on the global environment, including the greenhouse eect. All these measures increase the costs of landlling. Furthermore, legislation is restricting landlling of organic wastes but allowing biologically treated material to be used as landll cover (Commission of the European Communities, 1999). 3.5. Composting Composting, an aerobic biological process to decompose organic material, is carried out in either windrows or reactors. It is a common method to treat poultry slaughterhouse wastes, including screenings, otation tailings, grease trap residues, manure, litter, and sometimes also feather. Composting reduces pathogens, and composted material may be used as soil conditioner or fertiliser (DeBertoldi et al., 1983; Senesi, 1989). However, wastes with a high moisture and low bre content need considerable amounts of moisturesorbing and structural support to compost well (Tritt and Schuchardt, 1992). In addition, emission to air, water, and land may present a problem, especially in windrow composting, and this may also reduce the nitrogen (fertilising) content in the compost (Tritt and Schuchardt, 1992). 3.6. Anaerobic digestion Anaerobic digestion is a biological process in which organic matter is degraded to methane under anaerobic conditions. Methane can then be used for energy to replace fossil fuels and thereby to reduce carbon dioxide emissions. Anaerobic digestion reduces pathogens and odours, requires little land space for treatment, and may treat wet and pasty wastes (Braber, 1995; Shih, 1987, 1993). In addition, any releases to air, water, and land from the process can be well controlled (reviewed by Braber, 1995; Shih, 1987, 1993). Most of the nutrients

also remain in the treated material and can be recovered for 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 of poultry slaughterhouse wastes are reviewed in detail in the following section.

4. Some fundamental aspects of anaerobic digestion of solid slaughterhouse wastes In this section, we will briey describe the metabolic pathways of anaerobic degradation of solid slaughterhouse waste. The eects of long-chain fatty acids (LCFAs) and ammonia on the degradation process will be discussed in detail because the compounds are important in the anaerobic digestion of solid poultry slaughterhouse waste. Attention will also be paid to the anaerobic degradation of feather and, briey, to the fate of pathogenic microorganisms in anaerobic digestion. 4.1. Degradation pathways A diversity of micro-organisms are involved in the many steps of anaerobic degradation of complex substrates, such as solid poultry slaughterhouse waste (Fig. 4), any of which may be rate-limiting, depending on the waste being treated as well as process conditions and operation (reviewed by Pavlostathis and Giraldo-Gomez, 1991). Solid slaughterhouse waste contains high amounts of dierent proteins and lipids. Fermentative bacteria, particularly the proteolytic Clostridium species, hydrolyse proteins to polypeptides and amino acids, while lipids are hydrolysed via b-oxidation to long-chain fatty acids (LCFAs) and glycerol (Koster, 1989; McInerney, 1988; Zinder, 1984) and polycarbohydrates to sugars and alcohols (Koster, 1989; Pavlostathis and Giraldo-Gomez, 1991; Zinder, 1984, Fig. 4). After that, fermentative bacteria convert the intermediates to volatile fatty acids (VFAs), hydrogen (H2 ), and carbon dioxide (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).


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1984). Ammonia and sulphide are the by-products of amino acid fermentation (Koster, 1989; McInerney, 1988; Zinder, 1984). Hydrogen-producing acetogenic bacteria metabolise LCFAs, VFAs with three or more carbons, and neutral compounds larger than methanol to acetate, H2 , and CO2 (Fig. 4). As these reactions require an H2 partial pressure of ca. 103 atm, they are obligately linked with micro-organisms consuming H2 , methanogens, and some acetogenic bacteria (Dolng, 1988; Zinder, 1984). Methanogens ultimately convert acetate, H2 and, CO2 to methane and CO2 (Fig. 4) (Vogels et al., 1988; Zinder, 1984). In the presence of high concentrations of sulphate, H2 consuming acetogenic bacteria and sulphate reducing bacteria compete with methanogens for H2 (Widdel, 1988; Zinder, 1984). 4.2. Eects of long-chain fatty acids on anaerobic digestion LCFA degradation may be the limiting step in the anaerobic degradation of solid slaughterhouse wastes (Broughton et al., 1998) because of the slow growth of LCFA-consuming bacteria (maximum growth rate usually below 1 d1 ) (Angelidaki and Ahring, 1995, reviewed by Hwu, 1997) and because the breakdown of LCFAs requires low (ca. 103 atm) H2 partial pressure (Novak and Carlson, 1970). On the other hand, the easily accumulating LCFAs may cause problems in anaerobic digestion of solid slaughterhouse waste (Broughton et al., 1998, Salminen et al., 2000) because they are toxic to anaerobic micro-organisms, particularly acetogens and methanogens (Angelidaki and Ahring, 1992; Galbraith et al., 1971; Hanaki et al., 1981; Hwu et al., 1996; Koster and Cramer, 1987; Rinzema et al., 1994; Roy et al., 1985). An additional problem is their tendency to form oating scum (Salminen et al., 2001b), for oating LCFAs may aect their bioavailability and toxicity and cause common obstacles such as fouled gas collection pipes and scum overow (Hobson and Wheatley, 1988; Pagilla et al., 1997). LCFAs are surface-active compounds and in aqueous systems behave like synthetic surfactants. The unionised form of LCFAs adsorbs initially to the microbial cell surface and is then taken up into the cell. Subsequently, acyl-CoA synthetase activates LCFAs, which are then degraded with a sequential removal of two-carbon units with acetate as end-product, i.e., via b-oxidation (Fig. 4) (reviewed by Hwu, 1997). Adsorption is also a mechanism of inhibition (Galbraith et al., 1971; Hwu et al., 1998). Both LCFA adsorption and inhibition depend on the concentration (Hwu et al., 1998), though the allowable concentration of LCFAs in digesters cannot be reliably determined as the inhibition also depends on several other factors. The inhibition is dependent on the type of bacteria present, and Gram-positive microorganisms and methanogens are more vulnerable to

LCFAs than Gram-negative microorganisms (Nieman, 1954; Roy et al., 1985). The inhibition depends, furthermore, on the specic surface area of sludge with suspended sludge being more vulnerable than granular sludge (Hwu et al., 1996). The carbon chain length and saturation of LCFAs, too, aect the inhibition (Galbraith et al., 1971; Komatsu et al., 1991; Koster and Cramer, 1987; Rinzema, 1988), saturated LCFAs with 1214 carbon atoms and unsaturated LCFAs with 18 carbon atoms being the most inhibitory (Nieman, 1954; Rinzema, 1988). In addition, LCFA toxicity to methanogens is synergistic, i.e., it increases in the presence of another LCFA (Koster and Cramer, 1987). On the other hand, various substances, including albumin, starch, bile acids, and cholesterol, may reduce the toxicity of LCFAs due to the formation of complexes or competitive adsorption at the cell wall (Nieman, 1954). Bentonite and calcium are also substances that may prevent LCFA inhibition, bentonite because of its occulating capability or cations of bentonite such as calcium (Angelidaki et al., 1990) and calcium from other sources because of such ions combined ability to form precipitates 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 may cause problems in anaerobic digestion of solid slaughterhouse waste, as unionised ammonia inhibits anaerobic microorganisms, particularly methanogens (Angelidaki and Ahring, 1993; DeBaere et al., 1984; Hansen et al., 1998; Hashimoto, 1986; McCarty and McKinney, 1961; Melbinger and Donnellon, 1971; Wiegant and Zeeman, 1986). Unionised ammonia is toxic because, unlike ammonia ions, it can readily diuse across the cell membrane (Kadam and Boone, 1996). Reportedly, unionised ammonia inhibits methanogenesis 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 and McKinney, 1961; Melbinger and Donnellon, 1971; Wiegant and Zeeman, 1986). Methanogens may adapt to ammonia concentrations several times the initial threshold level, i.e., the level beyond which methane production is possible only after a certain period of adaptation (Koster and Lettinga, 1988; Parkin et al., 1983). Angelidaki and Ahring (1993) postulated that adaptation results from the growth of new methanogens rather than metabolic changes in the methanogens already present, as proposed by Koster (1986). Ammonia is unlikely to cause a bactericidal eect, as diluting considerably accelerated the recovery from inhibition of a failed digester (Parkin et al., 1983). Recently, Hansen et al. (1999) found that even a small amount of sulphide (23 mg S 2 =l) may increase ammonia inhibition (4.6 g N/l),

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whereas activated carbon (2.5% w/w) or FeCl2 (4.4 mM) could relieve inhibition by reduction of sulphide concentration via adsorption onto activated carbon or precipitation as ferrous sulphide. Air stripping may be used to remove ammonia from materials to be digested (Liao et al., 1995), or ammonia may be recovered from an anaerobic digester in insoluble form as struvite by adding stoichiometric amounts of magnesium and orthophosphate (Kim, 1995; Maekawa et al., 1995). Addition of phosphorite ore was found to prevent ammonia inhibition in the anaerobic digestion of poultry manure, supposedly by either immobilizing methanogens on the mineral grains, which increases the buering capacity of the medium, or by exchanging 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 digestion because it degrades poorly under anaerobic conditions (reviewed by Bourne, 1993). Feather consists mainly of keratin, a brous protein, and it is the tight packing of the protein chain into a supercoiled polypeptide chain with a high degree of cross-linking by cystine disulphide bonds, which is mainly responsible for its poor degradability (reviewed by Bourne, 1993). Friedrich and Antranikian (1996) isolated an anaerobic bacterium, thermophilic Fervidobacterium pennavorans, that is capable of degrading native feather, and Williams and Shih (1989) isolated and characterised a featherdegrading bacterium, Bacillus licheniformis, from a digester treating manure and poultry feather (Williams et al., 1990). The latter bacterium, though isolated from an anaerobic habitat, grew maximally under aerobic condition, but its cell number declined slowly under anaerobic condition. Besides, the bacterium could degrade only autoclaved feather. Various pre-treatments have been shown to improve the nutritive value of feather for animal feed (El Boushy and van der Poel, 1990; Onifade et al., 1998; Papadopoulos, 1985). Several pre-treatments to increase the methane yield of feather were tested (Salminen et al., submitted). Combined thermal (120 C, 5 min) and enzymatic (commercial alkaline endopeptidase, 210 g/l) treatments increased its methane yield in the range of 3751%, whereas thermal (70120 C, 5 min1 h), chemical (NaOH 210 g/l, 224 h), and enzymatic treatments were less eective in yielding methane, increasing in the range of 532%. 4.5. Fate of pathogenic microorganisms in anaerobic digestion Pathogenic bacteria, parasites, and viruses may constitute a serious risk to animals and public health if

untreated poultry slaughterhouse waste is to be recovered for agriculture or animal feed (Marchaim et al., 1991; Shih, 1987, 1993). Anaerobic digestion has been shown to destroy pathogens, thermophilic being usually more eective than mesophilic digestion (Shih, 1987). A complete eradication of fecal coliforms and salmonellae was observed in a thermophilic digester (50 C), whereas a comparable mesophilic digester (35 C) destroyed them only partially (reviewed by Shih, 1987, 1993). The oocysts of Eimeria tenella, a pathogenic protozoan causing chicken coccidiosis, were inactivated 99.9% in a thermophilic digester and 9099% in a mesophilic digester, whereas thermophilic and mesophilic conditions reduced the counts of excreta-born fungal spores by 99 100% and 9498%, respectively (reviewed by Shih, 1987, 1993). Viruses may tolerate the conditions in an anaerobic digester considerably better than bacteria (reviewed by Turner and Burton, 1997), yet thermophilic treatment (at 55 C) with an appropriate holding time may destroy many of the viruses present in wastes. Anaerobic treatment at 50 C has been shown to destroy Mareks disease virus (Shih, 1993). Besides temperature, the destruction of pathogens in anaerobic digestion depends also on several other factors. For example, increasing the hydraulic retention time (HRT) may increase bacterial and viral destruction (Kun et al., 1989). A twophase anaerobic digestion reduced the number of pathogens even more than the conventional one-phase digestion (Kun et al., 1989). However, unstable performance or incomplete anaerobic digestion may, in fact, lower the ability of the process to reduce pathogens (Marchaim et al., 1991). To ensure the microbial safety of the digested material, sanitation, typically at 70 C for 1 h, or sterilisation of high-risk materials, at 133 C and 3 bars for 20 min, is usually required (Ling, 1997).

5. Experiences with anaerobic digestion of solid slaughterhouse wastes Recent advances in anaerobic digestion technologies have made it possible to treat an increasing diversity of wastes. Assuming that operation conditions are carefully optimised and economic viability can be achieved, anaerobic digestion competes well with other treatments of solid slaughterhouse waste (Banks, 1994; Tritt and Schuchardt, 1992). In this section, we review experiences with treating solid slaughterhouse waste, including also slaughterhouse waste other than those from poultry slaughterhouse. This is because there is limited information available about the anaerobic digestion of poultry slaughterhouse waste and because we consider that information about the treatment of slaughterhouse waste other than from poultry slaughterhouse may be useful in the design and operation of poultry slaughterhouse waste digesters. On the other hand, over the


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past decades a large number of studies have been conducted on the anaerobic digestion of poultry excreta (e.g. Webb and Hawkes, 1985a, 1995b). A comprehensive review of the subject is not presented in this paper. 5.1. Experiences with full-scale The number of full-scale anaerobic digesters treating only solid slaughterhouse waste is still limited (Table 2) and to our knowledge, no full-scale anaerobic digester treats solid poultry slaughterhouse wastes alone. In the UK in the year 1999 seven digesters treated solid slaughterhouse wastes, such as cattle paunch wastes, blood, and settlement tank solids, the largest of them 4050 t of waste/d (Banks and Wang, 1999). Banks (1994) described the performance of a 105 m3 digester treating cattle and lamb paunch contents, blood, and process wastewaters with an organic loading of 0.36 kg COD/m3 d and an HRT of 43 days: the process produced methane 0.18 m3 =kg CODadded . Fluctuations and an overload of blood in the feed, however, destabilised the process, evidently creating ammonia inhibition (Banks, 1994). Shih (1993) described two well-functioning, full-scale poultry manure digesters, one in Beijing and one in Shanghai, 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 (see Table 2). Over the past decades, there has been a number of full-scale applications of the anaerobic digestion of poultry excreta. 5.2. Experiences with laboratory-scale The anaerobic degradation and methane yield of dierent poultry slaughterhouse by-products and wastes were recently investigated in batch assays (Salminen et al., submitted). Poultry oal showed a high methane yield, 0.70.9 m3 of methane/kg VSadded (Table 1), but its production was considerably delayed due most likely to inhibition by LCFAs. Poultry blood, meat and bone trimmings produced 0.50.7 m3 of methane/kg VSadded , respectively, while feather showed the lowest methane yield of 0.21 m3 of methane/kg VSadded . Up to 0.67 m3 of methane/kg VSadded was produced from a solid poultry slaughterhouse waste mixture (bone and trimmings, blood, oal, and feather mixed in an approximate ratio as generated in the slaughterhouse: 42%, 16%, 32%, and 10% by weight, respectively) in batch assays (Salminen et al., 2000). Continuous anaerobic digestion of solid poultry slaughterhouse waste was found technically possible (Salminen and Rintala, submitted). The process was manageable 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, inuent feed characteristics, process conditions, and methane yield Reactor CSTR, 105 m


T (C)

HRT (d) 43

Loading rate 0.36 kg COD/m d


Methane yield 0.18 m =kg COD


References Banks (1994)

Cattle and lamb paunch Na contents, blood, and process wastewaters CSTR, 2 l Solid slaughterhouse 35 waste Two phases, (1) Cattle blood and rumen 35 HFR, 4 l (2) CSTR, paunch contents 1 l with zeolite as immobilisation matrix, 20 g/l CSTR, batch, 12 l Sheep tallow 35, 55 Two phases, (1) LB, Poultry mortalities 3 or 10 l (2) UASB, 2.35 or 3 l Two phase, LB and Poultry mortalities UASB CSTR, 5 l Poultry litter CSTR, 15 m3 CSTR, 5 l CSTR, 15 m3 CSTR, 5 l CSTR, 5 l Poultry manure Poultry litter Poultry manure Poultry manure Poultry manure 35, 55

50 (1) solids 230, liquid 2 (2) 210

0.8 kg VS/ m3 d 3.6 kg TS/m3 d

0.520.55 m3 =kg VS Salminen et al. (2000) 0.27 m3 =kg TS Banks and Wang (1999)

Na Na

520 g/l tallow (2.84 g COD/g) (1) 2279 g (2) <2 kg COD/m3 d Na 0.34.2 kg VS/m3 1.63 kg VS/m3 d 0.74.2 kg VS/m3 7.5 kg VS/m3 d 2.26 kg VS/m3 d Na

Na 0.201 m3 =kg wet weight

Broughton et al. (1998) Chen and Shyu (1998)

Na 35 35 35 50 34 35

Na 1229 2224 1229 4 40 1429

0.254 m3 =kg wet Chen (1999) weight d 0.140.22 m3 =kg VS Webb and Hawkes (1985a,b) 0.22 m3 =kg VS Saey et al. (1987) d 0.140.22 m3 =kg VS Webb and Hawkes (1985a) 0.29 m3 =kg VS Steinberger and Shih (1984) 0.20 m3 =kg VS Pechan et al. (1987) 0.240.26 m3 =kg VS Webb and Hawkes (1985b)

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

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HRT of 50 days and showed a methane yield of 0.55 m3 of methane/kg VSadded (Table 2). However, both HRT and loading were highly signicant for the performance of the process. At a loading of 1.02.1 kg VS/m3 d and a HRT of 12.525 days, the process appeared inhibited, as indicated by the accumulation of LCFAs and the declined methane yield (Salminen and Rintala, submitted). Accumulated LCFAs were proposed to be the main factor aecting the recovery of the process from inhibition (Salminen et al., submitted). Furthermore, the simulation model showed that the degradation patterns of solid poultry slaughterhouse waste involved complicated feedback connections, suggesting that the inhibition of propionate degradation by LCFAs and the inhibition of hydrolysis by a high propionate concentration constituted the rate-limiting step in the degradation of the waste in batch assays (Salminen et al., 2000). Webb and Hawkes (1985a) described a practicable treatment of poultry litter in mesophilic digesters (Table 2). Anaerobic treatment of poultry manure has been proven feasible as well (Table 2) (Barik et al., 1991; Webb and Hawkes, 1985b), though ammonia inhibition may cause diculties in the process (Hunik et al., 1990; Krylova et al., 1997; Pechan et al., 1987; Webb and Hawkes, 1985b). A complete degradation of up to 20 g/l of sheep tallow was shown in batch digesters under mesophilic conditions in ca. 90 days of incubation (Broughton et al., 1998). Under thermophilic conditions, though, and with a substrate concentration of 5 and 10 g/l, methane production was delayed by 43 and 48 days, respectively, and 20 g/l of tallow showed no methane production within 90 days of incubation. In these studies, LCFAs and VFAs accumulated considerably but were nally degraded to biogas, except in the thermophilic study with a tallow concentration of 20 g/l. Banks and Wang (1999) investigated the treatment of cattle blood and rumen paunch contents in a twophase process with uncoupled solids and liquid retention times. Compared to a single stage process, the two-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 apparently enhanced owing to the hydraulic ush, which prevented the accumulation of intermediates, the potential inhibitors of hydrolysis (Banks and Wang, 1999). Chen and Shyu (1998) investigated the anaerobic treatment of poultry mortalities in a combined UASB reactor and a leach bed. An 86% TS reduction and a methane yield of ca. 0.20 m3 =kg of wet weight of mortalities 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 which three leach beds were connected to one UASB in an

alternating fashion. The degradation of one batch of mortalities took about 62 days. 5.3. Co-digestion Co-digestion of wastes with varying characteristics is one way to dilute toxicants and to supply missing nutrients and a suitable moisture content (reviewed by Mata-Alvarez et al., 2000). However, transport costs and various policies of waste producers may limit the use of this process (reviewed by Mata-Alvarez et al., 2000). A mesophilic laboratory-scale digester, treating poultry slaughterhouse waste together with waste from a food packing plant and inoculated with mesophilic digested sewage sludge could handle loads up to 4.6 g VS/l d with an HRT of 18 days and produce methane up to 0.33 m3 /kg VSadded (Table 3). On the other hand, under similar conditions, digesters inoculated with mesophilic and thermophilic granular sludge failed apparently because of inhibition by ammonia and/or LCFAs (Salminen and Rintala, 1999). Co-digestion of manure and industrial organic wastes, including slaughterhouse waste, takes place in Denmark in a number of anaerobic digestion plants (Danish Institute of Agricultural and Fisheries Economics, 1999). Manure and slaughterhouse waste, including blood, fat, stomach, and visceral contents, and residues from a rendering plant, are also being treated in a plant in Sweden (Ling, 1997) (Table 3). Rosenwinkel and Meyer (1999) showed a successful treatment of slaughterhouse waste, hog, and cow stomach contents with sewage sludge in a pilot-scale, mesophilic digester at a loading of 2.9 kg TS/m3 d and an HRT of 17 days with a methane production of 0.23 m3 =kg TSadded . In another study, methane production in a sewage sludge digester treating otation tailings was possible at a loading of 1.5 kg TS/m3 d and an HRT of 15 days with a methane production of 0.32 m3 =kg TSadded (Table 3). Brinkman (1999) described a stable, thermophilic treatment of kitchen waste slurries and otation sludges from slaughterhouse wastes in a laboratory-scale digester at a loading of less than 3.5 kg COD/m3 d with an HRT of 32 days, but shock loads of 57.5 kg COD/m3 d caused an accumulation of LCFAs and VFAs. 5.4. Slaughterhouse wastewaters Anaerobic treatment of slaughterhouse wastewater is far more common than the treatment of solid slaughterhouse waste. In 1968 in Leeds, the UK, an anaerobic plant was built to treat slaughterhouse wastewater (Black et al., 1974). Treatment of slaughterhouse wastewater in high-rate anaerobic treatment processes has 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

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-scale plants operate in slaughterhouses in the Netherlands, Belgium, and New Zealand (reviewed by Johns, 1995), and anaerobic lagoons or covered anaerobic ponds are used to treat slaughterhouse wastewater in warm climates and where land cost is low as in Australia and New Zealand (reviewed by Cooper and Russel, 1992).

Rosenwinkel and Meyer (1999)


(1) 0.23 m =kg TS, (2) 0.32 m3 =kg TS

0.33 m3 =kg VS

Salminen and Rintala (1999)

Ling (1997)


6. Applications of digested material The recovery of anaerobically digested slaughterhouse waste for agriculture conserves and recycles nutrients and may reduce waste discharge and the use of chemical fertilisers, but the safety of the material must be carefully evaluated before use (Marchaim et al., 1991; Shih, 1987, 1993). Anaerobic digestion reduces pathogens and minimises odour, and nutrients remain mostly in the digested material (Shih, 1987, 1993). On the other hand, a major part of organic nitrogen is mineralised into ammonia, and any excess liquid rich in ammonia can be either spread as slurry on farmland or treated in a wastewater plant. In a study by Salminen et al. (2001a), anaerobically digested solid poultry slaughterhouse waste was shown rich in nitrogen (ca. 20% N of TS) but potentially phytotoxic. Fertilised with the material, carrots grew in 27-d plant growth assays almost as well as with a commercial mineral fertiliser used as reference (Salminen et al., 2001a), but the growth of Chinese cabbage was inhibited. In further 5-d phytotoxicity assays, probably organic acids present in the digested material inhibited the germination and root growth of ryegrass and Chinese cabbage. Organic acids are potential inhibitors of root growth and may cause ion loss in roots (De Vleeschauwer et al., 1981; Lee, 1977; Lynch, 1977, 1980; Manios et al., 1989; Marambe et al., 1993). The unionised and ionised forms of ammonia, too, may aect plant growth (Hill et al., 1997; Sundradjat, 1990; Tiquia and Tam, 1998; Wong et al., 1983). Aerobic post-treatment of anaerobically digested material may greatly reduce its phytotoxicity, as inhibitory compounds present in the material, including organic acids and ammonia, may be readily degraded aerobically or volatilised during the treatment, as found in a study of anaerobically digested solid poultry slaughterhouse waste (Salminen et al., 2001a). In addition, aerobic post-treatment of digested materials may enhance the physical and chemical properties of the material as well, though it may also result in a loss of nitrogen due to ammonia volatilisation (Marchaim et al., 1991; Sundradjat, 1990; Vermeulen et al., 1992). Anaerobically digested materials may sometimes be used in animal feed, though legislation is restricting this

Organic loading rate

(1) 2.9 kg TS/m d, (2) 1.5 kg TS/m3 d

2.5 kg VS/m3 d 25 Na


Table 3 Anaerobic co-digestion of solid slaughterhouse waste, inuent feed characteristics, and process conditions

HRT (d)

(1) 17, (2) 15

T (C)


(1) Hog stomach contents (25 vol%, 67% of loading) co-treatment in sewage digester, (2) otation tailings (25 vol%, 43% of loading) co-treatment in municipal digester Co-digestion of manure, slaughterhouse waste, and carcasses Poultry slaughterhouse wastes, and food packing plant wastes CSTR, 2 3700 m3 CSTR, 2 m

35 CSTR: continuously stirred tank reactor, Na: not available. CSTR, 3 l




4.6 kg VS/m3 d

E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 1326


practise. Studies of dried anaerobically digested poultry manure used as a feed supplement for growing chicks showed that 9095% of the phosphorus in the material is usable, and no toxicity or negative eects were discovered when up to 10% of the material was added in animal feed (Shih, 1993). Blood and other high nitrogen-containing fractions may be used to produce VFA and ammonia, as proposed by Banks (1994). Because of ammonias high buering capacity, considerable amounts of VFA could be produced from blood before the pH dropped to a level inhibitive of VFA production. Ammonia had to be rst precipitated and VFA extracted with solvents before distillation (purication) could take place (Banks, 1994).

Acknowledgements We thank the Academy of Finland for its nancial support (Grant No. 38044). References
Angelidaki, I., Ahring, B.K., 1992. Eect of free long-chain fatty acids on thermophilic anaerobic digestion. Appl. Microbiol. Biotechnol. 37, 808812. Angelidaki, I., Ahring, B.K., 1993. Thermophilic anaerobic digestion of livestock waste: eect of ammonia. Appl. Microbiol. Biotechnol. 38, 560564. Angelidaki, I., Ahring, B.K., 1995. Establishment and characterization of an anaerobic thermophilic (55 C) enrichment culture degrading long-chain fatty acids. Appl. Environ. Microbiol. 61, 24422445. 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, 469 472. 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., M artin, A., 1995a. Inuence of the organic volumetric 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, 351 357. 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 uidisedbed 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 compounds. 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.

7. Economics Lack of economic sustainability has so far limited the full-scale implementation of anaerobic digestion of solid wastes (Braber, 1995). The cost of anaerobic digestion depends greatly on local circumstances, including construction and labour costs, treatment capacity, possibilities of energy recovery, energy prices, and taxes as well as energy purchase taris, land price, markets, and prices of digested material. On the other hand, the quality of the digested material determines to a great extent its marketability and price, while the local status and cost of alternative technologies must be considered as well. Though capital investment may be somewhat higher in an anaerobic digestion plant than in a composting plant (reviewed by Mata-Alvarez et al., 2000), anaerobic digestion oers the added potential for recovering energy. Unlike in many other countries, electricity is fairly inexpensive in Finland; nevertheless, the increasing cost of landlling and the energy tax on fossil fuels should encourage the exploitation of renewable energy sources, thus making anaerobic digestion a highly competitive alternative for the treatment of the above wastes.

8. Final considerations Anaerobic digestion technology is practicable for the treatment of organic solid slaughterhouse waste to combine material recovery and energy production. Assuming that the operation conditions can be optimised and the process made economically sustainable, anaerobic digestion is fully competitive with other treatment options for the above wastes. However, since only a handful of full-scale plants exist so far, the construction and successful operation of full-scale demonstration plants is essential for gaining condence and experience for any comparison of treatment processes.


E. Salminen, J. Rintala / Bioresource Technology 83 (2002) 1326 Harper, S.R., Ross, C.C., Valentine, G.E., 1987. Feasibility of packedbed 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 2314. 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 University. 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 methanogens. 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 University. 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, 1720.

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 anaerobic digestion treatment of poultry mortalities. Bioresour. Technol. 63, 3748. 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, pp. 2333. 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 NH4 Cl 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 composting: a review. Waste Manag. Res. 1, 157176. De Vleeschauwer, D., Verdonck, O., Van Assche, P., 1981. Phytotoxicity 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: Haarukkapaloja 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, 28752882. 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. 26, 599602. 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 thermophilic anaerobic digestion of swine manure. Water Res. 33, 1805 1810. Hashimoto, A.G., 1986. Ammonia inhibition of methanogenesis from cattle wastes. Agric. Wastes 17, 241261.

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, 8187. 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 Lafayette, Indiana. 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., Mac e, S., Llabr es, 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, 16581667. 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 nutritional 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, pp. 239246. 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, 411 490.


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., Beltr an, S., 2000. Anaerobic pre-treatment of slaughterhouse wastewater using xed-lm reactors. Bioresour. Technol. 71, 143149. Pulsa, A., 1996. Turkistarhat tarvitsevat laadukasta teurasj atett a. Lihalehti 3, 3841, in Finnish. Rinzema, A., 1988. Anaerobic treatment of wastewater with high concentrations of lipids or sulfate. Ph.D. Thesis, Wageningen Agricultural University. 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 degrading long-chain fatty acids. Appl. Environ. Microbiol. 49, 702 705. 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. nen, J., Kuitunen, M., Ho gmander, Salminen, E., Rintala, J., H arko 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 anaerobic 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. Biotechnol. (submitted). 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. 21462151. 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 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 sulfurreducing 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 featherdegrading 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 parachinensis. Environ. Pollut. A 30, 109123. Zinder, S.H., 1984. Microbiology of anaerobic conversion of organic wastes to methane: recent developments. ASM News 50, 294298.

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 wastewater 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.