R eview : Comparison of 3 alternatives for large-scale processing of animal carcasses and meat by-products

Disposal of animal carcasses and meat by-products from food animal slaughter can be accomplished in several ways including anaerobic digestion, composting, and rendering. The ability of each of these methods to handle large quantities of material was examined from the standpoints of biosecurity, current environmental regulations, greenhouse gas emissions, and effective resource recovery. Assurance of biosecurity is challenging when animal carcasses and meat by-products are co-composted with manure and other materials. In addition, peer-reviewed, published field data indicate that significant quantities of methane and nitrous oxide are released during composting. Biosecurity can be ensured more easily in anaerobic digestion, and greenhouse gas emissions are low if digestate storage tanks are sealed. But, large-scale experience digesting meat by-products is limited, and health and environmental regulations are not fully developed. Rendering is a mature, regulated industry that entails cooking to remove water and destroy pathogens. It allows almost complete recovery of fat and protein from the raw material. Fuel consumption and other rendering plant operations emit about 25% as much carbon dioxide as complete aerobic decomposition of the meat by-products would release. If an equal quantity of meat by-products is processed by rendering, composting, and anaerobic digestion, the economic value of the rendered products is at least 3 times the value of the products resulting from anaerobic digestion and at least 5 times the value added to compost by inclusion of the meat by-products. These differences make rendering the most sustainable method for handling large quantities of animal carcasses and meat by-products.


INTRODUCTION
By 2020 worldwide consumption of meat is expected to exceed 300 billion kg/yr (Delgado et al., 1999), generating 100 to 150 billion kg/yr of meat by-products from food animal slaughter and a smaller quantity of fallen animals that never enter the human food chain.To support a sustainable future, this massive quantity of material must be handled with methods that are safe, environmentally responsible, and efficient with respect to recovery of valuable resources.
Rendering is the most common method of handling large quantities of fallen animal carcasses and meat by-products from food animal slaughter.In North America roughly 25 billion kg/yr of raw materials are rendered, producing about 5 billion kg of fats and a similar quantity of protein meals (Meeker and Hamilton, 2006).Other methods can be used to dispose of fallen animal carcasses, and several analyses of available options have been published (NABCC, 2004;Gwyther et al., 2011).Simple, inexpensive methods such as burial and open burning are used on small farms, but they can lead to water and air pollution.And, neither is practical for routine, large-scale use.Disposal in landfills is not allowed in the European Union and in many parts of the United States, and even where it is The Professional Animal Scientist 32 (2016) allowed, capacity limitations make landfill disposal impractical for the huge quantity of meat by-products generated from food animal slaughter.High-temperature incineration is favored in some cases when quick disposal of diseased animal carcasses and ensured pathogen destruction are deemed necessary to protect the public health.But the moisture content of carcasses and meat by-products leads to high energy costs that make incineration infeasible for routine, large-scale disposal.
Anaerobic digestion and composting have been practiced on farms for decades, mostly for the disposal of manure.Both of these methods have received increased attention in recent years as methods of handling other organic wastes, including animal carcasses and meat by-products.The objective of this article is to compare and contrast anaerobic digestion, composting, and rendering of animal carcasses and meat by-products.The key issues examined are biosecurity, environmental sustainability [especially greenhouse gas (GHG) emissions], and resource recovery.

Composting
Farmers have practiced composting for centuries, accumulating organic waste in piles, allowing it to decompose, and then using the residual material as fertilizer.The practice has also been adapted by urban dwellers as well to produce material that has several benefits to soil (USCC, 2015;EPA, 2016a).Municipalities and commercial entities have established large, central composting facilities in many communities to reduce burdens on landfills and facilitate the ability of citizens to recycle food and yard waste and produce compost for home use (EPA, 2014a).Larger-scale composting is normally accomplished in bounded bins or windrows.In some cases these are covered or lined to control moisture conditions and prevent pollution of nearby waterways (Kalbasi et al., 2005;Rozeboom et al., 2005).
Large-scale composting has also been applied in agricultural operations.Animal carcasses and meat byproducts can be composted if they are mixed or layered with roughly equal parts of manure and bulking materials such as straw or sawdust.Initially the meat by-products comprise from 5% (Hao et al., 2009) to about 30% (Gulliver and Gulliver, 2001) of the total mass.Complete degradation requires between 4 and 12 mo, depending primarily on the initial particle size of the meat by-products and ambient temperatures (Mukhtar et al., 2003;Stanford et al., 2007;Xu et al., 2007a,b;Hao et al., 2009).
Aerobic decomposition of organic material is exothermic, so compost piles and windrows are self-heating.After several weeks, temperatures in the most active regions will reach 55 to 70°C, plateau for a few weeks, and then decline gradually for months, eventually approaching the mean ambient temperature when degradation reactions wind down (Gulliver and Gulliver, 2001;Xu et al., 2007a,b;Hao et al., 2009).During this long period, compost should be mixed or turned occasionally to promote aerobic conditions and thus ensure that carbon is converted to carbon dioxide (CO 2 ) rather than methane (CH 4 ).The reported frequency of turning in actual practice varies from monthly to rarely, if at all (Gulliver and Gulliver, 2001;Stanford et al., 2007;Berge et al., 2009).

Anaerobic Digestion
Anaerobic digestion consists of a complex series of biochemical reactions in which microorganisms break down organic-rich material in the absence of oxygen to form primarily CH 4 and CO 2 .These reactions are usually conducted in the liquid phase.For simple hydrocarbons the overall result of the reaction sequence can be represented by the Buswell equation (Angelidaki and Sanders, 2004): In this equation n, a, and b are the number of carbon, hydrogen, and oxygen atoms, respectively, in the hydrocarbon molecule that is decomposed.This stoichiometric equation can be used to calculate the relative amounts of CH 4 and CO 2 produced under ideal conditions.For example, glyceryl trioleate, a model compound for the fats found in meat by-products, has the linear formula (C 17 H 33 COOCH 2 ) 2 CHOCOC 17 H 33 .Applying the Buswell equation to this compound, n = 57, a = 104, and b = 6, and the theoretical biogas from anaerobic digestion would have a composition of 70% CH 4 and 30% CO 2 .Theoretical yields have been published for the anaerobic decomposition of many substrates (Angelidaki and Sanders, 2004).When proteins are decomposed completely under anaerobic conditions, the CH 4 /CO 2 ratio is lower, typically about 55/45, and nitrogen in the protein is evolved primarily as ammonia (Angelidaki and Sanders, 2004;Krich et al., 2005).
In practice, anaerobic decomposition reactions rarely go to completion and produce the theoretical yield.When meat by-products are decomposed, reported CH 4 yields vary from 50% of the theoretical value to near 100% (Salminen and Rintala, 2002;Zhang, et al., 2007;Hejnfelt and Angelidaki, 2009).Biogas leaving the digester is typically a mixture of methane, carbon dioxide, water vapor, nitrogen, nitrogen oxides, ammonia, and hydrogen, plus hydrogen sulfide if sulfur is present in the feed material (Angelidaki and Sanders, 2004).When the process is stopped, the liquid or slurry by-product (digestate) that remains in the reaction vessel consists of undigested organics, water, and mineral matter.The evolved biogas can be burned on site to recover its thermal energy.Alternatively, the biogas can be refined to reduce the levels of components other than CH 4 and produce pipeline quality gas for sale.Digestate is usually stored on site and eventually applied to crops as fertilizer.
Various types of covered or closed reactors are used to conduct anaerobic digestion.For agricultural wastes, the most common are lagoons, concrete channels that function like plug-flow reactors, and mixed tanks (EPA, 2011).In the United States over 200 agricultural biogas systems are operating currently, most processing livestock manure (ABC, 2014).Hydraulic retention times of these large-scale systems are typically 40 to 55 d (Salminen and Rintala, 2002;Ek et al., 2011).Anaerobic decomposition of large molecules is endothermic, so heating is required to achieve and maintain operating temperatures that typically range from 10°C to 70°C (Masse et al., 2011).Meat by-products must be co-digested with 25 to 65% manure by weight to achieve acceptable results, and various other materials are added to the reactor in small quantities to control pH, corrosion, and odors (Ek et al., 2011).The fraction of meat by-products that can be fed to an anaerobic digester may be limited by the conversion of nitrogen in proteins to ammonia, which is inhibitory to CH 4 -forming microorganisms (Salminen and Rintala, 2002).

Rendering
Most rendering plants are continuous, industrial-scale operations that can process whole carcasses as well as meat by-products, including offal, blood, bone, and feathers from butcher shops and slaughterhouses, and grease collected from restaurants (Anderson, 2006).Renderers recover and sell 2 types of materials from meat by-products: fats and oils that are produced in various grades depending on the raw material processed, and protein-rich solids called meal.
Solid and semisolid material that enters a rendering process is first ground to a uniform size.Ground solids and liquid feeds are sent to a continuous cooker where they are heated to 115 to 145°C to evaporate moisture, melt fat, and kill pathogens (Anderson, 2006).The cookers are heated by steam, which is generated by burning natural gas, oil, and in some cases fat produced by rendering.Wood is used as a fuel in some countries.Water vapor boiled off the meat by-products is channeled through an entrainment trap to prevent the release of liquid and solid particles.
Vapor is condensed and sent to wastewater treatment, and noncondensable gases are pulled from the condenser and processed through an odor control system.
The slurry of liquid fat and solid bone and protein discharged from the cooker is sent to a drainer conveyor, where it is separated.Liquid fat falls into a settling tank beneath the conveyor.It is centrifuged to remove fine solids and sent to product storage and packaging.Solids removed from the bottom of the settling tank and from the centrifuge are recycled to join the feed entering the drainer conveyor.The solids retained by the drain conveyor are discharged to a screw press, which reduces the residual fat content to about 10% by weight.Fat pressed from the solids is sent back to the settling tank.The protein-rich cake that leaves the screw press is sent to final meal processing, packaging, and storage.

BIOSECURITY
The following assessment by Berge et al. (2009) frames the issue of biosecurity: "Part of the challenge associated with the disposal of animal carcasses includes protection of environmental, animal, and public health against potential microbiological threats.An animal carcass is composed of microbiologically active material that may contain viruses, bacteria, protozoa, parasites, prions, toxins, drug residues, and other chemicals.All of the biologically active materials need to be reduced to safe amounts, eliminated, or sequestered to minimize their potential hazard."This assessment applies to all meat by-products unless they have been sterilized.
Laboratory research and larger demonstrations have shown that compost-ing meat by-products with manure and bulking agents reduces the levels of viruses, bacteria, and other pathogens in the original materials substantially (Berge et al., 2009;Hao et al., 2009).But a review of the effectiveness of pathogen control in composting concluded that in many published studies pathogens survived despite the recommended time-temperature conditions apparently being met (Wichuk and McCartney, 2007).The authors of the review hypothesized that either the time-temperature requirements specified were inadequate or the apparent time-temperature criteria were not actually achieved in all regions of the heterogeneous compost pile.Data reported by Xu et al. (2007a,b) showed that significant temperature variations occur in large windrows, and other studies (Gale, 2004;Gwyther et al., 2011) have cautioned that bacteria that are not eliminated completely can recolonize during turning and near the end of the composting cycle when temperatures are lower.Furthermore, Franke-Whittle and Insam (2013) concluded that prions and spore-forming bacteria are not destroyed by composting, which can result in risk to animals that graze in pastures where compost containing meat by-products has been applied.Inclusion of a substantial fraction of feathers in compost apparently results in more effective decomposition of specified risk materials that may be present in meat by-products, though the mechanism of this effect is not clear (Xu et al., 2013).Berge et al. (2009) emphasized that close monitoring of large-scale composting operations is essential to achieving safe and effective results, and that "regulations to provide uniform standards for biosecurity, traceability, and environmental protection are necessary."Smith et al. (2005) provided insight into factors that control pathogen destruction in anaerobic digesters.Gwyther et al. (2011) reported that studies by different groups have yielded varying levels of success and that the European Union does not permit bio-digestion of carcasses without pretreatment to remove patho-gens.Masse et al. (2011) offered an assessment of biosecurity in anaerobic digesters that is similar to the conclusions of Berge et al. (2009) on composting."Before becoming a viable option for carcass disposal, research is needed to ensure that current processes are able to destroy potential pathogens and/or prions in carcasses and by-products, and to develop management systems (e.g., pre and/or post-treatment) that ensure complete sanitation of treated animal by-products.In addition, strict regulations and environmental policies must be in place to minimize public health risks." The rendering industry's approach to biosecurity has been described well by Hamilton et al. (2006).Rendering plants in North America are operated and controlled under an industry Code of Practice (NRA, 2010), which is the type of management system recommended by Masse et al. (2011) for anaerobic digestion.The rendering Code of Practice was developed by the Animal Protein Producers Industry.The code established minimum standards for practices that govern the maintenance and operation of rendering facilities to minimize physical, biological, and chemical hazards in rendered products.For example, the code requires that heat treatment in rendering processes must be sufficient to kill conventional pathogens that may be in the raw material.Rendering plants are audited for compliance with the Code of Practice by an independent third party, the Facility Certification Institute, and certified if they meet all requirements (Validus, 2016).
Rendering facilities in the United States that produce fats or proteins used in animal feeds are regulated at the federal level by the Animal and Veterinary Division of the Food and Drug Administration (FDA, 2016) and by the Animal and Plant Health Inspection Service of the US Department of Agriculture (APHIS, 2016).Recently, the Food Safety Modernization Act expanded Food and Drug Administration regulatory control over all animal food, including rendered ingredients (FSMA, 2016).
Current requirements include specific hazard controls, current good manufacturing practices, and extensive recordkeeping.The cooking process used in rendering plants has been shown to reduce prion infectivity by up to 2 logs (Taylor et al., 1995), but protein meals produced in rendering plants that process ruminant materials are prohibited by law from being added to ruminant animal feeds (Hamilton et al., 2006).

Regulated Emissions, Discharges, and Disposals
In the United States, Congress passes broadly worded laws to protect the environment, and federal agencies that work under the executive branch of government are authorized to create and enforce more specific regulations.The Environmental Protection Agency (EPA) has overall authority with respect to air and water emissions and solid waste.The EPA has delegated much of its regulatory authority to individual states, and in some cases, authority over environmental regulations has been delegated further to local agencies.
Rendering is a mature industry, and every rendering plant in the United States is subject to state or local regulations pertaining to air emissions, wastewater discharges, and solid waste disposal.The emission, discharge, and disposal limits permitted by industrial plants of a certain type and size are not identical in every state and municipality, but they are quite similar in most.Local regulatory agencies may be more restrictive in the limits placed on industry if the local ambient air or waterway conditions do not meet federal standards.Rendering plants and other industrial facilities are subject to fines or even closure if they exceed their permitted emission, discharge, and disposal limits.
In general, home and small-farm composting operations are not subject to environmental laws.Most large-scale composting and anaerobic digestion operations are regulated, but the specifics of environmental laws pertaining to these processes are still under development.Many, if not most, of the air emission, wastewater discharge, and solid waste disposal regulations that apply to composting and anaerobic digestion do not address specifically the inclusion of animal carcasses or meat by-products in the process.Over the next decade, it seems likely that these regulations will become more uniform, but they still vary considerably from state to state (CIWMB, 2009;EPA, 2014b).As an example, Berge et al. (2009) noted that "although composting as a form of routine or emergency animal carcass disposal has been approved in several states, other states have no rules and some prohibit the practice."

GHG Emissions
Several gases are recognized as having the potential to trap heat in the atmosphere.Greenhouse gas emissions are usually reported as carbon dioxide equivalents (CO 2 e).The most common GHG are CO 2 , CH 4 , and nitrous oxide (N 2 O).Water vapor is a greenhouse gas but is excluded from most discussions because it is ubiquitous.Conversion from actual CH 4 and N 2 O emissions to CO 2 e is based on the IPCC AR4 global warming potential of each gas (Solomon et al., 2007).Carbon dioxide is assigned a value of 1, and over a 100-yr time horizon the global warming potentials of CH 4 and NO 2 are 25 and 298, respectively.
Currently, the United States has no GHG regulations in force.The EPA has proposed limits on GHG emissions from power plants, and limits on other sources may follow.However, nothing is certain given the political and policy differences that exist within Congress.Despite the lack of regulatory action, many companies in the United States have adopted voluntary policies to reduce GHG emissions, and many consumers have expressed their preferences for products and processes that are perceived to be sustainable environmentally.
Figure 1 compares GHG emissions and market value of products that result from processing 1,000 kg of meat by-products by 3 alternative technologies: rendering, anaerobic digestion, and composting.The GHG comparison is gate to gate with the inlet gate for each process being the point at which meat by-products are received at the process plant and the outlet gate being the point at which process products leave.For each alternative the composition of the entering raw material was assumed to match the average distribution of carcasses and other meat by-products currently rendered in North America as reported by Gooding (2012).Overall, this material is approximately 21% fat, 22% protein, and 57% water by weight.Carbohydrate content is essentially nil.On a dry weight basis, 5 to 10% of the "protein" is actually mineral matter (ash) found in feathers, bones, and other materials that remains in the solid phase during rendering.The composition of animal carcasses and meat by-products processed certainly varies somewhat by location and time, but these figures provide a reasonable and common basis for comparison of alternative disposal methods.The calculations used to estimate the GHG emissions and product values from each alternative process are explained in the following sections.GHG Emissions from Rendering.The Fats and Proteins Research Foundation, an affiliate of the National Renderers Association, has available online a spreadsheet tool that enables Fats and Proteins Research Foundation members to input data and calculate the carbon footprint of their rendering plants (FPRF, 2016).Gooding (2012) developed the carbon footprint tool for the Fats and Proteins Research Foundation and presented representative results based on data from several sources, including Lopez et al. (2010), who surveyed 25 rendering plants in North America to determine fuel and electricity use and evaluate other current practices.
The rendering process separates meat by-products into a fat product, a protein product, and water, which is driven off as vapor or sent to wastewater treatment.Approximately 99% of the organic and mineral matter in the raw material leaves the process in one or the other of the product streams, and 1% is lost to wastewater treatment (Gooding, 2012).Greenhouse gases are emitted primarily by burning fuels to produce steam for heating in the rendering process.Typical heat loads and distribution of fuels used to supply heat in North America were obtained from Lopez et al. (2010) and reported in Gooding (2012).Overall, rendering requires a heat input of 2,300 MJ/1,000 kg of meat by-products processed.Greenhouse gas emission factors for purchased fuels (natural gas and #2 and #6 oils) were obtained from lifecycle inventories published by the Na-tional Renewable Energy Laboratory (NREL, 2013).Emission factors for grease and fat burned in the process were estimated from average composition data (Lopez et al., 2010) and stoichiometric calculations, assuming complete combustion.Overall, in a typical North American rendering plant, fuel burning results in the release of 150 to 160 kg of CO 2 e/1,000 kg of meat by-products processed.
Purchased electricity is the second largest source of GHG emissions associated with rendering.These emissions are designated as "Utility GHG" in Figure 1.Approximately 70 kWh/1,000 kg of meat by-products is used to operate size-reduction equipment, pumps, mixers, and other mechanical equipment.The GHG emissions associated with power pro- duction do not occur at the rendering plant site, but they are assigned to the process in accordance with a common protocol used for GHG accounting (WRI, 2004).To prepare Figure 1 the breakdown of power generation by energy source was updated from the study by Gooding (2012) to reflect the 2014 United States grid average (EIA, 2014).In the last few years, the use of coal has declined from 52 to 39%, and the use of natural gas and renewables has increased.Greenhouse gas emission factors for each fuel used to generate electricity were taken from the National Renewable Energy Laboratory (NREL, 2013) inventory.For every 1,000 kg of meat by-products rendered, 35 to 40 kg of CO 2 e emissions are associated with purchased electricity.Emissions of N 2 O and CH 4 , with their CO 2 equivalent factors applied, were included in the calculations for fuels burned on site and for generation of electricity off site.Despite the high global warming potential factors of CH 4 and N 2 O, the National Renewable Energy Laboratory emission data indicate that GHG contributions from these gases are negligible to 2 significant figures.
Wastewater treatment results in emission of 5 to 10 kg of CO 2 e (Gooding, 2012), yielding a total of 200 kg of CO 2 e/1,000 kg of meat by-products rendered as shown in Figure 1.To put the total GHG emissions in perspective, the average weight percent of carbon in fats and proteins is 76 and 27%, respectively.If all of the carbon in 1,000 kg of meat by-products of the composition defined above were decomposed to CO 2 , 800 kg of CO 2 would be emitted.GHG Emissions from Anaerobic Digestion.Meat by-products are normally co-digested with manure and other materials, but the results in Figure 1 and the calculations described in this section include only GHG emissions associated with processing 1,000 kg of meat by-products.Contributions from co-digested manure and other materials were ignored.Anaerobic co-digestion of the same mix of carcasses and meat by-products used for the rendering calculations would require size reduction, transfer into the digestion vessel, heating to the digestion temperature, maintenance of temperature over the required digestion time, mixing during the digestion process, and transfer of biogas and residual solids out of the vessel.Broadly applicable estimates for most of these thermal and electrical requirements of anaerobic digestion were not found in published literature so the following analogies were drawn between steps in the anaerobic digestion and rendering processes.
• Electrical requirements for size reduction should be approximately the same for anaerobic digestion and rendering.Overall, the analogies and approximations indicate that anaerobic digestion of 1,000 kg of meat by-products should require 15 to 20 kWh or 25% as much electrical energy as rendering the same material.Generation of the electricity to meet these requirements will result in the emission of 10 kg of CO 2 e/1,000 kg of meat by-products.
Thermal energy requirements of anaerobic digestion should be less than those of rendering, which requires heating of all meat by-products to at least 115°C and boiling off a fraction of the water.Anaerobic digestion requires only heating from ambient to digestion temperature and then maintaining the digestion temperature.Heat losses depend on ambient conditions and whether the digestion vessel is below ground or above ground and how it is insulated.Assuming initial heating from 20 to 70°C and then replacing 5% loss per day for 40 d (both using steam generated at 85% boiler efficiency), the thermal energy requirement for anaerobic digestion is estimated to be 600 MJ/1,000 kg of meat by-products.If biogas containing 60% CH 4 and 35% CO 2 is burned to meet these requirements, the resulting GHG emissions will be 50 kg of CO 2 e/1,000 kg of meat by-products digested.
Liebetrau et al. ( 2013) conducted field tests on 10 biogas plants in the German agriculture sector to evaluate GHG emissions.They found that emissions from digester vessels were low, typically on the order of 0.01% of the CH 4 produced, but emissions from digestate storage tanks varied from near zero at plants with wellsealed tanks to over 11% of the CH 4 produced in plants that had open digestate tanks.When the theoretical yields reported by Angelidaki and Sanders (2004) are applied to the raw material used as a basis for the calculations in Figure 1, the theoretical CH 4 yield is 190 kg of CH 4 /1,000 kg of meat by-products.In the worst case consistent with data reported by Liebetrau et al. (2013), losses of CH 4 to the environment from digestate tanks would be 20 kg of CH 4 or 500 kg of CO 2 e/1,000 kg of meat by-products digested.
In summary, an anaerobic digestion plant that co-processes 1,000 kg of meat by-products and produces raw biogas and digestate will emit to the environment GHG totaling approximately 60 kg of CO 2 e if sealed digestate storage tanks are used or as much as 500 kg of CO 2 e if CH 4 is allowed to escape from open digestate storage tanks.Because this analysis encompasses only the anaerobic digestion plant and on-site biogas and digestate storage facilities, the estimated GHG releases do not in-clude other emissions that will occur farther downstream.When raw biogas is burned, CO 2 that was produced in the anaerobic digester and CO 2 that is produced in the combustor will be released to the environment unless a CO 2 capture system is used.Liebetrau et al. (2013) also measured significant CH 4 and N 2 O emissions from downstream sections of 10 German plants that refined or burned biogas, and Masse et al. (2011) cited evidence of N 2 O emissions when digestate was applied to land.GHG Emissions from Composting.Numerous published reports have described co-composting of meat by-products with manure and other materials, but only 2 have provided sufficient comparative data to quantify the GHG emissions attributable to the meat by-products.Xu et al. (2007a,b) conducted 2 large-scale studies in western Canada, each lasting about 10 mo, one with adult cattle mortalities and the other with calf mortalities.Each study compared side-by-side composting in two 2 × 2 × 30 m windrows that were identical except for the presence or absence of the animal carcasses.Farm equipment was used to assemble the windrows and turn the contents of each windrow twice over the duration of the experiment, but no data were reported on the use of fuel or electricity.Hao et al. (2004) estimated fuel consumption in equipment used to turn windrows at 0.22 to 0.27 L/1,000 kg of material turned.Calculations based on recommendations by Gulliver and Gulliver (2001) yielded a fuel use estimate 4 times higher than by Hao et al. (2004).Figure 1 shows the range of estimated fuel use.No estimate is available for consumption of electricity at a composting facility, but it should be minimal.
Greenhouse gas emissions were measured frequently over the course of each experiment conducted by Xu et al. (2007a,b), and chemical analyses were conducted on each material originally added to the compost windrows and on the final compost, which was sampled at several locations in each windrow.In each study the windrow with mortalities had significantly higher GHG emissions than the control.By comparing emission data from the control windrows to emission data from the windrows with mortalities, we calculated the GHG emissions attributable to the mortalities.Each study also provided data on total mass and composition of all materials initially in the windrows, with and without mortalities present, and data on the total mass and composition of the final compost.By comparing emission data to the difference in mass and composition of the initial windrows and mass and composition of the compost, we evaluated closure of the mass balances on animal carcasses.In the study conducted with adult cattle mortalities (Xu et al., 2007b), the following were found: • Emission data indicated that 77% of the C in the cattle mortalities was emitted as CO 2 and 4% was emitted as CH 4 .Initial and final mass and composition data indicated that 77% of C in the cattle mortalities was lost, which is close to the total of 81% C loss indicated by the emission data.• Emission data indicated that 6% of the N in cattle mortality proteins was emitted as N 2 O. Initial and final mass and composition data indicated that 59% of N in the cattle was lost, which is much higher than the measured 6% loss as N 2 O.The additional loss could have been in the form of NH 3 emissions, which were not measured.
In the study conducted with calf mortalities (Xu et al., 2007a), the following were found: • Emission data indicated that 45% of the C in the calf mortalities was emitted as CO 2 and 19% was emitted as CH 4 .Initial and final mass and composition data indicated that 82% of C in the calf mortalities was lost, which is higher than the 64% loss indicated by the emission data.• Emission data indicated that 9% of the N in calf mortality proteins was emitted as N 2 O. Initial and final mass and composition data indicated that 39% of N in the calf was lost, which is much higher than the measured 9% loss as N 2 O.The additional loss could have been in the form of NH 3 emissions, which were not measured.
Overall the 2 composting studies by Xu et al. (2007a,b) yielded somewhat different results with respect to GHG emissions attributable to the bovine mortalities.Mass balances on C and N were not completely consistent in either study when initial windrow contents were compared with measured emissions and final compost composition.These discrepancies are not surprising given the physical size (120 m 3 ) and mass (over 100,000 kg) of each windrow and the duration of the studies (~300 d each).
The measured emission data from the 2 studies were converted to CO 2 e attributable to the bovine mortalities and scaled to a basis of 1,000 kg of meat by-products.The results are shown as a range in Figure 1.The adult mortality study indicated that GHG emissions attributable to the mortalities were 2,500 kg of CO 2 e/1,000 kg of meat by-products.The calf study indicated emissions of 4,000 kg of CO 2 e/1,000 kg of meat by-products.Because co-composting of the cattle mortalities resulted in significant emissions of CH 4 and N 2 O, both of these results are well above the GHG emissions that would have been released if all C in the meat by-products had simply been decomposed to CO 2 .

RESOURCE RECOVERY: EFFICIENCY AND ECONOMIC VALUE
This section focuses on the efficiency of resource recovery and the economic value of products that result from composting, anaerobic digestion, and rendering of animal carcasses and other meat by-products from food animal slaughter.

Composting
In the composting study with adult cattle mortalities present (Xu et al., 2007b), total nitrogen (TN) content of the final compost was 25% higher than in the control treatment without mortalities.Ammonium (NH 4 + ) content was 27 times higher, and the C/N ratio was lower.All of these differences presumably resulted from the protein content of the carcasses.Inclusion of carcasses did not have a significant (P > 0.05) effect on water content, total carbon, nitrates (NO 3 − ), or nitrites (NO 2 − ) of the final compost.In other words, it is not possible to say with 90% confidence that the final levels of these variables were affected by the presence of cattle mortalities.
The results from the study that composted calf mortalities (Xu et al., 2007a) were somewhat different.Ammonium and NO 3 − levels were each 6 times higher when mortalities were present, but these differences were not enough to make TN significantly higher.The C/N ratio was slightly lower.Inclusion of carcasses did not have a significant (P > 0.05) effect on water content, total carbon, or NO 2 − content of the final compost.
As a soil amendment, compost is claimed to have numerous benefits (USCC, 2015; EPA, 2016a).Based on the Canadian studies, however, the only significant differences between the final compost produced with cattle mortalities present were increased levels of TN, NH 4 + , and NO 3 − , with increased NO 3 − being significant in the calf study only.Overall, 11 kg (adult study) to 19 kg (calf study) of TN was contributed to the final product by co-composting 1,000 kg of mortalities.Various forms of nitrogen fertilizer are sold in North America with peak prices rarely exceeding $1/kg of TN in recent years (Knorr, 2015;ERS, 2016).Thus, the studies conducted by Xu et al. (2007a,b) indicate that co-composting 1,000 kg of meat by-products could add to the final compost as much as $10 to $20 in TN value.
The studies by Xu et al. (2007a,b) reported no data on the fate of phosphorus (P) in co-composted animal carcasses and meat by-products.On average, carcasses and meat by-products have a P content of about 1% by weight on a wet basis.The economic value of P fertilizers has averaged about $4/kg of P in the United States over the last 10 years (ERS, 2016).If all P in 1,000 kg of animal carcasses and meat by-products were converted to its maximum fertilizer potential by co-composting, this could add up to $40 in P value to the final compost produced, but it is unlikely that the full economic potential can be achieved.Larger bones that contain a significant fraction of the P in carcasses and meat by-products are not broken down completely by composting (Xu et al., 2007a,b), and the physical and chemical state of some of the P in the final compost will not be ideal for use as fertilizer.

Anaerobic Digestion
Anaerobic digestion produces crude biogas that can be burned to recover heat value or to produce electricity.Alternatively, the biogas can be refined to pipeline quality and sold.Anaerobic digestion also produces digestate that can be applied to crops as fertilizer.With the composition of meat by-products defined above (20% fat, 22% protein, and 57% water by weight), the theoretical CH 4 yield from processing 1,000 kg of by-products is 190 kg.Methane has a lower heating value of 50 MJ/kg, and a recent study valued biogas at $4.30/ GJ (Informa Economics, 2013).This implies that the biogas produced from anaerobically decomposing 1,000 kg of meat by-products could be worth as much as $40.
None of the published studies on codigesting meat by-products provided sufficient data to estimate quantitatively what fractions of the N and P in co-digested materials were left in the digestate.The maximum economic value can be estimated by assuming that all N and P in co-digested meat by-products will be retained in the digestate in a form consistent with their maximum fertilizers value, $1/kg for TN and $4/kg for P. Proteins are roughly 16% N by mass, which means that co-digesting 1,000 kg of meat by-products could yield a digestate containing 35 kg of TN as well as 10 kg of P, assuming complete retention of P in the solid or liquid phase.
In summary, the maximum possible economic value of products obtained from digesting 1,000 kg of meat byproducts is $40 for the biogas and $75 for the digestate.In reality, CH 4 yields from anaerobic digestion range from 50 to 90%, some N from proteins will be lost in the biogas during decomposition, some P contained in larger bones will not be decomposed to fertilizer grade material, and some of the N and P that is retained in the digestate slurry will not be in a physical and chemical state that justifies maximum fertilizer value.Thus, the likely range for the value of products obtained from co-digesting 1,000 kg of meat by-products is $50 and $100.

Rendering
About 1% of the OM in meat byproducts is lost to wastewater treatment during the rendering process.The other 99% is separated and sold as fat or protein meal.The market value of these products depends somewhat on the specific raw material rendered (e.g., beef tallow is usually valued somewhat higher than poultry fat), and the value of each product varies over time.Over the last 4 yr, the market value of rendered products in North America (weighted by the amount of each product in each category sold each year) has averaged $0.87/kg for fat and $0.59/kg for protein meals (Swisher, 2015).Annual averages were within ±3% of these 4-yr averages.Thus, rendering 1,000 kg of meat by-products of the basis composition would yield 200 kg of rendered fat and 210 kg of protein meal with a combined market value of $300.This is 3 to 6 times the value of products from anaerobic digestion and 5 to 10 times the value of products from composting.

Food Recovery Hierarchy
The relative market values of products obtained from rendering, anaerobic digestion, and composting are consistent with the hierarchy of sustainable food waste management developed by the US Environmental Protection Agency (EPA, 2014a).The EPA's Food Recovery Hierarchy is shown in pictorial form in Figure 2 (EPA, 2016b).
The most sustainable practice is to reduce food waste at points of production, sale, and human consumption.The next best practice is to get food that is wasted to people who need it.If this is not feasible, food waste should be fed to animals, which is the level at which rendering enters the hierarchy of sustainable practices.Currently, about 85% of rendered fats and protein meals are used as ingredients of animal feed (EPA, 2014a).The other 15% of rendered products fall into the next best practice, industrial use, which includes conversion of food waste into thermal or electrical energy.Some rendered fat is now converted into biodiesel fuel, and some fats and protein meals are converted into a variety of industrial products.Biogas produced by anaerobic digestion falls into the level of industrial use, and digestate and compost are in the next level down, nutrient-rich soil amendments.All 3 of the meat byproduct conversion processes considered here are superior to the least preferred practices on the EPA hierarchy, incineration and landfill disposal.

RESULTS AND DISCUSSION
In this study 3 methods of handling large quantities of animal carcasses and meat by-products from food animal slaughter were compared and contrasted with respect to biosecurity, environmental sustainability, efficiency of resource recovery, and economic value of products.Of the 3 processes examined rendering provides the greatest assurance that pathogens will be kept out of the food supply and the environment.The ability of the rendering process to destroy pathogens is well established, and the industry is highly regulated by the Department of Agriculture and the Food and Drug Administration in the United States and by comparable agencies in other developed countries.Anaerobic digestion can destroy pathogens if effective time and temperature conditions are ensured, but there is little experience co-digesting meat by-products on a large scale and monitoring pathogen destruction during the digestion process.Composting can also destroy pathogens, but the nonhomogeneous nature of decomposing solids makes the monitoring and assurance of pathogen destruction especially challenging.Standard procedures and regulatory oversight for biosecurity have not been established for handling carcasses and meat by-products by anaerobic digestion or composting.
In developed countries industries such as rendering are permitted to discharge only limited, well-regulated amounts of air and water pollutants and solid wastes.It is reasonable to assume that large-scale anaerobic digestion and composting operations will have to meet similar requirements, but regulations that apply to composting in particular are still developing.Greenhouse gas emissions are not currently regulated in the United States and many other countries, but most people think they should be reduced to avoid undesirable climate change.Greenhouse gas emissions from the rendering process are equivalent to converting to CO 2 and releasing about 25% of the C in the animal carcasses and meat by-products processed.In the gateto-gate analysis used in this study, anaerobic digestion emits less GHG than rendering if digestate storage tanks are sealed well.If the exit gate were extended farther downstream to examine the fate of products from each process, both biogas and diges- tate release their sequestered C in their initial use, primarily as CO 2 .Except for the small fraction of fat that is converted into biodiesel fuel, rendered products are used in ways that sequester carbon for longer time periods.With respect to GHG emissions, composting appears to be a poor choice for disposal of meat by-products (and probably for many other types of organic wastes).We found only 2 published studies that report sufficient data to conduct mass balances on C and N in co-composted animal carcasses or other meat byproducts.Emissions of CO 2 , CH 4 , and N 2 O measured during these studies indicated that total GHG emissions were 3 to 5 higher than what would have resulted from converting all of the C in the initial material to CO 2 and releasing it to the atmosphere.
Composting ranks low on the US EPA Food Recovery Hierarchy in terms of effective waste management.It produces only a relatively low-value material in comparison to anaerobic digestion or rendering.Biogas produced by anaerobic digestion is higher on the EPA hierarchy, and the combined economic value of biogas and digestate is about twice that of compost.Rendering ranks highest of the 3 processes on the EPA hierarchy because it can convert approximately 99% of the fats, proteins, and nutrients in meat by-products into valuable ingredients of animal feeds.Currently, about 85% of rendered products are used to produce feeds, with the balance going into fuels and other industrial products.Overall, the fats and protein meals produced by rendering are worth 3 to 6 times as much as the biogas and digestate produced by anaerobically digesting the same mass of meat by-products.

IMPLICATIONS
The analysis presented in this paper shows that rendering has several advantages over composting and anaerobic digestion for the safe and effective handling of large quantities of animal carcasses and meat by-products from food animal slaughter.Biosecurity is more easily ensured; health, safety and environmental regulatory requirements are clearly defined; GHG emissions are lower; and the effectiveness and economic value of resource recovery are superior.
Notwithstanding the advantages of rendering for general use, other alternatives will be preferred for handling carcasses in some circumstances.In a mass animal emergency such as an avian influenza outbreak in a poultry facility, top priorities are likely to be the quick biological stabilization and minimization of risk to the public (Miller, 2015).In such cases burning, on-site burial, or composting might be the most appropriate method of disposal.On-site composting might be the most attractive option for small farmers who occasionally need to dispose of fallen carcasses.Constructing a small compost pile certainly requires lower capital investment than purchasing and installing anaerobic digestion or rendering equipment, and maintaining of a compost pile might cost less than sending carcasses to an off-site disposal facility.For owners of large farms and feed lots, anaerobic digestion will continue to be a viable method of producing fuel and handling large quantities of manure and a relatively small mass of carcasses.
To ensure public safety and environmental responsibility, all methods used to dispose of animal carcasses and meat by-products from food animal slaughter must be subject to appropriate regulatory constraints.In any situation, if biosecurity and regulatory compliance can be ensured by more than one alternative, cost is likely to be a major factor in the final choice.

Figure 1 .
Figure 1.Gate-to-gate comparison of rendering, co-digestion, and co-composting 1,000 kg of meat by-products in terms of greenhouse gas (GHG) emissions and economic value of products.CO 2 e = carbon dioxide equivalent.