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Occurence and survival of viruses in composted human feaces

1 The composting process

1.1 Introduction

An important problem that the modern society has to face is the disposal of increasing quantities of waste. The European Union alone produces approximately 1,300 million tonnes of waste per year /1/. Due to the environmental and economical concerns associated with sanitary landfilling and incineration, increasing attention has been given to the practice of recycling and to the use of organic waste for agricultural purposes.

Organic waste products are rich in organic carbon and relatively poor in inorganic nitrogen, which is more bioavailable for plants compared with organic nitrogen. The reuse of organic waste in agriculture requires a process of stabilization ("maturation"), which consists in the degradation of organic matter accompanied by a transformation of organic forms of nitrogen into inorganic forms, reduction of the total mass, elimination of pathogenic organisms and removal of undesirable odours.

Composting is one method for stabilization of organic waste products. Other methods include aerobic digestion, anaerobic digestion, lime stabilization and heat treatment /2/. Composting is based on the decomposition of organic matter by microorganisms under aerobic conditions. The types of waste materials most commonly used for production of compost are yard waste, sewage sludge, municipal solid waste, household waste, industrial and agricultural by-products (wood, animal droppings, etc.).

Composting is regarded as a fully sustainable practice, since it aims at both conservation of the environment, human safety and economically convenient production /3/. The use of compost contributes to conservation of the environment by reducing both utilization of non-renewable resources and consumption of energy for waste treatment and production of chemical fertilizers. Composting indirectly also contributes to human safety by avoiding an improper fate or disposal of organic wastes. Furthermore, due its low cost, compost is convenient to the farmer, but even more to the society by avoiding the use of expensive solutions for waste disposal.

1.2 Process description

Composting is an aerobic process during which microorganisms convert an organic substrate into stabilized organic matter with production of heat. The process generally starts by mixing dewatered organic waste with a bulking agent, such as wood chips, yard trimmings, bark, rice hulls, municipal solid waste or previously composted material. Bulking agents are used to add a source of carbon, lower moisture content, provide structural support, increase porosity and favour aeration. The mixture is then composted in the presence of air for a period of 2-4 weeks depending on the type of system used, followed by a maturation phase (curing) of approximately the same duration. Finally, the compost product can be screened to remove unwanted components or to recover the bulking agent, and prepared for a particular market and purpose.

The composting mass is a dynamic microbial ecosystem, in which different groups of microorganisms develop and become predominant during the different phases of composting. The process consists of at least three different phases: the mesophilic phase, thermophilic phase and the maturation (curing) phase.

During the mesophilic phase, mesophilic bacteria utilize readily available organic matter, determining a rapid increase of temperature. The temperature can reach 55° C in a few days and go up to 80° C if the system is not properly controlled /4/. The increase of temperature is accompanied with a radical change in the physical and chemical characteristics of the initial waste material.

The thermophilic phase is characterized by the growth of thermophilic bacteria, fungi and actinomycetes. Among the thermophilic organisms found in compost, there are various species of fungi, actinomycetes and endospore-forming bacteria (mainly Bacillus spp.)/5-7/. Thermophilic bacteria play an important role in the degradation of proteins and carbohydrates, whereas actinomycetes and fungi contribute to the degradation of more complex compounds like cellulose and lignin /2/.

During the maturation phase, the low amount of readily available nutrients determines a reduction in the microbial activity and consequently in the production of heat. This phase allows further stabilization, reduction of pathogens and decomposition of cellulose and lignin. Particularly important during this phase is the formation of humic and fulvic acids, which confer valuable fertilization properties to the compost product.

1.3 Systems of composting

Although there exists a number of different composting methods and technologies, there are three main systems of centralised composting: aerated static pile process, windrow process and enclosed systems. The following paragraphs provide a short description of each system. Small-scale technologies for decentralised composting at the household level are also briefly described.

1.3.1 Aerated static pile systems

This system consists in the formation of piles of dewatered organic waste mixed with a bulking agent. The piles can be covered with screened compost to reduce odours and to maintain a high temperature inside the pile. Aeration is provided by means of blowers and air diffusers (Fig. 1.1). Aerated static piles are most commonly used for homogeneous materials (e.g. sludge) and are not appropriate for heterogeneous materials that need to be mixed during composting (e.g. municipal solid waste).

1.3.2 Windrow systems

The windrow system is the least expensive and most common approach. The mixture of dewatered organic waste and bulking agent is stacked in rows called windrows and the composting mass is aerated by turning the windrows either manually or mechanically (Fig. 1.1). Turning programs are generally designed to ensure the different aeration rates required during the different phases of the composting process. Alternatively, temperature can be used as a turning indicator, so that windrows are turned when a certain temperature (usually 55 or 60° C) is reached.

1.3.3 Enclosed (in-vessel) systems

These systems are enclosed into containers (i.e. vessels) to ensure control of temperature, oxygen concentration and odours. Due to their high cost, enclosed systems are particularly appropriate when a high quality of the compost product is required. The vessel can be anything from a silo to a concrete-lined trench. The silo-type systems rely on gravity to move the composting material through the vessel, whereas in other enclosed systems (e.g. agitated bed system), the material is moved through the vessel by mixing, combining the advantages of windrow and aerated static pile systems (Fig. 1.1).

Fig. 1.1.
Schematic description of the main systems of centralised composting.

A number of different containers are used to collect and store human faeces at the household level. Often such containers or vaults are simple plastic units located beneath the toilets, i.e. urine-separating toilets. The containers often have a lid with an inserted ventilator for removal of malodour. In addition to faecal matter, containers will contain toilet paper, various amounts of urine and the users may also add saw dust or other substances to maintain a relative dry environment and enhance the composting process.

Little composting and temperature development seems to be occurring when faecal matter is collected and stored at the household level. This is mainly caused by nearly anaerobic conditions and a low content of organic matter. Thus, only minor reductions in pathogen numbers can be expected in the majority of such decentralised systems for collection and storage of faeces. Faeces collected in decentralised systems will therefore most often need to be transported and composted in centralised systems if reductions in pathogens are to be obtained according to current legislation (sections 1.3.1-1.3.3).

1.4 Factors to be controlled during composting

Several physical and chemical parameters influence the activity of microorganisms during composting. Temperature, aeration and moisture are the most important parameters /8,9/. Their control is essential to ensure both stability and hygienic safety of the final product.

1.4.1 Temperature

Temperature is probably the most important factor to be controlled during composting. While temperatures between 45 and 55° C ensure the best degradation rates of the compost material, temperatures above 55° C maximize pathogen reduction /9/. Above 60° C, the degree of microbial diversity is markedly decreased, with negative consequences on the degradation process /10/. Accordingly, the choice of the operational temperature will influence both the stability and the hygienic quality of the final product.

A wide variation of temperature can exist within the composting mass. For example, in aerated static pile systems the core temperature can reach 70° C, while the outer zone remains near ambient temperature /11/. Temperature is controlled by adjusting the aeration levels in the case of aerated systems or by turning the windrows in the case of windrows systems. Particular systems have been developed to ensure that the air supply rate is appropriate to the composting requirements of the local mass /9/. This is unlike traditional systems, where the same supply rate is applied to the whole of the mass regardless of the degradation stage.

1.4.2 Aeration

Aeration provides oxygen to the aerobic organisms necessary for composting. In general, anaerobic conditions prolong the duration of the composting process and, above all, lead to relatively lower temperatures with adverse effects on sanitation. Oxygen is not only necessary for aerobic metabolism of microorganisms, but also for oxidizing the various organic molecules present in the composting mass /8/. Aeration has also the important function to control temperature as well as to remove the excess of moisture and gases.

The air requirements for composting depend on the type of waste, the process temperature to be reached, the stage of the process (i.e. higher requirements in the early stages) and the moisture content. Air can be supplied by agitation in the windrows process, by forced aeration in the aerated static piles or by a combination of the two in aerated/agitated systems.

1.4.3 Moisture

Moisture control is also an important factor to be controlled during composting as it influences structural and thermal properties of the material, as well as the rate of biodegradation. The initial moisture content generally varies between 55 and 65% depending on the material used /9/. During composting, a loss of water occurs as a consequence of evaporation. Reduction of the moisture content below 30-35% must be avoided since it causes a marked reduction of the microbiological activity and a premature end of the process due to exsiccation. Too much moisture should be also avoided as it interferes with aeration by clogging the pores in the composting heap /8/.

There is not a target value for the final moisture content. Most composting processes operate with moisture contents between 40-60%. In agitated or turned systems, a trained operator is able to evaluate whether the material is too dry or too wet and make appropriate adjustments. This is in contrast to aerated static pile systems, where a measurement of the moisture content is needed. However, the wide variation in the moisture contents throughout the pile mass makes such measurement difficult /9/. Moisture can be controlled either directly by adding water or indirectly by changing the operating temperature or the aeration regime.

1.4.4 Carbon/nitrogen ratio

The control of the ratio of carbon to nitrogen (C/N ratio) is important because the microbes responsible for the degradation process need adequate levels of nitrogen. The optimal carbon/nitrogen (C/N) ratio in the starting material is around 25 /8/. A too low C/N ratio slows decomposition and increase nitrogen loss through ammonia volatilisation, especially at high pH and temperatures values. A to high C/N ratio (>35) delays the process, since microorganisms must oxidize the excess of carbon until a more convenient C/N ratio for their metabolism is reached /8/. The C/N ratio of the starting material can be adjusted prior to composting. In the case of human faeces, the addition of a carbon source (e.g. bark, wood shavings or straw) is needed due to their low C/N ratio /5-10//12/.

1.5 Properties and use of compost

The compost product is a humus-like material with excellent properties as a fertilizer. Compost enhances plant growth by providing nutrients, improving root penetration and in some cases reducing plant disease. The positive effect of certain compost products on plant disease control has been attributed to competition for nutrients, antibiotic production and predation by beneficial microorganisms, as well as activation of disease resistance genes in plants /13/. Depending on the degree of maturity and quality, compost can be used in vine yards, mushroom farming, agri- and horticulture, reforestation, preparation of sport fields, maintenance of parks, gardens and motor-way embankments, and rehabilitation of mines and sand pits.

Compost, especially when derived from biosolids, contains less nitrogen and nutrients compared with other types of treated organic waste as a consequence of dewatering, dilution of nutrients by addition bulking material and loss of ammonia during the composting process. However, nutrients are released more slowly and are available to plants over a longer period of time /14/. The slow release of nutrients is more consistent with plant uptake needs and reduces leaching of nitrogen, which is an important environmental concern associated with the use of other types of conventional fertilizers and soil conditioners /15/.

Compost is not only a good fertilizer but also an excellent soil conditioner. Application of compost to land improves aeration, water-holding capacity, nutrient content and structure of the soil. Due to these properties, compost is also effectively used for landscaping, erosion control, landfill cover, turf remediation, alleviation of compacted soil, and wetland restoration /16,17/.

Compost used for a specific purpose is more efficient when specially designed (i.e. tailored compost). For example, compost intended to prevent erosion may not give the best results when used to alleviate soil compaction. Tailored compost is adjusted to fit a specific application and soil type by controlling the maturity, pH, density, particle size, moisture, salinity and organic content of the final product.

Innovative uses of compost are bioremediation and biofiltration /18/. Compost bioremediation refers to the use of microorganisms in a mature, cured compost to sequester or breakdown contaminants in water or soil. This practice has proven effectiveness in degrading or altering many types of contaminants, such as chlorinated and non-chlorinated hydrocarbons, wood-preserving chemicals, heavy metals, pesticides, petroleum products and explosives /18,19/. Compost biofiltration implies the physical removal of contaminants in water or air by filters composed by multiple layers of tailored compost. This practice has been successfully used for separation of physical debris, surface scum and chemical contaminants from stormwater (i.e. stormwater management), as well as for disposal of volatile organic compounds and odour control /18/.

1.6 Hazard to man and the environment

The use of compost may be associated with hazards to man and the environment. Depending on the original raw material, compost products may contain various chemical and microbiological contaminants causing health and environmental risks. Man and the environment are exposed to contaminants during production, storage and utilization of compost. Fig. 1.2 summarizes the different means and routes of contamination and their risk implication.

Fig. 1.2.
Pathways of contamination with chemical and microbiological pollutants during production and utilization of compost. Adapted from Déportes et al. /20/.

1.6.1 Chemical risk

Composts can contain a wide range of toxic substances, including inorganic and organic compounds. The contamination of the finished product generally originates from the primary material. Composts derived from municipal solid wastes, sewage sludge and yard wastes may contain relative high concentrations of toxic chemicals. In the case of composted human faeces, contamination with toxic chemicals seems to represent a relative minor hazard also when composted human faeces are used as fertilizers in agriculture.

The most important class of toxic compounds that can occur in compost is represented by heavy metals. These elements have the characteristics of being highly toxic and scarcely biodegradable. According to a recent risk assessment study /20/, the highest risk is associated with hand-mouth contact and ingestion by children of compost heavily contaminated with cadmium, chromium, lead or mercury. The risk that humans are seriously exposed to metals through the food chain appears to be lower, since most compounds do not accumulate in vegetables, and accumulate in offal rather than in meat of animals /20/.

Although the chemical risk associated with the application of compost to soil appears to be of little importance, heavy metals persist in soil for many years and repeated application might lead to an accumulation of these pollutants. For this reason, both European and American regulations define not only concentration limits in compost, but also concentration limits in soil and maximum annual loads /21,22/.

1.6.2 Microbiological risk

The microbiological risk associated with the production and the use of compost is the possible infection of humans, animals or plants by pathogens occurring in raw materials used for composting as well as by pathogens developing during the composting process.

Human and animal pathogens are particularly frequent in raw material when such material contains faecal matter, food residuals or animal wastes. The principal pathogenic bacteria, helminth and protozoan parasites occurring in human faeces are listed in Table 1.1. The occurrence of pathogenic viruses in human faeces is presented and discussed in chapter 2.

Table 1.1.
Main pathogenic bacteria, helminths and protozoa excreted in human faeces. Adapted from Feachem et al. /23/ and U.S. Environmental Protection Agency /24/.

The microbiological hazard to humans arising from spreading of compost appears to be low if adequate temperatures and exposure times have been obtained during composting /25/. The heat generated during the oxidation process destroys most pathogens present in raw materials. Furthermore, the composting mass turns to be an unsuitable substrate for the growth of some pathogens due to loss of moisture, depletion of nutrients and microbial antagonism /25/. A recent risk assessment study has estimated that compost does not contain adequate levels of Salmonella and parasites to represent a risk for human health /20/. According to this study, the infective dose of E. coli (10⁶) is not likely to be reached after ingesting a mixture of soil and compost, whereas the infective dose of enterococci (10⁹) may be attained only in cases of pica.

Plant pathogens may be present in residues of infested plants used for composting (e.g. composting of yard waste). The risks of plant infection are very low for most soil-born viruses, as the vectors (nematodes or fungi) needed for plant infection are destroyed during composting /26/. Higher risk are associated with the presence in raw materials of the tobacco mosaic virus (TMV), as this virus is not completely inactivated during composting and can be directly transmitted to plant roots without a vector. Accordingly, compost from plant residues infested by the TMV should not be used in susceptible crops /26/.

Some fungi and bacteria developing during the process of composting constitute a potential risk for both workers at composting plants and users of compost /15,20/. These organisms are bound to dust produced during composting and can heavily contaminate the atmosphere of composting plants /27/. The most frequently studied organism is the fungus Aspergillus fumigatus, an opportunist pathogen causing allergies, asthma and respiratory infections. Risks derive not only from living organisms, but also from spore and endotoxins of bacterial origin /15,20/.

The consequences of this form of air pollution (i.e. bioareosol) on occupational health are not clear. The available epidemiological studies are inadequate to determine whether exposure to bioareosol have a significant impact on human health /28/.

1.7 Legislation

This section introduces the current legislation on production and use of compost in Denmark, in the EU and in the USA. None of the current regulations specifically address the sanitary aspects regarding composted human faeces. The production and the use of compost originating from human faeces are generally regulated by the legislation on sewage sludge.

1.7.1 In Denmark

According to the Danish legislation /29,30/, compost derived from sewage sludge can be used without sanitary restrictions only if it has been processed in a closed reactor and exposed to minimum 70° C for at least one hour (controlled sanitation). The compost product has to be free of Salmonella spp. and may contain less than 100 CFU of faecal streptococci per g of finished product. Composted sewage sludge derived from open-air systems cannot be used as a fertilizer in edible crops or parks. When applied to forest soils, the forests must be closed to the public for a period of 6 months. The application of sewage sludge on grassland is prohibited for one year before grazing, and on forage crops before harvesting.

Organic waste other than sewage sludge can be treated by controlled composting (³ 55° C in all material for at least two weeks) without any sanitary restriction. The only exception is given by composted household waste, which has to be plough in when applied to areas used for cloven-footed animals. Details about the Danish guidelines can be seen elsewhere /29,30/(http://mst.dk/).

1.7.2 In the EU

The EU strategy for waste management is based on minimization, reuse, material recycling, energy recovery and safe disposal. Since 1975, the Member States have to take appropriate steps to encourage the prevention, recycling and processing of waste, and to ensure that waste is disposed without endangering human health or without harming the environment /31/.

The EU directive of 1986 on sewage sludge invited the Member States to prohibit the use of untreated sludge in agriculture and the use of any type of sludge in grassland to be grazed, in forage crops to be harvested within a short period and in grounds intended for the cultivation of fruit and vegetables which are in direct contact with soil and normally eaten raw /21/. Furthermore, the directive established the concentration limits of heavy metals in soil and sludge, and defined the maximum quantities of heavy metals that can be introduce into soil per unit of area and time.

In 2001, the Commission communicated to the Council and the European Parliament its intention to broaden the sewage sludge directive to cover all types of sludge and all land spreading operations (not only use in agriculture) /32/. In the same year, a working document was draft by the EU Directorate of General Environment as a basis for preliminary discussions to improve the present legislation for biodegradable waste management /33/.

1.7.3 In the USA

The production and use of compost is regulated in the Part 503 rule of the Environmental Protection Agency (EPA)/34/. The rule is based on 3 parameters for determining the quality of biosolids, i.e. sewage sludge which has been treated and meets state and federal standards for land application: presence of pollutants, presence of pathogens and attractiveness to vectors (e.g. rodents, birds, flies or mosquitoes). Biosolids that meet the most stringent limits for all 3 parameters are designated as Exceptionally Quality (EQ). These products are exempted from the general requirements, management practices and site restrictions defined in the EPA Part 503 rule. They can therefore be used with no more restrictions than any other fertilizer or soil amendment product.

The first parameter that must be assessed to determine the overall quality of biosolids is the levels of pollutants. EPA chose to determine the pollutant limits based upon a scientific risk assessment. The risk assessment process considered 14 representative pathways by which humans, animals and plants are exposed to pollutants present in biosolids /35/. Details on pollutant limits can be found in the EPA website (http://www.epa.gov/).

The second parameter in determining biosolids quality is the presence of pathogens. The EPA Part 503 rule states that the producer is responsible for monitoring and certifying pathogen reduction. Two classes of biosolids (A and B) are defined based on pathogen density limits (Table 1.2). In addition to the requirements on pathogen density, class A biosolids must be treated by one of the Processes to Further Reduce Pathogens (PFRP), such as composting, heat drying and high-temperature aerobic digestion. For class B biosolids, producers may document compliance by analysing the material for faecal coliform levels (Table 1.2). Alternatively, class B biosolids must be treated by one of the Processes to Significantly Reduce Pathogens (PSRP), such as aerobic digestion, anaerobic digestion, air drying and lime stabilization /34/.

Table 1.2.
Pathogen density limits for land application of biosolids in the USA /34/.