Summary and conclusions, Danish Environmental Protection Agency

Occurence and survival of viruses in composted human feaces

Summary and conclusions

Recycling of organic waste reduces the environmental and economical problems associated with waste disposal. Any type of organic waste, including human faeces and urine, can be recycled and utilized for agricultural or other purposes, avoiding recourse to waste disposal and allowing return of nutrients to soils and plants. In Denmark, there is an increased interest in recycling of human excreta. Compared with traditional sewerage-based sanitation systems, this practice regards human excreta as a resource to be used rather than as a waste to be disposed. Recycling of human excreta benefits the environment and may contribute to production of safe agricultural products by avoiding the use of chemical fertilisers.

The reuse of excreta requires a process of stabilization, which consists in the degradation of organic matter accompanied by elimination of pathogenic organisms, reduction of the total mass and removal of undesirable odours. Composting represents a suitable method for stabilization of faecal material. The process of composting is based on the decomposition of organic matter by microorganisms under aerobic conditions. Aeration can be provided by means of blowers and air diffusers in aerated static pile and enclosed (in-vessel) systems, or by periodical turning of the composting heap in windrow systems. This report only addresses survival of viruses during centralised controlled composting, as decentralised composting, e.g. at the household level, is less likely to generate the adequate heat required for virus inactivation. Also, control of temperature and other parameters are often not possible in decentralised composting systems.

The aim of this report is to provide the knowledge necessary to evaluate the possible occurrence of pathogenic viruses in human composted faeces, with particular regard to the conditions existing in Denmark. The report contains a review of the literature on the occurrence of pathogenic viruses in human faeces and their survival during storage, treatment and utilization of composted faeces. The information available on this subject was scarce and scattered over the literature. Therefore, the Danish Environmental Protection Agency identified the need to collect such information and make it available for decision-making and risk assessment in relation to future recycling of human excreta.

Based on this review, none of the presently known viral pathogens occurring in human faeces appears to be able to survive composting if the process is properly managed according to the current legislation on composting in Denmark and other European countries. In particular, exposure to 55° C for two weeks (i.e. controlled composting) or 70° C for one hour (i.e. controlled sanitation), as required by the Danish legislation, appears to ensure a complete inactivation of all pathogenic viruses occurring in human faeces.

Viral inactivation during composting is mainly due to the heat generated by microbial degradation, which determines irreversible damage of the viral structure To a lesser extent, viruses are also inactivated by the antiviral activity of proteolytic enzymes produced by bacteria and by ammonia released as a consequence of protein degradation.

The efficiency of composting in viral inactivation has been demonstrated by several studies on composting of sewage sludge, animal faeces and other types of organic waste. Nevertheless, some studies have pointed out the difficulty in maintaining the necessary parameters (i.e. temperature, aeration and moisture content) and controlling them in the routine practical operation, in particular for windrow systems.

The monitoring and documentation of key parameters like temperature, aeration and moisture are essential to ensure a complete inactivation of viruses during composting. Enclosed systems are the safest systems for composting of human faeces, as they ensure a better control of such parameters. In contrast, windrow systems do not guarantee efficient heat exposure and virus elimination due to the influence of ambient temperature on the surface of the windrows. Static aerated piles have an intermediate efficiency in pathogen removal and their use is suitable for situations where the use of close reactors is not affordable.

Independent of the system used, viruses can survive the composting process only if certain zones of the heap are not exposed or exposed for too short times to the temperatures required for viral inactivation. In order to ensure the safety of the final product, it is necessary to monitor the efficiency of composting plants in pathogen reduction. Different systems are available for this scope, including direct process validation (i.e. "germ-carriers" inoculated with viral indicators are inserted into the heap and analyzed at the end of the composting process), indirect process supervision (i.e. control of temperature, dry matter and pH within the heap) and end-product analysis.

Virus survival in composted human faeces depends not only on the conditions used for composting, but also on the storage conditions. Virus numbers decrease during storage of faeces, due to their incapability to replicate outside of the host and susceptibility to environmental conditions. However, the die-off rate of viruses present in human faeces is extremely variable depending on both the type of virus and the storage conditions. While 100 days of storage appear to be sufficient to determine complete inactivation of enteroviruses, hepatitis A virus (HAV) is reduced only 1-2 log units when contaminated manure is stored for 70 days at low ambient temperature.

The presence of enteric viruses can be substantially reduced during storage by enhancing high pH and low moisture conditions. Alkaline conditions can be achieved by the addition of wood ash, lime or other alkaline substances. Faecal dehydration may be enhanced by the addition of different substances, e.g. soil. The effect of aeration on virus survival in faeces should be further studied with the scope to develop possible applications in the design and construction of urine-diverting toilets.

The most important pathogenic viruses shed in human faeces are adenoviruses, astroviruses, caliciviruses, enteroviruses, HAV, hepatitis E virus (HEV) and rotaviruses. All these enteric viruses lack an envelope, which make them relative resistant to heat and acid pH conditions compared with enveloped viruses. The most heat-resistant human pathogenic virus is HAV, for which temperatures of 60° C for 30 min or 80° C for 10 min have been reported not to be sufficient for complete inactivation. However, even HAV is inactivated under temperature conditions comparable to those used for composting (e.g. 60° C for 10 hours).

In Denmark, all the major groups of enteric viruses are present in the population except for the HEV, the presence of which is mainly limited to developing countries. The incidence of HAV was estimated to be about 1.5 cases per 100.000 inhabitants in the year 2000. Rotaviruses are more common than other viruses causing diarrhoea in young children (adenoviruses, astroviruses and caliciviruses). The occurrence of enteroviruses in faecal specimens from symptomatic patients is around 13-23%. Caliciviruses have been found to be implicated in approximately 40% of food-borne disease outbreaks.

Based on data on the occurrence of viruses in sewage in Denmark which has been estimated to 10³ to 10⁵ PFU/100 g for enteroviruses (including HAV) and 2 to 10² PFU (Plaque Forming Units)/100 g for rotaviruses, the concentration of viral particles in human faeces collected for composting would be expected to exceed these numbers. Adenovirus, astrovirus and rotavirus should be more frequent from late autumn to early spring, whereas enteroviruses are likely to be more common during the summer period.

Enteric viruses can persist for a long time after application of contaminated sludge to soil, as demonstrated by their recovery in sludge burials 6 months after the last sludge disposal. High temperature and low moisture are the two main factors affecting the persistence of viruses in soil. Accordingly, viruses seem to persist longer during the winter than during the summer. The persistence of viruses in soil is also influenced by the type of soil, with clay soils allowing a longer survival of viruses compared with sandy and muck soils. HAV has appears to survive in soil longer than other enteric viruses.

No studies are available on the risks posed to human health by the use of composted human faeces. A recent risk assessment study has estimated that urban waste compost does not contain adequate levels of Salmonella and parasites to represent a risk for human health. It should be noted that viruses are generally characterised by lower infective doses (1 to 10²) compared with bacteria (10² to 10⁶). However, differently from bacteria, viruses are not capable of replicating outside of the human body. Consequently, low numbers of viruses accidentally survived to composting cannot multiply during storage of the compost product or after its application to land.