Killing Potential Pathogens in Compost – Cold and Calculated

There is hope that smaller communities and institutions who want to compost their own organic waste can do so safely and produce a pathogen free compost. Its been traditionally understood that if we can’t achieve temperatures of > 55 C during composting, we have no hope of killing the potential pathogens and the resulting compost is not safe.

Based on the information reviewed in the last few blogs, as well as our own experience with small scale composting, we are able to produce a pathogen free compost on the small scale. During the review in the last few blogs, we learned that:

  1. pathogen kill during composting is as much about the microbial community as it is about temperature
  2. 40% of compost in small scale composters met the Class A compost requirements – while 60% of large scale composters met requirements for Class A compost

Our own experience with small scale composting confirms that Class A compost can be achieved at lower temperatures. During our compost operator training in November 2016, we created a 100 kg compost recipe that included at least 25% catering waste, 10% poultry litter and yard waste. It was composted for two weeks in an insulated composter, where it achieved 55 C for 2-3 days. We knew that the material on the edges did not meet the requirements for pathogen kill. Following the two weeks of composting, we screened the material to < 1″, placed the material in a garbage bucket outside with a lid, and promptly forgot about it.

As we were preparing for the April compost operator course, we tested the material in the bucket. On November 18, 2016, the compost contained > 2080 MPN/g of both E.coli and fecal coliform. In a second measurement on March 27, 2017, the compost contained < 6.1 MPN/g of both E. coli and fecal coliform.

Was this an anomaly or could this be repeated? We made two batches of compost that included 30-50% food catering waste and the balance yard waste. Again, it was composted for two weeks, screened to < 1″, and placed in covered garbage buckets. This time we thought we would follow it along a bit more closely – and what we found was fascinating! E.coli and fecal coliform counts started high, but actually went higher before dropping and being no longer measureable!

E. coli counts in two small scale batches of compost stored in garbage buckets outside at about 20 C.

E. coli counts in two small scale batches of compost stored in garbage buckets outside at about 20 C.

The data confirm that pathogen free compost can be achieved at cooler temperatures by paying attention to the microbial community.

From our observations so far, it appears that potential pathogen kill was faster at moisture contents of 60% compared to moisture contents of 50%. We are currently testing this theory with another batch of compost that is currently sitting right beside my desk in our office!

We will report on that later as well as on practical implications of VNBC (viable but not culturable) organisms in finished compost.

In the next few blogs, we will focus on the fascinating topic of odour during the composting process.

 

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Helping us Pass the Sniff Test for Composting – the Amazing Actinobacter

The Sniff Test helps us produce great compost with minimal negative effects for our communities. If we get the composting process right, we allow the Actinobacter to flourish. Actinobacter produce geosmin, a compound that we can smell in the parts per trillion which gives the compost a pleasant earthy odour (Gerber and Lechevalier 1965).

“Freshly plowed soil has a typical odor which was undoubtedly detected even by primeval men and extolled in all tongues by bucolic poets” (Gerber and Lechevalier 1965)

The flourishing of Actinobacter during composting has been termed as a sign of composting success (Arnold 2011). Who are the Actinobacter and why should we be amazed by them? Actinobacter are a group of filamentous fungi like bacteria that used to be called Actinomycetes.

“Actinobacter are Gram-positive bacteria that constitute one of the largest bacterial phyla, and they are ubiquitously distributed in both aquatic and terrestrial ecosystems. Many Actinobacteria have a mycelial lifestyle. They have an extensive secondary metabolism and produce about two-thirds of all naturally derived antibiotics in current clinical use, as well as many anticancer, anthelmintic and antifungal compounds. Consequently, these bacteria are of major importance for biotechnology, medicine and agriculture” (Barka et al. 2016.)

Some Actinobacter thrive at thermophilic composting temperatures in the 55-65 C range and are important for decomposition of lignin and celluloses, as well as killing potential pathogens.

“Thermophilic actinobacteria thrive at relatively high temperatures ranging from 40-80 C. These are of two types: strictly thermophilic and moderately thermophilic actinobacteria. The former can grow in the temperature range between 37 and 65 C, but optimum proliferation takes place at 55-60 C. While moderately thermophilic actinobacteria thrive at 28-60 C and require 45-55 C for optimum growth, another group known as thermotolerant actinobacteria can survive at temperatures up to 50 C.” (Shivlata and Satyanarayana 2015).

Many of us, including myself, were aware and taught that Actinobacter were important in the composting process, but they were not very active until later in the active composting sate and during curing (Environment Canada 2013). I stand corrected, and now join others who had already figured out that Actinobacter are very important, even in the primary thermophilic phase of the composting process. I learned by experience in our small scale composter, where the white Actinobacter were obvious even after one week of composting food waste at high temperatures! I also learned that when the composting process is going well, we can smell that earthy smell even after one week.

Actinobacter growth in 50% food waste compost after one week of composting - adequate aeration and temperature management is the key.

Actinobacter growth in 50% food waste compost after one week of composting – adequate aeration and temperature management is the key.

Actinobacter were identified as important primary decomposers during the thermophilic composting of sewage sludge within the first few days of composting (Nakasaki et al. 1985). They observed that the Actinobacter did not grow at temperatures above 70 C.

During composting of municipal organics in Sweden, Actinobacter comprised less than 10% of the microbial population at a full-scale composting plant, whereas earlier observations in a pilot study indicated that Actinobacter constituted 50% of the microbial population during composting (Steger et al. 2007). In further work in Finland, it was noted that the presence of Actinobacter in the thermophilic stage indicated a fast, well-aerated composting process, whereas Clostridium spp (producers of bad odor) indicated an oxygen limiting environment even at high temperature and high pH (Partenan et al. 2010).

We can conclude that there is at least a double benefit to encouraging Actinobacter to flourish at our composting facilities:

  1. Actinobacter produce geosmin, which has a more positive and earthy odour, rather than the disagreeable odours that may of us are familiar with at compost facilities and
  2. Actinobacter produce compounds known to discourage pathogens, not only in the composting process, but also plant pathogens when the compost is used for crops.

Its all about the Sniff Test! With good design of our compost facilities and good management of the composting process, we can do it!

References

Arnold, P. 2011. Actinomycetes: The Sign of Composting Success. Compost Council of Canada. Atlantic Regional Workshop, Halifax , NS. March 15, 2011

Barka, E.A., P. Vatsa, L. Sanchez, N. Gaveau-Vaillant, C. Jacquard, H-P. Klenk, C. Clement, Y. Ouhdouch and G.P. van Wezel. 2016.  Taxonomy, physiology, and natural products of Actinobacteria. Microbiol. Mol. Biol. Rev 80: 1-43 doi:10.1128/MMBR00019-15

Environment Canada. 2013. Technical Document on Municipal Organics Processing. ISBN: 978-1-100-21707-9

Gerber, N.N. and H.A. Lechevalier. 1965. Geosmin, an Earthy-Smelling Substance Isolated from Actinomycetes. Applied Microbiology: 13: 935-938.

Nakasaki, K. M. Sasaki, M. Shoda and H. Kubota. 1985. Effect of temperature on composting of sewage sludge. Applied and Environ. Microbiol: 50: 1526-1530.

Partanen, P. J. Hultman, L. Paulin, P Auvinen and M. Romantschuk. 2010. Bacterial diversity at different stages of the composting process. BMC Microbiology 2010. 10:94 http://www.biomedcentral.com/1471-2180/10/94

Shivlata, L. and T. Satyanarayana. 2015. Thermophilic and alkaliphilic Actinobacteria: biology and potential applications. Frontiers in Microbiology doi:10.3389/fmicb.2015.01014

Steger, K., A.M. Sjogren, A Jarvis, J.K. Jansson and I. Sundh. 2007. Development of compost maturity and Actinobacteria populations during full-scale composting of organic household waste. J. Applied Microbiol: ISSN 1364-5072 doi:10.1111/j.1365-2672.2006.03271.x

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High Airflow Rates Reduces Odor and Kills Pathogens Faster

Supplying adequate air to composting material, particularly in the first week, dramatically reduces the potential for odour emission later. It appears that adequate aeration early in the process also encourages a microbial community that is antagonistic to potential pathogenic organisms. While traditionally we have thought that the greatest requirement for aeration is heat removal, it appears that the greatest requirement for air in the first few days or week of composting is to provide adequate oxygen.

How much air is enough? Recommendations from the literature suggest from 5.6 m3 air per tonne per hour (Smet and Langenhove 1998),  6-10 m3 air per tonne per hour (Shen et al. 2011), to more than 30 m3 air per tonne per hour (Arslan et al. 2011). The volume of air also depends primarily on the readily available carbon in the composting material. The size of the pile, the moisture content and bulk density affects the ability of the air enter and be distributed in the compost pile.

In our small scale experiments, we observed natural convective aeration rates up to 100 m3/air/dry tonne with 25-35% food waste and 65-75% yard waste.

Temperature of a food waste yard waste blend and corresponding airflow into the bin

Temperature of a food waste yard waste blend and corresponding airflow into the bin

Oxygen concentrations remained above 18%. We observed that when we restricted airflow, oxygen concentrations could drop to 0-1% within 24 hours during the first few days of composting.

We blended the composting material after one week. At that time there was already negligible odor. After the end of the second week, the distinct odor associated with Actinobacteria (geosmin, or an earthy smell) was obvious. We further noticed that after three months of further curing, the fecal coliform and E. coli was not detectable.

These observations have also been made by others in large scale compost facilities. In some excellent research in Scandinavia, Sunberg et al. (2013) observed that aeration rates of 25 m3/h/dry tonne during composting of foodwaste/yardwaste blends dramatically reduced odour and increased populations of Actinobacter and Bacillus, compared with aeration rates of 1.5-3 m3/h/dry tonne, which resulted in dramatically increased odor throughout the composting process, as well as a proliferation of anaerobic bacteria. They concluded:

“An important strategy for reducing odour from food waste composting is to rapidly overcome the initial low pH phase. This can be obtained by a combination of high aeration rates that provide oxygen and cooling, and additives such as recycled compost.”

There are a number of practical recommendations resulting from the requirement for high aeration rates early in the composting process:

  1. The compost facility must be designed to provide and allow high enough aeration rates that encourage the beneficial microbes that eliminate odour and pathogens.
  2. The compost facility must be designed with adequate odour control to manage the high rates of air emission during the first few days of composting. This is the period where potential odour compounds already present in the composting material may be released into the air.
  3. Because the compost dries quickly at these high aeration rates, the compost system must allow turning or mixing the material after 1-2 weeks.
  4. After 1-2 weeks, odour control requirements may be minimal if the compost continues to be managed properly.

In conclusion, our nose is an incredible tool. If we smell compounds characteristic of anaerobic activity, we are likely to have sustained odour and possibly sustained potential pathogens in our compost. On the other hand, when the compost smells like earth after a week or two, we may be more likely to have successful pathogen kill.

The fascinating facts here is that our nose is very sensitive to both the unpleasant smells associated with anaerobic activity such as butyric acid, as well as the positive smells such as geosmin associated with Actinobacter. Our noses can detect both butyric acid (unpleasant smell), and geosmin (earthy smell) at concentrations of parts per trillion.  Its an amazing world!

References

Arslan, I, U. Ayhan, and M. Topal. 2011. Determination of the effect of aeration rate on composting of vegetable and fruit waste.  Clean Soil Air Water DOI 10.1002/clen.201000537

Shen YJ, Ren LM, Li GX, Chen TB, Guo R. 2011. Influence of aeration on CH4, N2O and NH3 emissions during aerobic composting of a chicken manure and high C/N waste mixture. Waste Management 31(1): 33-38. DOI: 10.1016/j.wasman.2010.08.019.

Smet E, and HV Langenhove. 1998. Abatement of volatile organic sulfur compounds in odorous emissions from the bio-industry. Biodegradation 9(3): 273-284. DOI: 10.1023/a:1008281609966.

Sundberg, C., D. Yu, I. Franke-Whittle, S. Kauppi, S. Smars, H. Insam, M. Romantshcuk and H. Jonsson. 2013. Effects of pH and microbial composition on odour in food waste composting. Waste Management 33: 204-211.

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Pathogen kill – more than just high temperatures?

Temperatures > 55 C are required for at least a few days to  achieve pathogen kill during composting. We would then naturally agree that if the high temperature requirement was not met, we would have a higher risk of potential pathogens in our compost. Unfortunately, experience does not always support this conclusion. We cannot assume that just because we met the > 55 C requirement, our compost is pathogen free! It is clear that there is more to potential pathogen kill than simply high temperatures!

In a study of 19 small scale composters where the temperature rarely exceeds 55 C, 60% of samples had fecal coliform counts < 1000 MPN (Class A compost) (Cornell Composting Institute (2004). In contrast, with large scale composting facilities (no biosolids), 40% had fecal coliform counts < 1000 MPN (Brinton et al. 2009). This is surprising in that one would expect that > 95% of the compost from large scale facilities would meet Class A requirements, and that > 95% of the compost from small scale composters to fail! Christensen (2002) also observed high E. coli counts in the compost from large scale thermophilic compost facilities, and suggested that a longer time is required for pathogen kill.

While some have suggested that fecal coliform counts are not representative of potential pathogenic organisms, there does not appear to be evidence to support this. Brinton et al. (2009) measured a positive relationship between fecal coliform and E. coli. The Cornell Composting Institute (2004) observed that small scale composters that did not include meat waste actually had higher E.coli counts than those that did. In our own research with small scale composting of food waste, fecal coliform and E. coli counts were the same, suggesting that most of the fecal coliform were E.coli. When we measured discharges from food waste compost facilities, elevated concentrations of E. coli as well as fecal coliform were observed.

Research and experience suggests that microbial diversity is required to kill potential pathogens, and that this microbial diversity is as important or even more important than the high temperatures! In our own small scale work, we were intrigued about why fecal coliform and E.coli counts were < 3 MPN/g after 3 months of “curing” at 12-15 C, following two weeks of composting at 40-50 C.  It was a small scale batch of 25% foodwaste plus 10% poultry litter, which was expected to have a significant fecal coliform and E.coli count!

Others have observed fecal coliform and E.coli destruction at lower temperatures. Henault-Ethier (2007) observed reduction of fecal coliform and E.coli to <1000 MPN/g after 16 days of vermicomposting at 25 C. They attributed the reduction primarily to the microbial diversity in the composting environment.  Henault-Ethier et al. (2016) concluded that E. coli destruction during low temperature composting was primarily due to antagonistic activity of the indigenous microbial population.  Kim and Jiang (2010) reported that E. coli and Salmonella inoculated in autoclaved compost survived for a much longer time than in composts that did not have the microbes killed, suggesting that the microbial diversity in compost was very important to kill potential pathogens that survived the high temperature phase, or were introduced during curing. Paniel et al. (2010) added a number of different pathogenic bacteria to composting green waste, biowaste, sewage sludge and municipal solid waste, and concluded that the indigenous microbial community was critical for the destruction of pathogens during a 25 C curing process. Kim et al. (2011) concluded that the survival of E. coli O157:H7 in compost was negatively correlated with the population of indigenous microbes, particularly the actinomycetes and fungi.  Doffner and Brinton (1995) observed the survival of potential pathogenic organisms at temperatures > 55 C in the composting process and concluded:

“These results suggest that the mechanism for removal of these microorganisms during aerobic composting is complex and not simply the result of a thermal physical environment”

The importance of the microbial community in the destruction of potentially pathogenic bacteria was already reported almost 60 years ago!

“Pathogen destruction during the composting process may occur primarily as a result of two actions: a) thermal kill by sufficiently high time-temperature, and b) kill by antibiotic action or by the decomposing organisms or their products. In light of recent findings, the latter may be equally important as the former” (Wiley, 1962)

The microbiology of composting is even more amazing than I had first considered, where the the microbiology of pathogen kill is more than high temperatures and competition for carbon. In the next posts, we will review aeration requirements and their relevance to odour control and microbial diversity and pathogen kill, and how temperatures > 60 C in the composting process may decrease microbial diversity, which may delay the destruction of potentially pathogenic organisms.

References

Brinton, W.F. Jr., P. Storms and T.C. Blewett. 2009. Occurrence and Levels of Fecal Indicators and Pathogenic Bacteria in Market-Ready Recycled Organic Matter Composts. Journal of Food Protection 72: 332–339.

Cornell Composting Institute. 2004. Hygienic implications of small scale composting in New York State. Final Report of the Cold Compost Project.

Christensen, K.K., M. Carlsbaek, E. Norgaard, K.H. Warberg, O. Venelampi, and M. Brogger. (2002) Supervision of the sanitary quality of composting in the Nordic countries: evaluation of 16 full-scale facilities. Nordic Council of Ministers, Environment TemaNord 2002: 567.

Droffner, M.L. and W.F. Brinton. (1995) Survival of E. coli and Salmonella populations in aerobic thermophilic composts as measured with DNA gene probes. Zbl. Hyg. 197, 387-397.

Henault-Ethier, L. 2007. Vermicomposting: from microbial and earthworm induced effects in bacterial sanitation to the chemistry of biodegradation under batch or continuous operation. M.Sc. Thesis, Concordia University, Montreal, Quebec.

Henault-Ethier, L, V.J.J. Martin and Y. Gelinas. 2016. Persistence of Escherichia coli in batch and continuous vermicomposting systems. Waste Management 56: 88-99.

Kim, J. and X. Jiang. 2010. The growth potential for Escherichia coli O157:H7, Salmonella spp. and Listeria monocytogenes in dairy manure based compost in a greenhouse setting under different seasons. J. Applied Microbiology DOI: 10.1111/j.1365-2672.2010.04841.x

Kim, J., C.M. Miller, M.W. Shepherd Jr., X Liu and X. Jiang. 2011. Impact of indigenous microorganisms on Esherichia coli O157:H7 growth in cured compost. Bioresource Technology 102: 9619-9625.

Paniel, N., S. Rousseaux, P. Gourland, M. Poitrenaud and J. Guzzo. 2010. Assessment of survival of Listeria monocytogenes, Salmonella Infantis and Enterococcus faecalis artificially inoculated into experimental waste or compost. J. Applied Microbiology 108: 1797-1809.

Wiley, J.S. 1962. Pathogen survival in composting municipal wastes. J. Water Pollution Control Federation 34: 80-90

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Are we feeding potentially pathogenic microorganisms during curing?

Inactivating potential pathogens during composting is a two step process. The first step is the thermophilic or temperature kill process that kills most potentially pathogenic microorganisms. The second step is removal of readily available energy compounds for potentially pathogenic organisms. We are well aware that some potential pathogens survive the thermophilic stage either because they are in cooler zones in the composting material or they are able to enter a VBNC state (viable but not culturable). We normally assume that during the curing process, aerobic microbes that decompose the more resistant carbon compounds flourish and outcompete the potentially pathogenic microbes that thrive on readily available energy compounds.

Is it possible that in some of our curing processes, we may actually be feeding and culturing potentially pathogenic microbes? Can thermotolerant anaerobic microbes such Clostridia decompose cellulose and other more resistant carbon compounds and produce readily available carbon compounds to feed potential pathogenic bacteria?

Presence of Clostridia in Finished Composts

Anaerobic microorganisms such as Clostridia survive the composting process (Bohnel and Lube 2000, Jones and Martin 2003, Cornell Waste Management Institute 2004). While testing 94 marketable composts in the US, 70% of the composts contained measurable Clostridia and 20% contained > 1000 CFU/g. (Brinton et al. 2009).

If oxygen limiting conditions persist during composting and curing, Clostridia produce odorous substances that persist (acetic, butyric and valeric acids) (Partanen et al. 2010, Sundberg et al. 2013, Yu 2014).

Volatile Fatty Acid Production in Composts

Clostridia are anaerobic bacteria that decompose cellulose and other organic materials, producing short chain organic acids such as acetic and butyric acids. Butyric acid production is well known with animal feed storage (silage), where Clostridia flourish if the grass silage is not properly processed.

In a study of over 700 finished composts from throughout the US, Brinton (1998) measured > 500 ppm volatile fatty acids in 95% of the composts. Volatile fatty acids including acetic, propionic and butyric acids are excellent and easily degradable carbon sources for aerobic bacteria during the composting process.

Presence of E. coli in Finished Composts

In the study of 94 marketable composts in the US, Brinton et al. (2009) found that more than 50% of composts contained quantifiable fecal coliform bacteria, and that the fecal coliform counts were closely related to the measured E. coli. Many other research reports have discussed potential pathogen regrowth or its persistence during the composting  and curing process despite high temperatures.

Many of the potentially pathogenic organisms are known as facultative anaerobic bacteria. This means that they would prefer to use oxygen as an electron acceptor, but  are able to use other electron acceptors if oxygen is not available.

Are the Anaerobic Bacteria Feeding the Fecal coliform and E. Coli?

If our curing process occurs on large piles, where little to no oxygen is present, could Clostridia and other anaerobic bacteria continue to produce readily available carbon in the form of volatile fatty acids in anaerobic microsites, which then allow potential pathogenic microorganisms to thrive by consuming these volatile fatty acids in the presence of oxygen?

It may help understand some of the “frustration” over the “persistence” of fecal coliform during the compost process, leading some of us to suggest “false positives”.

Perhaps we need to focus on maintaining an aerobic environment to limit the ability of Clostridia and other obligate anaerobic bacteria to thrive, rather than simply focusing on keeping the temperatures high, particularly given that both Clostridia and many of the potential pathogenic organisms are thermotolerant?

In the next blog, we will address potential pathogen kill at lower temperatures during compost curing.

References

Bohnel, H., and K. Lube 2000. Clostridium botulinum and bio-compost. A contribution to the analysis of potential health hazards caused by bio-waste recycling. J. Vet. Med. B Infect. Dis. Vet. Public Health: 47: 785-795

Brinton, W. F. 1998. Volatile organic acids in compost: Production and Odorant Aspects. Compost Science and Utilization 6: 75-82.

Cornell Waste Management Institute. 2004. Hygienic implications of small-scale composting in New York State: Final Report of the Cold Compost Project.

Jones, P., and M. Martin. 2003. A review of the literature on the occurrence and survival of pathogens of animals and humans in green compost. WRAP (Waste and Resources Action Programme, UK.

Partanen, P., J. Hultman, L. Paulin, P Auvinend and M. Romantschuk. 2010. Bacterial diversity at different stages of the composting process. BMC Microbiology 2010 10: 94 doi.org/10.1186/1471-2180-10-94.

Sundberg, C., D. Yu, I. Franke-Whittle, S. Kauppi, S. Smars, H. Insam, M. Romantshcuk and H. Jonsson. 2013. Effects of pH and microbial composition on odour in food waste composting. Waste Management 33: 204-211.

Yu, D. 2014. Microbial community profiling of biodegradable municipal solid waste treatments – aerobic composting and anaerobic digestion. PhD thesis. Faculty of Biological and Environmental Sciences, University of Helsinki, Finland.

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Managing Potential Pathogenic Bacteria – MPN or CFU – are they the same?

Fecal coliform and E. coli in compost or leachate is usually reported in MPN per g compost or MPN per 100 mL water (or leachate). Sometimes we see results in CFU/g, or per 100 mL. Is there a difference?

CFU refers to “colony forming units”, whereas MPN refers to “most probable number”.  The difference is that CFU/100ml is the actual count from the surface of a plate, and MPN/100ml is a statistical probability of the number of organisms (American Public Health 2012). The US EPA appears to prefer MPN rather than CFU “because a colony in a CFU test might have originated from a clump of bacteria instead of an individual, the count is not necessarily a count of separate individuals.” (US EPA 2003).

It is important to note that some test methodology for specific organisms report the results in CFU, whereas for fecal coliform and E.coli, MPN is most often used.

Although we would intuitively think that CFU and MPN should be equivalent, and we normally assume that they are, research suggests that this is not always the case. One research report indicated that “especially in fall, E. coli concentrations in MPN are one order of magnitude greater than that in CFU” (Cho et al. 2010).

The Organic Matter Recycling Regulation, the Approved Water Quality Guidelines for British Columbia (BC MOE 2001), the CCME Compost Quality Guidelines (CCME 2005) and the US EPA (US EPA 2003), and the UK Compost Regulation (BSI 2011) report the fecal coliform requirements for compost in MPN per g solids.

References

BC Ministry of Environment. 2001. Approved Water Quality Guidelines Microbiological Indicators 2001. (http://www2.gov.bc.ca/assets/gov/environment/air-land-water/water/waterquality/wqgs-wqos/approved-wqgs/miceoindicators-or.pdf)

BSI. 2011. PAS 100:2011. Specification for Composted Materials. http://www.wrap.org.uk/sites/files/wrap/PAS%20100_2011.pdf

CCME 2005. Guidelines for Compost Quality. PN 1340 (http://www.ccme.ca/files/Resources/waste/compost_quality/compostgdlns_1340_e.pd)

Cho, K.H., D. Han, Y. Park, S.W. Lee, S.M. Cha, J.H. Kang and J.H. Kim. 2010. Evaluation of the relationship between two different methods for enumeration fecal indicator bacteria: colony-forming unit and most probable number. J. Environ Sci (China) 22: 846-50.

American Public Health Association, American Water Works Association, Water Environment Federation. 2012. Standard Methods for the Examination of Water and Waste Water.

US EPA 2003. Environmental Regulations and Technology. Control of Pathogens and Vector Attraction in Sewage Sludge (Including Domestic Septage) Under 40 CFR Part 503. EPA/625/R-92/013(https://www.epa.gov/sites/production/files/2015-04/documents/control_of_pathogens_and_vector_attraction_in_sewage_sludge_july_2003.pdf)

 

 

 

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