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Public Health Bacteriology of Commercially Composted Domestic Food and Garden Waste by the 11 Councils in Northern Ireland - Persistence Of Clostridium perfringens and Implications for Local Food Safety.

ABSTRACT Background New legislation has been introduced in Northern Ireland from April 2017, requiring domestic households to recycle all domestic food waste items. The purpose of this study was to examine the bacteriology of compost derived from this source which is supplied free-of-charge to the public for horticultural use. Methods Municipal compost samples were compared microbiologically with commercial garden compost samples, examining total viable count and diversity of bacteria cultivated. Results The municipal compost had a mean Total Viable Count (TVC) of 1.53 × 108 colony forming units (cfu)/ g compost, whereas the commercial garden compost had a mean TVC of 4.5 × 107 cfu/g compost. Campylobacter, Salmonella and Listeria were not isolated from any compost. Twenty-three bacterial genera were represented amongst the 46 organisms recovered. Of these, Pseudomonas aeruginosa and Clostridium perfringens were the most clinically significant. Discussion The application of municipal compost to cultivate non-food plants, such as roses and flowers presents minimal risk, provided safe handling practices are adopted and hands are thoroughly washed and dried afterwards. However, if applied to soil growing food produce, it is important that municipal compost does not enter the food chain without an effective critical control point which would prevent germination of spores of Clostridium perfringens. Risk may be increased in products such as marinades, home canning, home bottling and associated products. These methods of food preparation are common in ethnic Eastern European populations in Northern Ireland, where awareness of risk needs to be increased.


INTRODUCTION
New legislation has been introduced in Northern Ireland (NI) from April 2017, requiring households in each of the 11 local council regions to recycle all domestic food waste items. As a result, NI households collect all uneaten food, food that has passed its "Best Before" or "Use By" date and raw food, including raw meat. Items are usually deposited into brown bins, used solely for collecting domestic organic waste, although some councils, for example, Ards and North Down Borough Council, use green bins. Food waste is collected along with other sources of domestic organic waste from each household, including garden waste materials. The waste is usually collected on a bi-weekly basis by the local council authority and sent for commercial composting. At certain times of the year, residents can freely collect the composted material, termed "Rosey-lea" from their local council, especially during International Compost Awareness Week, usually in April-May each year. Given that waste food UMJ is an open access publication of the Ulster Medical Society (http://www.ums.ac.uk). The Ulster Medical Society grants to all users on the basis of a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International Licence the right to alter or build upon the work non-commercially, as long as the author is credited and the new creation is licensed under identical terms. entering the composting cycle may be heavily contaminated with foodborne pathogens, we examined the public health bacteriology of the composted material which the public may use for the cultivation of fruit and vegetables.

Source of composts and sampling protocol
Two types of compost were examined in this study, municipal compost from domestic food and green waste material (n=10) and commercially available garden compost (n=2 Clostridium perfringens was the only organism which was isolated from both municipal and commercial composts and all other organisms isolated were unique to that compost type. In addition, this species was the most frequently isolated (5/46; 10.8%) from compost.
Campylobacter, Salmonella and Listeria were not isolated from any compost sample examined.

DISCUSSION
The recent requirement to recycle all food waste material in Northern Ireland and the potential for NI householders to utilise the resulting compost provides challenges for public health. Local council guidance now requires all domestic food waste to be collected for commercial composting. Significantly, this includes raw meat (red meats, chicken, pork and fish) which may contain foodborne bacterial pathogens, such as Salmonella, Campylobacter, Listeria and pathogenic E. coli organisms. A failure to eliminate these pathogens during the composting process will allow their potential reentry into the food chain, when used for growing fruits and vegetables.
Recycling waste is a prudent idea for a sustainable green environment but there must be checks and balances to ensure minimum public health risk. EU legislation for recycling food/animal waste ingredients recommends stringent composting pit temperatures of 70 o C or separate exposure to this temperature for at least 1 hr before the batch is released back to human and/or animal habitats. Whilst these organisms may have the potential to infect humans, they generally remain infrequent causes of infection. However, there are two notable exceptions; the Gramnegative bacterium Pseudomonas aeruginosa (P. aeruginosa), and the Gram-positive spore-forming bacterium, Clostridium perfringens (C. perfringens). C. perfringens was isolated in 4/10 municipal composts as well as in both commercial garden composts.
Three species of Pseudomonas were isolated from the compost material; P. aeruginosa, P. mendocina and P. stutzeri. Of these, P. aeruginosa is the most clinically significant, particularly in patients with cystic fibrosis (CF), where this organism is responsible for increased morbidity and mortality. 1 CF patients and the parents of CF children often alter their lifestyle in order to reduce the risk of contact with P. aeruginosa by avoidance of reservoirs of this organism, especially water sources (hot tubs, jacuzzis). This report has identified municipal compost as a source of P. aeruginosa, so CF families should be aware of the risks of handling compost or home-grown produce.
Although C. perfringens may be commensal in the human intestine, illness is caused by eating food contaminated with large numbers of C. perfringens bacteria that produce sufficient toxin to cause illness. The incubation period is usually 6-24 hours post ingestion, followed by diarrhoea and abdominal cramps, but generally not with fever or vomiting. Symptoms usually last up to 24h, although in severe cases, symptoms can last for one to two weeks. 2 C. perfringens can survive high temperatures. During cooling and holding of food at temperatures from 12°C-60°C, the bacteria may grow and they can grow very rapidly between 43°C-47°C. 2 C. perfringens is an important aetiological agent of foodpoisoning in Northern Ireland, where 24 cases were recorded in 2016. 3 Of these, the majority (17; 70.8%) were in patients aged 65 years or older, with the remainder (7; 29.1%) in patients 45-64 years, representing an age specific incidence of 5.7 and 1.5 per 100,000 population. It is unknown if any of these cases were related to produce grown in compost.
Nevertheless, it is important that we examine the implications of this data. Foodborne outbreaks of C. perfringens involving leafy and vine-stalk vegetables have been described. 4 The growing social trends of sustainability and consuming organic foodstuffs, as well as an ageing susceptible population are factors which could exacerbate C. perfringens foodpoisoning. Growing and cooking home produce has become more popular in recent years, especially amongst older people.
In Eastern European cultures, there is a tradition of preserving food through home canning, as well as preparing food marinades, which have a relatively high pH and are left at room temperature to mature. Such practices have led to outbreaks of Clostridium food-poisoning. 5,6 Therefore, whilst it may be relatively safe for the NI indigenous population to immediately prepare dishes from home-grown vegetables, where Clostridium-contaminated compost has been applied, Marinating or home canning may increase Clostridium growth and create a food safety vulnerability amongst some ethnic groups.
In conclusion, the composts examined in this study contained a diverse range of bacteria, which may cause human infection. In particular, Clostridium perfringens is an important foodborne pathogen. The application of compost to cultivate non-food plants, such as roses and flowers presents minimal risk, provided safe handling practices are adopted and hands are thoroughly washed and dried after completion of gardening activities. However, if compost is applied to soil growing edible produce, it is important that the produce does not enter the food chain domestically or commercially without the inclusion of an effective critical control point, which would eliminate Clostridium perfringens and prevent germination of its spores. The latter is particularly important if home canning and marinating are employed -such practices are common in ethnic Eastern European populations in NI, where educational awareness needs to be increased to avoid potential food-poisoning. Anyone handling compost should ensure that their hands are washed with warm water and soap and are thoroughly dried after exposure.