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General enquiries on this form should be made to: Defra, Science Directorate, Management Support and Finance Team, Telephone No. 020 7238 1612 E-mail: [email protected] SID 5 Research Project Final Report SID 5 (Rev. 3/06) Page 1 of 34

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General enquiries on this form should be made to:Defra, Science Directorate, Management Support and Finance Team,Telephone No. 020 7238 1612E-mail: [email protected]

SID 5 Research Project Final Report

SID 5 (Rev. 3/06) Page 1 of 23

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NoteIn line with the Freedom of Information Act 2000, Defra aims to place the results of its completed research projects in the public domain wherever possible. The SID 5 (Research Project Final Report) is designed to capture the information on the results and outputs of Defra-funded research in a format that is easily publishable through the Defra website. A SID 5 must be completed for all projects.

This form is in Word format and the boxes may be expanded or reduced, as appropriate.

ACCESS TO INFORMATIONThe information collected on this form will be stored electronically and may be sent to any part of Defra, or to individual researchers or organisations outside Defra for the purposes of reviewing the project. Defra may also disclose the information to any outside organisation acting as an agent authorised by Defra to process final research reports on its behalf. Defra intends to publish this form on its website, unless there are strong reasons not to, which fully comply with exemptions under the Environmental Information Regulations or the Freedom of Information Act 2000.Defra may be required to release information, including personal data and commercial information, on request under the Environmental Information Regulations or the Freedom of Information Act 2000. However, Defra will not permit any unwarranted breach of confidentiality or act in contravention of its obligations under the Data Protection Act 1998. Defra or its appointed agents may use the name, address or other details on your form to contact you in connection with occasional customer research aimed at improving the processes through which Defra works with its contractors.

Project identification

1. Defra Project code FO0307

2. Project title

Horizon scanning to anticipate future crop safety and quality issues related to pressures resulting from changes to the crop environment (including climate change)

3. Contractororganisation(s)

Warwick HRIUniversity of WarwickWellesbourneWarwickCV35 9EF     

54. Total Defra project costs £ 52,254(agreed fixed price)

5. Project: start date................ 01 April 2007

end date................. 31 March 2008

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6. It is Defra’s intention to publish this form. Please confirm your agreement to do so...................................................................................YES NO (a) When preparing SID 5s contractors should bear in mind that Defra intends that they be made public. They

should be written in a clear and concise manner and represent a full account of the research project which someone not closely associated with the project can follow.Defra recognises that in a small minority of cases there may be information, such as intellectual property or commercially confidential data, used in or generated by the research project, which should not be disclosed. In these cases, such information should be detailed in a separate annex (not to be published) so that the SID 5 can be placed in the public domain. Where it is impossible to complete the Final Report without including references to any sensitive or confidential data, the information should be included and section (b) completed. NB: only in exceptional circumstances will Defra expect contractors to give a "No" answer.In all cases, reasons for withholding information must be fully in line with exemptions under the Environmental Information Regulations or the Freedom of Information Act 2000.

(b) If you have answered NO, please explain why the Final report should not be released into public domain

Executive Summary7. The executive summary must not exceed 2 sides in total of A4 and should be understandable to the

intelligent non-scientist. It should cover the main objectives, methods and findings of the research, together with any other significant events and options for new work.Crop contaminants of a biological or microbiological nature can impact on the quality and safety of produce. This review covers contaminants that might be introduced into the food chain during crop production, including microorganisms that are pathogenic to plants and humans; plant pathogens that produce compounds toxic to humans; microorganisms pathogenic to humans that can contaminate crop plants during production; microorganisms that impact on product quality; and finally, material derived from insects and other animals. The review focuses on the impact of external drivers on future contamination issues. The main drivers included in this report are regulations, voluntary initiatives, processing, changing farming practices, waste management and climate change. Within each of these main categories, both positive and negative effects on crop contaminants are likely to occur (see below). The most important drivers that are likely to increase crop contamination in the field in the future are 1) a decrease in the number of active ingredients approved to control plant pathogens, insects and other fauna in the field, glasshouse, and in store, and 2) an increase in temperature due to climate change. However, overall, fewer biological and microbiological contaminants are likely to reach the consumer as a consequence of the continual improvement of certain regulations, farming practices, processing techniques and voluntary initiatives. Regulations considered by this report cover those for pesticide use, manure applied to land as fertiliser and those affecting food hygiene and safety. A key impact is likely to be a decrease in available active ingredients, which may lead to an increase in contamination by organisms that are controlled currently by pesticides, if alternative control measures are not available. More restricted application of manures to agricultural land, with longer closed seasons, are likely to lead to decreases in contamination from human-pathogenic microorganisms that can contaminate crops during production. Tighter controls on food hygiene and safety will lead to increased control of contaminating organisms throughout the food chain. Voluntary Initiatives play a major role in crop production, and in turn impact on crop contamination. Those covered by this report include the Assured Produce schemes and retailer initiatives, Codes of Good Agricultural Practice, the Pesticide Voluntary Initiative and retailer approved pesticide lists. We believe that the key impacts of voluntary initiatives on crop contamination are likely to be positive, leading to further reductions in contamination. For example, better and more controlled use of pesticides and spraying equipment through the Pesticides Voluntary Initiative, should target certain crop contaminants more efficiently, thus reducing their numbers. Codes of Good Agricultural Practice, if followed correctly, should reduce the possibility of crop contamination with most groups of organisms. Similarly, increased microbiological monitoring of inputs; increased pressure to improve hygiene standards on farm and in packing/processing and storage environments on farm; and application of Hazard Analysis Critical Control Point (HACCP) based control systems from farm-to-fork will all reduce contamination throughout the chain. However, it is possible that retailer approved pesticide lists may restrict available chemical control options further, which could lead to some loss of control for certain groups of crop contaminants, if alternatives are unavailable or unapproved.Changing farming practices considered by this report cover organic production; an increase in energy and other novel crops; protected cropping; environmental stewardship schemes; water use; farm diversification; moves towards reduced tillage; and issues affecting stored grain. Several of these drivers

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might result in potential modest increases in crop contamination. For example: 1) an increase in organic farming may increase the amount of contamination from insects and other fauna on organic produce, and microorganisms impacting on product quality (spoilage microorganisms), due to pesticides not being used; 2) wheat grown more frequently or on a larger scale as a dual food and energy crop may lead to an increase in contamination with microorganisms producing mycotoxins or those producing aeroallergenic spores; 3) increased production of novel crops might lead to an increase in microorganisms that produce mycotoxins (specific to those novel crops) as well as new pest insects; 4) farm diversification may increase public access to farms, possibly increasing exposure of the public to aeroallergens, and leading to an increase in contaminants of animal origin (e.g. hairs and excreta from rodents), particularly if farm diversification activities include food retail outlets or campsites; 5) reduced tillage may increase contamination of crops with microorganisms that produce mycotoxins, and also increase insects and other fauna through more crop residues left on the soil surface. Processing drivers that may impact on contaminants which are considered in this report include new technology (driven by retailer demands); reduced use of chemicals in the processing plant and in recycled water; and alterations in packaging. In general, we believe that current processing practices will lead to a reduction in contaminants. For example, increased application of packaging technologies that prolong shelf life, more rapid and controlled transport of products, and many novel technologies are likely to lead to reduced contamination. To balance this, consumer demand for “minimally processed” and fresh food, for additive or “chemical free” products that reduce the usage of compounds such as chlorine in wash water, or the incorrect or poor application of processing and packaging technologies by low technology companies, may all lead to increases in contamination reaching the consumer.Waste management; In the context of this report, ‘waste’ refers to any biological material that could potentially contribute to crop contamination. If correctly carried out, processing of crop waste is likely to minimise the likelihood of further contamination. However, microorganisms surviving in crop debris or plant waste that is not ploughed in may increase the risk of contamination for the following crop. If on-farm waste composting is not carried out correctly (i.e. correct temperatures are not maintained), there is an increased risk of contamination with human-pathogenic microorganisms from manures and slurries that form part of the compost being returned to agricultural land. Although anaerobic digestion can reduce pathogen numbers, it cannot safely eliminate all pathogens from the digestate, potentially leading to an increased risk of crop contamination with microorganisms that can impact on human health and product quality. As further restrictions are placed on the amount of manure that can be applied to land as fertiliser, there may be an increased need to store or transport waste manure off-farm. This action could lead to a potential increase in cross-contamination with microorganisms pathogenic to humans. Although all of these scenarios are likely to occur, we do not believe that they present a high risk to the food chain. Climate change scenarios considered by this report include the major conclusions outlined by UKCIP 2002, i.e. increased temperatures, changes in rainfall patterns (leading to increased irrigation requirements) and ‘extreme’ events. We believe that temperature increase in particular is a key driver in increasing crop contamination. For example, 1) increased temperatures may increase the risk of aeroallergenic spores from plant pathogens contaminating crops; 2) fungi that produce mycotoxins could become more prevalent in warmer conditions; 3) conditions could become more suitable for microorganisms that impact on product quality, with faster growth rates and sporulation in some cases; 4) milder winters could increase the survival of insects and microorganisms; and 5) insect contamination of crops could increase, with more generations per season.Impact of crop contaminants on human health and product quality; For the majority of the population, plant pathogens do not impact directly on human health, although aeroallergens are an important consideration for the general population, as airborne spores of some plant pathogens may sensitise humans and cause bronchial infections and asthma. Mycotoxins produced by fungal plant pathogens can have very serious human health implications if ingested and, consequently, regulations stipulate maximum permitted levels. Product quality can be affected if mycotoxin levels are too high. Microorganisms from the environment that are pathogenic to humans, which can contaminate crops during production, may not obviously affect product quality. However, the lack of visual quality defects means that produce contaminated by these microorganisms is more likely to be consumed, and this can lead to food-poisoning. Microorganisms that cause obvious visual spoilage are unlikely to impact on human health, as affected food is unlikely to be consumed, although this group can have a significant effect on product quality. Produce contaminated with insects, other animals and materials derived from animals is likely to be rejected by consumers.Marketability of products and risk assessment; Product marketability could be threatened by poor quality and safety, affected by the withdrawal of pesticides or restrictions on their use; occurrence of novel pest and diseases; or changes in environmental conditions of crop growth, harvest, storage and processing. Opportunities for maintaining or improving marketability include changes in consumer attitudes to product quality; improved varieties; improvements in education and training of growers/workers; more effective control measures; and shortening of supply chains. The main risks identified in this work are restrictions placed on pesticides, and increased temperatures occurring with climate change, which are drivers that can impact on several groups of contaminants across a wide sector.

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Project Report to Defra8. As a guide this report should be no longer than 20 sides of A4. This report is to provide Defra with

details of the outputs of the research project for internal purposes; to meet the terms of the contract; and to allow Defra to publish details of the outputs to meet Environmental Information Regulation or Freedom of Information obligations. This short report to Defra does not preclude contractors from also seeking to publish a full, formal scientific report/paper in an appropriate scientific or other journal/publication. Indeed, Defra actively encourages such publications as part of the contract terms. The report to Defra should include: the scientific objectives as set out in the contract; the extent to which the objectives set out in the contract have been met; details of methods used and the results obtained, including statistical analysis (if appropriate); a discussion of the results and their reliability; the main implications of the findings; possible future work; and any action resulting from the research (e.g. IP, Knowledge Transfer).

IntroductionThis project consisted of a literature review to determine the extent of knowledge on the effect of contaminants on crop safety and quality. The areas to be investigated were as follows:

1. A review of the contaminants occurring currently in crop production in the UK. 2. A review of the methods available currently to farmers/growers to help them avoid crop contamination 3. A review of the likely impact of external drivers on contamination 4. A review of the impact of contamination of crops 5. A review of the marketability of products

All objectives have been met in full.

Crop plants are grown in non-sterile environments and are consequently susceptible to contamination from a variety of sources, many of which are biological or microbiological in origin. This report aims to summarise biological contaminants that can arise during crop production, and give an indication of the likely impact that external drivers could have on such crop contamination in the future in the UK. The nature of this report means that not all possibilities for future events can be considered, and unforeseen circumstances may impact on crop contaminants in ways not described here. Contaminants considered in this report include:

microorganisms pathogenic to both plants and humans microorganisms that are pathogenic to plants but that also produce compounds toxic to humans microorganisms from the environment that are pathogenic to humans that can contaminate crop plants

during the production process microorganisms that can impact on product quality insects, other animals, and materials derived from animals

Physical contaminants such as glass, metal, plastic etc., or chemicals that are not microbiological in origin are not within the scope of this report.

Objective 1: A review of the contaminants currently present in crop production in the UKThis Objective is included in the Appendix to this report. It comprises tables listing contaminants in each of the groups above and a brief description of each group.

Objective 2: A review of the current control methods to avoid contamination of crops available to farmers/growersThis Objective is also included in the Appendix to this report. It covers chemical and biological control options, and good practice measures to avoid crop contamination. Alternative measures are also considered briefly, which may show promise for the future or need further research and development. The section focuses on control measures that may be applied during the growing season, as well as chemical control that may be applied during further on-farm processing (such as disinfectants applied during washing).

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Objective 3: A review of the likely impact of external drivers on contaminationTable 3.1 (see Appendix) provides a summary of the possible impact of various drivers on future crop contamination with the groups of contaminants detailed in Objective 1. These are discussed more fully below.

3.1 Regulation Regulations are in place to prevent or minimise the impact of certain aspects of agricultural practice that may cause environmental damage or harm to human health. These include, for example, the risk of water pollution from agricultural wastes, pesticides and fertilisers; the risk of soil contamination from sewage sludge and pesticides; and air pollution from air-borne pesticides, among others (Better Regulation Task Force, 2000). Many regulations in force in UK law originate from European Commission directives, and therefore require compliance in order to avoid infraction proceedings and fines. It is not within the scope of this review to examine all regulations relating to agriculture in the UK. However, examples of important regulations that might impact on crop contamination are discussed below.

3.1.1 Regulations affecting pesticide usePesticides are used to control numerous pests and pathogens that can contaminate crops in the field or in storage. However, because of their toxicity and potential to cause environmental damage pesticide use is regulated closely. Many pesticides (or active chemical ingredients) have been banned from use in recent years, leaving farmers to rely on alternative chemicals to control pests and pathogens, or find alternative control measures. Regulations controlling the use of pesticides may also impact on the control of pests in storage. For example, there has been a loss of insecticides available for use in grain stores, and following the withdrawal of methyl bromide, there are limited options available to fumigate stores.

The European Commission Review Programme is currently reviewing active ingredients for inclusion on a positive list of substances that have been shown to be without unacceptable risk to humans or the environment (www.pesticides.gov.uk). At the end of this review process, there is set to be a loss of active ingredients that can be used by growers and farmers. The Plant Protection Products Regulations implement the European Directive (91/414/EEC) in the UK.

In addition to the legislation relating directly to pesticide approval, other regulations may also limit the use of pesticides in the future. For example, the EU Water Framework Directive seeks to ensure that all rivers, lakes, ground and coastal water reach a good ecological and chemical status by 2015, through tackling diffuse pollution (www.defra.gov.uk). Diffuse pollution from agriculture includes pesticides, as well as nutrients such as nitrates and phosphorus. Within the Water Framework Directive, the daughter Directive on Priority Substances lists 33 substances (including pesticides) that may be restricted in the future.

However, if regulations result in pesticides being further restricted or withdrawn from use, and no alternative control measures exist, this could leave crops vulnerable to increased infection from plant pathogens and infestation by pests, and may result in a greater carry-over of contaminants into the food chain. A loss of active ingredients or pesticides will have the biggest impact on contaminants that are currently controlled to a large extent by chemical means. These include plant pathogens that produce compounds toxic to humans; microorganisms that impact on product quality; and insects (Table 3.1; Appendix).

3.1.2 Regulations affecting manure applicationThe application of manure to land as a fertiliser is specifically regulated through the Nitrates Directive (91/676/EEC) in order to control the amount of nitrogen that is applied to farmland. This directive limits the amount of manure per hectare to that containing 170kg N, in Nitrogen Vulnerable Zones (NVZs). Manure applied to land as fertiliser is a potential source of contaminants in the field, particularly for the category of microorganisms that may cause enteric illness in humans, and detailed guidelines exist for growers to manage farm manures to reduce the risks of microbiological contamination of ready-to-eat crops (Food Standards Agency, 2005).

Through the Nitrates Directive, the application of manure to farmland may change in the future, or become more restricted. Currently there is need to increase the area of NVZs from 55% to 70% in England, and legislation to designate more land as NVZs is being implemented (Defra, 2007b). A consultation was held recently about proposed changes to the Nitrates Directive for 2008, and the question was asked whether to have discrete zones (as currently exist), or to apply the restrictions to the whole of England. The consultation is now closed, but the outcome could have an impact on growers who use manure as fertiliser in parts of England that were not previously designated NVZs.

Proposals that may impact on crop contamination by microorganisms found in manure include establishing a lower whole farm manure N loading limit; extending the length of the closed spreading periods for organic manures; and prohibiting the use of high pressure, high trajectory application techniques for spreading organic manure. A change in regulation could result in fewer and more controlled applications of manure, thereby potentially reducing the risk of crop contamination through this means. On-farm storage of excess (waste)

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manure will most likely need to increase if manure application to farmland is restricted further. This may lead to cross-contamination elsewhere (see section 3.5.4 under waste management). It is also worth noting that although manures can technically be applied to horticultural land, multiple growers’ assurance schemes forbid this and no crop sold fresh should have had manure applied.

3.1.3 Regulations affecting food hygiene and safetyFood hygiene laws regulate businesses producing or harvesting plant products, to prevent contamination, and controls are in place to ensure that contaminants do not proceed further up the food chain. For example, Commission Regulation (EC) No 2073/2005 on microbiological criteria for foodstuffs sets limits for the presence of contaminating microorganisms such as E. coli in vegetables, fruits and products thereof. If unsatisfactory levels are recorded, action should be taken to make improvements in production hygiene or the selection of raw materials.

There are also regulations for the maximum levels of contaminants in food, including mycotoxins (Commission Regulation (EC) No 1881/2006). Levels are currently set for most groups of mycotoxin, and these are reviewed periodically to deal with changing situations and prevent dangerous levels of mycotoxins entering the food chain. Although this will not impact on the level of contamination that occurs in the field, this regulation does ensure that there are control points to stop contaminants harming human health.

These food hygiene regulations could have an impact on growers and farmers if unacceptable levels of contaminants are found, as this will mean possibly rejected crops, or changes to production may be required to reduce contamination in the field.

The key legislation affecting food is as follows: 1990 Food Safety Act1993 93/43/EEC Directive on the Hygiene of Foodstuffs1993 315/93 EEC Council Regulation Community procedures for contaminants in food1995 Food Safety General Food Hygiene Regulations2002 178/2002 EC Regulation General Food Law 2005 852/2004 EU Regulation Hygiene of Foodstuffs 2005 2073/2005 EC Regulation on Microbiological Criteria for Foodstuffs2006 The Food Hygiene General Regulations

The key requirements of the above legislation can be summarised into the following key actions that farmers/growers, including those involved in processing, are required to implement (please note that this list is not exhaustive).

All reasonable precautions must be taken to prevent contamination of food at any stage of production. Due diligence needs to be demonstrated through the keeping of records, for example cleaning records,

training records and laboratory results. A preventative system based on Hazard Analysis Critical Control Point (HACCP) principles and industry

codes of practice should be followed. Food must not be unfit or so contaminated that it would unreasonable to expect it to be eaten. Food hazards present at the level of primary production should be identified and adequately controlled. Food and feed business operators at all stages of production, processing and distribution are required to

ensure that foods or feeds satisfy the requirements of food law which are relevant to their activities and shall verify that such requirements are met.

In certain cases specific microbiological criteria must be met, for example Listeria monocytogenes in sprouted seeds.

Producers should have a documented traceability system in place. Primary producers will need to follow good practice and manage their operations in such a way that

hazards are acceptably controlled. Primary producers must respect other existing legislation in terms of veterinary medicines, plant

protection products, feed additives, zoonoses and disposal of waste. In addition, primary producers will need to keep facilities, vehicles, equipment etc. clean and, as

necessary, disinfected. They will need to use clean water; ensure staff handling foodstuffs are in good health and trained on

health risks; control pests; take account of any test results; and keep some basic records.

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The key impacts of regulations on crop contamination are likely to be: A decrease in available chemicals used to control plant pathogens, insects and other fauna in the field,

glasshouse, and in store. A potential increase in contamination by organisms that are currently controlled by pesticides if

alternatives are not available, including plant pathogens that produce compounds toxic to humans; microorganisms that impact on product quality; and insects.

More restricted application of manures to agricultural land, with longer closed seasons may lead to a potential decrease in contamination from human-pathogenic microorganisms that can contaminate crops through manure application during production.

Tighter controls on food hygiene and safety through food hygiene laws, leading to a reduction in levels of microbial contamination in food and feed.

3.2 Voluntary initiatives

Although there is substantial legislation in place that can influence crop contamination in the field, and the extent to which it is controlled further up the food chain, voluntary initiatives and assurance schemes play a major role in encouraging good agricultural practice, which in turn can impact on crop contamination. In some respects, the impact of retailer-driven schemes can be greater than generic codes of practice (Martinez et al. 2007).

3.2.1 Assurance schemes and retailers requirements There are various voluntary farm assurance schemes, providing guidelines to growers and farmers to assure customers that certain standards have been maintained during production. Examples of these include The Red Tractor Scheme, the LEAF Marque (Linking the Environment And Farming), and the Soil Association organic standard (www.defra.gov.uk). Under The Red Tractor Scheme, any food marked with the Red Tractor logo can be traced back to farms with an Assured Food Standards licence. Individual schemes within the Red Tractor Scheme include Assured Combinable Crops (covering cereals, oilseeds and protein crops) and Assured Produce (covering fruit, salad and vegetables) (www.defra.gov.uk). The Assured Produce scheme publishes standards for providing safe food of good quality. The Generic Crop Protocol Standards include sections on aspects such as site history and management; irrigation; crop protection; harvest and storage; and pollution control and waste management (Assured Produce, 2007). There are also specific protocol standards for individual crops. Compliance with the standards ensures that growers can supply to any supermarket or retailer.

GlobalGAP (formerly known as EurepGAP) is an international assurance scheme, which is a private sector body that sets voluntary standards for the certification of agricultural products around the globe. The GlobalGAP standard is primarily designed to “reassure consumers about how food is produced on the farm by minimising detrimental environmental impacts of farming operations, reducing the use of chemical inputs and ensuring a responsible approach to worker health and safety as well as animal welfare”. The basis is an equal partnership of agricultural producers and retailers who wish to establish efficient certification standards and procedures. Typical requirements for fruit and vegetables under this scheme are as follows (taken from Trienekens and Zuurbier (2007)):

Traceability of products (a documented system is required). Record keeping of farm activities (to be stored for 2 years). Record keeping of varieties and rootstocks (e.g. quality certificates of seeds, nursery stock health

certificates). Record keeping of site history and site management (e.g. site characteristics, crop rotation). Soil and substrate management (e.g. soil mapping, soil erosion management). Record keeping of fertilizer usage, pesticides usage (e.g. type, quantities, applications). Record keeping of irrigation activities (quality and supply of water, rainfall documents). Record keeping of harvesting activities (documented hygiene protocol, records on operations). Waste and pollution management (types, quantities, recycling plan). Attention to worker health, safety and welfare (e.g. first aid boxes, training records). Attention to environmental issues (e.g. dealing with wildlife, biodiversity). Internal audit (one internal audit against the Eurep-GAP standard every year, Eurep-GAP check list).

In addition to the schemes mentioned above, which are applicable across various sectors and retailers, individual retailers (particularly the larger supermarkets) may have their own requirements and demands from their suppliers, e.g. Tesco Nature’s Choice.

In order to be able to supply the retail market, growers need to comply with the standards that are published. These generally improve agricultural practice, and if followed correctly, may decrease contamination of crops.

3.2.2 Government Codes of Good Agricultural Practice

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Codes of Good Agricultural Practice have been considered elsewhere as a means available to growers to reduce crop contamination through avoidance (see Objective 2, section 2.3). Good agricultural practice means ”a practice that minimises the risk of causing pollution while protecting natural resources and allowing economic agriculture to continue”. (www.defra.gov.uk). The codes are voluntary, but give practical advice and guidance on how to stay within the law (as dictated by numerous regulations), and are written in language that is generally easier to understand than the official regulations. Although the Codes of Good Agricultural Practice focus on means to avoid environmental pollution, this can also impact on crop contamination. For example, there is evidence that diffuse pollution from agriculture can lead to up to 25-50% of bacterial pollution in water (Defra, 2007a). This pollution could increase the microbial loading of water used for irrigation, potentially spreading contaminant microorganisms. Following the Code of Good Agricultural Practice for water could reduce this initial diffuse pollution, which may in turn decrease crop contaminants present in irrigation water.

Other UK Codes of Good Agricultural Practice include those for the reduction of fusarium mycotoxins and ochratoxins in UK cereals (Food Standards Agency, 2007a; Food Standards Agency, 2007b). Another voluntary code is the “Plant health code of practice for the management of agricultural and horticultural waste ”, which also aims to encourage best practice in the disposal of waste from plant produce (www.defra.gov.uk). Correct disposal of contaminated crop debris or the treatment of water used for washing produce can reduce the occurrence of crop contaminants.

3.2.3 Pesticides Voluntary InitiativeThe original Pesticides Voluntary Initiative (VI) was a package of measures, developed by the agricultural and agrochemical industries, and agreed by the Government, which aimed to minimise the impact of pesticides on the environment. It was set up initially as an alternative to a proposed pesticide tax. The VI included over 40 different projects or activities designed to promote best practice in the use of pesticides and ran for five years, from April 2001 to March 2006. Due to its success, the VI has continued since 2006 (www.voluntaryinitiative.org.uk). Best practice in the use of pesticides may decrease crop contamination, as pests and pathogens should be targeted more effectively and efficiently.

3.2.4 Retailer approved pesticide listsAlthough reductions in pesticide use are largely driven by environmental concerns, there is also substantial pressure from supermarkets and consumers to reduce pesticide residues on fresh produce. Other organisations can influence consumer demands as well. For example, a briefing document by Friends of the Earth suggested that supermarkets should do even more to reduce pesticide use in order to reduce residues found on food (Friends of the Earth, 2004).

Most major supermarkets have their own ‘supermarket-approved’ pesticide lists, which are often more restrictive than the UK approved pesticide list. For example, the Co-Operative has a list of banned pesticides on their website (www.co-operative.co.uk). This supermarket also has a separate list of pesticides “allowed with permission only”, requiring written permission for growers to continue using them to supply the Co-Operative. Other supermarkets have also devised approved lists. For example, Tesco has reviewed pesticide use, with 300 uses being removed and extra controls put in place to reduce pesticide levels. Marks & Spencer have also agreed with their suppliers to stop using 60 different pesticides worldwide, and also have a list of pesticides “allowed with permission only”. Their long-term goal is to sell residue-free produce.

However, retailers’ demands for reduced pesticide use, beyond that restricted by UK legislation, means that in order to continue supplying the market growers are further constrained in the chemicals they can use to control pests and pathogens. It is outside the scope of this report to assess whether the pesticides approved by retailers are sufficient to control crop contaminants as categorised in this report. However, if retailer restrictions are in place without available alternatives, this could lead to a potential increase in crop contaminants.

The key impacts of voluntary initiatives on crop contamination are likely to be: A decrease in contamination if the standards published by various farm assurance schemes and the

Codes of Good Agricultural Practice are followed correctly. Better and more controlled use of pesticides and spraying equipment, through the Pesticides Voluntary

Initiative, which should target certain crop contaminants more efficiently, thus reducing their numbers. Retailer approved pesticide lists may further restrict available chemical control options, potentially

leading to some loss of control for certain groups of crop contaminants if alternatives are unavailable or unapproved.

Reduced contamination through the application of HACCP based control systems from farm-to-fork. Increased pressure to improve hygiene standards on farms, and in packing/processing and storage

environments on farms. Increased microbiological monitoring of inputs (such as water) and products, thus increasing the

detection of contamination, and reducing the amount of contaminated product reaching the market.

3.3 Changing farming practices

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A study of long-term trends affecting the farming industry, carried out for Defra in July 2005, researched and analysed the key drivers that are expected to affect the farming industry in England in the next 10-15 years, with the aim of describing the future structure of the industry in terms of the number, size and distribution of the dominant farm types that form the industry (English Food and Farming Partnerships, 2005). This report stated that “in general, the outlook for horticulture is positive, with cheaper labour becoming available from Eastern Europe, extended growing seasons occurring and consumer attitudes turning more towards healthy fresh produce. In addition, UK food companies are keen to avoid food miles on fresh produce and so will be keen to increase sourcing from within the UK and depending upon consumer attitudes to GM production, there are substantial opportunities for the sector here, especially with regard to plant breeding and disease resistance”.

One of the future trends reported is that there may be an increase in the use of contracting services, with shared machinery being used. Shared machinery could allow for cross-contamination if equipment is not cleaned thoroughly. Other farming practices are discussed more fully below.

3.3.1 Organic farmingIn recent years, there has been an increased interest in organically produced food, i.e. food produced using a farming system without the input of synthetic agrochemicals, and using practices that minimise environmental damage. However, in 2002, only 30% of organic products consumed in the UK were actually produced here (www.defra.gov.uk). An Action Plan to develop organic farming in England was initiated with the aim of having 70% of the organic produce consumed in Britain produced domestically by 2010, in line with figures for conventionally farmed produce. By 2004, the figure for domestically produced organic food was 44%, showing an increase on just two years before.

The area of land used for organic farming has increased over the past decade, with a large increase occurring in the late 1990s and early 2000s. For example, in 1996 there were 82000 hectares of organic land in the UK, and this had increased to a maximum of 741000 hectares by 2003 (http://www.ukagriculture.com). Since then, the total land area used for organic farming has decreased slightly, and in 2007 619783 hectares of organic land were recorded in the UK (National Statistics, 2007).

Although increases have been seen over recent years, the organic farming sector is still small in comparison with conventional farming. For example, organic land in 2007 totalled 3.6% of the total agricultural land (National Statistics, 2007), and organic crops in particular constitute a small percentage of the total area grown (Table 3.3.1). It is predicted that the area of organic land used for crops in the UK will not increase substantially in the near future.

Table 3.3.1: Organically produced crops as a percentage of the total area of crops grown in the UKCrop % of total area for crop categoryCereals 1.7Other crops 1.1Fruit and nuts 5.5Vegetables 3.1Source: (National Statistics, 2007)

A recent review, looking at the safety of organic produce, included some categories of microbiological contaminants including those pathogenic to humans and those producing mycotoxins (Magkos et al., 2006). Across studies comparing contaminants in organic and conventional farming, no significant differences were found in contaminant levels. Some studies did indicate higher contamination in organic produce, whereas other studies did not. Research on the levels of mycotoxins found in organic or conventionally produced food showed mixed and conflicting results, with some studies indicating more mycotoxin contamination with organic produce, and other studies showing less or equal mycotoxin contamination, when compared with conventional produce (Magkos et al., 2006; Rembialkowska, 2007).

Organic farmers rely on manures, as well as green manures such as clover, to provide fertility rather than chemical fertilisers. The use of farmyard manures may increase the risk of contamination with certain microorganisms. However, conventional farmers also use manures to increase fertility, and the same restrictions apply to both farming systems with regard to the amount, type and rate of manure application under the Nitrates Directive. There is no extra hazard in organic farming from applying manures, but rather the risk comes from whether the manure is sufficiently well composted before application. However, organic land has increased populations of different wildlife species, which may increase contamination of crops with faecal pathogens from birds and animals (Magkos et al., 2006). As organic farming cannot rely on synthetic chemicals to control microorganisms, insects and other fauna, there may be an increase in contaminants that can impact on product quality.

3.3.2 Energy crops

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The EU has set a target that 20% of EU energy consumption must come from renewable energy sources by 2020. The UK’s contribution to meeting this target is still to be decided. However, the use of biofuels for transport and biomass for heat and electricity are expected to play a significant role in meeting the targets. The main crops that can provide energy include short rotation coppice (e.g. willow), Miscanthus, Canary grass, straw, forest material and tree management residues, cereals (e.g. wheat), oilseeds, sugar beet and fodder beet (www.defra.gov.uk).

In many cases the crops grown for energy are not food crops, and thus the impact of crop contaminants on human health and product quality is limited in these situations. However, some crops such as wheat may be grown for dual purposes to provide both food and energy, and an increase in wheat production may impact on the occurrence of contaminants such as mycotoxin-producing fungi. It may be speculated that crops grown for bioenergy should have low energy inputs in growing them, which may mean that certain crops are not sprayed for pest and disease control, possibly leading to greater contaminants in those crops. In addition, cereals are a source of aeroallergenic spores from various fungi, and an increased area of land used for cereal production, to meet energy and food requirements, could increase the incidence of airborne spores.

In order to meet the requirements for bioenergy production, an increased land area may be required to grow bioenergy crops, and some crops (e.g. oilseed rape, wheat) may be grown in shorter rotations, leading to crop-specific pathogens or pests building up over time. Other energy crops such as short-rotation coppice willow or Miscanthus may provide a longer-term habitat for insects and other wildlife, which could increase the contamination of neighbouring food crops with insects and materials derived from animals.

3.3.3 Other novel cropsAside from the production of more energy crops, in the future there is also likely to be an increase in novel crops that have previously not been grown to a great extent in the UK, and horticulture may see an expansion into new crops e.g. viticulture (English Food and Farming Partnerships, 2005). These crops may have new contaminant issues that are not currently present in UK agriculture, or may increase the prevalence of other contaminants that are currently a problem, if the host range overlaps. For example, Sclerotinia spp. can infect sunflowers, which may increase the inoculum potential of this pathogen in the area where the new crop is grown, leading to potential contamination of other susceptible food crops. This may lead to an increase in spoilage of those crops. In addition, new pests and pathogens may also be associated with the new crops, bringing unforeseen contamination issues, and fungi that produce mycotoxins may also be associated with novel crops.

3.3.4 Protected and semi-protected croppingProtected or semi-protected cropping can extend the growing season and provide opportunities to increase quality and consistency of supply. Typical crops grown under protection in glasshouses include salad crops such as tomatoes, cucumbers, lettuce, peppers, herbs and celery, whereas semi-protected crops grown in tunnels include soft fruit such as raspberries and strawberries. Over recent years there has been an increase in the use of semi-protected cropping for soft fruit (http://www.hdc.org.uk).

Due to the enclosed environment, protected cropping provides increased control of environmental conditions, pests and pathogens. This has the potential to decrease crop contamination by insects, other animals, and microorganisms that can influence product quality. In addition, monitoring and trapping of insects can be carried out to greater effect in a protected environment, and there is an increased opportunity to use biological control measures. Under semi-protected cropping, there may also be less disease pressure, due to the ability to provide some control over environmental conditions.

However, it has also been reported that certain insects may rapidly multiply under cover compared to an open field, and that (semi-)protected cropping may encourage the development of new pests, or change the status of others (Gordon et al., 1997). Greater numbers of insects could increase the contamination of soft fruit, and removal of these is difficult as soft fruit is typically not washed. In the future, there may be a further increase in the use of protected or semi-protected cropping in the UK, either for crops currently grown under these conditions, or for other crops that may benefit from a more controlled environment, to extend the growing season and to keep up with the demand for fresh produce. Depending on the crops and the availability of control measures, this could either increase or decrease crop contamination compared with crops grown in open fields.

3.3.5 Environmental stewardshipEnvironmental stewardship is an agri-environment scheme consisting of three main elements: Entry level stewardship, Organic Entry Level Stewardship, and Higher Level Stewardship. Within the scheme, various environmental management options are available, including areas of land left uncultivated; inclusion of wild-bird seed mixtures, or pollen and nectar seed mixtures on arable land; over-wintered stubbles; or beetle banks to provide habitat for birds and other animals (www.defra.gov.uk). Habitats for wildlife provided by environmental stewardship may increase the potential for contamination by insects and other animals, or material derived from animals. For example, areas of grassed land set aside for environmental stewardship can provide a habitat for the pests of cereals, bridging the gap between summer crops and the emergence of winter crops (Holland and

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Oakley, 2007). Also, habitat provision could increase populations of natural predators of pests. Whilst this may potentially provide some form of biological pest control, this could also increase the number of casual intruders as contaminants. Increased wildlife could also potentially increase the risk of contamination by microorganisms that are human pathogens, through faecal contamination by birds and other animals.

3.3.6 Water use (irrigation changes – see also climate change)Without factoring in future irrigation requirements due to climate change, it has been estimated that the amount of irrigation required in the UK will increase by 45% from 1995 to 2021, to 245 million m 3 (Groves et al., 2002). This is driven solely by the commercial advantage provided by crop irrigation. Further increases may be expected if growers change to the production of higher value crops that require irrigation. The majority of salad crops are irrigated by overhead booms and through direct abstraction of surface water, possibly posing a risk of contamination by microorganisms pathogenic to humans that have entered the water course through run-off from fields where manure has been applied.

An increase in irrigation could lead to a greater spread of contaminants within a crop through splash dispersal. However, the type of irrigation that is used can have an impact on contamination, and if growers changed to drip irrigation instead of spray irrigation, this could decrease the amount of contaminant spread. Overall, drip irrigation is considered to be more efficient, but more expensive, than spray irrigation.

3.3.7 Diversification of farmsFarm diversification includes letting out farm buildings for non-agricultural use; establishment of farm shops; development of sport and recreation; and tourist accommodation and catering. Of the cropped farms in England, 62% have diversified activities, with horticulture having a high proportion of processing or food retail outlets, and cereals and other general cropping having the highest proportion of sport and recreation (Defra, 2008). However, the highest percentage of farm diversification involves letting out farm buildings for non-agricultural use. In the future, larger rural populations will increase the possibilities for diversification into leisure activities (English Food and Farming Partnerships, 2005).

One of the main effects of increased farm diversification is the increase in the numbers of members of the public coming onto farm land. This could impact on crop contaminants in various ways. For example, there may be increased exposure of the public to pathogenic microorganisms such as aeroallergens. In addition, domestic dogs brought onto farmland could increase the possibility for microorganisms pathogenic to humans contaminating crops through excrement. Alternatively, increased rubbish and litter accumulation (e.g. from campers) may increase the presence of rodents, and thus the incidence of crop contamination from material of animal origin. 3.3.8 Reducing tillage There is a trend world-wide for reducing the extent of tillage practices in order to conserve soil, and in Europe conservation (minimal) tillage is gaining interest (Holland, 2004). Conservation tillage is often practiced in areas where soil erosion is a problem, and involves lesser cultivation of the land to retain more crop residues at the surface. It is defined as a system that leaves 30% or more of the soil surface covered by crop residues after planting (Bockus and Shroyer, 1998). This helps to hold the soil together and also aids the retention of soil moisture (Holland, 2004).

A reduction in tillage, leaving more of the crop residues on the soil surface, can increase the survival of crop-associated microorganisms, which can survive on the crop debris and go on to infect the following crop. In addition, the crop residues can provide a habitat for insects and other fauna. Mycotoxin-producing microorganisms that overwinter on crop residues can potentially increase the risk of contamination the following season.

3.3.9 Stored grainImportant contaminants in stored grain include insects, mites, and mycotoxin-producing fungi. Within the environment of stored grain, these contaminants are often related to each other and interactions between them frequently occur, e.g. insect movement and proliferation can cause moisture redistribution and the formation of ‘hot-spots’ in bulk grain, which allow for fungi to grow. Fungal spores may also be redistributed by insects and mites. Mycotoxins that are produced pre-harvest will remain stable, but fungi such as Penicillium verrucosum can also produce ochratoxin A in store (HGCA, 2003).

Grain drying and cooling are important steps in controlling spoilage, and new technologies as well as improvements in monitoring should reduce contamination of stored grain. For example, a drum drying system was tested using rye grain, and resulted in a decreased risk of spoilage by fungi when the grain was stored properly afterwards. Although this technique did not eliminate mycotoxins that had already formed on the grain, it did reduce the number of viable fungi (Kristensen et al., 2005)

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A LINK project is currently underway to address issues of grain storage and food safety (“Defining and managing risks to safety and quality during food and feed grain storage”). The drivers include the loss of pesticides for use in stores and new legislation on the permitted levels of ochratoxin A formed during storage. These issues have been discussed previously under section 3.1.1 and 3.1.3 on regulations. Another driver is climate change. Increased temperatures may mean that it is more difficult to cool grain, thus increasing the chance of contamination. Changes and improvements in storage facilities could make the process easier to manage.

The key impacts of changing farming practices on crop contamination are likely to be: An increase in organic farming may increase the amount of contamination from insects and other fauna

on organic produce, and microorganisms impacting on product quality (spoilage microorganisms). If wheat is grown more frequently or on a larger scale as a dual food and energy crop there may be an

increase in contamination with microorganisms producing mycotoxins or those producing aeroallergenic spores.

Increased production of novel crops may lead to a potential increase in microorganisms that produce mycotoxins (specific to those novel crops), as well as new pest insects.

An increase in wildlife habitats provided by environmental stewardship may lead to an increase in contamination of crops by microorganisms pathogenic to humans, through faecal contamination.

A possible increase in contamination through farm diversification activities providing sources and vectors for contamination, e.g. increased public exposure to aeroallergens; increase in contaminants of animal origin and human pathogenic microorganisms from domestic pets and rats attracted to food retail outlets and campsites.

By reducing tillage, more crop residues left on the soil surface may increase contamination of crops with microorganisms that produce mycotoxins, and also increase contamination by insects and other animals.

3.4 Processing

3.4.1 New technologies Consumers are demanding ‘minimally processed’ and ‘fresh foods’, which in many cases requires a short supply chain, with rapid and controlled transport of produce. Retailers are driven by the demands of their market and the competitiveness between them, with new product development being crucial to these aims. This is leading to the adoption of less conventional or novel techniques in processing. Examples of this include the use of UV light (Yaun et al., 2004) or Ohmic heating in an attempt to reduce the contamination of fresh fruits and vegetables. UV light has been installed by a major UK sweetcorn producer and an Ohmic heating plant is used by a conserve processor in order to retain the integrity of the fruit in the conserve.

New technologies may also be driven by retailer demands for high precision or automation. For example, a Horizon Scanning report by the HSE (HSE Horizon Scanning Intelligence Group, 2007) estimates that there are “currently around 21,000 service robots in use worldwide, performing tasks such as milking cows, handling toxic waste and assisting surgeons.” Robots that are programmed to perform complex tasks are now entering workplaces within the food industry. If these are disinfected and maintained correctly, they may decrease the amount of contamination that proceeds up the food chain, or prevent further contamination from poor hygiene by removing the human element in food handling. Knorr (1998) illustrated the future processing techniques through the “Technology Hill”. Developments in technology in the future are likely to lead to decreased contamination.

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3.4.2 Chemical use and recycling water (from processing)Microbial contamination in water used to wash or rinse fresh produce can increase the overall microbial count at the end of the process, and it has been noted that this can result in the microbial counts increasing progressively until the end of shelf life (Allende et al., 2004). Thus it is very important to have an effective cleaning and disinfection programme in place, as “every step from production through to consumption will influence the microbiology of fresh produce” (Allende et al., 2004). The consumer desire for ‘additive free’ products is reducing the amount and use of more traditional chemicals such as chlorine and chlorine dioxide in fruit and vegetable washing plants. This may result in contaminants present on fresh produce not being removed and therefore continuing up the food chain to impact on product quality and safety. Restrictions placed on chemicals added to water used for washing could increase the potential for cross-contamination.

Waste water from washing can be re-used after appropriate treatment. In some cases, disposal of waste may be unavoidable, although untreated liquid waste should never be disposed of on arable or horticultural land. Liquid wastes usually have a primary treatment (screening, sedimentation, filtration) and a secondary treatment (biological oxidation by filter beds or oxidation ditch systems). However, these treatments cannot be relied on to eliminate pathogens from high risk waste, which needs further treatment such as UV-irradiation, heating, microfiltration, ozonation or disinfection by environmentally acceptable chemicals (Plant Health Code of Practice for the Management of Agricultural and Horticultural Waste; www.defra.gov.uk).

3.4.3 PackagingModified Atmosphere Packaging (MAP) is commonly used to extend the shelf life of minimally processed foods by lowering the amount of oxygen present in the package and replacing it with carbon dioxide. This slows the growth of fungi and bacteria that may cause quality changes to the fresh produce, thereby reducing spoilage. However, there is some reported concern that this might not have a similar effect on some pathogenic bacteria that can still grow in atmospheres of high carbon dioxide, e.g. Clostridium botulinum was found to grow on shredded cabbage stored at room temperature in MAP (De Roever, 1998; Allende et al., 2004). In addition, it has been found that MAP can increase shelf life but that Listeria monocytogenes can still grow on produce at refrigeration temperatures. This means that although the spoilage microorganisms are controlled by the packaging and refrigeration, L. monocytogenes could proliferate to high levels under these conditions (De Roever, 1998).

Another development in packaging technology includes antimicrobial packaging, in which the “package, the product and the environment interact to extend the lag phase and/or reduce the growth rate of microorganisms” (Suppakul et al., 2008). This extends the shelf-life of the product and preserves safety and quality. Antimicrobial substances incorporated into packaging include bacteriocins such as nisin; chitosan; acids, salts and anhydrides; enzymes; and plant extracts (Joerger, 2007). The use of naturally derived substances is of increasing interest, and examples of antimicrobial materials containing plant extracts include low-density polyethylene (LDPE) impregnated with clove extract, grapefruit seed extract, or rhubarb extract (Suppakul et al., 2008).

The key impacts of drivers from processing on contamination are likely to be: An increase in contamination due to consumer demand for “minimally processed” and fresh food. An increase in cross contamination of microorganisms that can impact on human health or product

quality, due to consumer demands for additive or “chemical free” products that reduce the use of compounds such as chlorine in wash water.

A decrease in contamination levels through more rapid and controlled transport of products. A decrease in contamination through the development of new technologies to treat or process products. A decrease in spoilage contamination through the increased application of packing technologies that

increase shelf life. A potential increase in pathogenic organisms through the incorrect or poor application of processing and

packaging technologies by low technology companies.

3.5 Waste managementFor the purposes of this report, agricultural waste is taken to mean any biological material that could potentially contribute to crop contamination. Thus, farm waste, including items such as plastics, pesticide containers and old tyres etc., is not considered.

3.5.1 Plant wasteWaste management on farms is regulated by The Agricultural Waste Regulations. Exemptions from these regulations that relate to plant material on farms include burning waste plant material in the open (exemption 30); chipping, shredding, cutting or pulverising waste plant matter (exemption 21); deposit of plant tissue at the place of production (exemption 48); composting biodegradable waste from agricultural premises only (exemption 12) (www.environment-agency.gov.uk). Another exemption (exemption 7A) allows for waste from vegetable pack houses to be land spread (www.environment-agency.gov.uk). The latter waste is not actually considered to be agricultural waste per se as it results from an industrial process.

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The Defra “Plant health code of practice for the management of agricultural and horticultural waste” gives guidelines for the disposal of plant waste on farms. This voluntary code of practice describes measures to minimise plant health risks from the management of residues and associated waste of plant produce. This material includes soil, wash water, trimmings and peeling, out-grades and other plant debris. Guidelines on reducing waste include leaving excess plant material in the field after trimming or grading to be grazed by livestock, or ploughed in. Ploughing in crop residues does not require an exemption from waste licensing. Waste from initial processing (washing/trimming) done on farm also needs to be disposed of in a safe manner to avoid potential contamination of growing crops. Crop debris or plant waste left in the field and not ploughed in may pose a risk of contamination if it provides a habitat for survival of contaminants.

3.5.2 CompostingEU targets are in place to reduce the amount of biodegradable waste going to landfill, and thus on-farm composting may increase in the future. Farmers can compost material from their own land, including livestock manures, slurries, or green waste (e.g. hedge or tree trimmings, or plant waste that is not left in situ after harvest). In addition, waste material from other farms can be brought onto the farm carrying out the composting (off-farm composting). Municipal waste may also be composted on farms, up to a limit, under a waste exemption licence.

Guidance is available on producing composts, including the process requirements, inputs, quality control, and end-user requirements or expectations (PAS100 (Publicly Available Specification); http://www.esauk.org/waste). Thus there are quality controls that apply for any compost that is subsequently taken off the farm or sold elsewhere. Composts meeting The Quality Protocol for Compost are no longer considered waste and may be transported off farm. However, there is no guarantee that farmers composting their own waste for use on their own farms will have the appropriate facilities to adhere to the quality guidelines of PAS100, which could potentially impact on the levels of contaminants returned to the soil if composting is not carried out properly. Some pathogens can survive composting procedures, which could lead to an increase in contamination of crops with plant-pathogenic microorganisms or microorganisms that can impact on human health.

3.5.3 Anaerobic digestionAnaerobic digestion creates conditions conducive for the breakdown of organic matter by bacteria in the absence of air (Warburton, 1997). This form of waste management can convert residues from food processing and farming into products that can benefit farmers, e.g. biogas, fibre that can be used as a soil conditioner, and a liquor that can be used as liquid fertiliser. Digesters can either be on-farm units, or large centralised units to deal with waste from numerous sites (Warburton, 1997). There is an increase in the popularity of anaerobic digestion as a waste disposal means, as an alternative to landfill. In addition, some residues that are currently land-spread could be used as a feedstock for anaerobic digesters.

Although composting typically kills pathogens if correct temperatures are maintained, anaerobic digestion reaches lower temperatures and may not eliminate all pathogens. This can potentially increase the risk of crops becoming contaminated with pathogenic microorganisms that survive the process, when the digestate is spread onto land. For example, mesophilic anaerobic digestion (35oC) will not significantly reduce the infectivity of slurry contaminated with parasites, and studies have shown that Salmonella sp. can remain in digestate from mesophilic anaerobic digestion, possibly persisting due to poor mixing within the digester (Warburton, 1997). Sclerotia of the onion pathogen Sclerotium cepivorum have also been found to be at least partially viable following anaerobic digestion (Termorshuizen et al., 2003). Maintaining higher temperatures (70oC) for 30 minutes is required to eliminate all pathogens (Warburton, 1997).

Centralised anaerobic digesters may have feedstocks brought in from elsewhere, potentially bringing crop contaminants onto site. Spreading digestate onto land requires compliance with good agricultural practice and any regulations protecting water quality or nitrate vulnerable zones.

3.5.4 ManuresManure and slurries are not classified as waste when used as soil fertilisers on clearly identified parcels of land (i.e. within plant fertiliser requirements and to fulfil requirements of NVZ legislation). However, manure and slurries may be identified as waste if they are not used in a lawful manner for soil fertilisation on defined parcels of land, and there may be certain circumstances where manures or slurries are regarded as waste (www.defra.gov.uk). This is particularly likely when they are transported off farm.

There may be an increased need for storage of manures on farms where they are considered waste, due to restrictions on the amounts of manure allowed to be applied to land in NVZs. The transport and storage of manure waste may increase the potential for cross-contamination with microorganisms that can impact on human health. Solid waste can be treated by being composted, or through anaerobic digestion, aerobic digestion, boiling, steaming, or dry heat.

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The key impacts of waste management on crop contamination are likely to be: Microorganisms surviving in crop debris or plant waste that is not ploughed in may increase the risk of

contamination for the following crop. If on-farm composting is not carried out correctly, there is an increased risk of contamination with

human-pathogenic microorganisms from manures and slurries that form part of the compost feedstock being returned to agricultural land.

Although anaerobic digestion can reduce pathogen numbers, it cannot safely eliminate all pathogens from the digestate, potentially leading to an increased risk of crop contamination with microorganisms that can impact on human health and product quality.

A potential increase in cross-contamination with microorganisms pathogenic to humans when waste manure is stored or transported.

3.6 Climate change Four climate change scenarios have been presented for the UK, based on future levels of emissions (Hulme et al., 2002). For the purposes of this report, we have used the general conclusions for predicted climate change in the UKCIP02 report as an indicator for changes in temperature and rainfall. In general the UKCIP02 models indicate hotter drier summers, with milder wetter winters, and more extreme events (e.g. flooding) (Hulme et al., 2002).

3.6.1 Increased temperatureOver the past 100 years global temperatures have increased by 0.6oC, and temperatures in the UK have increased by approximately 1oC. Predicted changes for the future include average annual temperature rises (2-3.5oC by 2080s, depending on the scenario), with greater warming in the south, and an increase in the temperature of UK coastal waters. The UK’s thermal growing season for plants is longer now than at any time since records began (Hulme et al., 2002).

Increased temperature could mean an increase in crop contamination in the future. For example, there is a trend for increased spore concentrations of aeroallergens to occur with increased temperatures. Alternaria spp. spores have been recorded at increased levels over recent years, and trends show an earlier seasonal start and longer seasonal duration (Corden and Millington, 2001). The number of days with a spore count above 50 Alternaria spores per cubic metre has risen, and there has been a positive correlation between spore counts and the maximum temperatures recorded (Corden and Millington, 2001). Other research has also suggested that there may be an increase in spore numbers and an earlier start to the spore season with increased temperature (Beggs, 2004).

Some fungi producing mycotoxins may become more prevalent if the temperature increases towards their optimum growing temperature. See Table 3.6.1 for the optimal conditions for different mycotoxigenic fungi (Murphy et al., 2006). Note that some of these optima have been determined from growth in laboratory conditions and not in field or storage.

Table 3.6.1 Optimal growing conditions of mycotoxin-producing fungi (taken from Murphy et al. (2006))Microorganism (mycotoxin) Temp 0C Aw

Aspergillus flavus, A. parasiticus (aflatoxin) 33 0.99Aspergillus ochraceus (ochratoxin) 30 0.98Penicillium verrucosum (ochratoxin) 25 0.90-0.98Aspergillus carbonarius (ochratoxin) 15-20 0.85-0.90Fusarium verticillioides, Fusarium proliferatum (fumonisin) 10-30 0.93Fusarium verticillioides, Fusarium proliferatum (DON) 11 0.90Fusarium graminearum (zearalenone) 25-30 0.98Penicillium expansum (patulin) 0-25 0.95-0.99

Higher temperatures (including warmer coastal waters) could mean that pest insects or other contaminants could migrate to the UK from the continent, leading to new contamination issues. These could become established initially in protected or semi-protected cropping systems. Several cereal pest insects including aphids and weevils have been recorded as having an increased incidence with increasing temperature, or after milder winters, and some have been found to be spreading north and west across the UK (Holland and Oakley, 2007).

Poor storage of cereals is a problem for quality control, with rejections costing over £3 million a year. A warmer climate may make it more difficult to cool grain, affecting infestations by storage pests, with the risk of insect contamination increasing, and potentially further increasing the possibility of contamination with fungi that produce mycotoxins in stores. Increased temperatures may impact on other stored crops e.g. cabbage or onions, if it becomes more difficult to maintain cool conditions in “ambient” stores.

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Warmer temperatures will also allow some pest insects to produce more generations per year, increasing the risk for contamination. In addition, high temperatures may reduce the effectiveness of some pesticides, leading to poorer control of certain pests or pathogens. In contrast, extreme temperatures may also be detrimental to the survival or reproduction of some current pests and pathogens in the UK. It is difficult to say with certainty which groups of contaminants will increase or decrease on which crops.

3.6.2 Increased winter rainfallPredicted changes in winter rainfall indicate that in the future winters will be wetter (Hulme et al., 2002). This could increase slug populations, particularly with milder winters also occurring, which could increase contamination of some fresh produce. In contrast, too much water can be devastating for some pests, affecting their survival and reproduction and disrupting behaviour patterns. In addition, raindrops can physically dislodge pests from host plants, possibly resulting in reduced contamination by some insects.

3.6.3 Decreased summer rainfallPredicted changes in summer rainfall indicate that, in the future, summers will be slightly drier (Hulme et al., 2002). High temperatures and dry conditions in summer will become more common. Regarding the occurrence of aeroallergen spores, there has been a slight negative correlation with daily rainfall (Corden and Millington, 2001). Decreased summer rainfall (coupled with an increased temperature) could increase the occurrence of microorganisms that produce aeroallergenic spores.

3.6.4 Increased irrigation requirementsWith increased temperatures and a decrease in summer rainfall, soil moisture is likely to be reduced in the future. This will lead to an increased requirement for irrigation. Depending on the type of irrigation that is used (spray or drip), this could increase the occurrence of certain crop contaminants. For example, water splash from overhead irrigation could increase crop contamination with microorganisms that are pathogenic to humans, or those that impact on product quality (See section 3.3.6).

3.6.5 Extreme events Climate change could increase the frequency of extreme events, such as flooding or drought, in the future. These extreme or unusual events could increase contamination from various sources. For example, in 2007, a warm spring followed by a warm, wet summer was ideal for rat breeding, and it was reported that because of the waterlogged and flooded fields, many rat populations were seeking shelter in farm buildings (Farmers’ Guardian, 7 September 2007). Increased rat populations could increase contamination of stored produce such as harvested grain. Leptospirosis (Weil’s disease) is largely transmitted to humans through rats, although other animals (livestock and wildlife) can also carry the spirochaetes that cause the disease. The disease is contracted through contact with water or soil contaminated with animal urine, and flooding may cause the spread of the disease through the movement of rats as well as run-off from farmland. This potentially increases the risk of crop contamination by this human-pathogenic microorganism.

Extreme events like very wet summers (as seen in 2007) may also mean that grain has to be harvested wet, which could increase the risk of mycotoxin contamination. The wet weather also means that disease spread through other crops, such as cavity spot on carrots and parsnips, could increase.

The effects of flooding or drought on pest and pathogen populations will vary according to species and the timing of the event, with some contaminants increasing in dry conditions and others increasing more when it is wet.

The key impacts of climate change on crop contamination are likely to be: An increase in temperature may lead to an increased risk from aeroallergenic spores from plant

pathogens contaminating crops, possibly leading to greater incidences of asthma and bronchial related illness.

Fungi that produce mycotoxins could become more prevalent in warmer conditions, or may produce different mycotoxins under different temperature optima.

Milder winters could increase the survival of insects and microorganisms, and insect contamination of crops could increase with more generations per season.

Conditions could become more suitable for microorganisms that impact on product quality, with faster growth rates and sporulation in some cases.

Objective 4: A review of the impact of crop contamination on human health and product quality

4.1 Impact on human healthThe different types of biological crop contaminants (given in Objective 1) can impact on human health to various degrees. Each of the categories will be dealt with individually below.

4.1.1 Microorganisms pathogenic to plants and also humans

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For the majority of the population, plant pathogens do not impact directly on human health, as these microorganisms do not infect non-compromised humans to cause disease. However, for the sector of the population that is susceptible to infection by plant pathogens (e.g. CF patients) the impact on human health can be severe, and may even be life-threatening. However, it is unclear how many cases of human infection by plant pathogens are actually caused directly from crop contamination, and infections may occur through direct transmission from patient to patient.

Aeroallergens are an important consideration for the general population, as airborne spores of plant pathogens may sensitise humans and cause bronchial infections and asthma. For people suffering from severe asthma, increased numbers of airborne spores from plant pathogens can increase hospital admissions, or even deaths in severe cases (Beggs, 2004). Future concerns may be that the group of at-risk or susceptible people will increase, resulting in more cases where plant pathogens infect humans opportunistically. Alternatively, strains of other plant-associated microorganisms not currently able to infect humans may be able to cross hosts in the future and have implications for human health.

4.1.2 Microorganisms that are pathogenic to plants but also produce compounds toxic to humansMycotoxins produced by fungal plant pathogens can have very serious human health implications if ingested, with acute toxic, carcinogenic, mutagenic, teratogenic, or estrogenic effects (van Egmond and Speijers, 1999). Because of this, the amount of mycotoxins present in food is carefully regulated. However, although limits may be set for the amount of mycotoxins permitted in various food products, it is difficult to monitor the amounts of mycotoxin potentially consumed on an individual basis, and how that might affect an individual’s health over time. The current impact of mycotoxin consumption on human health in the UK is difficult to quantify.

4.1.3 Microorganisms from the environment that are pathogenic to humans that can contaminate crop plants during the production processFood-poisoning by microorganisms contaminating fresh produce can impact on human health by causing diarrhoea, cramps, vomiting, nausea, abdominal pain, dehydration, fatigue, weakness, and fever. In some severe cases, other symptoms can include double vision, slurred speech, respiratory failure, and sometimes even death (van Schothorst, 1999). There has been a trend to increase the amount of fresh produce that we eat (e.g. 5-a-day campaign), and in some cases, pre-packed salads have been sources of contamination with enteric bacteria. Fresh produce accounts for approximately 8% of reported food poisoning outbreaks (Hughes et al., 2007). As more emphasis is placed on healthier eating, and increased consumption of fresh or minimally processed foods, the frequency of these outbreaks might increase. Table 4.1 (see Appendix) lists various groups of crops and the likely impact of crop contamination with human-pathogenic microorganisms on human health, depending on whether they are typically eaten raw (more likely to have contaminants impacting on human health) or cooked before consumption (less likely to have contaminants impacting on human health).

4.1.4 Microorganisms that can impact on product qualityPlant pathogens and microorganisms that cause obvious visual spoilage are unlikely to impact on human health, as affected food is unlikely to be consumed. Early stages of produce infection may go unnoticed by consumers, however, and such infected produce may be consumed. The impact of this on human health is difficult to determine, but may result in typical symptoms of food-poisoning.

4.1.5 Insects, other animals and materials derived from animals Crop contaminants of animal origin (i.e. insects or insect fragments) are generally considered to be non-hazardous to humans. However, because of the aesthetic appearance of food, any product contaminated in this way is unlikely to be consumed, thus the impact on human health is considered to be low.

4.2 Impact on product qualityProduct quality is important throughout the food chain, and poor quality items may be rejected at different points through the production process. This can affect growers and farmers if their produce is rejected, e.g. batches of cereals rejected for having levels of mycotoxins that are too high. Consumers are concerned with product quality when they purchase food, and will not buy fresh produce that has obvious visual defects such as mould growing on it. Once purchased, the next stage where consumers are interested in product quality is when they come to eat the produce. At this point, food that has “gone-off” or has obvious microbial growth will also be rejected. The different groups of microorganisms listed below can impact on product quality at different stages of the food chain, and have various impacts on product quality.

4.2.1 Microorganisms pathogenic to plants and also humansProduct quality may be affected by this group as they are plant pathogens. Infected produce may have visual symptoms of decay or other quality defects.

4.2.2 Microorganisms that are pathogenic to plants but also produce compounds toxic to humans

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Product quality can be affected by plant pathogens producing mycotoxins, and if the levels are too high, the product will be rejected for human consumption. This group of microorganisms can have a significant impact on quality.

4.2.3 Microorganisms from the environment that are pathogenic to humans that can contaminate crop plants during the production processProduct quality may not be obviously affected by these human-pathogenic microorganisms as they are not plant pathogens. The lack of visual quality defects means that produce contaminated by these microorganisms is more likely to be consumed. For example, a study of bacterial numbers on lettuce at various stages in the production and processing chain (reception, shredding, washing, draining, rinsing, centrifugation and packaging) indicated that shredding, rinsing and centrifugation, in particular, increased bacterial numbers (Allende et al., 2004). This study also illustrated that the sensory quality of the product was still acceptable after 7 days of storage, but that the microbial quality was unacceptable and that the numbers of certain bacteria were too high for food safety (Allende et al., 2004).

4.2.4 Microorganisms that can impact on product qualitySpoilage microorganisms have a significant impact on product quality and losses due to contamination with this group can be high. Indicators of poor product quality include visual defects; obvious microbial growth; off-odours; off-flavours; texture breakdown; and cloudiness, sediments or films forming in juices. It is difficult to determine the true impact of spoilage microorganisms on product quality because of the amount of fresh produce that is discarded after purchase due to spoilage “at home”. A report by WRAP indicated that fruit and vegetables are the most frequently wasted food that is potentially edible. Research suggests that “about 40% (by weight) of the food thrown away that could have been eaten is fresh fruit and vegetables (which includes potatoes)”, and that one of the main reasons for food being thrown away is due to a loss of quality or that it was past its use-by date (www.wrap.org.uk).

4.2.5 Insects, other animals and materials derived from animals Product quality may be affected by this group of contaminants, depending on the extent of the contamination, and produce contaminated with insects or animal hairs are likely to be rejected by the consumer.

Objective 5: A review of the marketability of products

5.1 ThreatsProduct marketability can be threatened by poor quality and safety and contaminants have a significant impact on product marketability. Major threats include:

Decreased control of crop contaminants due to restrictions placed on pesticides and chemicals. o Withdrawal of pesticides due to regulatory impact, resulting in poor control of pests and

pathogens.o Restrictions placed on pesticide use by retailers’ demands, possibly resulting in fewer options to

control pests and pathogens.o Reductions in chemicals used to wash produce or in further processing.

Increased temperatures due to climate change could increase the incidence of crop contamination.o Novel pests and pathogens emerging that are not controlled by current measures.o Insects may be better able to overwinter successfully and produce more generations.o Grain drying and cooling could be more difficult in warmer conditions, potentially increasing

contaminants such as mycotoxigenic fungi, insects or mites.o Cooling other stored produce could be more difficult in warmer conditions, potentially increasing

contaminants that cause spoilage.o Increased irrigation requirements may lead to contaminant spread through splash dispersal if

spray or overhead irrigation is used.

Other threats to product marketability include: Extreme climate events such as flooding or drought may have unpredictable outcomes on crop

contaminants. Wheat grown on a larger scale as a bioenergy crop may increase the incidence of mycotoxigenic fungi

contaminating crops. Mycotoxigenic fungi could also overwinter on stubble following reduced tillage. Novel crops may bring new contaminants that are currently unknown/unpredictable. Semi-protected cropping may increase the survival of certain insects on soft fruit, which may be difficult to

remove as the produce is not washed. Increased on-farm composting and anaerobic digestion may result in contaminants being returned to

land, if the procedures are not carried out correctly.

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Waste manure storage and transport off farm could increase cross-contamination of human pathogenic microorganisms (this is in contrast to manure applied as a fertilizer, where restrictions on application may reduce contamination of crops).

Poor hygiene by workers, leading to potential contamination by human-pathogenic microorganisms. Farm diversification activities may lead to minor increases in contamination of crops through public

access to farmland. Wildlife habitats created on farms can increase the risk of contamination from insects, materials derived

from animals, or microorganisms pathogenic to humans resulting from faecal contamination. Examples of changing farming practices that might create wildlife habitats include environmental stewardship, organic farming, reduced tillage leaving stubble as a habitat, and long-term energy crops such as short-rotation coppice willow or Miscanthus.

Modified packaging may extend the shelf-life of products through decreasing contamination by spoilage microorganisms, but still allow for the growth of human-pathogenic microorganisms that affect food safety. These human-pathogenic microorganisms might not affect product quality visually, thus increasing the risk of consumption of contaminated produce.

Impact of food-poisoning scares/outbreaks on consumer choices, e.g. if an outbreak of food-poisoning is traced back to a specific product and reported in the news, consumers may not buy that product in the short-term, thus affecting marketability.

5.2 OpportunitiesOpportunities to maintain or increase the marketability of products in the future include:

Limiting contamination of crops during the growing seasono Better hygiene controls along the food chain, including the education and training of growers and

seasonal workers of the principles of HACCP at farm level.o Ensuring compliance with farm assurance schemes, following codes of Good Agricultural

Practice, and encouraging best practice in the use of pesticides.o Increased monitoring to increase detection rates of potential contaminants.o Protected cropping can provide a controlled environment where product quality and safety can be

maximised. o Drip irrigation where necessary to avoid splash dispersal.

New developments and improved technology o Easier registration procedures for biological control agents to become part of an IPM programme o Alternative measures of control could be developedo New technology and methods to remove contaminants from fresh produceo New technology in processing and packaging to decrease contaminants reaching consumerso Improvements in storage facilities and new technology for grain drying and coolingo Improved crop varieties

Food hygiene laws will ensure good quality and safe food reaches the consumers. Shorter supply chains (fewer food miles on fresh produce). Education of consumers to accept products that are of lesser visual quality but still safe to eat.

5.3 Risk assessmentHazard means anything that can cause harm, and risk is the probability that a hazard will lead to harm. For the purposes of this report, crop contaminants are hazards that can affect the marketability of products by affecting product quality and safety.

In this section we have used Table 3.1 as a starting point, and have taken the categories where a specific driver is likely to cause a moderate increase in contaminant levels for one or more of the different contaminant groups considered in the report (Table 3.1; categories designated ++). The drivers include regulations restricting pesticide use; increased land used for organic farming; decreased chemical use in recycled water in processing; and temperature increases with climate change. Categories where a specific driver is likely to cause a small increase in contaminant levels (+) are not considered here, but are also potential threats to product marketability, albeit on a lesser scale or under specific circumstances.

By assessing the likelihood of these drivers occurring, against the severity, the potential risk to product marketability can be determined. Severity here is determined from the number of contaminant groups that may be affected by the driver, i.e. if only one contaminant group is affected, the severity may be low, whereas if three groups are affected the severity could be high. Table 5.1 shows the matrix used in this report to carry out a risk assessment on the marketability of products, based on product quality and safety.

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Table 5.1: Matrix used to determine risk (likelihood of occurrence x severity)

Severity of occurrence

Likelihood of occurrence Low Moderate High

Low Low Low/moderate Moderate

Moderate Low/moderate Moderate High

High Moderate High Very high

Key: A low risk means that the product marketability is unlikely to be affected. A moderate risk means that the product marketability may be affected. A high risk means that the product marketability is likely to be affected. A very high risk means that the product marketability is very likely to be affected.

Using the matrix above (Table 5.1), a risk assessment is presented in Table 5.2 of the drivers that are considered most important threats to increased contamination. Restrictions placed on pesticides and increased temperature are the two drivers that may cause a very high risk to product marketability in the future. These are drivers that can affect the cropping sector as a whole. Whilst the other drivers considered in Table 5.2 may cause an increase in certain groups of contaminants, the risk of this to product marketability is lower, and may only affect certain sectors e.g. organically produced crops, or minimally processed fresh produce.

Table 5.2: Risk assessment for drivers that may cause a moderate increase in one or more contaminant groups (++ categories in Table 3.1)

Driver Likelihood of occurrencea

Severity of occurrenceb

Risk to product marketability

Restricted pesticide use High High Very high

Increased land used for organic farming (crops)

Moderate Low Low/moderate (organic produce only)

Decreased chemical use in recycled water in processing

Moderate Moderate Moderate

Temperature increases with climate change High High Very higha Likelihood of occurrence has been evaluated from evidence presented earlier in Objective 3. See individual sections for further detail.b Severity is determined from Table 3.1 (see Appendix)High = driver causes a moderate increase (++) in three or more groups of contaminants Moderate = driver causes a moderate increase (++) in two groups of contaminantsLow = driver causes a moderate increase (++) in one group of contaminants

Sources of information and further workInformation included in this report has been collected from diverse sources including peer reviewed research papers, published reports, Government websites and expert sources. The accuracy and reliability of these data has been accepted and used as a basis for expert opinion to reach conclusions. In this way, it has been possible to identify possible trends for the impact of drivers on groups of contaminant microorganisms and insects. However, it has not been possible to quantify accurately changes in populations of contaminants.

Further work would be required to model changes in contaminant populations and to provide a more detailed analysis of the risks imposed by specific drivers.

AcknowledgementThe project team thank Lynne de Motte (Research & Consultancy Network) for her input.

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References to published material9. This section should be used to record links (hypertext links where possible) or references to other

published material generated by, or relating to this project.

ReferencesAllende A., Aguayo E., Artés F., 2004. Microbial and sensory quality of commercial fresh processed red

lettuce throughout the production chain and shelf life. International Journal of Food Microbiology 91, 109-117.

Assured Produce, 2007. Generic Protocol Standards 2007 (July revision). Beggs P.J., 2004. Impacts of climate change on aeroallergens: past and future. Clinical & Experimental

Allergy 34, 1507-1513.Better Regulation Task Force, 2000. Environmental Regulations and Farmers.Bockus W.W., Shroyer J.P., 1998. The impact of reduced tillage on soilborne plant pathogens. Annual

Review of Phytopathology 36, 485-500.Corden J.M., Millington W.M., 2001. The long-term trends and seasonal variation of the aeroallergen

Alternaria in Derby, UK. Aerobiologia 17, 127-136.De Roever C., 1998. Microbiological safety evaluation and recommendations on fresh produce. Food

Control 9, 321-347.Defra, 2007a. Consultations on Diffuse Water Pollution From Agriculture information leaflet, rev.October

2007. Defra, 2007b. Defra's statement of forthcoming legislation for 2007. February 2007.Defra, 2008. Farm diversification - Statistical release January 2008. p.22.English Food and Farming Partnerships, 2005. A study of long-term trends affecting the farming industry.

A report for Defra Farming Regulation Strategy Division.Food Standards Agency, 2005. Managing Farm Manures for Food Safety. Guidelines for growers to

reduce the risks of microbiological contamination of ready to eat crops. Food Standards Agency, 2007a. The UK Code of Good Agricultural Practice to Reduce Fusarium

Mycotoxins in Cereals. p.15.Food Standards Agency, 2007b. The UK Code of Good Storage Practice to Reduce Ochratoxin A in

Cereals. p.12.Friends of the Earth, 2004. Pesticides in supermarket food. Briefing July 2004. p.7. Gordon S.C., Woodford J.A.T., Birch A.N.E., 1997. Arthropod pests of Rubus in Europe: Pest status,

current and future control strategies. Journal of Horticultural Science 72, 831-862.Groves S.J., Davies N., Aitken M.N., 2002. A report to The Food Standards Agency: A review of the use of

water in UK agriculture and the potential risks to food safety. p.148.HGCA, 2003. The grain storage guide. Second edition.Holland J.M., 2004. The environmental consequences of adopting conservation tillage in Europe:

reviewing the evidence. Agriculture, Ecosystems and Environment 103, 1-25.Holland J.M., Oakley J., 2007. Importance of arthropod pests and their natural enemies in relation to

recent farming practice changes in the UK. HGCA Research Review No. 64.HSE Horizon Scanning Intelligence Group, 2007. Short report: Robot Realities Sr007. Hughes C., Gillespie I.A., O'Brien S.J., The Breakdowns in Food Safety Group, 2007. Foodborne

transmission of infectious intestinal disease in England and Wales 1992-2003. Food Control 18, 766-772.

Hulme M., Jenkins G.J., Lu X., Turnpenny J.R., Mitchell T.D., Jones R.G., Lowe J., Murphy J.M., Hassell D., Boorman P., McDonald R., Hill S., 2002. Climate Change Scenarios for the United Kingdom: The UKCIP02 Scientific Report, Tyndall Centre for Climate Change Research, School of Environmental Sciences, University of East Anglia, Norwich, UK. p.120.

Joerger R.D., 2007. Antimicrobial films for food applications: A quantitative analysis of their effectiveness. Packaging Technology and Science 20, 231-273.

Knorr D., 1998. Technology aspects related to microorganisms in functional foods. Trends in Food Science & Technology 9, 295-306.

Kristensen E.F., Elmholt S., Thrane U., 2005. High-temperature treatment for efficient drying of bread rye and reduction of fungal contaminants. Biosystems Engineering 92, 183-195.

Magkos F., Arvaniti F., Zampelas A., 2006. Organic food: Buying more safety or just peace of mind? A critical review of the literature. Critical Reviews in Food Science and Nutrition 46, 23-56.

Martinez M.G., Fearne A., Caswell J.A., Henson S., 2007. Co-regulation as a possible model for food safety governance: Opportunities for public-private partnerships. Food Policy 32, 299-314.

Murphy P.A., Hendrich S., Landgren C., Bryant C.M., 2006. Food mycotoxins: An update. Journal of Food Science 71, R51-R65.

National Statistics, 2007. Organic Statistics, United Kingdom. Joint Announcement by the Agricultural Departments of the United Kingdom, Defra.

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Rembialkowska E., 2007. Quality of plant products from organic agriculture. Journal of the Science of Food and Agriculture 87, 2757-2762.

Suppakul P., Sonneveld K., Bigger S.W., Miltz J., 2008. Efficacy of polyethylene-based antimicrobial films containing principal constituents of basil. LWT - Food Science and Technology 41, 779-788.

Termorshuizen A.J., Volker D., Blok W.J., ten Brummeler E., Hartog B.J., Janse J.D., Knol W., Wenneker M., 2003. Survival of human and plant pathogens during anaerobic mesophilic digestion of vegetable, fruit, and garden waste. European Journal of Soil Biology 39, 165-171.

Trienekens J., Zuurbier P., 2007. Quality and safety standards in the food industry, developments and challenges. International Journal of Production Economics doi:10.1016/j.ijpe.2007.02.050.

van Egmond H.P., Speijers G.J.A., 1999. Natural toxins I: Mycotoxins. In: K van der Heijden, M Younes, L Fishbein and S Miller Eds International Food Safety Handbook. Marcel Dekker, Inc., New York, pp. 341-355.

van Schothorst M., 1999. Microbiological and hygenic aspects of food safety. In: K van der Heijden, M Younes, L Fishbein and S Miller Eds International Food Safety Handbook: Science, international regulation, and control. Marcel Dekker, Inc., New York, pp. 27-46.

Warburton D. (Ed) 1997. Anaerobic digestion of farm and food processing residues. Good Practice Guidelines. p.57.

Yaun B.R., Sumner S.S., Eifert J.D., Marcy J.E., 2004. Inhibition of pathogens on fresh produce by ultraviolet energy. International Journal of Food Microbiology 90, 1-8.

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