Pesticides in Perspective Introduction The column begins with an article on a topic that is important to all of us human exposure to pesticides through our diet. The question that consumers increasingly ask concerning pesticides is ``is my food safe to eat?'' This article attempts to put these concerns into perspective gives a little background to the UK surveillance scheme and uses UK data to illustrate what regulators are doing to ensure that the food eaten in the UK is safe. It is hoped that at a later date articles will appear in the column outlining what is done (with relevant results) in the rest of Europe and provide details about the US surveillance scheme and also policies/procedures in other parts of the world. The author of this article has had a very varied career.Professor Ian Shaw obtained an Honours degree in Pesticides residues in food{ Consumers are becoming more concerned about food contaminants; pesticide residues feature high in their list of worries. In this overview an attempt is made to put these concerns in perspective. Food monitoring and human exposure data are used to illustrate what regulators are doing to ensure that the food we eat is safe. Food safety is an emotive issue in most developed countries although concern amongst consumers about the food they eat varies according to the trust that they have in their countries' regulatory systems and the persuasive powers of their press. The UK public's interest in food safety issues began in earnest when in 1986 Edwina Currie the then Minister of Health brought to the Country's {The opinions expressed in the following article are entirely those of the authors and do not necessarily represent the views of either The Royal Society of Chemistry the Editorial or Editorial Board of JEM Zeneca Agrochemicals or those of the Column Editor.34N J. Environ. Monit. 2000 2 This journal is # The Royal Society of Chemistry 2000 Biochemistry from the University of Bath and gained his PhD in Biochemistry (Toxicology) at the University of Birmingham. He is a Fellow of both the Royal Society of Chemistry and Institute of Biology and for two years served as a JP (Justice of the Peace). His various occupations have led him from University Lecturer to a short time in industry to the Central Veterinary Laboratory where he became Head of the Biochemistry Department and Ænally to become Professor of Toxicology and Head of the Centre for Toxicology at the University of Lancashire.At the time of writing Professor Shaw is about to take up a new appointment in New Zealand. He has been a member of a range of committees and has held a number of honorary positions too many to list here. They have included the Working Party on Natural Toxicants in Food and the attention that Salmonella was a common contaminant of poultry and that its presence in eggs could lead to severe food poisoning. The press seized upon this issue and created a furore which raged for months and resulted in the temporary demise of the British egg industry.Since then there have been many food scares all fuelled by a press eager to amplify the issues. These scares including the effects of bacteria of the genus Listeria on the consumers of soft cheeses and of course bovine spongiform encephalopathy (BSE) which virtually destroyed the British beef industry and had signiÆcant political repercussions throughout Europe. The concern about food safety reached a crescendo when consumers and activists objected to the introduction of genetically modiÆed food. This battle will rage for many years as the David-like activists Æght the Goliath global companies who not only stand to make vast sums of money out of their ingenious inventions but also have enormous political power in countries such as the USA.Pesticides Working Party on Veterinary Residues in Animal Products and he is also a Visiting Consultant Toxicologist to Preston Health Authority in the UK. He is currently a Member of the UK Government's Advisory Committee on Pesticides a Member of the UK Government's Advisory Committee on Animal Feedingstuffs and he is Chairman of the UK Government's Pesticide Residues Committee (formerly the Working Party on Pesticide Residues). It is in this latter capacity that he writes this current article. I hope that you like myself Ænd his article to be both informative and provocative. Dr Terry Clark Column Editor Zeneca Agrochemicals E-mail Terry.Clark@aguk.zeneca.com The regular press interest in food scares has heightened consumer awareness of food safety.As a result consumers have begun to question how food is produced and what it contains as they no longer accept that the food available on market shelves is necessarily safe. Therefore one issue of general concern is the use of pesticides in farming1 and the consequent presence of pesticide residues in food.2 The hidden risks in food When questioning shoppers in a supermarket whether they were concerned about residues of pesticides in their food. All replied Yes! When asked about natural toxins no one knew what was meant. This is an interesting paradox because it is likely that the natural toxins in food present a greater risk to the consumer than pesticide residues.Psoralens a group of naturally occurring pesticides in parsnips celery parsley and related vegetables are photoactivated carcinogens often present at concentrations of tens or hundreds of mg kg21. They are present in every parsnip stick of celery and leaf of parsley that we eat. On the other hand pesticide residues are not omnipresent and their residues are generally at exceptionally low concentrations. Psoralens must present a greater risk to the consumer of parsnips than any of the pesticide residues that are likely to be present in parsnips simply because psoralens are carcinogens. The testing necessary before a pesticide is approved for use in countries of the developed world make it extremely unlikely that a carcinogenic pesticide could ever be approved.These hidden risks from natural toxins such as psoralens are often ignored when concerns about food are raised by the media and political lobby groups; but perhaps this is understandable because the only way to control levels of these natural toxins in food is by genetic modiÆcation! It is important that speciÆc risks (e.g. pesticides in food) are considered in the context of related unavoidable or accepted risks (e.g. natural toxins in food). If this is done properly pesticides are likely to be very low in the hierarchy of life's risks. Assuring the consumer that food is safe Governments are obviously keen to assure national and international consumers of food produced within their countries is safe for consumption.From the point of view of pesticide residues this generally involves the operation of surveillance schemes. Such schemes generally comply with national legislation and involve the analysis of prescribed numbers of samples of food for selected pesticides on an annual basis. The number of samples analysed varies greatly from country to country. For example in Europe the greatest number of samples analysed on a per capitum population basis is in Sweden (100161026 per capitum in 1996; total number of samples analysed~8908)2 and the smallest is in the UK (1561026 per capitum; total number of samples analysed~878).2 Is this a reØection of the individual country's concern for consumer well being? Countries that rely on fruit and vegetable exports often appear towards the top of the samples analysed per capitum league table.For example Holland analysed 70661026 samples per capitumin 1996 (total number of samples analysed~11015)2 and was 2nd in the European league table. A third of food consumed in the UK contains pesticides The UK runs a pesticide residues food surveillance programme via the independent Pesticide Residues Committee [PRC; formerly the Working Party on Pesticide Residues(WPPR)]. The independence of the Committee is important because it gives credibility to published data. The budget for the Programme in 1999/2000 is £1.67 million most of which will be spent on analysis.Data from the PRC show that approximately 30% of food consumed in the UK contains measurable residues of pesticides (Table 1) and that approximately 1% contains residues above the maximum residue limit (MRL–a statutory limit based on good agricultural practice (GAP)– compliant use of pesticides. It should be noted that MRL is not a safety parameter because toxicological considerations are not taken into account in its derivation). The frequency of food contamination by pesticides is remarkably stable. This suggests that if we accept the use of pesticides in food production as they are currently used then we must also accept these residues. Indeed from the point of view of human health there is perhaps good reason to accept the situation because acceptable daily intake (ADI; the intake necessary each day of an entire lifetime to result in harm–this is a safety parameter) exceedances are extremely rare.Indeed in the UK there have been no exceedances in the past 4 years. ADIs are based on single pesticides but our diet contains complex cocktails of pesticide residues and there are no data to allow us to decide what effect these might have on the consumer in the long term. Despite this it is likely that such effects will be minimal because the total intake of pesticides with food is very low (and not continuous) when Table 1 Frequency of residues of pesticides in food determined as part of the UK's monitoring programme Percentage Above MRL With Residues Year 30 31 34 vv 1 1 v1 29 26 v1 1.3 19943 19954 19965 19976 19997 Pesticides compared with other toxins (e.g.natural plant toxins). Perhaps the best argument for reducing the use of pesticides is the proven deleterious effect that pesticides have on the environment. The rapidly increasing anti-pesticide lobby are having a signiÆcant effect upon pesticide use. For example public concern about pesticide residues in food has led to supermarkets controlling the use of particular pesticides by their growers (e.g. Alar a plant growth regulator) in order to present a market advantage over their rivals. Supermarkets are very powerful in this respect and their demands can result in signiÆcant changes in pesticide usage both nationally and internationally.This combined with the organic movement and environmental lobby will almost certainly force farmers to reduce pesticide use over the coming years. It will be interesting to see if this is reØected in a reduced residues frequency. Problematic pesticides in 1998 Yams and carbendazim The recently published results of the UK's 19987 monitoring programme have highlighted areas of concern. In 1998 there was an apparent rise in the frequency of residues above MRLs (Table 1). This was because 75% of yams contained residues of the fungicide carbendazim above its MRL (none exceeded the ADI). On the face of it this is a signiÆcant problem particularly for West Indian families who might include Yams as a major carbohydrate source in their diet.However the reason for these MRL exceedences was because a default MRL (based on the analytical limit of determination for carbendazim) had been set for carbendazim in yams because GAPtrials data were not available. These were therefore only technical exceedances. Discussions between the UK government and the yam exporting countries will hopefully result in an import tolerance being set which means that even though the yams imported into the UK in 1999 might contain residues of carbendazim similar to those for 1998 they will not exceed MRLs. If a correction is made to the MRL exceedance frequency for 1998 (i.e.yam data are removed) the value is v1% and therefore does not represent an increase over previous years (Table 1). 35N J. Environ. Monit. 2000 2 Pesticides Illegal chlormequat in UK pears Residues data cannot all be explained away. In the 1998 UK survey7 80% of UK-grown pears were found to contain the growth regulatory pesticide chlormequat. Chlormequat is not approved for use in the UK therefore this represented an illegal use of the pesticide. There are two issues here the fact that growers were using a pesticide illegally and the potential harm that this might cause the consumer of pears. The latter is particularly important because pears and pear juice are commonly used in proprietary and home-prepared infant foods.Infants are an important high risk group because their food intake per unit body weight in high. ADI calculations showed that one of the pears was only marginally below the ADI (residues in pear~11 mg kg21; ADI~15 mg kg21). This is a situation that regulators and government take very seriously. On this occasion a follow-up study was initiated and legal action taken against the offending growers. Unfortunately the follow-up study showed no improvement in the situation. It is to be hoped that the legal action against growers will `Ære a shot across the bows' of other potential illegal users. We will not know whether the strategy has been successful until the 1999 survey is complete. In the meantime consumers are possibly being exposed to unacceptably high residues of chlormequat.However in terms of risk this pales into insigniÆcance when considered in the context of other high risk activities such as driving a car for example. Lindane in continental-style chocolates A rather unexpected residue problem arose in 1998;7 73% of high-quality continental-style chocolate on sale in the UK was found to contain lindane (chexachlorocyclohexane; c-HCH) an organochlorine (OC) pesticide banned in many countries. There were no ADI exceedences and from the point of view of human health there was little or no concern because most people would only eat small quantities of this expensive commodity on a relatively irregular basis. The lindane originated from the cocoa butter used in the manufacture of the chocolate.Cocoa is grown in parts of the world where pesticide regulation and use is poor and therefore residues are difÆcult to control. This is an example of where the power of the supermarkets could eliminate the problem; press interest9 in the issue led to public 36N J. Environ. Monit. 2000 2 concern which in turn meant that supermarkets were forced to assure their customers that their chocolates were safe. There is no doubt that supermarkets will put considerable pressure on their suppliers to ensure that their source of chocolates does not contain lindane residues. In turn the suppliers will pressurise the manufacturers and the manufacturers will only buy cocoa butter from growers who do not use lindane.This is a useful chain reaction to help minimise pesticide use even in countries where pesticide use is poorly controlled. Lindane in Milk in 1995 Lindane is a hydrophobic organochlorine (OC) which has an afÆnity for lipids and is therefore commonly found in high lipid content foods. For many years UK milk has contained just detectable residues of lindane partly due to its continued use in the UK (particularly in sugar beet growing) and partly because its residues are relatively long-lived in the environment. In 19954 unexpectedly high lindane residues were found in milk sampled in June. Lindane residues in subsequent months' samples continued to rise reaching a peak in September (Fig.1). The milk levels in September were only marginally below the ADI. Residues near to the ADI in a staple dietary commodity (i.e. milk potatoes bread) are worrying. Fortunately October's residues were signiÆcantly reduced and therefore a potential crisis did not come to fruition. In such cases it is important to explain the effect in order to attempt to prevent its re-occurrence. In this case there were several important contributory factors. The year in question 1995 had a hot Fig. 1 Lindane residues in UK milk in 19954 and 1996.5 Graph reproduced by kind permission of MAFF Publications London. summer and it is possible that milking cows were marginally malnourished and so in order to maintain their milk output it is likely that they mobilised fat reserves.It is well known that animal fat reserves contain long lived lipid-soluble residues (e.g. lindane DDT) therefore lindane from fat reserves might have been mobilised and incorporated into milk. In addition since the summer's drought had resulted in a poor cereal grain and forage crop that these commodities were imported. It is possible that such imports contained lindane and were incorporated into compound feed which was fed to dairy herds. These explanations could not be proved or even investigated. However in 19965 (Fig. 1) a slight increase in milk lindane levels occurred at approximately the same time as the previous years enormous increase. This was possibly due to farmers feeding their cattle left over compound feed from the previous year.Surprisingly the 1998 survey7 showed for the Ærst time that no milk samples contained detectable lindane residues. Vinclozolin in lettuce–an ongoing problem Vinclozolin is a fungicide used in lettuce growing. Its approval for use in the UK was revoked because of its potential toxicity to workers applying it to lettuces in greenhouses. It is an androgenreceptor blocker and therefore might interfere with sexual development in boys and have effects on sperm production and secondary sex characteristics in men. Despite this toxicity it is still approved for use in several European countries including France. Warmer countries probably do not grow their lettuces in greenhouses and therefore the exposure risk to workers applying the vinclozolin in the open air is lower than within the conÆned space of a greenhouse; this may explain why vinclozolin is approved in some EU member states.Despite its ban in the UK residues of vinclozolin have been detected in UKgrown winter lettuce for at least 6 years (Table 2). These residues present a negligible risk to the consumer because their concentration is far too low to result in an anti-androgen effect. Nevertheless residues indicate that the pesticide has been used illegally by UK growers and therefore action must be taken. Much to the chagrin of the lettuce growers lettuce imported from countries where vinclozolin is approved for use is legal in the UK providing its residues do not exceed the MRL.This clearly illustrates that the MRL is a trading standard rather than a safety factor. At no time have vinclozolin residues exceeded the ADI and presented a risk to the consumer. The only injured party in this incident is MAFF (Ministry of Agriculture Fisheries and Foods) whom some UKgrowers seemreluctant to obey. Human exposure monitoring It is difÆcult to assess human exposure to pesticides. Several studies have measured pesticide residues in human fat5 or milk,6,10 both matrices are good indicators of long-term exposure but tell little of the subject's exposure to shortlived pesticides such as the organophosphates (Ops) or pyrethroids. In a MAFF study5 of pesticides in human fat in the UK 99% of samples analysed (n~203) had detectable residues of DDT (as p,p'-DDT o,p- DDT p,p'-TDE and/or p,p'-DDE).Since the fat samples were taken at routine autopsy it is likely that most of the subjects were at least 70 years old and therefore had lived through times when DDT was permitted in the UK. Their residues reØect their lifetime exposure. Twenty-three percent of the subjects had DDT fat residues between 1 and 9.3 mg kg21 which suggests higher exposures. These people might have been exposed directly during DDT's hey day or might have been fond of oily Æsh Table 2 Residues of vinclozolin in UK winter lettuce Samples with vinclozolin residues (%) Year 19975 19986 3.2 (n~94) 5.7 (n~70) which contains higher residues of OCs than most other foods.In the same MAFF study5 other long half-life OCs were also found in human fat (Table 3). Again these residues are indicative of the subjects' lifetime exposures to these pesticides rather than indicating recent exposure. It is interesting that the OC with the shortest environmental half-life namely lindane has the lowest human fat residue frequency. Pesticides in human milk Levels of pesticide residues in breast milk of women fromdifferent countries give an indication of exposure to pesticides in their respective countries. For example in the USA p,p'-DDT was found at 0.039 mg kg21 in breast milk,11 whereas for milk from women in Faridok India a residue level of 13.81 mg kg21 was reported.12 This perhaps illustrates the difference in DDT use policies between the two countries.This point is illustrated very well indeed if women fromthe former East Germany are compared with women from West Germany. Milk p,p'-DDT residues in the former have been reported13 at 2.28 mg kg21,whereas in the latter a value of 0.81 mg kg21 is reported.13 In this example even though the women originated from bordering countries their countries' national policies on DDT use is likely to account for the vast difference in pesticide residues found in their milk. Very recent studies10 in Indonesia have shown breast milk DDT residues as high as 17.7 mg kg21 even though the country insist that DDT is no longer used.During the author's last trip to Indonesia some time was spent talking to farmers in the Puncak region 50 miles outside Jakarta. From four farmers with whom DDT was discussed three indicated that they regularly used DDT on their crops. Clearly government policy has not yet Æltered through to the farmers. Table 3 Frequency of OC residues in human fat (n~203) in a MAFF study5 Samples with detectable residues (%) Pesticide Chlordane 53 DDT 99 Dieldrin 59 b-HCH 98.5 Lindane (c-HCH) 3 Heptachlor 30 Hexachlorobenzene 94 Pesticides Should we ban pesticides? The consumers perception of the risk of pesticides residues in food is far greater than the actual risk. Indeed it is likely that natural toxins in food present a far greater risk.Driving to the shop in a car to buy food represents a far greater risk by orders of magnitude than the toxic effects of pesticides in food. Therefore it is folly for the lobby groups to use residues in food as part of their argument to reduce the use of pesticides. They would be much wiser to concentrate their campaigning efforts on the effects of pesticides on the environment. The environmental impact of pesticides is a far sharper nail for the pesticides cofÆn than residues in food. References 1 M. Sharpe J. Environ. Monit. 1999 1 33N. 2 I. C. Shaw in Pesticide Chemistry and Bioscience–the Food Environment Challenge ed. G. T. Brooks and T. R. Roberts The Royal Society of Chemistry Cambridge 1999. 3 MAFF Annual Report of the Working Party on Pesticide Residues 1994.MAFF Publications London 1995. 4 MAFF Annual Report of the Working Party on Pesticide Residues 1995.MAFF Publications London 1996. 5 MAFF Annual Report of the Working Party on Pesticide Residues 1996.MAFF Publications London 1997. 6 MAFF Annual Report of the Working Party on Pesticide Residues 1997.MAFF Publications London 1998. 7 MAFF Annual Report of the Working Party on Pesticide Residues 1998.MAFF Publications London 1999. 8 Organic food–the way to go? Health Which? 2000 February 8±11. 9 J. Blythman Toxic shock. The Guardian 1999 16 September 14±15. 10 I. C. Shaw E. Burke F. Suharyanto and G. Sihombing Environ. Sci. Pollut. Res. in the press. 11 D. R. Mattison T. Wohlleb Y. To S. Lamb M. A. Faitak R. C. Walls and S. G. Selevan Ark. Med. Soc 1992 88 553. 12 R. L. Kalra Environ. Pollut. 1994 85 179. 13 New Scientist 1991 130 19 14 I. C. Shaw and J. Murad Jakarta Post 1998 10 March. Ian Shaw{ Centre for Toxicology University of Central Lancashire Preston UK PR1 2HE {Present address Environmental Science and Research Institute Christchurch Science Centre Christchurch New Zealand. 37N J. Environ. Monit. 2000 2