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4 Animal Production Systems DIRECT AND INDIRECT DLC PATHWAYS INTO FOOD PRODUCTS As discussed in Chapter 3, dioxin and dioxin-like compounds (referred to collectively as DLCs) may enter the animal feed to human food chain through both direct and indirect pathways. The direct environmental pathways include: air-to plant/soil, air-to plant/soil-to animal, and water/sediment-to fish (EPA, 2000~. Whether newly produced or from reservoirs, DLCs deposit on vegetation, soils, and in water sediments from the atmosphere or through agricultural pesti- cides, fertilizers, and irrigation, and are retained on plant surfaces and in the surrounding soil and sediment in waterways. It is estimated that 5 percent of aerial deposits of DLCs in terrestrial environments are retained on plants and the remaining 95 percent ultimately reaches the soil (Fries and Paustenbach, 1990~. The soil-borne DLCs then become a reservoir source that could reach plants used for animal feeds by volatilization and redeposition or as dust. Modeling studies by Trapp and Matthies (1997) indicated that volatilization of polychlorinated dibenzo-p-dioxins (PCDDs) from soil into vegetation is only significant in the case of highly contaminated soils. DLCs from contaminated plant products that are consumed by animals bioaccumulate in the animals' lipid tissues. DLCs can enter aquatic systems via direct discharge into water, by deposi- tion onto soil, and by runoff from watersheds. Aquatic animals accumulate these compounds through direct contact with the water, suspended particles, and bot- tom sediments, and through their consumption of other aquatic organisms. Lim- ited mass balance studies in dairy animals indicate that air and water are negli- gible sources of DLCs (McLachan et al., 1990~. Thus, both terrestrial and aquatic 71

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72 DIOXINS AND DIOXIN-LIKE COMPOUNDS IN THE FOOD SUPPLY food animals may be exposed to DLCs primarily through soil-based ecological pathways. In addition to environmental pathways, animal agriculture practices in the United States may incorporate indirect pathways of DLC exposure that lead to contamination of plant and animal by-products used to formulate animal diets and manufacture animal feeds. These indirect pathways have the potential to produce elevated DLC levels in animals. Exposure to a contaminated commercial agricultural environment, such as through animal contact with pentachlorophe- nol-(PCP) treated wood used in animal housing (a practice now banned), through animal-feed contamination episodes (e.g., DLCs in poultry in the United States [EPA, 2000; FDA, 1997; FSIS, 1997, 20021), andthroughcontaminatedcitrus- pulp products in Belgium (Allsopp et al., 2000), have resulted in isolated groups of animals with high exposure levels (van Larebeke et al., 2001~. When point- source contamination episodes, such as those mentioned above, were identified, they were removed once causation was determined. Figure 4-1 shows the pathways through which DLCs enter into animal feed and human food systems. The figure shows sources and major routes (dark ar- rows) and minor routes (light arrows) by which DLCs can cycle between com- partments and ultimately reach humans. In Figure 4-1, the environmental reservoir represents the major production source and recyclable reservoir for DLCs. As stated in the EPA draft reassess- ment (see Chapter 2), there are a number of sources from which DLCs are derived (chemical processing, incineration processes, and other human activities), and most DLCs are stored in environmental reservoirs such as soils and sediments. DLCs are transported through atmospheric routes to animal forage, feed, and grasses used for feed; to vegetables, fruits and cereals consumed by humans; and to terrestrial and aquatic animals consumed by humans. The route of exposure through vegetables, fruits, and cereals consumed by humans is generally consid- ered a minor pathway, but, surface contamination by soils may increase expo- sure. Atmospheric contamination may also occur in plant products intended for animal rather than for human consumption, and may be eaten directly by a terres- trial food animal or used in animal feed, and thus may become a major source of DLC exposure to animals. The pathway to aquatic animals also is a major route by which DLCs can enter the human food supply. Aquatic organisms can accumulate elevated DLC levels from recent atmospheric deposition or historical reservoirs of DLCs in sediments or terrestrial drainage areas. These DLCs can enter the aquatic food web and concentrate in commercially important aquatic species, although levels of DLCs vary within this environment. Direct human exposure occurs through eating fish or shellfish that contain elevated levels of DLCs. This pathway repre- sents the exposure scenario that may predominate in subsistence fishers or spe- cific ethnic groups (see Chapter 5~.

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ANIMAL PRODUCTION SYSTEMS / 1 Harvested Cereals, Forage, Grasses, Others ENVIRONMENT Generation Chemical Processing Combustion Worldwide Reservoir Sediments Waterways Soils -it` Vegetables, Fruits, Cereals 1K Terrestrial Animals \ 73 Animal Feed + Fishmeal, Fishoils, Animal Fats and Products HUMAN FOODS Meat, Fish, Dairy, Eggs, Fruits, Vegetables, Cereals Humans Aquatic Animals .~ FIGURE 4-1 Pathways leading to exposure to dioxin and dioxin-like compounds through the food supply. Boxes depict point sources in the pathways. Dark arrows refer to path- ways with a greater relative DLC contribution than the pathways with light arrows. Aquatic animal by-products may be used in animal feeds. The feeds may include cereals, forages, and terrestrial animal by-products. These feeds may then be fed to other terrestrial and aquatic animals, potentially contributing to their DLC load. This loop may provide an important intervention step in interrupting the DLC cycle. Terrestrial and aquatic animals represent the principal pathways

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74 DIOXINS AND DIOXIN-LIKE COMPOUNDS IN THE FOOD SUPPLY for the production of meat, dairy products, eggs, and fish for human consumption and are therefore the primary route for introduction of DLCs to humans. The focus of this chapter is the identification of potential steps in agricultural production where interventions can be put in place to reduce DLC exposure to humans through the food supply. LIVESTOCK PRODUCTION SYSTEMS Livestock, for the purposes of this section, are defined as mammalian and avian species raised for human food production. Livestock production encom- passes a wide range of management systems, from predominantly extensive range and pasture systems for cow-calf and sheep production, to intensive production of poultry, pork, and dairy products. Extensive production will be used here to indicate systems in which animals have direct access to soils, including animals held in unpaved feedlot settings. Conversely, intensive production will be limited to animal production systems in which direct access to soil is eliminated. Livestock are recognized as DLC accumulators based on the amount of exposure they receive through their environment and diet. DLC exposure levels may be influenced by the production system employed and by other local envi- ronmental factors. The primary sources for DLC contamination of livestock can be categorized as environmental exposures, water sources, and feed rations. Cur- rent data suggest that animals raised on pasture grasses and roughage will be more likely to have higher DLC levels than concentrate-fed animals (Fries, 1995a). However, the relative weights of these factors may be influenced by the selected production system. Identification of Points of Exposure The DLC exposure risk to animal production systems can be predicted, to some extent, because environmental sources and chemical characteristics that allow these compounds to persist are known. However, quantitative, and some- times qualitative, data about DLC levels in specific production systems and local environments may be limited. Therefore, estimations of the relative risks for various production scenarios have been used where data are not available. Grain-Based Diets Grains that are traditionally fed to livestock (e.g., corn, wheat, oats, and barley) are not likely to acquire DLC contamination during production. Grains that are produced in pods, in inedible sheaths, or in shells are considered to have minimal opportunities for deposition or aerosol contamination pathways (Travis and Hattemer-Frey, 1991~. These characteristics are common in all the indig- enous grain foodstuffs used in North America. However, grain by-products, bran

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ANIMAL PRODUCTION SYSTEMS 75 or middling, and recycled grains and vegetable by-products may contain residual DLC levels as a result of concentrated surface contamination contributed by local incinerators or by persistent soil contamination from past herbicide application (Roeder et al., 1998~. These products may comprise a substantial portion of the rations fed to individual groups of animals and thus increase exposure risk, whereas they represent minimal risks for larger animal populations. The significance of DLC contamination of grains and forage may be better understood by comparing relative risks. Travis and Hattemer-Frey (1991) pre- dicted a total concentration for 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) (wet weight) of 59 pa/kg in forages compared with 4.1 pa/kg in grains and protected produce. They also demonstrated the relatively higher exposure risk for forages compared with grains as a DLC source, although DLC contamination levels for concentrate-fed animals may vary in response to differing feed ingredients. Grasses and Forage Diets Intake of pasture grasses or roughage is considered to be the most important DLC exposure factor in extensive animal production systems. Grasses and forage represent a recognized pathway for organic contamination by air to leaf vapor transfer, deposition, and root uptake. Plant-root uptake of DLCs from soils has been shown to be minimal for most plants, except for members of the cucumber family (Fries, 1995a). Volatilization is not believed to be a major pathway for DLC contamination because of the relative vapor pressure for these highly chlo- rinated compounds (Shut et al., 1988, as reported in Roeder et al., 1998~. These relationships have been demonstrated by the observation that the levels of PCDD and polychlorinated dibenzofuran (PCDF) congeners in forage were not related to the concentration of DLCs in the soils in which they were grown (Hulster and Marschner, 1993~. Plant DLC concentrations are a reflection of the environmental contamina- tion levels in the areas where, and at times when, grown. Deposition of TCDD on the outer surface of plants is the primary route of contamination (Travis and Hattemer-Frey, 1991~. Aerial deposition efficacy depends on particle size, leaf area and roughness, and plant biomass and density (Fries, 1995a). Rain may move DLC particles to the soil or to the lower portions of the plants, where animals would be exposed to them during grazing, but they would be excluded from forage that was harvested. Commoner and colleagues (1998) observed that concentrations of DLCs in air and concurrently grown vegetation were linearly proportional. However, on eight farms located in two states they observed that for grazing dairy cows there was a greater than tenfold difference in DLC levels (0.027-0.346 pg toxicity equivalents [TEQ]/g) in the plant-based diets consumed by the cows, thus dem- onstrating diversity in the retention of DLC contaminants on the plants (Com- moner et al., 1998~. The density of grasses (spring pastures versus summer and

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76 DIOXINS AND DIOXIN-LIKE COMPOUNDS IN THE FOOD SUPPLY fall) available for grazing or the provision of supplemental feeds may reduce DLC uptake by reducing soil ingestion (Fries, 1995b). Roughages that are har- vested and stored reflect the environmental contaminant levels during their grow- ing periods, although some forage processing techniques, such as hay drying, may reduce DLCs through volatilization (Archer and Crosby, 1969, as reported in Fries, 1995b). Some livestock production systems utilize nearly equivalent amounts of grain and roughage in animal diets, particularly for lactating dairy cattle. In these mixed diets, DLC levels would be intermediate between those of grain- and roughage-based diets. Soil Soil represents a significant reservoir for DLC contamination under grazing conditions and is a source of run-off and sediments that contaminate waterways. The bioavailability of DLCs in this reservoir varies from 20 to 40 percent, de- pending on the source from which they were generated (Fries, 1995a). Ninety- five percent of aerial contamination will eventually reach the soil (Fries and Paustenbach, 1990~; therefore, soil will reflect the environmental load from all sources for the area, both current and historic. It has been estimated that grazing dairy and beef animals may receive at least 20 and 29 percent, respectively, of DLCs per day through soil ingestion (Travis and Hattemer-Frey, 1991), and pasture conditions through the grazing season may significantly influence this uptake (Fries, 1995b). Animals in unpaved feed- lots also consume small amounts of soil that may lead to detectable residues (Fries et al., 1982, as reported in Fries, 1995a). In addition, soil erosion and sediment production will contaminate surface water sources, which may further enhance total daily DLC exposure levels under range conditions. Water The strongly lipophilic nature of DLCs reduces the potential for contamina- tion of water except through soil contamination. Filtration water systems (mu- nicipal or private) or wells with no surface contamination likely contain minimal DLC levels, whereas sediment particles in other water systems may contain adsorbed DLCs. This is important in the case of aquatic environmental contami- nation because surface water, used by grazing livestock, may represent another DLC exposure route as animals stir up sediments when they enter the waterways to drink. The contribution, however, of surface water to DLC accumulation in livestock is unknown.

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ANIMAL PRODUCTION SYSTEMS Aerosols 77 Aerosol contamination contributes to environmental DLC sources through particle deposition onto plants and soils. Although limited data are available on the effects of inhalation of DLCs in livestock production, balance studies in lactating cows have shown inhalation exposure and water contamination to be negligible sources for DLCs (McLachlan et al., 1990~. Manure Manure contamination is a reflection of the DLC intake of the animal that may add to soil burdens if used in compost. Coprophagous activities, particularly in swine and poultry, may also contribute to DLC recycling. However, there is not enough available data to adequately characterize DLC exposure risks from manure, particularly as related to animal recycling effects. Point-Source Contaminants Animal housing and handling facilities may be a source for DLC contamina- tion because of the materials used in their construction. Prior to the 1980s, woods treated with pentachlorophenol (PCP) were used in feed bunks, fencing, and other structural components for livestock buildings, particularly for ruminants. Dioxin and furan contamination of the PCP-treated woods resulted in a point- source reservoir. Animals that licked the wood structure or came in contact with exposed feeds developed detectable DLC residue levels in their fat stores. Once identified, the use of these treated woods in animal contact areas stopped, and some remediation of existing facilities was completed. As older facilities have been remodeled, additional sources have been removed. Other products, such as greases, oils, or other organic chemicals that come into contact with animals or animal feeds, may present additional opportunities for point-source contamination. Inadvertent or purposeful contamination of high- fat animal feeds has been reported. For example, inadvertent DLC production was recently discovered in the chelation process of a mineral supplement (Per- sonal communication, H. Carpenter, Minnesota Department of Health, April 2, 2002~. Such occurrences illustrate the spectrum of potential point-source con- tamination events that must be considered in DLC reduction efforts. The contamination levels found in deposits of ball clay used in animal feeds from one region demonstrate that DLCs can appear in a wide range of natural environments (Hayward et al., 1999), which represent another inadvertent point source of contamination. These deposits, the result of natural combustion pro- cesses that occurred centuries ago, remain as a reservoir until uncovered.

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78 DIOXINS AND DIOXIN-LIKE COMPOUNDS IN THE FOOD SUPPLY Management Practices The relative importance of the various pathways of exposure for animals is influenced by the production system under which the animals are raised. As described earlier, animals have direct access to soils during their residence in an extensive production system (which includes unpaved feedlots), and animals are limited to facilities or are under conditions where direct access to soil is elimi- nated in an intensive production system. The percentage of products in each category (beef, lamb, pork, poultry, eggs, and dairy) produced under the two management systems varies, based on economic conditions, resources available, market opportunities, geography, and animal health and management concerns. Ruminants (e.g., cattle and sheep) are the species most likely to be produced in extensive systems. Extensive systems are expected to generate greater DLC ex- posure to food animals than intensive systems, due to direct contact with soil and greater consumption of forage products by the animals, however, there are lim- ited data regarding geographic variations in soil contamination levels with which to quantify the differences. Extensive Production In extensive production systems, environmental media are potential sources of DLC contamination. The levels of DLC contamination in these sources, and in grazing livestock, will reflect the local history of environmental releases. Soils and vegetation may accumulate DLCs on their surfaces, but little migration or absorption into the plants is expected to occur. Sediments in ponds and streams may be DLC sources to the extent that livestock have direct access to these waters and are able to stir and ingest sedi- ment while drinking. Forage and grasses harvested and supplied as supplemental animal feeds may also contribute to DLC contamination levels; however, since soil ingestion is reduced, so is the total daily DLC exposure. Thus, poultry, swine, and other animals that ingest soil during food foraging activities will have higher DLC exposure potentials than those not exposed to soil. Intensive Production Intensive operations remove an animal's access to soils and ground water sources and thus limit their opportunities for DLC exposure. Thus, both aerosol exposure and surface water contact are minimized by the facilities in which the animals are raised. In most intensive animal production operations, feeds are provided in processed forms, and, for monogastric animals, are primarily grain- based in composition. Because of these factors, environmental DLC contamina- tion is less likely to occur in intensive than in extensive operations. As analytical methods improve and costs are reduced, air and water quality sampling will

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ANIMAL PRODUCTION SYSTEMS 79 permit more precise comparisons of exposure between intensive and extensive operations. If the rations fed to animals do not include forages or grasses, expo- sure is further reduced. However, a shift in animal production practices from extensive to intensive to reduce exposure may have economic, sustainability, and animal welfare consequences that are beyond the scope of this report. ANIMAL HUSBANDRY PRACTICES As discussed in the previous section, foods of animal origin in commercial channels may be derived under either extensive or intensive production systems. In many cases, the production system will not be readily identifiable at the meat counter, although specialized or niche products may offer this information to differentiate themselves from other suppliers. When this is not the case, a general knowledge of the dominant production types for these products may provide guidance as to the likely production system, which will in turn enable a better evaluation of the relative risks of DLC contamination from various animal food sources. The paucity of analytical data to characterize DLC contamination within food animal species, however, makes the assessment of risks difficult, but based on general production systems risks, it can be expected that a range of DLC exposures exists within each class of meats, milk, fish, and eggs. Ruminants Beef and Lamb Production Grazing livestock and those fed contaminated forages can be expected to reflect the environmental burdens for these localized areas of access. This obser- vation has a direct impact on beef production at the cow-calf and stocker-calf stages where the primary source of nutrients is forage. Similar concerns can be raised with range-lamb production. Since DLCs are not readily taken up by plants and deposited onto grains and other edible plant parts, it is possible for beef and lamb feeder animals placed on predominately grain diets in an extensive feedlot system to reduce DLC intake levels after pasture exposures (Lorber et al., 1994~. Removal of known point-source contaminants, reduced atmospheric DLC pro- duction, and the subsequent reduced soil contamination levels will, in turn, re- duce expected DLC levels in extensively managed animals. However, because animal-based fats and protein ingredients may be added to the diets of animals in intensive production systems, DLCs can accumulate in the animals' tissues, al- though DLC levels are likely to be much lower than those found in animals on pasture-based diets. The second major source for contamination for beef and lamb is feeds and feedstuffs. As discussed previously, forages are the major source of DLC expo- sures for ruminant species. Nearly 35 percent of U.S. land area (788 million

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80 DIOXINS AND DIOXIN-LIKE COMPOUNDS IN THE FOOD SUPPLY acres) is devoted to grazed forest land, grassland pasture and range, or cropland pasture (Vesterby and Krupa, 2001~. Because of the great expanses of land in the western United States, grazing is the predominant agricultural land use in this area (Figure 4-2~. Intensive forage production can be found throughout the midwestern and eastern regions and primarily on irrigated lands in some western areas of the United States. More concentrated grazing and forage production practices are found in southern, midwestern, and eastern regions. Cow-calf, sheep, and lambs are predominantly raised under extensive condi- tions in all regions (Figures 4-3, 4-4, and 4-5~. Large feedlots for finishing cattle and sheep are found predominately in the plains states of Texas, Oklahoma, Nebraska, and Colorado (Figure 4-6~. These feedlots are extensive but concen- trated operations. Forage supplies are generally of local origin, but grains may be imported into the area. Smaller feedlots are found predominately in the states east of the Missouri River and in California. A few intensive (total confinement) finishing lots can be found in the midwestern and eastern regions, but they repre- sent a minimal percentage of total beef and lamb production. These smaller feedlot operations, irrespective of production system, use locally produced feed- stuffs. g~:~ ~ . .~ (. {I-.? ^N Otis; it: ~ f '+77 ~ l ~ ' _- ~ ~ ~ . A ~ ~ . {, 1 2 ~ 3 ~ '~ .) - ... . ,, ,~ ?x' . ~ ~ ~ ~ C At.' ~~ j - .; . ~ < ~t Is ~ L'~''^^.''~ a'- ~) I- ~ ~ as, ~ _ ~ , , .,.4 ~ , , it, ~ ~ , ; , i, <, ~ , ~ ~ ~~ ~ A - ~ -t ~ ~ 1 < C , ,~~ ·~., ~ , ~,~ ~ V ~ · ~ ~~m A ~ . ~ ~ . . ~ . A ~ ., ~ _ , . , . , · ~ · ~ . L. , ~ \~ ~ _ · ~ . . . ' {'. S ~ 2 ' he ~ ~ . ~ · 3 \ ~ , 4,~, i ~ t ~ ·, ~ ~.2S,,.i, . ,,. ~ 5w~ ~ ~ ~ ~ twit .—Hi ~~ ''an '_' ~ ? " it [~ ?- ~~ lip ~ 4 Y A:- : —~~ ~ ~ ' -~ 2 ~ ~ i {~ 22 ~2 l~ ~ ~, g > ~ D t ~ ~ , 5 ~ A I, — , . 5 2 ~ ~ ~ ~ . ~ _ ~ _ ~ jam t ~ . 3 ~ . . .~ ~ . in. .~ ..~ (~ ~ I3. ' ~ ~ 5~ . . ~—~ ~ ~ —~~ <¢L~ ~5~ ~ ~~} Van ~ ~ ~ . A ~ ~5~ ·2 ,· 'it .-'i'5.>2 -'-I ~ - ~ >.z~ 5 ~~ I. . ~—A,; . Z 'S . — ~ · ~ · j · ~ · · — ~ h ~ it? ~ 2 . ~ L _ ~ ~ ~~ j3~2~ S ~ 4 ~ ·~ ~ ~ ~ _t ~ 5P~i?3~Www i004000 ~,~zp~- ~ ~ i ~ Z ~ ~ ~ ~ ~ ,~ ~ .( ~ ~~ < = C ~ ~ ~ A- ~ r ~ ~ ~ are. ~ . s ~ "I,W2~ ~ Z ~ ' ~ ~ ' J ~ V ~ ~ ~ ~[ off ~ ~ 2~ x<~ ,~ ~ f ~ ei, ~ ~ i~j~ ~5~ , ~ , ~ ~<3 ~ 1~ ~ ~ S. 1~ ilk 5 ·-~ 5P ~ ~ · · —~~ SS Hi_ ~~. |~A ~ ~ ~ ~ ~ · ~ ', me. ' .; ' P ~ ~ A ~ ~ ~ ~ ~ \~ '' 2/ ~ ~~d 1 ~\ ~ ~ Z' ill 7],y,~p ~—\5 ~~ LIZ 1~*~ ~ ~5lt~ FIGURE 4-2 Geographic distribution of pastureland in the United States, 1997. SOURCE: NASS (19991.

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---a ~ ~ > ~7 FICORE 4-3 Ceogr~bic ~s~ibuUon of beef cows in me United Stags, 1997. SOWS: BASS (1999, am. United ages gal ~,~4 FICORE 4-4 Ceogr~Nc ~s~ibuUon of came ad caves in me United Stags, 1997. SOME: BASS (19997

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ANIMAL PRODUCTION SYSTEMS TABLE 4-6 Example of a Least-Cost, Starter-Phase Feed Formulation for Hogs 99 Ingredient Typical Amount (%) Amount Without Animal Products (%) Corn Wheat byproducts Soybean meal Fish meal Calcium carbonate Dical or mono dical phosphate Salt Animal fat Trace minerals and vitamins pack Corn Total percent Total ingredient costa 51.5 11.0 30.0 1.0 1.0 1.5 0.5 3.0 0.5 51.5 63.0 0.0 33.0 0.0 1.0 2.0 0.5 0.0 0.5 63.0 100 100 $127.00 $126.00 aA hog-starter product without animal fat or other animal products is much lower in protein so the time to complete grow-out will be increased. Certification Programs The U.S. Department of Agriculture (USDA) has some certification pro- grams for various feed ingredients, although none are specific to DLCs. Distribution The distribution mode for feed ingredients and products should be consid- ered as a potential means for distributing DLCs. The distribution conveyances used for animal-feed ingredients require that all containers be cleansed and se- quenced to protect feed ingredients from harmful contaminants, including DLCs. FOOD PROCESSING AND PACKAGING Most food sources have the potential to contain some level of DLC contam~ . nation, depending on the area from which they originated and the agricultural practices under which they were grown or raised. Once these foods sources are destined for the food supply (e.g., harvested, collected, slaughtered, caught), they are prepared for market and then for consumption. For some foods, this requires minimal processing and packaging; for others, significant opportunities for addi- tional DLC contamination exist.

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100 DIOXINS AND DIOXIN-LIKE COMPOUNDS IN THE FOOD SUPPLY Composite and Processed Foods Processed foods, including foods containing significant levels of animal fat, such as sausage, bacon, fondues, and products fried in animal fat (e.g., fried snack foods), contribute to DLC intakes. Processed foods may contain varying levels of DLCs depending on the DLC content of each ingredient in the compos- ite food. Therefore, all mixtures of processed foods containing animal, dairy, or fish fats should be considered as potential sources of DLCs. Water, used in processing and contained in the products themselves, prob- ably does not contribute to the overall DLC load. In a study of the persistence of TCDD metabolites in lake water and sediment (under laboratory conditions), Ward and Matsumura (1978) determined that most of the TCDD spiked into a mixed water-sediment sample is partitioned with the sediment, leaving less than 4 percent of the metabolites in the water itself. Food Processing and Packaging Information on the entry or generation of DLCs in the processing and pack- aging of foods is limited. However, analysis of current practices and procedures may be useful in predicting potential sources of entry of DLCs into the food supply by these routes (Table 4-7~. Processing There are numerous ways that food is processed, some of which may alter the DLC content in foods, and some of which may not. The processes that are not likely to alter the DLC content in foods are: . Processing, mixing, and blending foods (e.g., a blend of cereal grains), and forming and molding foods (e.g., bread, pie crusts, biscuits, confec- tions) at ambient temperatures (although much higher temperatures have been found to decompose DLCs) (Zabik and Zabik, 1999) Other ambient processing techniques such as sorting, cutting, and sepa- rating debris The process of flame peeling used in onion processing may generate DLCs due to the high processing temperature, but they may also be washed away in the process Blanching, pasteurization, heat sterilization, baking, and roasting Freeze processing products sold and maintained as frozen foods (e.g., frozen fruits, vegetables, and meat products) (Larsen and Facchetti, 1989) and chilled and refrigerated storage of fresh and processed foods (freeze- drying or freeze-concentration of certain substances may increase the ratio of DLCs relative to the mass of the resulting processed food)

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ANIMAL PRODUCTION SYSTEMS TABLE 4-7 Effects of Food Processing Methods on Levels of Dioxin and Dioxin-like Compounds (DLCs) 101 Processing Methods Effect on DLC Levels Raw material preparation Cleaning Wet cleaning Dry cleaning Removing contaminants/foreign bodies Sorting Shape and size sorting Color sorting Weight sorting Peeling Flash steam peeling Knife peeling Abrasion peeling Flame peeling Mixing and forming Mixing Solids mixing Liquids mixing Forming Bread molders Pie and biscuit farmers Confectionery molders Separation and concentration of food components Centrifugation Filtration Expression Extraction using solvents Membrane concentration May reduce or remove DLCs No effect on DLCs No effect on DLCs No effect on DLCs No effect on DLCs No effect on DLCs May reduce or remove DLCs (adsorbed to surface) May reduce or remove DLCs (adsorbed to surface) May reduce or remove DLCs (adsorbed to surface) Process used for onions, may generate DLCs, but may also be washed away during process, no fat content in onions to hold DLCs No effect on DLCs No effect on DLCs No effect on DLCs No effect on DLCs No effect on DLCs Could concentrate and reduce existing DLCs in lipid and aqueous phases, respectively (e.g., milk separation, more concentrated in cream, less concentrated in skim milk) May concentrate or reduce existing DLCs May concentrate or reduce existing DLCs May concentrate existing DLCs as in fish-oil production May concentrate existing DLCs or introduce DLCs from solvent residues May concentrate existing DLCs continued

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102 TABLE 4-7 Continued DIOXINS AND DIOXIN-LIKE COMPOUNDS IN THE FOOD SUPPLY Processing Methods Effect on DLC Levels Fermentation and enzyme technology Fermentation Enzyme technology Blanching Theory Effect on foods Pasteurization Theory Heat Sterilization In-container sterilization Ultra high-temperature (UHT)/aseptic processes Evaporation and distillation Evaporation Distillation Baking and roasting Theory Frying Shallow (or contact) frying Deep-fat frying Chilling Fresh foods Processed foods Cook-chill systems Chill storage Freezing Theory Freeze drying and freeze concentration Freeze drying (lyophilization) Freeze concentration Packaging Interactions between packaging and foods Printing Filling and sealing of containers Filling Sealing Labeling No effect on DLCs No effect on DLCs No effect on DLCs No known effect on DLCs No effect on DLCs No effect on DLCs No effect on DLCs May concentrate existing DLCs No effect on DLCs No effect on DLCs No effect on existing DLCs, could be introduced from contaminated oils or fats No effect on existing DLCs, could be introduced from contaminated oils or fats No effect on DLCs No effect on DLCs No effect on DLCs No effect on DLCs No effect on DLCs May concentrate existing DLCs May concentrate existing DLCs May introduce DLCs from packaging May introduce DLCs from inks and pigments No effect on DLCs No effect on DLCs No effect on DLCs

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ANIMAL PRODUCTION SYSTEMS . . . . 103 Frying meats, fruits, or vegetables, unless DLCs are introduced into the food by contaminated fats and oils during frying. Processes that may alter DLC content of foods are: Heat processing of meats, which has been shown to reduce DLC levels through the loss of fats (Petroske et al., 1998; Stachiw et al., 1988~. (However, because high temperatures and other favorable conditions can produce DLCs, research should be undertaken to determine if high-tem- perature processing in baking, extrusion, puffing, and short-time, high- temperature pasteurization has an impact on DLC levels in the finished food product.) Extraction and drying during food processing, specifically, the extraction of fat or moisture. For example, a food that had its moisture content reduced would exhibit an increased DLC content as a percent by weight, even though it would contain the same total DLC content as the original food (e.g., dehydrated peas); expression of oils from food products may concentrate DLCs from the original intact food into the oil intended for consumption (e.g., fish oil production); and certain forms of extraction using solvents may concentrate existing DLCs or may introduce them from solvent residues. Separation of raw milk, during which existing DLCs will be reduced in the skim milk (aqueous phase) and increased in the cream (lipid phase). (Products made from skim milk and standardized low-fat milk will have lower DLC concentrations than those produced with full-fat milk or cream. Products with a higher fat content, such as cheese, in which much of the aqueous content has been removed in the form of whey, would have a relatively higher DLC concentration than the same volume of food with more water and less fat content.) Trimming and cutting fat from meat products, similar to extraction, re- duces the DLC content of the prepared food. Filter processing may involve the use of filtering agents that contain DLCs and therefore could become a source of food contamination. Ex- amples include the frequently cited ball-clay incident in chicken feeds (Hayward et al., 1999) and the identification of 1,2,7,8-tetrachlorodi- benzofuran (TCDF) and 2,3,7,8-TCDD as low-level contaminates intro- duced into coffee filter papers in Japan (Hashimoto et al., 1992~. (Cur- rently, maximum levels of PCDDs and PCDFs in filter paper have been established at 0.00038 to 3.6 pg TEQ/g of paper, with about one-third of the total PCDD and PCDF contamination being eluted from the filter paper during coffee brewing. Hot water elutes low levels of DLCs; there- fore, the existing low level of contamination could be avoided by rinsing the filter prior to use.)

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104 DIOXINS AND DIOXIN-LIKE COMPOUNDS IN THE FOOD SUPPLY Food safety food-processing procedures such as irradiation, ozonation, ultra- violet light, sunlight, and chlorination have not been examined for their impacts on DLC levels. Packaging With the exception of fresh vegetables, virtually all foods sold to the public are packaged. Generally, the packaging material is glass, metal, paperboard, or films. Paperboard may also have a film layer. Films may be made from various density polymers or flexible metals of several layers, which support moisture control, migration of specific molecules, gas barriers, physical support, and pack- age labeling and graphics. There are no reported incidences of glass or metal packaging that alter DLC levels in the products they contain. Furthermore, there is no reason to suspect they would alter DLC levels given their composition and stability. There have been incidences of chemicals migrating from paperboard pack- aging to foods (Cramer et al., 1991; Garattini et al., 1993; LaFleur et al., 1991; Ryan et al., 1992~. Other researchers have attempted to predict this migration (Chung et al., 2002; Franz, 2002; Furst et al., 1989~. The Dow Chemical Com- pany has undertaken the development of analytical methodology capable of de- tecting the presence of 2,3,7,8-TCDD and 2,4,7,8-TCDF in low-density polyeth- ylene matrices at concentrations between the range of 200 and 400 parts per quadrillion (Nestrick et al., l991~. Other analytical methods, currently in use, are discussed in Chapter 2. While attention regarding human exposure to DLCs has concentrated on the ingestion of animal products as the most likely source of human exposure, food processing and packaging might play a minor role DLC contribution. IMPORTED FOODS Food imports to the United States have increased steadily in the last two decades (see Table 4-8~. The average share of imports in U.S. food consumption has risen from 6.8 percent to 8.8 percent. Consumption of imported cereal, fruits, and vegetables has risen from 10 to 12 percent since the early 1980s, and im- ported animals product (including fish and seafood) consumption has risen from 3 to 4 percent (Jerardo, 2002~. More reliable sources, reversed seasonality, im- proved shipping and storage technology, wider ethnic food preferences, and vari- ous economic factors have contributed to these trends. As import shares increase, ensuring the safety of the U.S. food supply be- comes more challenging. The U.S. government regulates and monitors, from farm to table, the production, processing, and transportation of foods produced in the United States. The targeted monitoring and regulation of the overseas produc- tion of foods destined for the United States, while theoretically possible, would

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ANIMAL PRODUCTION SYSTEMS TABLE 4-8 Summary of Import Shares of U.S. Food Consumption (%)a 105 Years Food Groups 1981-1985 1986-1990 1991-1995 1996 1997 1998 1999 2000 Total food consumption 6.8 7.3 7.4 8.1 8.5 8.8 8.8 8.8 Animal productsb 3.2 3.4 3.2 3.2 3.2 4.0 4.2 4.2 Red meat 6.7 8.1 7.3 6.4 7.1 7.7 8.2 8.9 Dairy products 1.9 1.8 1.9 2.0 1.9 2.9 2.9 2.7 Fish and shellfish 50.9 56.0 56.0 58.5 62.1 64.7 68.1 68.3 Animal fat 0.5 0.7 1.4 1.4 2.3 2.3 2.5 2.8 Crops and productsC 9.9 10.6 10.6 11.9 12.5 12.4 12.1 12.3 Fruits, juices and nuts 12.0 16.5 15.5 14.9 16.7 16.9 18.2 18.7 Vegetables 4.8 6.1 5.9 7.8 8.0 9.0 8.9 8.8 Vegetable oils 15.7 19.7 19.3 19.2 20.9 21.0 17.9 20.2 Grain cereals 1.6 3.1 6.7 7.2 7.0 7.4 6.5 6.3 Sweeteners and candy 19.8 9.8 9.1 14.8 14.8 10.4 8.5 8.0 aCalculated from units of weight, weight equivalents, or content. bImport shares of poultry and eggs are included, but negligible. Red meats are estimated from carcass weights. CIncludes coffee, cocoa, and tea for which import shares are 100 percent. Also includes crop content of beer and wine. DATA SOURCE: Jerardo (2002). tax the system beyond its capacity. There is significant variation in DLC environ- mental contamination levels and agricultural, processing, and packaging prac- tices among countries. Some monitoring programs, such as FDA's Total Diet Study, may include some imported foods; however, the country of origin is not currently documented. As a result, current food safety laws require that imported foods meet the same safety standards as domestically produced foods, although it is difficult to specu- late on the relative levels of contaminants in imported foods. Mirroring the differences in their domestic control programs, FDA and USDA's Food Safety and Inspection Service (FSIS) rely on different systems to reach food safety goals. FDA relies primarily on physical inspection and chemi- cal analysis of port-of-entry samples of a small proportion of imported foods, particularly from those countries where food safety systems do not meet U.S. standards. FSIS enforces the Federal Meat Inspection Act, the Poultry Products Inspection Act, and the Egg Products Inspection Act. These laws are applicable to domestic and imported products, which must meet the same standards for safety, wholesomeness, and labeling. Meat, poultry, and egg products may be imported into the United States only from countries that FSIS has evaluated and found to have equivalent science- based systems of food inspection that include mandatory HACCP processing

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106 DIOXINS AND DIOXIN-LIKE COMPOUNDS IN THE FOOD SUPPLY systems. The equivalence evaluation process has two parts: analysis of an appli- cation from a prospective exporting country followed by an on-site audit in the applicant country. Once a country is deemed to be equivalent, it may certify establishments for export to the United States. FSIS verifies the continuing equivalence of exporting countries through annual on-site audits of foreign in- spection systems and daily port-of-entry inspections in the United States. All shipments of imported meat, poultry and egg products are reinspected by FSIS at ports-of-entry. Each shipment is inspected for proper documentation and condition of containers. Additional types of inspection may be made on randomly selected individual lots of product, including product examinations for physical defects or laboratory analyses for chemical residues or microbiological contami- nation. Products that fail FSIS inspection are refused entry to the United States and must be reexported, reconditioned (if approved by FSIS), converted to non- human food use (if approved by FDA), or destroyed under FSIS supervision. Absent a system for monitoring DLCs in imported foods, reduction of expo- sure from this food source will be difficult to achieve. Testing for DLCs, espe- cially in animal products, must rely on the standard domestic surveillance pro- grams. Since there are no current standards for allowable DLC levels in foods, rejection of those sampled foods that are determined to be high in DLCs can only be based on pesticide limits set in or on raw agricultural commodities. Other potential interventions are not applicable to imported foods. SUMMARY As stated in the introduction, DLCs are undesirable contaminants in the environment that serve no beneficial purpose and have a number of adverse biological effects in a wide variety of organisms, including humans. The focus of this chapter has been on identifying and describing DLC entry into agricultural pathways and subsequent exposure of the general U.S. population, as illustrated in Figure 4-1. Individuals or specially identified groups may be exposed to higher or lower DLC levels through alternative pathways, and it is possible that an unintended release or production of DLCs could result in high levels of contami- nation in any one of these pathways. Terrestrial and aquatic animal management practices, animal feed formula- tions, and food processing and packaging present the primary potential interven- tion opportunities. Because of the reuse of animal products through feed manu- facturing and the potential for bioconcentration of DLCs, animal feed practices may be especially important in reducing exposure to DLCs through foods.

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