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PAPER
Dietary exposure models for nitrates and nitrites Jean A. T. Pennington* Models to assess dietary exposure of population groups to nitrates and nitrites should be based on the major sources of these substances in foods. Most models require the use of food consumption information and will, therefore, be flawed by the problems that exist with current dietary intake assessment methods. The Total Diet Study model would probably not provide representative coverage of the nitrites in processed meats. A nitrate/nitrite database model requires the gathering and compiling of published data and data from industry on the nitrate and nitrite content of foods. A nitrate/nitrite core food model requires the identification of the foods most responsible for nitratelnitrite consumption in the US. and routine collection and analyses of these products. The large database model uses the database of a national food consumption survey and assigns nitrate and nitrite values to all the foods (based on available data and imputation). A processed meat production/consumption model focuses only on nitrites The nitrate/nitrite core food model is the added to processed, cured meats. prefetred approach. Published by Elsevier Science Ltd Keywords:
Dietary exposure;
exposure
models; nitrates/nitrites
INTRODUCTION This paper suggests several approaches to estimating dietary exposure to nitrates and nitrites. These approaches are based on the current knowledge of methods for assessing food intake, the accuracy of daily energy (calorie) intake estimates, the Total Diet Study (TDS) exposure model and the profiles of nitrates and nitrites in foods.
DIETARY
INTAKE
ASSESSMENT
Nutrition studies with relatively small numbers of patients or participants, such as clinical trials, intervention studies or research studies, may use resourceintensive methods for assessing food (and food Division of Nutrition Research Coordination, National Institutes of Health, Natcher Building, Room 5AN32A, 4.5 Center Drive, Bethesda, MD 20892-6600, U.S.A. *Corrcsponding author. Tel: 001 301 594 8824; Fax: 001 301 480 3768; e-mail:
[email protected]
component) intakes. These methods include weighted food intakes, duplicate food portions (for analysis) and dietary histories (3-hour interviews, including 24-hour recalls). The methods used in national and other large-scale nutrition surveys to assess dietary exposure to nutrients and other food components include 24-hour recalls, food diaries and food frequency questionnaires. These methods are used in the larger surveys because they are efficient in terms of time and cost and have a low respondent burden. The goal of the dietary methods used in surveys is to generally determine what people usually eat and the quantities that are usually consumed. When the information on food consumption is merged with a food composition database that has values for the food components of interest, investigators can calculate the daily intake of different food components and provide exposure estimates that can be reported by the demographic variables of a population such as age, gender, race, ethnic group, urbanization, geographic region, income or education. The methods for assessing food intakes have been in place for many years. They have served the nutri-
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tion community well and have formed the basis for what is known about dietary patterns in the United States (US). Although the basic methods have not changed over the years, there have been many improvements in how the food consumption information is collected. The major innovation has probably been the use of computer-assisted dietary interviews. These interviews allow for consistency in the level of detail obtained from subjects, and they provide tools for probing to get more detail about the foods and quantities consumed. Computer-assisted dietary interviews tend to be more standardized than oral interviews, as the computer does not weary across the day, as a personal interviewer might, after doing 10 or 20 interviews a day. There have also been innovations in food models and food pictures (some of which are computerized) over the years to help survey participants remember and estimate the serving sizes (portions) of the foods they eat. Simultaneously, there have been continuous improvements in food composition databases as more foods are analyzed for more food components and as analytical techniques and instrumentation improve and become more accurate and reliable. Innovations in computer hardware and software have also added to the improvement of food composition databases.
ACCURACY
OF DIETARY
INTAKES
Each of the methods for assessing food intake has some inherent flaws, with some methods being better than others for specific purposes. The method of choice is the one that is best for the particular purposes of the survey or study and that can be done within the resource limitations of the project. The accuracy and reliability of some methods depend, to some extent, on the talents of those who administer the methods (ie do interviews or provide instructions and follow-up) and on the knowledge, cooperation and understanding of the participants. Some dietary information must be obtained by proxy (ie by parents, care-takers or spouses) for young children, older people or survey participants who are not able to provide the information themselves or who are not available when the information is being collected. Proxy information may not be as accurate as selfreported information. One source of error with the dietary assessment tools for surveys (24-hour recalls, food diaries and quantitative food frequencies) is the participants’ difficulty in estimating the quantities of each food consumed. Food models and pictures are often used to assist the survey participants in estimating serving portions. Other problems are the participants’ memory (especially for 24-hour recalls and food frequencies) and honesty (as when face-to-face with the dietetic interviewer). Perhaps the most difficult problem to overcome is the fact that the methods used to collect the dietary information tend to inter-
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fere with the usual intake patterns. Thus, the methods may be accurate because they reflect what was eaten, but not necessarily reliable because what was eaten is not typical. The opportunity to keep a food diary may be an invitation for a survey participant to eat properly on the days of data collection. Keeping a food diary allows survey participants to put a much stronger focus on their food intake and may cause restrained eating on the day(s) of record keeping. Most survey participants are notified when they will have a 24-hour recall and may eat differently on the day prior to the interview. Although changes that improve dietary patterns among survey participants are encouraged, such changes may not last beyond the survey time period and may distort the usual pattern. Some recent reports (Lichtman et al., 1992; Clark et al., 1994; Johnson et al., 1996) indicate that dietary intake methods may not be accurate for individual assessments of energy (calorie) intake. If the measurement of energy intake is not accurate, then the measurements of intakes of nutrients and other food components is unlikely to be accurate either. The doubly labeled water technique is considered to be both accurate and reliable for the measurement of total daily energy expenditure (Schoeller and Hnilicka, 1996). This technique is considered the gold standard by which to measure or compare energy intakes. Studies by Clark et al., 1994; Johnson et al., 1996; Martin et al., 1996; Sawaya et al., 1996 and Warwick and Baines, 1996 have compared energy intakes using 24-hour recalls and/or food diaries with energy expenditure based on the doubly labeled water method and concluded that there are indeed concerns with estimates of energy intakes, ie the energy intakes and expenditures were not comparable. In these cases, the 24-hour recalls and/or food diaries underestimated energy intake compared with the energy expenditure determined by the doubly labeled water method. Results from Martin et al. (1996) indicated that energy expenditure of female subjects exceeded reported calorie intake by about 20%. Total daily energy intakes reported from US national surveys tend to be low, especially for teenage girls and the elderly. Average energy intakes below those recommended by the National Academy of Sciences (NAS, 1989) have been reported from the 24-hour recalls of the First and Second National Nutrition Examination Surveys Health and (NHANES I and II) and the 24-hour recalls and 2-day diaries of the US Department of Agriculture (USDA) Nationwide Food Consumption Surveys (NFCS) and Continuing Surveys of the Food Intakes of Individuals (CSFII). Recent work by Sawaya et al. (1995) investigated the energy needs of elderly women (using the doubly labeled water technique) and concluded that the NAS recommendations for energy do not underestimate the energy requirements of older women.
Dietary exposure
Although it is suspected that the energy intakes from national nutrition surveys are underestimated, it is not possible to apply a correction factor that might boost the energy intake (and hence other dietary components) to a more realistic level because it is not known if the methods for assessing food intake underestimate all foods equally or underestimate selected foods (eg alcohol, desserts, snacks, butter or salad dressing).
TOTAL
DIET
STUDY
EXPOSURE
MODEL
Because food composition databases for some food components are not complete (ie information for all food components in the 3000-7500 foods in the databases of US national surveys is not available), models to assess dietary intake (or exposure) have been developed. One model is the Food and Drug Administration’s (FDA) Total Diet Study (TDS) which focuses on core foods of the US food supply 1987; Pennington, (Pennington and Gunderson, 1992a,b; Pennington et al., 1996). The core foods, identified from national food consumption surveys, are purchased four times each year and analyzed in FDA laboratories for the food components of interest. The unique features of this model are that it relies on core foods and that these core foods are obtained from grocery stores and restaurants across the US and analyzed in laboratories, rather than using data from a database. This model allows for the development of a database on core foods that, over time, becomes quite sophisticated as more and more values are accrued. The database then provides a solid foundation for estimating variances for the food components in each food. The original TDS in 1961 had one composite diet for a young, adult male. The foods were homogenized as one mixture, and aliquiots were analyzed for the food components of interest. In subsequent years, the TDS foods were analyzed as 11 or 12 weighted, cornposited food groups (eg grain products, leafy vegetables, meats, milk products and fruits). The program was then expanded to include three age-sex groups (young adult males, infants and 2-year-old children). In 1982, the program began analyzing individual core foods to prevent the dilution effect that occurs when foods are mixed together and to develop a database on the composition of individual core foods. (The dilution effect prevents the determination of a component if it occurs at very low levels and/or if it occurs in only one or a few of the foods within a composite.) Also the analysis of weighted food composites allows only one mixture of foods (ie representation of only one age-sex group) to be evaluated, or it requires considerable work to include additional age-sex groups. Analysis of individual foods allows greater coverage of population subgroups, because the daily intakes of foods for different groups can then be simulated and calculated
models for nitrates and nitrites: J. A. T. Pennington
on the computer. The age-sex groups represented in the TDS study were increased from three to eight in 1982 and then to 14 in 1991, to give better coverage of the US population. The TDS seems to work well for pesticide residues, industrial chemicals, radionuclides, heavy metals and nutritional minerals, although there have been no studies to test the accuracy or reliability of the daily intake estimates. Some comparisons of mineral intakes using the long method (database values in 3000-7500 foods) and the short method (analytical values in core foods) have been made, and the results indicated similar intakes by age-sex groups (Pennington and Wilson, 1990; Pennington, 1992a). The TDS model, which is based on the average intake of foods for the age-sex groups and the average composition data of foods, appears to be adequate to obtain general information for monitoring purposes, ic to monitor the nutritional safety and adequacy of the food supply for selected food components. As noted above, however, the national surveys probably underestimate energy consumption. Therefore, exposure estimates from the TDS are probably also underestimated. The TDS model has not been used for special population groups (eg low income or vegetarians), and it does not allow for the evaluation of extreme or unusual diets in a population (ie diets with large amounts of particular foods or food types).
PROFILES IN FOODS
OF NITRATES AND DIETS
AND NITRITES
Based on the available literature (Appendix A), the primary dietary sources of nitrates and nitrites include plants (some vegetables and a few fruits), processed, cured meat, fish and poultry (to which nitrites have been added), and possibly water, especially if there is runoff or contamination by nitrate or nitrite from agricultural sources. Plant foods are the primary sources of nitrate, while processed, cured meats are the primary sources of nitrites. Plants Nitrate (and some nitrite) occurs in some, but not all, plant foods. Some plants, like spinach, accumulate more in their edible tissues than others. Considerable variability is observed in the nitrate and nitrite concentrations of plants depending on species, variety, plant part, state of maturity and environmental conditions, such as drought, harvest temperatures, nutrient deficiencies, insect damage, use of herbicides and/or insecticides and application of nitrogen-based fertilizers to stimulate plant growth (Taylor, 1990a). The nitrogen in fertilizers is oxidized to nitrate and nitrite in the soil and absorbed by the plants. Some plants produce the enzyme nitrate
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reductase, which will convert nitrate to nitrite, but in most plants the majority of the nitrate remains in that form. Some bacteria in plant tissues also carry nitrate reductase and can convert the nitrate in plant tissues to nitrite. There are many published papers that provide evidence for the presence of nitrate in plant foods (Appendix A). A few of the more recent papers (Borawska et al., 1994; Hunt and Turner, 1994; Nabrzyski and Gajewska, 1994; Rostkowski et al., 1994) report that lettuce, spinach, red beets, fennel, cabbage, parsley, carrots, celery, potatoes, cucumbers, radishes and leeks are high (or higher than other vegetables) in nitrate. Nitrite in most vegetables and fruits is very low (0 to < 1 mg/kg). The amount of nitrite in carrot juice stored at room temperature increased from 0.1 to 83 mg/kg, while the nitrate level decreased from 261 to 46 mg/kg (Nabrzyski and Gajewska, 1994). Processed/cured meats, fish, poultry Nitrites are the salts of nitrous acid, and both sodium nitrite (NaNO,) and potassium nitrite (KNO,) may be used as curing agents in meat to develop and stabilize the pink color associated with cured meats, to enhance the cured flavor and to function as an antioxidant (ie retard lipid oxidation). Sodium nitrite, the more commonly used nitrite, is also an antimicrobial agent that inhibits Clustridium botulinum growth and toxin production in cured meats (Igoe, 1989). Meat products that may contain nitrites include bacon, bologna, corned beef, frankfurters, luncheon meats, ham, fermented sausages, shelf-stable canned, cured meats, perishable canned, cured meat (eg ham) and a variety of fish and poultry products. The concentrations used in these products, which have limitations for the upper levels, are specified by governmental regulations (Lewis, 1989; Davidson, 1997). FDA and USDA regulations covering the addition of nitrites to foods are found in the Code of Federal Regulations (CFR) (21CFR 170.60, 172.170 and 172.175 for FDA regulations and 9 CFR 318.7 for USDA regulations). Nitrate, the salt of nitric acid, may also be used in meat curing to develop and stabilize the pink color associated with cured meat; however, it is not effective in producing the curing reaction until it is chemically reduced to nitrite. Nitrate has an effect on flavor and also functions as an antioxidant. It is available as both sodium and potassium nitrate, with the sodium form being more common (Igoe, 1989). Sodium nitrate is an antimicrobial agent that can be used in meat, poultry and some smoked or cooked fish (21CFR 171.170, 172.177, 173.310 and 181.33 and 9 CFR 318.7 and 381.147). In the US, in dry sausages, sodium ascorbate is often used in combination with nitrates and nitrites at concentrations of up to 550 mgfkg. Ascorbates, isoascorbates, or erythorbates accelerate the reduction of
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nitrous acid to nitric oxide, thus enhancing color development, reducing residual nitrite and retarding the formation of N-nitrosamines, a class of potent carcinogens (Ricke and Keeton, 1997). Cassens (1997) notes that the residual nitrite level in cured meat products in the US has declined dramatically (by about 8OYo) since the mid-1970s. This change has resulted from lower use levels of nitrite, increased use of ascorbates, improved process control and altered formulations.
Water Little information is available on nitrate and nitrite levels in drinking water. The reports that are available generally concern problems with water contamination. Drinking water may contain nitrates and/or nitrites from fertilizer runoff in farm communities (NAS, 1972). Considerable water is used during food preparation and cooking. Fruits and vegetables may be rinsed and cooked in water. Some grain products (oatmeal, rice and pasta) and meats (stew meat and chicken) are cooked in water. Water is also used to make stews and soups and is an ingredient in many entrCe and dessert recipes. Coffee and tea are usually made from local water, whilst other beverages (fruit juices and juice drinks) can be made by adding local water to frozen or powdered concentrates. Thus, the amount of nitrate and/or nitrate available from water is dependent on the water source (reservoir, ground, bottled or filtered), the level of nitrate and/or nitrate in the source and the quantity of water consumed. Another variable is the use of water purifying systems in homes that may remove nitrates and nitrates.
NITRITE
INTOXICATION
Both nitrate and nitrite can be hazardous to humans if ingested in large amounts. The reduction of nitrate produces nitrite, which can be acutely toxic to humans. Nitrites may react with primary amines to form the alcohol and nitrogen gas; the reaction with leads to nitrosamines. The secondary amines following identifies circumstances under which nitrite (or nitrate) intoxication has occurred: (1) Some cases of nitrite intoxication have involved salts addition of meat-curing inadvertent containing nitrite to other foods. These outbreaks have not involved bacterial conversion of nitrate to nitrite (Taylor, 1990a). (2) Contamination of ground water with nitrate from fertilizer use has occurred. Ground water is often used as drinking water on farms and in farming communities. (3) Spinach or other nitrate-accumulating plants grown on soil over-fertilized with ammonia or fertilizers can accumulate other nitrogenous hazardous levels of nitrate. This situation can
Dietary exposure
become more serious if nitrate-reducing bacteria proliferate on these foods, so that some of the nitrate is converted to the more hazardous nitrite. Several cases of infant food poisoning have resulted from spinach or other plants containing excessive nitrate and/or nitrite from excessive amounts of nitrogen-based fertilizers (Taylor, 1990b). (4) Improper storage of spinach and carrot juice at temperatures encourages bacterial elevated growth and has contributed to cases of nitrite intoxication involving bacterial formation of of nitrate-containing nitrite. Proper storage plants at refrigerated temperatures will prevent bacterial nitrite formation (Taylor, 1990a). To improve the safety of some foods (eg carrot juice), attempts have been made to reduce the initial nitrate content using lactic acid bacteria (Buckenhuskes, 1997).
(5)
(6)
(7)
(8)
NITRATES
AND NITRITES
IN DIETS
The following is a chronological listing (based on publication date) of some reported estimates of nitrates and/or nitrites in daily diets from 1973 to 1997. (Tahlr I provides a summary.)
(1) The
estimate from Fassett (1973) for the US population suggests about 50 mg nitrate/day from water, 300 mg nitrate/day from food and 20 mg nitrite/day from food. The 1981 NAS Report (NAS, 1981) concluded (2) that 87% of dietary nitrate was from vegetables, whilst 39%~ of dietary nitrite was from cured meat, 34% from baked goods and cereals and 16% from vegetables. Walters (1980) estimated daily intake of nitrite as (3) 12.15 mg/day, which included 0.02 mg in foods, 1.20 mg added to foods, 10 mg from nitrate (converted to nitrite) and 0.33 mg formed endogenously in the stomach. (4) Knight et ul. (1987) estimated a mean intake of 95 mg of nitrate and 1.4 mg nitrite per day in British diets. Vegetables provided over 90% of the nitrate intake and cured meats provided 65% of the nitrite. Drinking water added another Table I
(9)
models for nitrates and nitrites: J. A. T. Pennington
13.5 mg of nitrate to daily intake, giving a daily total of 108.5 mg of nitrate. The authors noted large regional variations in the intake of nitrates and nitrites. Ellen et al. (1990) used the 24-hour duplicate portion technique with 110 adult volunteers in the Netherlands and found an average daily intake of 53 mg of nitrate. Only 16 of the diets contained measurable nitrite, and the highest daily intake was 0.7 mg. Gangolli et al. (1994) published a risk assessment for nitrate and nitrite in European diets. They concluded that vegetables constituted more than 85% of the average daily intake of nitrates. An estimation from Meah et al. (1994) for the United Kingdom (LJK) population is based on the 1985 U.K. Total Diet Study. It suggests nitrate intakes of 54 mg nitrate/day, primarily from vegetables, and 2.4-4.2 mg of nitrite/day. An estimate based on hospital diets in Bialystok, Poland, in June 1995 (Borawska ef al., 1996) suggests an intake of 311 mg nitrates/day (85% from vegetables) and 2.16 mg nitrites/day from meat and meat-containing products. A Finnish study in 1967-72 (Dich et al., 1996) estimated an intake of 77 mg nitrate/day and Vegetables provided more 5.3 mg nitrite/day. than 90% of the nitrate, while nitrite was mainly provided by cured meat products.
Thus, reported estimates of daily nitrate intake are between 53 and 350 mg/day and reported estimates of nitrite intake are between 0 and 20 mg/day. The primary variables for nitrate intake are the type of vegetables consumed, the levels of nitrate in the vegetables, the amount of vegetables consumed and the level of nitrate in the water supply. The main variables for nitrite intake are the levels of nitrite in cured, processed meat and the amounts of these products consumed.
POTENTIAL DIETARY EXPOSURE MODELS FOR NITRATES/NITRITES A suitable dietary exposure model for nitrate and nitrite requires answers to the following questions:
Dietary exposure to nitrates and nitrites
Nitrate (mgiday)
Nitrite (mgiday)
Reference
Notes
300 so IO 95
20
Fassett, 1973
US estimate
12.15 1.4 (65% from meats)
Walters, 1980 Knight et al., 1987
British diet
13.5 53 54 311 77
(from food) (from water) (from food’ > 90% from vegetables) (from water)
O-O.7 (mainly vegetables) (85% vegetables) ( > 90%~vegetables)
2.4-4.2 2.16 (from meat) 5.3 (mainly cured meats)
Ellen et al., 19YO Meah et al., 1994 Borawska et al,, 1996 Dich et al., 1996
Netherlands, 24.hour duplicate portions from 110 adults UK Total Diet Study Polish hospital diets Finnish diets
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Dietary exposure models for nitrates and nitrites: J. A. T. Pennington
(1) Is
the interest in both nitrate and nitrite, or only one of these compounds? (2) Is the interest in naturally-occurring or added nitrate and nitrite, or both? (3) Is the interest in total intakes, or in the specific food sources of nitrate and nitrite? (4) Should the dietary exposure model be for purposes of nutrition monitoring, or for epidemiological, intervention or case-control studies? (5) Are the desired results average intakes, average intakes with standard deviations, or ranges of intakes and what age, sex and other demographic variables are of interest? (6) Is there interest in vulnerable populations, eg children, the elderly or vegetarians? Five potential dietary exposure models for nitrates and nitrites are briefly outlined below. The first four models assume an interest in total dietary exposure from both natural and added sources of nitrate and nitrite, although they could be modified to focus only on added sources. The fifth model only looks at added sources. Nitrate and nitrite from water sources also need to be considered in the estimation of daily intakes. The best way to do this might be to obtain information on the levels of nitrates and nitrites in local water supplies and multiply by the average quantity of water consumed on a daily basis by each age-sex (or other demographic) group.
Current TDS model Although the TDS model, described above, seems to work well for food components that are naturally present or that are unintentional food additives (eg pesticide residues, radionuclides or heavy metals), the model does not work well to assess dietary exposure to an intentional food additive, unless the additive is present in all brands of a specific commodity. The example of iodine, as one of the TDS minerals, illustrates some problems that occur when the food component of interest exists naturally in foods, and may also be present as an intentional food additive. Iodine exists naturally in plants (extracted from soil and water) and in animal foods; however, the highest levels of iodine are found in milk and products made with milk (because of the iodine in feed supplements and in iodophor cleaning solutions used in dairy farms); in foods containing the food additive erythrosine (FD&C Red No. 3); and in some breads and other baked products containing iodate dough conditioners (some breads and bread products). Erythrosine (which is 47% iodine by weight) may be found in some ready-to-eat breakfast cereals, candies, pastries, marischino cherries and other foods. Other red food colorings do not contain iodine and food labels do not usually specify the specific coloring agent used. The iodine content of some TDS food samples varied, depending upon whether or not the foods contained these uninten-
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tional and/or intentional food additives. Another major variable is the use of iodized salt which contains 400 mcg iodine per teaspoon. (The Recommended Dietary Allowance for iodine for adults is 150 mcg/day.) In addition, a single TDS analytical sample is a composite of three subsamples of a food from three cities in one geographic region. For processed foods, the subsamples may be of the same brand or of mixed brands. This adds to the variability of iodine concentrations in certain foods. The levels of iodine from the additives, especially erythrosine and iodized salt, overshadow the iodine that is present, naturally, in foods. A separate dietary exposure model needed to be developed for iodine that considers the various sources of this mineral. The current TDS model (Pennington, 1992aPennington, 1992b) contains 265 core foods, including 40 vegetables, 26 fruits and 23 meat, fish and poultry items. If nitrates and nitrites were added as analytes to the TDS program, the 265 foods could be analyzed for these food components, and daily intakes could then be calculated for the 14 age-sex groups. The current TDS model probably contains sufficient plant foods to estimate dietary exposure to nitrates. However, only six of the TDS meat items (ham, bacon, frankfurters, bologna, ham luncheon meat and salami) would likely contain nitrites. In the TDS model, these six foods would represent the entire consumption of processed, cured meat by the US population and may not provide accurate exposure estimates for nitrites. Nitrate/nitrite database model This model focuses on the development of a database that would provide information on the average levels of nitrate and nitrite in individual foods. This model requires the gathering and compiling of published data on the levels and variability of nitrate and nitrite in vegetables, fruits and water, and the gathering and compiling of what is published and available from food companies and trade associations about levels of nitrite and nitrate in processed, cured meats and other foods. The database would need to have complete documentation so that the source of each data point would be identified. The database would include information on the number of samples, the sampling design, the date and location of analysis, the analytical methods and the mean and standard deviation, median and range of the reported values. In addition, the foods would need to be clearly described as to species, variety, part of plant, maturity and preparation and cooking methods (for vegetables and fruits) and brand and/or trade name and manufacturer (for processed, cured meats). The foods identified in this database could be merged with food consumption data from the Third National Health and Nutrition Examination Survey (NHANES III) or from the USDA 1994-96 Continuing Survey of the
Dietary exposure
Food Intakes of Individuals (CSFII) to estimate nitrite and nitrate consumption for specified age-sex (and other demographic) groups. The gathering together of the available food composition data on nitrates and nitrites would be very valuable in determining the range and variation of these food components in plant foods and in processed, cured meats. Such a compilation would also provide a basis for determining what the next steps should be to improve the database (ie what foods need to be analyzed or reanalyzed because data are lacking or variable).
Core foods for nitrate/nitrite
model
This model focuses on the identification of core foods for nitrates and nitrites. The NHANES III food composition database of 7000 foods and the 1994-96 CSFII database of 7500 foods could be used to identify the potential sources of nitrate and nitrite, eg vegetables, fruits, cured meats and mixed dishes with cured meats. These foods could then be listed in decreasing order of consumption (grams/day) for the Similar products (eg various surveyed population. types of luncheon meats, hot dogs and bacon) could be grouped and one item from each group could be selected to represent the group. The group consumption could be assigned to the selected item, which would then be designated as a core food. The core foods could be obtained from grocery stores and analyzed for levels of nitrates and nitrites. Daily intakes of the nitrates and nitrites could then be based on consumption data from calculated, NHANES III or 1994-96 CSFII. Population groups with the highest intakes, possibly teenagers, teenage boys, young children, young adult men or vegetarians could be identified. This model would include only core foods that contain nitrites and nitrates. In light of the difficulty of analyzing 7000 to 7500 foods for nitrates and nitrites, this model may be the more efficient, as it would focus on the foods highest in these components and allow for identification of the demographic groups with the highest intakes.
Large database
model
This model would use the food consumption data of the NHANES III or 1994-96 CSFII and thus retain all that is known about the daily intakes of many different foods by age-sex (and other demographic) groups from these surveys. This model requires that values for nitrates and nitrites be assigned to all 7000 or 7500 foods in the survey databases. Values for foods that probably contain nitrates or nitrites, but for which data are not available, would need to be estimated (based on a similar food). Zeros would be imputed for foods not likely to contain nitrates or nitrites. Nitrate and nitrite values for mixed dishes (ie any food containing vegetables, fruits or processed, cured meats) would need to be imputed, based on the
models for nitrates and nitrites: J. A. T. Pennington
ingredients. Once values are assigned to all the foods in the database, the daily intakes of nitrate and nitrite for the population subgroups can be estimated. This model would allow for the identification of the nitrates and nitrites intake ranges and for the identification of the profiles of individuals with high and low percentiles of nitrate and nitrite intakes.
Processed
meat production/consumption
model
This model focuses only on nitrites added to processed, cured meats. The production model would require that information be obtained about the availability of nitrite-containing meats to the US population and the levels of nitrite in these products. From this information, and with additional information on exportation and importation of processed, cured meats, one could estimate the availability of nitrite per capita from this source. Nitrite availability figures will be higher that actual consumption because waste and other uses of processed, cured meats (eg pet food) is not considered. The consumption model requires information on the levels of nitrites in cured meats. These data can then be used with cured meat consumption information from NHANES III or the 1994-96 CSFII, to obtain estimates of nitrite consumption. This model does not provide total nitrite intake. nor does it provide information about nitrates. If data from the NHANES III or 1994-96 CSFII are to be used to estimate nitrite exposure (as all of the above models suggest), it is important to estimate nitrite intakes for the whole population and for eaters on/y. The eaters only would include only those people who reported eating processed, cured meats on the days they were interviewed or kept dietary records. The average nitrite intakes for the eaters ody will be higher than those for the entire population, and there might be considerable difference between the two information from the estimates. For example, 1977-78 USDA NFCS (Table 2) indicates that average intakes of processed, cured meats (g/day) are considerably smaller when calculated as the average for all survey participants, rather than as the average for eaters on/y.
Table 2
Intake of selected, processed, cured meats*
Frankfurters Bologna Salami Ham (may or may not be cured)
5%of participants eating at least once in 3 days
Average intake for eaters on 1 of 3 days (giday)
Average intake for all survey participants (g/day)
18 I6 4 16
76k41 49_+32 MI+_42 90 * 69
13.7 7.8 2.4 14.4
*Data are from the 1977-78 USDA Nationwide tion Survey (Pao et ul., 1982).
Food Consump-
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Dietary exposure
models for nitrates and nitrites: J. A. T. Pennington
SUMMARY There appear to be no current estimates of nitrate or nitrite consumption in U.S. diets. Based on what is known and published about nitrates and nitrites in foods and previous reports about the intakes of these compounds in diets, the following is concluded:
contents in a whole day’s hospital diet during the spring season. Roczniki Akadamii Medycznej Bialystok 41, 202-209 Borawska, M., Omieljaniuk, N., Rostkowski, J., Otlog, T. and Hamid, F. (1994) Value of nitrates and nitrites in selected vegetables and potatoes sold in the marketplace of Bialystok in the years 1991-1992. Rocznik Ranstw Zakl Higiene 45,89-96 vegetables. In: Food Microand Frontiers. Eds. Doyle, M. P., Beuchat,
Buckenhuskes, H. J. (1997) Fermented biology Fundamentals
L. R. and Montville, T. J. ASM Press, Washington DC
(1) Approximately
80-95% of dietary nitrate comes from plant foods, mostly vegetables and a few fruits. Intakes are variable based on individual intakes of vegetables and fruits and on the variable levels of nitrates in these products. Estimated intakes of nitrate range from 53 to 350 mg per day. Only very low levels of nitrite are present in plant foods. (2) There are inherent and environmental variables that determine the nitrate and nitrite content of vegetables and fruits. The major variables seem to be species, maturity, fertilizer application and storage temperature. Because of the variability, average levels for nitrates and nitrites in foods may have wide ranges and large standard deviations. The nitrate and nitrite content of drinking water (3) can be variable, especially if there is a source of contamination such as runoff from fertilizers added to farmlands. (4) Most dietary nitrite comes from nitrite food additives in processed, cured meats (luncheon meats, hot dogs and ham). Some other meat products also contain added nitrite (smoked fish, canned, processed meat and some processed chicken), but these foods are not as commonly consumed. Intake of nitrite is variable, depending primarily on the amount of processed meat products that are consumed. The range of dietary nitrite intake has been reported to be 0 to 20 mg/day. The nitrate and nitrite content of processed, (5) cured meats, fish and poultry (where it is added as a food additive) is predictable and should be within limits set by government regulations. (6) Estimates of dietary nitrite intake by eaters only is probably more useful for estimating dietary exposure than average intakes for the whole population. (7) The best model for estimating dietary exposure to nitrates and nitrites may be the core food approach, where the core foods are selected on the basis of their nitrates and nitrites content. (8) Dietary exposure models based on national food consumption surveys should consider the potential for underestimation of total food intake (and hence the potential for underestimation of various food components).
REFERENCES Borawska, M., Markiewica, R., Omieljaniuk, N., Witkowska, A., Jurkian, A. and Krzesiewicz, J. (1996) The nitrate and nitrite
392
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Cassens, R. G. (1997) Residual nitrite in cured meat. Food Technology 51,53-55
Clark, D., Tomas, F., Withers, R. T., Chandler, C., Brinkman, M., Phillips, J., Berry, M., Ballard, F. J. and Nestel, P. (1994) Energy metabolism in free-living, ‘large-eating’ and ‘smalleating’ women: studies using 2H,( 18)O. British Journal of Nutrition 72, 21-31
Davidson, P. M. (1997) Chemical preservatives and natural antimicrobial compounds. In: Food Microbiology Fundamentals and Frontiers. Eds. Doyle, M. P., Beuchat, L. R. and Montville, T. J. ASM Press, Washington DC Dich, J., Jarvinen, R., Knekt, P. and Lenttile, P. L. (1996) Dietary intakes of nitrate, nitrite and NDMA in the Finnish Mobile Clinic Health Examination Survey. Food Additives and Contaminants 13,541-552
Ellen, G., Egmond, E., Van Loon, J. W., Sahertian, E. T. and Tolsma, K. (1990) Dietary intakes of some essential and nonessential trace elements, nitrate, nitrite and N-nitrosamine by Dutch adults: Estimated via a 24-hour duplicate portion study. Food Additives and Contaminants 7, 207-221
Fassett, D. W. (1973) Nitrates and Nitrites. In: T&cants Occurring Naturally in Foods, 2nd edn. National Academy of Sciences, Washington DC Gangolh, S. D., van den Brandt, P. A., Feron, V. J., Janzowsky, C., Koemal, J. H., Spellers, G. J. A., Spiegelhalder, B., Walker, R. and Wishnok, J. S. (1994) Nitrate, nitrite and N-nitrosocompounds. European Journal of Pharmacology 292, 1-38
Hunt, J. and Turner, M. K. (1994) A survey of nitrite concentrations in retail fresh vegetables. Food Additives and Contaminants l&327-332
Johnson, R. K., Driscoll, P. and Goran, M. I. (1996) Comparison of multiple-pass 24-hour recall estimates of energy intake with total energy expenditure determined by the doubly labeled water method in young children. Journal of the American Dietetic Association 96, 1140-1144 Igoe, R. S. (1989) Dictionary of Food Ingredients. Van Nostrand Reinhold, NY, p. 94 Knight, K. M., Forman, D., Al-Dabaagh, S. A. and Doll, R. (1987) Estimation of dietary intake of nitrate and nitrite in Great Britain. Food Chemistry and Toxicology 5, 277 Lewis, Sr, R. J. (1989) Food Additives Handbook. Reinhold, NY, pp. 314-315, 397
Van Nostrand
Lichtman, S. W., Pisarska, K., Berman, E. R., Pestone, M., Dowline. H.. Offenbacher. E.. Weisel. H.. Heshka, S., Matthe%, D: E. and Heymsfielb, S. B. ‘(1992) Discrepancy between self-reported and actual caloric intake and exercise in obese subjects. New England Journal of Medicine 327, 1893-1898
Martin, L. J., Su, W., Jones, P. J., Lockwood, G. A., Tritchler, D. L. and Boyd, N. F. (1996) Comparison of energy intakes determined by food records and doubly labeled water in women participating in a dietary-intervention trial. American Journal of Clinical Nutrition 63, 483-490
Meah, M. N., Harrison, N. and Davies, A. (1994) Nitrate and nitrite in foods and the diet. Food Additives and Contaminants 11,519-532
Nabrzyski, M. and Gajewska, R. (1994) The content of nitrates and nitrites in fruits, vegetables and other foodstuffs. Rocznik Ranstw Zakl Higiene 45,167-180
Dietary exposure
NAS (National Academy of Sciences) (1972) Committee on Nitrate Accumulation, Agricultural Board, Division of Biology and Agriculture, National Research Council. Accumulation of Nitrate. National Academy Press, Washington DC
models for nitrates and nitrites: J. A. T. Pennington
samples of soil. Journal of the Science of Food and Agriculture 20,321-325 Angelotti, R. (1978) Nitrates, nitrites and ascorbate bate) in bacon. Federal Register 43, 20992
(or isoascor-
NAS (National Academy of Sciences). (1981) The Health Effects of Nitrate, Nitrite, and N-Nitroso Compounds. National Academy Press, Washington DC
Baranova, M.. Mala, P., Pleva, J. and Jackova. A. (1994) Cumulation NO, in foodstuffs and raw materials of animal origin. Archivum Veterinaricum Polonicum 34, 63-6X
NAS (National Academy of Sciences). (1989) Subcommittee on the Tenth Edition of the RDAs. Recommended Dietary Allowances 10th edn. National Academy Press. Washington DC, p 3.3
Barker, A. V.. Peck, N. H. and MacDonald, G. E. (1971) Nitrate accumulation in vegetables. I. Spinach grown in upland soils. Agrononiy Journal 63, 126
Pao, E. M., Fleming, K. H., Guenther P. M. and Mickel, S. J. (1982) Foods Commonly Eaten by Individuals: Amount Per Day and Per Eating Occusion. USDA Home Economics Research Report No. 44. Washington DC
Bednar, C. and Kies, C. (1994) Nitrate and vitamin C from fruits and vegetables: impact of intake variations on nitrate and nitrite excretions of human. Plant Foods and Human Nutrition 45, 7 l-80
Pennington. J. A. T. (1992a) 1990 Revision of the FDA’s Total Diet Study. Journal of Nutrition Education 24, 173-178
Beijaars, P. R., van Dijk, R. and van der Horst, G. M. (1994) Determination of nitrate in vegetables by continuous flow: interlaboratory study. JAOAC International 77. 1522-1529
Pennington, J. A. T. (1992h) Total Diet Studies: The Identification of core foods in the U.S. Food Supply. Food Additives and Contaminanrs 9, 253-264 Pennington, J. A. T., &par, S. C., Parfitt, C. H. and Edwards, C. W. (1996) History of the Total Diet Study (Part II). JAOAC International 79, lh3- I70 Pennington, J. A. T. and Gunderson. E. L. (1987) A history of the Food and Drug Administration’s Total Diet Study, 1961 to 1987. Journal of the Association of Official Analytical Chemists 70, 772-782 Pennington, J. A. T. and Wilson, D. B. (1990) Daily intakes of nine nutritional elements - analyzed v calculated values. Journul qft/wAmerican Dietetic Association 90, 375-38 I Ricke, S. C. and Keeton, J. T. (1997) Fermented meat, poultry and fish products. In: Food Microbiology Fundamentals and Frontiers. Eds. Doyle, M. P., Beuchat. L. R. and Montville, T. J. ASM Press, Washington DC Rostkowski, J.. Borawska, M., Omieljaniuk, N. and Otlog, K. (1994) Content of nitrates and nitrites in early vegetables and potatoes sold in the marketplace of Bialystok in the year 1992. Rocznik Ranstw Zukl Higiene 45, 8 l-87 Sawaya, A. L., Saltzman, E., Fuss, P., Young, V. R. and Roberts, S. B. (1995) Dietary energy requirements of young and older women determined by using the doubly labeled water method. American Journal of Clinical Nutrition 62, 338-344 Sawaya, A. L., Tucker. K., Tsay, R., Willett, W., Saltzman, E., Dallal, G. E. and Roberts, S. B. (1996) Evaluation of four methods for determining energy intake in young and older women: comparison with doubly labeled water measurements of total energy expenditure. American Journal qf Clinical Nutrition 63. 491-499 Schoeller, D. A. and Hnilicka, J. M. (1996) Reliability of the doubly labeled water method for the measurement of total daily energy expenditure in free-living subjects. Journal of Nutrition 126, 3488-3543 Taylor, S. L. (199Oa) Other microbial intoxications. In: Foodborne Diseases, Ed. Cliver, D. 0. Academic Press Inc., NY Taylor, S. L. (1990b) Chemical intoxications. In: Foodborne Diseases, Ed. Cliver, D. 0. Academic Press Inc., NY Walters, C. L. (1980). The exposure of humans to nitrite. Oncoloa 37, 289-296 Warwick, P. M. and Baines, J. (1996) Energy expenditure in freeliving smokers and nonsmokers: comparison between factorial, intake-balance and doubly labeled water measures. American Journal of Clinical Nutrition 63, 15-21
Bianchi, E., Bruschi, R., Draisci, R. and Lucentini, L. (1995) Comparison between ion chromatography and a spectrophotometric method for determination of nitrates in meat products. Zeitschrift fnr Lebenschmittel -Untersuchung und -Forschung 200, 256-260 Bintoro, V. P., Cantin-Esnault, D. and Alary, J. (1996) A survey of nitrate contents in Indonesian milk by enzymic analysis. Food Additive.7 and Contaminants 13, 77-87 Bintoro, V. P., Cantin-Esnault, D. and Alary. J. (1995) Validation of a modified spectrophotometric method for the determination of nitrate in dry milk using 2-set-butylphenol. Analyst 120, 2747-2753 Borawska, M.. Markiewica, R., Omieljaniuk, N., Witkowska, A., Jurkian, A. and Krzesiewicz, J. (1996) The nitrate and nitrite contents in a whole day’s hospital diet during the spring season. Roczniki Akadamii Me&znej Bialystok 41, 202-209 Borawska, M., Omieljaniuk, N., Rostkowski. J.. Otlog, T. and Hamid, F.( 1994) Value of nitrates and nitrites in selected vegetables and potatoes sold in the marketplace of Bialystok in the years 1991-1992. Roczik Ranstw Zakl Higiene 45, 89-96 Brown, J. R. and Smith, G. E. (1967) Nitrate ilccumulation in Kgetable Crops as Influenced by Soil Fertility Practices, Research Bulletin No. 920. University of Missouri, Columbia. MO Burvkin, A. I., Makeeva, I. A., Dikun, P. P., Iamshanov. V. A., Shendrikova, I. A., Kalinina, I. A., Zlobina, N. S., Bezrukikh, V. B.. Sobolev. G. S. and Shevelcv. K. V.(l994) \ , Benz(ajovr\ encs and N-nitrosamines in dry dairy products. Vopro.9 Pitaniya 5, 16-18 ll,
Cassens, R. G. (1997) Residual nitrite in cured meat. Food Technology 51. 53-5s Cassens, R. G. (1995) Use of sodium nitrite in cured meats today. Food Technology 49, 72-80, 115 Chu, J.J., XII, Y. C. and Ye, B. F. (1994) N-nitroso-compounds of pickes in the areas with high incidence of digestive cancers and their mutagenic effects. Chung-Hua Yu Fung I Hsueh Tsa Chih 28. 202-205 Cornee, J., Lairon, D., Veleroa, J., Guyader, M. and Berthezene, P. (1992) An estimate of nitrate nitrite, and N-nitrosodimethylamine concentrations in French food products or food groups. Science des Alimentations 12, I55 Crosby, N.T., Foreman, J. K., Palframan, J. F. and Sawyer, R. (1972) Estimation of steam-volatile N-nitrosamines in foods at the 1 mcgikg level. Nature 238, 342-343 Csiba. A., Szentgyorgyi, M., Juhasz, S. and Lombai, G. (1996) A high-performance liquid chromatographic (HPLC) method for the simultaneous determination of nitrite and formaldehyde from foods. Acta Veterinaria Hungaricu 44, l65- 172
APPENDIX A: REFERENCES FOR LEVELS OF NITRATES AND NITRITES IN FOODS
de Angelis, R. C.. Terra, I. C., Scialfa, J. H. and Klemps, I. (1996) Dietary nitrite and scavenger antioxidants trace elements. International Journal of Food Science and Nutrition 47, 23-26
Adriaanse, A. and Robbers, J. E. (1969) Determination of nitrite and nitrate in some horticultural and meat products and in
Dellisanti, A., Cerutti, G. and Airoldi, L. (1996) Volatile N-nitrosamines in selected Italian cheeses. Bulletin of Environmental Contamination and Toxicology 57. 16-2 1
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Dietary exposure models for nitrates and nitrites: J. A. T. Pennington
Dich, J., Jarvinen, R., Knekt, P. and Lenttila, P. L. (1996) Dietary intakes of nitrate, nitrite and NDMA in the Finnish Mobile Clinic Health Examination Survey. Foods and Additive Contaminants 13,541-552
Dusdieker, L. B., Getchell, J. P., Liarakos, T. M., Hausler, W. J. and Dungy, C. I. (1994) Nitrate in baby foods. Adding to the nitrate mosaic. Archive of Pediattic and Adolescent Medicine 148, 490-494
Heisler, E. G., Siciliano, J., Krulick, S., Porter, W. L. and White, J. W. (1973) Nitrate and nitrite content of market potatoes. Journal of Agriculture and Food Chemistry 21, 970
Hendricks, J. D., Shelton, D. W., Loveland, P. M., Pereira, C. B. and Bailey, G. S. (1995) Carcinogenicity of dietary dimethylnitorsomorpholine, N-methyl-N’-nitro-N-nitrosoguanidine and dibromoethane in rainbow trout. Toxicological Pathology 23, 447-457
Ezeagu, I. E. and Fafunso M. A. (1995) Effect of wilting and processing on the nitrate and nitrite contents of some Nigerian leaf vegetables. Nutrition and Health 10, 269-275
Hotchkiss, J. H. (1981) Review of analytical methods for N-nitrosamines in foods. Journal of the Association of Official
Fazio, T., Damico, J. N., Howard, J. W., White, R. H. and Watts, J. 0. (1971) Gas chromatographic determination and mass spectrometric confirmation of N-nitrosodimethylamine in smoke-processed marine fish. Journal of Analytical Food
Howard, J. W., Fazio, T. and Watts, J. 0. (1970) Extraction and gas chromatographic determination of N-nitrosodimethylamine in smoked fish: Application of smoked, nitrite-treated chub.
Chemistry 19, 250-253
Fazio, T., White, R. H., Dusold, L. R. and Howard, J. W. (1973) Nitrosopyrolidine in cooked bacon. Journal of the Association of Official Analytical Chemists 54, 919
Fazio, T. and Havery, D. C. (1982) Volatile N-nitrosamines in direct flame dried processed foods. In: N-Nitroso Compounds: Occurrence and Biological Efsects, Eds. Bartshc, H., O’Neill, I. K., Castegnaro, M. and Okada, M. International Agency for Research on Cancer, Lyon, France, p. 277
Analytical Chemists 64, 1037-1054
Journal of the Association of Official Analytical Chemists 53, 269
Hunt, J. (1994) A method for measuring nitrite in fresh vegetables. Food Additives and Contaminants 11, 317-325 Hunt, J. and Turner, M. K. (1994) A survey of nitrite concentrations in retail fresh vegetables. Food Additives and Contaminants II, 327-332 Jackson, W. A., Steel, J. S. and Boswell, V. R. (1967) Nitrates in edible vegetables and vegetable products. American Society of Horticultural Science 90, 349
Ferreira, I. M., Lima, J. I., Montenegro, M. C., Perez, 0. R. and Rios, A. (1996) Simultaneous assay of nitrite, nitrate and chloride in meat products by flow injection. Analyst 121, 1393-1396
Kamm, K., McKeown, G. G. and Smith, D. M. (1965) New colorimetric method for the determination of the nitrate and nitrite content of baby foods. Journal of the Association of Official
Feth, J. H. (1966) Nitrogen compounds review. Water Resource Research 2, 41
Keeney, D. R.(1970) Nitrates in plants and waters. Journal of Milk
in natural water - A
Fiddler, W. (197.5) The occurrence and determination of N-nitroso compounds. Toxicological Applications in Pharmacology 31, 352 Fiddler, W. and Pensabene, J. W. (1996) Supercritical fluid extraction of volatile N-nitrosamines in fried bacon and its drippings: method comparison. JAOAC International 79, 895-901
Analytical Chemists 48, 892 and Food Technology 33,425
Keybets, M. J. H., Groot, E. H. and Keller, G. H. M. (1970) Air investigation into the possible presence of nitrosamines in nitrite-bearing spinach. Food and Cosmetic Toxicology 8, 167 Kolari, 0. E. and Aunan, W. J. (1972) Proceedings of the 18”’ Meeting of Meat Research Workers, University of Guelph, p. 422
Fine, D. H. (1982) Nitrosamines in the general environment and food. In: Nitrosamines and Human Cancer, Ed. Magee, P. N. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, p. 199.
Lee, C. Y., Stoewsand, G. S. and Downing, D. L. (1972) NY Food and Life Science Quarterly S(l), 8
Follett, M. J. and Ratcliff, P. W. (1963) Determination of nitrite and nitrate in meat products. Journal of the Science of Food and
Manning, P. B., Coulter, S. T. and Jenness, R. (1968) Determination of nitrate and nitrite in milk and dry milk products. Journal of Dairy Science 51, 1725-1730
Agriculture 14, 138
Fudge, R. and Truman, R. W. (1973) Journal of the Association of Public Analysts 11, 19 Gray, J. I. and Collins, M. E. (1978) Formation of N-nitrosopyrrolidine in fried bacon. Journal of Food Protection 41,36
Grebniak, N. P., Vankhanen, V. D., Vykhovanets, T. A. and Grebniak, L. V. Health survey of nitrate load in preschool institutions. Voprosj Pitaniya 5, 28-30 Harvey, D. C. and Fazio, T. (1982) Estimation of volatile N-nitrosamines in rubber nipples for babies’ bottles. Food Chemistry and Toxicology 20, 939
Harvey, D. C. and Fazio, T. (1985) Human exposure to nitrosamines. Food Technology 39, 80-83 Harvey, D. C. and Fazio, T. (1983) Survey of baby bottle rubber nipples for volatile N-nitrosamines. Journal of the Association of Official Analytical Chemists 66, 150
Harvey, D. C., Fazio, T. and Howard, J. W. (1978) Trends in levels of N-nitrosopyrolidine in fried bacon. Journal of the Association of Oficial Analytical Chemists 61, 1380
Harvey, D. C., Hotchkiss, J. H. and Fazio, T. (1981) Nitrosamines in malt and malt beverages. Journal of Food Science 46, 501 Harvey, D. C, Hotchkiss, J. H. and Fazio, T. (1982) Rapid determination of volatile N-nitrosamines in non-fat dry milk. Journal of Dairy Science 65, 182
Hedler, L. and Marquardt. P. (1968) Occurrence of diethylnitrosamine in some samples of food. Food and Cosmetic Toxicology 6,341-348
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Markowska, A., Kotkowska, A., Furmanek, W., Gackowska, L., Siwek, B., Kacprzak-Strzalkowska, E. and Blonska, W. (1995) Content estimation of nitrates and nitrites in vegetables from the province of Lodz. Rocznik Panstw Zakl Higiene 46,341-348 Markowska, A., Kotkowska, A., Furmanek, W., Gackowska, L., Siwek, B., Kacprzak-Strzalkowska, E. and Blonska, A. (1995) Studies on the contents of nitrates and nitrites in selected fresh and heat processed vegetables. Rocznik Panstw Zakl Higiene 46, 349-355
Maynard, D. N. and Barker, A. V. (1972) Horticultural Science 7, 224
McNamara,
A. S., Klepper,
L. A. and Hageman,
R. H. (1971)
Journal of Agricultural Food Chemistry 19, 540
Meah, M. N., Harrison, N. and Davies, A. (1994) Nitrate and nitrite in foods and the diet. Food Additives and Contaminants l&519-532 Mulhern, F. J. (1975) Nitrates, nitrites and salt. Federal Register 40, 52614
Nabrzyski, M. and Gajewska, R. (1994) The content of nitrates and nitrites in fruits, vegetables and other foodstuffs. Rocznik Panstw Zakl Higiene 45, 167-180
NAS (National Academy of Sciences) (1972) Committee on Nitrate Accumulation, Agricultural Board, Division of Biology and Agriculture, National Research Council. Accumulation of Nitrate. National Academy Press, Washington D.C. Ologhobo, A. D., Adegede, H. I. and Maduagiwu, E. N. (1996) Occurrence of nitrate. nitrite and volatile nitrosamines in
Dietary exposure
certain feedstufffs 11,109-l 14
and animal products. Nuln’tiorz and Health
Peck, N. H., Barker, A. V., MacDonald, G. E. and Shallenberger, R. S. (1971) Nitrate accumulation in vegetables. 11. Table beets grown in upland soils. Aqonoq .l~~~rna/63, 130
models for nitrates and nitrites: J. A. T. Pennington
Sen. N. P., Baddoo, P. A. and Seaman, S. W. (1994) Rapid and sensitive determination of nitrite in foods and biological materials by How injection or high-performance liquid chromatography with chemiluminescence detection. Jmtrnnl q/ Chromntograp~y A 673. 77-84
Pensabene, J. W., Fiddler. W., Maxwell, R. J., Lighttield. A. R. and Hamspon, J. W. (1995) Supercritical fluid extraction of N-nitrosamines in hams processed in elastic rubber nettings. JAOAC Internationrtl 78, 144-748
Siciliano, J.. Krulick, S., Heisler. E. Cr. and White, Jr., J. W. (1975) Nitrate and nitrite content of some fresh and processed market vegetables. Jorrnzul of ilgriculture ctttd Food Chemistg’ 23. 46 I-404
Phillips, W. E. J. (1971) Naturally occurring nitrate and nitrite in foods in relation lo infant methaemoglobinacmia. Food and Cosmetic 7i,xicologv 9, 2 I Y
Simon, C. (IY(lh) Nitrite poisoning from spinach. Luncet 1. 872
Prakash. D.. Nath, P. and Pal. M. (1995) Composition and variation in vitamin C. carotenoids, protein, nitrate and oxalate contents in Cclosia leaves. Plunt Foods and Human Nutrition 47, 22 1-226 Randolph, W. F. (1980) Dimethylnitrosamine in malt beverages; Availability of guide. Federal Register 45, 39341 Richardson, W. D. (1907) Nitrates in vegetable foods, in cured meats and elsewhere. Journul of the American Chemical Sociem 29, 1757 Rostkowski, J., Borawska, M., Omieljaniuk, N. and Otlog, K. (1994) Content of nitrates and nitrites in early vegetables and potatoes sold in the marketplace of Bialystok in the year 1992. Rocznik Punstw Zakl Higienge 45, 8 l-87
Sjoherg, A. M. and Alanko, T. A. (1994) Spectrophotometric determination of nitrate in baby foods: collahorativc study. JA(?AC Internutiotutl 77, 425-430 White, J. W. (197.5) Relative significance of dietary sources of nitrate and nitrite. Journal of Agriculture and Food Chemistty 23, 886-891 (correction in Journal of A,yriculture and Food Chemistry 24, 202, 1976) Wilkens, L. R., Kadir, M. M., Kolonel, L. N., Nomura, A. M. and Hankin. J. H. (1996) Risk factors for lower urinary tract cancer: the role of total fluid consumption, nitrites and nitrosamines, and selected foods. Cancer Epidemiology Biomarkers nnd Prelwtion 5, Ihl-166 Wilson, J. K. (1949) Aponony
.Journa/ 41, 20
Sanz, Y., Vila, R., Toldra, F.. Nieto, P. and Flores, J. (1997) Effect of nitrate and nitrite curing salts on microbial changes and sensory quality of rapid ripened sausages. Internntional Journal of Food Microbiology 37, 225-229
Winton, E. F., Tardiff, R. G. and McCabe, L. J. (lY71) Nitrate in drinking water. Journal of the Americun Water Works Association 63. 95
Scanlan, R. A. (1983) Formation and occurrence of nitrosamines in food. Cancer Re.warch (.%_q$emct~t) 43. 24353-24408
Wright, M. J. and Davison, K. L. (1964) Nitrate accumulation in crops and nitrate poisoning in animals. In: Advances in Agronott~y 16, Ed. Norman A. G. Academic Press, NY, p. 197
Seel, D. J.. Kawabata, T., Nakamura, M., Ishibashi, T., Hamano, M.. Mashimo. M.. Shin. S. H.. Sakamoto. K.. Jhee. E. C. and Watanabe. S. (1994) N-nitroso compounds in two nitrosated food products in southwest Korea. Food Chemistty and Taxicokogy 32. I 117-l I23
Zou, X. N.. Lu. S. H. and Liu, B. (1994) Volatile N-nitrosamines and their precursors in Chinese salted fish - a possible etological factor for NPC in China. International Journul of Cancer 59, 155-158
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