Journal of the Science of Food and Agriculture
`
`J Sci Food Agric 86:10–17 (2006)
`DOI: 10.1002/jsfa.2351
`
`Review
`Nitrate in vegetables: toxicity, content, intake
`and EC regulation
`Pietro Santamaria∗
`
`Dipartimento di Scienze delle Produzioni Vegetali, University of Bari, Via Amendola 165/A, 70126 Bari, Italy
`
`Abstract: Nitrate content is an important quality characteristic of vegetables. Vegetable nitrate content is
`of interest to governments and regulators owing to the possible implications for health and to check that
`controls on the content are effective. Nitrate itself is relatively non-toxic but its metabolites may produce
`a number of health effects. Until recently nitrate was perceived as a purely harmful dietary component
`which causes infantile methaemoglobinaemia, carcinogenesis and possibly even teratogenesis. Recent
`research studies suggest that nitrate is actually a key part of our bodies’ defences against gastroenteritis.
`In this review are reported: (1) vegetable classification as a function of nitrate accumulation; (2) vegetable
`contribution to the total dietary exposure of nitrate; (3) European Commission Regulation No. 563/2002
`which sets limits for nitrate in lettuce and spinach; (4) the maximum levels set in some countries for
`beetroot, cabbage, carrot, celery, endive, Lamb’s lettuce, potato, radish and rocket; (5) the results of
`surveys on the nitrate content of vegetables in Italy and other European countries.
` 2005 Society of Chemical Industry
`
`Keywords: nitrate content; nitrate toxicity; vegetable quality; limits for nitrate
`
`compounds, which form when nitrite binds to other
`substances before or after ingestion (for example, the
`amines derived from proteins), are toxic and can
`lead to severe pathologies in humans.8,9 Thus, the
`assessment of the health risk of nitrate to humans
`should encompass the toxicity of both nitrite and
`N-nitroso compounds.8
`Sources of nitrate, nitrite and N-nitroso compounds
`are normally exogenous,10 but endogenous formation
`of these compounds has also been demonstrated in
`both laboratory animals and humans.2
`The best-known effect of nitrite is its ability to react
`with haemoglobin (oxyHb) to form methaemoglobin
`(metHb) and nitrate:
`− + oxyHb(Fe2+
`
`NO2
`
`) −−−→ metHb(Fe3+
`
`) + NO3
`
`−
`
`INTRODUCTION
`Nitrate is a naturally occurring form of nitrogen
`and is an integral part of
`the nitrogen cycle in
`the environment. Nitrate is formed from fertilizers,
`decaying plants, manure and other organic residues.
`It is found in the air, soil, water and food (particularly
`in vegetables) and is produced naturally within the
`human body.1 – 4 It is also used as a food additive,
`mainly as a preservative and antimicrobial agent.3,4 It
`is used in foods such as cheese and cheese products,
`raw and processed meats, edible casings, processed
`fish, fish products, spirits and liqueurs.
`Due to the increased use of synthetic nitrogen fer-
`tilizers and livestock manure in intensive agriculture,
`vegetables and drinking water may contain higher
`concentrations of nitrate than in the past.
`
`NITRATE TOXICITY
`The presence of nitrate in vegetables, as in water and
`generally in other foods, is a serious threat to man’s
`health. Nitrate per se is relatively non-toxic,3,5 but
`approximately 5% of all ingested nitrate is converted
`in saliva and the gastrointestinal tract to the more toxic
`nitrite.6,7 The only chronic toxic effects of nitrate
`are those resulting from the nitrite formed by its
`reduction by bacterial enzymes.5 Nitrite and N-nitroso
`
`As a consequence of the formation of metHb the
`oxygen delivery to tissue is impaired.11,5
`Once the proportion of metHb reaches 10%
`of normal Hb levels, clinical
`symptoms
`(from
`cyanosis—the blue discoloration of
`the skin due
`to the presence of deoxygenated blood—through
`to asphyxia—suffocation) occur. This potentially
`fatal condition is known as methaemoglobinaemia,
`or blue baby syndrome.1,11 Children and adults
`are far
`less susceptible to methaemoglobinaemia
`
`∗ Correspondence to: Pietro Santamaria, Dipartimento di Scienze delle Produzioni Vegetali, University of Bari, Via Amendola 165/A, 70126
`Bari, Italy
`E-mail: santamap@agr.uniba.it
`(Received 23 July 2004; revised version received 9 February 2005; accepted 29 June 2005)
`Published online 1 November 2005
` 2005 Society of Chemical Industry. J Sci Food Agric 0022–5142/2005/$30.00
`
`10
`
`Human Power of N Company
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`the induction of
`than young infants, because of
`methaemoglobin reductase during the physiological
`post-weaning period. Babies less than three months old
`are particularly susceptible to methaemoglobinaemia.
`This is believed to occur because of infants’ higher
`levels of
`fetal oxyHb still present
`in the blood,
`which oxidizes to metHb more readily than non-
`fetal oxyHb. In addition,
`infants have less of the
`reductase needed to reconvert the metHb back to
`oxyHb, have a proportionately higher intake of nitrate
`through drinking water by body weight, and have a
`higher reduction of nitrate to nitrite due to low gastric
`acidity.5,12
`Two cases of blue baby syndrome were recently
`investigated in Wisconsin (USA). Both cases involved
`infants who became ill after being fed formula that
`was reconstituted with water from private wells. Water
`samples collected from these wells during the infants’
`illnesses contained nitrate N concentrations of 22.9
`−1.11
`and 27.4 mg L
`Nitrite as such, and nitrate when reduced to
`nitrite, may react with amines or amides to form
`carcinogenic N-nitroso compounds.5 Nitrosation can
`occur mainly in two situations: (1) during storage and
`ripening of the food product1 and (2) in the stomach
`from the action of salivary nitrite produced through
`enzymatic reduction of endogenous or exogenous
`nitrate.13 Since the discovery of the carcinogenicity
`of N-nitrosodimethylamine in rats by Magee and
`Barnes,14 N-nitroso compounds have been shown to
`be carcinogenic in more than 40 animal species.2
`These include mammals, birds, reptiles and fish, and
`there is no reason to suspect that human beings are
`uniquely resistant.15
`Several authors have suggested that the risk for the
`development of stomach cancer is positively correlated
`with three factors: (1) the nitrate level of drinking
`water, (2) the urinary excretion of nitrate and (3) the
`occurrence of atrophic gastritis.8 Epidemiological
`studies have not provided any evidence that there is an
`increased risk of cancer related to high nitrate intake
`from sources other than vegetables.2 In some cases
`studies revealed a negative correlation between nitrate
`intake and gastric cancer,2,16,17 because vegetables
`are an excellent source of vitamins, minerals and
`biologically active compounds.18,19
`Some years ago, Vermeer et al.20
`showed the
`endogenous formation of carcinogenic N-nitroso com-
`pounds (N-nitrosodimethylamine and N-nitrosopi-
`peridine) after intake of nitrate at the acceptable daily
`intake (ADI, see below) level in combination with a
`fish meal rich in amines as nitrosatable precursors.
`The vegetables used in the research (cauliflower, peas,
`carrots and green beans) were low in nitrate, and
`their mean vitamin C content (an anti-carcinogenic
`−1 vegetables.
`agent) was approximately 170 mg kg
`Thus, the amount of vitamin C (and other antiox-
`idants) in these vegetables appeared insufficient to
`prevent nitrosamine formation.20 The same Danish
`research group has shown that nitrate can interfere
`
`Nitrate in vegetables
`
`with iodine uptake by the thyroid, resulting in hyper-
`trophy of the thyroid, the gland responsible for many
`of the body’s endocrine and hormonal functions.21
`More recently, another research group has shown
`a positive relationship between the incidence of
`childhood-onset insulin-dependent diabetes mellitus
`and levels of nitrate in drinking water.22 Their findings
`−1 of
`suggest that the threshold for the effect is 15 mg L
`NO3 (less than one-third of the EC limit for nitrate in
`drinking water), which is considered both worrying23
`and puzzling.24
`Recent research suggests that dietary nitrate may
`have beneficial effects, based on the hypothesis that
`nitric oxide (NO) formed in the stomach from dietary
`nitrate has antimicrobial effects on gut pathogens and
`a role in host defence.12,25,26
`The potential beneficial effects of nitrate have been
`the subject of limited research; however, there was
`enough evidence in several areas including prevention
`of microbial
`infections, reduction of hypertension
`and cardiovascular diseases, and reduction in the
`risk of gastric cancer, to lead two researchers to
`publish a paper entitled ‘Are you taking your
`nitrate?’24
`Finally, it is important to cite the text ‘Nitrate
`and man: toxic, harmless or beneficial?’ which, as
`suggested by the title, is a broad-ranging review of the
`role of nitrate in human health.27 The authors critically
`review the evidence relating to the reported adverse
`effects of nitrate and note that a plausible hypothesis
`(the toxicity of nitrate) has been transformed into a
`practically sacrosanct dogma, in spite of the lack of
`proof.27
`However, an intake of vegetables and consumption
`of drinking water with such a high nitrate content that
`the ADI is exceeded for a prolonged period should
`be avoided.28 Thus, in order to gain as much as
`possible from the indisputable benefits of vegetables,
`a reduction in nitrate levels is highly desirable for
`consumers and probably profitable for farmers.29
`
`ACCEPTABLE DAILY INTAKE
`The concept of ADI is defined by the Joint Expert
`Committee of the Food and Agriculture (JECFA)
`Organization of the United Nations/World Health
`Organization (WHO) for substances intentionally
`added to food or
`for contaminants
`(pesticides,
`herbicides and fertilizers).3,4 In view of the well-
`known benefits of vegetables and the lack of data
`on the possible effects of vegetable matrices on the
`bioavailability of nitrate, JECFA considered it to be
`inappropriate to compare exposure to nitrate from
`vegetables with ADI or to derive limits for nitrate
`in vegetables directly from it.3 In the absence of an
`appropriate alternative approach in the literature the
`consequences of nitrate intake exceeding the ADI are
`discussed.
`The JECFA and the European Commission’s
`Scientific Committee on Food (SCF) have set an
`−1 bodyweight.3,4,30 – 32
`ADI for NO3 of 0–3.7 mg kg
`
`J Sci Food Agric 86:10–17 (2006)
`
`11
`
`Page 2 of 8
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`

`

`Table 1. Estimated intakes of NO3 from sources other than food additives at the global level (after Hambridge34)
`Major contributors to total intake (µg mg−1)
`
`Intake
`−1)
`(mg day
`
`40
`28
`20
`55
`155
`
`ADIa
`(µg mg−1)
`200
`100
`100
`250
`700
`
`P Santamaria
`
`Regional diet
`
`Middle Eastern
`Far Eastern
`African
`Latin American
`European
`
`a Based on 60 kg body weight.
`
`The USA Environmental Protection Agency (EPA)
`Reference Dose (RfD) for nitrate is 1.6 mg nitrate
`−1 bodyweight (bw) per day (equivalent to
`nitrogen kg
`−1 bw per day).5
`about 7.0 mg NO3 kg
`The JECFA and SCF have proposed an ADI for
`−1 bw32,
`NO2 of 0–0.078,9 and 0–0.06 mg NO2 kg
`respectively, while the EPA has set an RfD of
`−1 bw per day (equivalent
`0.1 mg nitrite nitrogen kg
`−1 bw per day).5
`to 0.33 mg NO2 kg
`The SCF retains that the ADIs are applicable to all
`sources of dietary exposure.30,31
`
`NITRATE INTAKE
`The three main sources of nitrate intakes are
`vegetables, water and cured meat.1,33
`Vegetables constitute the major dietary source of
`nitrate, generally providing from 300 to 940 mg g−1
`of the daily dietary intake (Tables 1 and 2). Their
`contribution to nitrite intake is low, and in fact lower
`than that from cured meat products.1,10,33 Nitrite
`−1
`is found in plant foodstuffs, typically 1–2 mg kg
`of fresh vegetable weight.46 Potatoes, however, can
`−1.46 Higher amounts of
`contain up to 60 mg NO2 kg
`
`Table 2. Estimate of nitrate daily intake (drinking water not included)
`and contribution of vegetables in various countries
`
`Country
`
`NO3 (mg
`person−1)
`148a
`Belgium
`European Union 18–131b
`Finland
`77
`France
`121
`Germany
`68
`
`Italy
`Poland
`Spain
`Sweden
`
`149
`65–85
`60
`50
`
`The Netherlands
`UK
`USA
`
`52
`95
`73
`
`Vegetable
`contri-
`butionc
`(µg mg−1)
`93
`100
`92
`85
`72
`
`90
`ND
`ND
`ND
`
`ND
`94
`90
`
`a Included only vegetables and fruit.
`b Included only vegetables.
`c Not detected.
`
`12
`
`Reference
`
`Dejonckheere et al.35
`SCF32
`Dich et al.36
`Corn ´ee et al.37
`Selenka and
`Brand-Grimm38
`CSS39
`Borawska et al.40
`ACAPV41
`Jagerstad and
`Nilsson42
`Ellen et al.43
`Knight et al.44
`NRC45
`
`Vegetables
`
`Water
`
`Cereals
`
`650
`450
`300
`650
`900
`
`200
`300
`400
`150
`50
`
`100
`150
`150
`50
`<50
`
`Fruit
`
`50
`100
`100
`100
`50
`
`nitrite are found in contaminated food or in broken
`vegetable tissues in food stored for several days at
`room temperature.33
`Compared with the current ADIs, the ingestion
`of only 100 g of
`raw vegetables with a nitrate
`−1 will already lead to an
`concentration of 2500 mg kg
`intake of 250 mg NO3. Consuming this item alone, for
`a person of 60 kg, would exceed the ADI for nitrate by
`13%. Calculating in the partial conversion of nitrate to
`nitrite (5%) after such consumption, the current SCF
`−1 bw) would be exceeded
`ADI for nitrite (0.06 mg kg
`by 247%.
`A statistical exposure model has shown that in
`the adult population in the Netherlands 15% had
`daily intakes regularly exceeding the ADI;47 in young
`children this may rise to 45%.47
`In its last report, the SCF32 reviewed from a public
`health standpoint the presence of nitrate in foodstuffs
`in general, and vegetables in particular, and stated that
`the total intake of nitrate is normally well below the
`acceptable daily intake (Table 2). The major sources
`are potatoes and lettuce, the first because they are
`vegetables consumed in the largest quantity mainly
`(Table 3), the latter due to its high nitrate content.32
`The SCF31,32 recommended continuation of efforts to
`reduce exposure to nitrate via food and water since
`nitrate can be converted into nitrite and nitrosamines,
`and urged that good agricultural practices are adopted
`to ensure nitrate levels are as low as reasonably
`achievable.
`In previous research, nitrate intake from vegetables
`was estimated using the data on average daily per
`capita consumption of vegetables provided by the
`Italian National Institute of Nutrition49 and on average
`nitrate content from the research work: nitrate daily
`−1; over 300 mg g−1
`intake from vegetables was 71 mg d
`of nitrate intake was derived from the consumption of
`lettuce and Swiss chard.50
`Dietary exposures to nitrate for vegetarians are very
`similar to those of other consumers and are below the
`ADI. The average dietary exposure of the vegetarians
`−1 and the highest nitrate
`in a UK study was 83 mg d
`−1.51,52
`exposure was 209 mg d
`
`NITRATE CONTENT IN VEGETABLES
`There are several
`factors affecting NO3 uptake
`and accumulation in vegetable tissues, e.g. genetic
`
`J Sci Food Agric 86:10–17 (2006)
`
`Page 3 of 8
`
`

`

`Table 3. Food consumption and nitrate daily intake in some countries of European Union (after Schuddeboom48)
`
`Nitrate in vegetables
`
`Food group
`
`Potato
`
`Other vegetables
`
`Fruit
`
`Country
`
`Germany
`Denmark
`The Netherlands
`UK
`Germany
`Denmark
`The Netherlands
`UK
`Germany
`Denmark
`The Netherlands
`UK
`
`Food
`consumption
`(g person−1)
`112
`166
`131
`160
`73
`114
`150
`162
`101
`120
`125
`91
`
`Average
`concentration
`−1 fm)
`(mg kg
`93
`80
`60
`120
`721
`440
`800
`136
`70
`30
`20
`25
`
`−1 fm)
`Table 4. Classification of vegetables according to NO3 content (mg kg
`
`Low
`(200–500)
`
`Broccoli
`Carrot
`Cauliflower
`Cucumber
`Pumpkin
`‘Puntarelle’ chicory
`
`Middle
`(500–1000)
`
`Cabbage
`‘Cima di rapa’ (broccoli rab)
`Dill
`‘Radicchio’
`Savoy cabbage
`Turnip
`
`Very low
`(<200)
`
`Artichoke
`Asparagus
`Broad bean
`Brussels sprouts Eggplant
`Garlic
`Onion
`Green bean
`Melon
`Mushroom
`Pea
`Pepper
`Potato
`Summer squash
`Sweet potato
`Tomato
`Watermelon
`
`NO3 intake
`(mg person−1)
`10.5
`13.3
`7.9
`19.0
`52.6
`50.2
`120.0
`22.0
`7.1
`3.6
`2.5
`2.3
`
`High
`(1000–2500)
`
`Celeriac
`Chinese cabbage
`Endive
`Escarola
`Fennel
`Kohlrabi
`Leaf chicory
`Leek
`Parsley
`
`Contribution
`to nitrate intake
`(µg mg−1)
`113
`185
`66
`339
`564
`697
`857
`393
`76
`50
`18
`41
`
`Very high
`(>2500)
`
`Celery
`Chervil
`Cress
`Lamb’s lettuce
`Lettuce
`Radish
`Red beetroot
`Rocket
`Spinach
`Swiss chard
`
`factors, environmental factors (atmospheric humidity,
`substrate water content,
`temperature,
`irradiance,
`photoperiod) and agricultural factors (nitrogen doses
`and chemical forms, availability of other nutrients, use
`of herbicides, etc.).53 – 55
`Of the factors studied, nitrogen fertilization and light
`intensity have been identified as the major factors that
`influence nitrate content in vegetables.56 In particular,
`light intensity and nitrate content in soil before or at
`harvest are known to be critical factors in determining
`nitrate levels in spinach53 or other leafy vegetables.55,57
`Generally, nitrate-accumulating vegetables belong
`to the families of Brassicaceae (rocket,
`radish,
`mustard), Chenopodiaceae (beetroot, Swiss chard,
`spinach) and Amarantaceae; but also Asteraceae
`(lettuce) and Apiaceae (celery, parsley) include species
`with high nitrate contents (Table 4).
`Nitrate content can vary also within species,
`cultivars and even genotypes with different ploidy.58
`The differing capacities to accumulate nitrate can
`be correlated with differing location of the nitrate
`reductase activity,59 – 61 as well as to differing degree of
`nitrate absorption and transfer in the plant.53,62
`
`Nitrate content differs in the various parts of a
`plant.50 Indeed, the vegetable organs can be listed by
`decreasing nitrate content as follows: petiole > leaf >
`stem > root > inflorescence > tuber > bulb > fruit >
`seed.50,63
`The highest nitrate-accumulating vegetable is
`rocket,50 a leafy vegetable popular in the Mediter-
`ranean region.55,64,65 A number of species of the
`Brassicaceae family are grouped under the name of
`rocket belonging to the Eruca Miller and Diplotaxis
`DC. genera. Eruca is present in both wild and cul-
`tivated forms; Diplotaxis is known as a wild type. In
`Diplotaxis, two surveys carried out in Italy show NO3
`−1.50,66content reaches up to 9300 mg kg
`
`Rocket absorbs NO3 very quickly64,65 and NO3
`concentration in leaves can be much higher than in
`−1 NO3 nitrogen
`the growth medium. With 1 mmol L
`in a hydroponic nutrient solution, NO3 accumulation
`ratio (expressed as the ratio between the concentration
`in leaves and in nutrient solution) was, respectively,
`55 for E. vesicaria and 101 for D. tenuifolia.67
`Soil-less systems offer a clear advantage to tradi-
`tional ones in the management and control of plant
`
`J Sci Food Agric 86:10–17 (2006)
`
`13
`
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`

`

`P Santamaria
`
`mineral uptake during the various phases of the grow-
`ing cycle. One advantage of these growing systems is
`that they can be used to produce vegetables with low
`nitrate accumulation.55,65,68
`
`trend for reduction. So, ‘some Member States need
`to maintain the established transitional period to
`authorise the placing on the home market of lettuce
`and/or spinach grown and intended for consumption
`in their territory’.72 This derogation requires annual
`monitoring to be carried out to demonstrate that
`LIMITS TO MAXIMUM LEVELS OF NITRATE IN
`nitrate levels in these crops are acceptable on public
`health grounds and that growers follow a ‘code of good
`VEGETABLES
`agricultural practice’.72
`To protect public health in response to the SCF’s
`The UK is currently applying this derogation for
`considerations of nitrate in food,30 – 32 in 1997 the
`both lettuce and spinach along with Ireland. A
`European Member States agreed an EC Regulation
`derogation for spinach presently applies in Finland,
`setting limits for nitrate in lettuce and spinach (EC
`Denmark and the Netherlands. However, maximum
`Regulation No. 194/97).69 The main purpose of this
`limits do apply to lettuce and spinach imported from
`EC Regulation was to harmonize limits for nitrate in
`Member States and third countries. The derogation
`these vegetables, as the different national limits set by
`for lettuce ended on 1 January 2005. An extension of
`some Member States were causing trade difficulties
`this derogation is currently under consideration within
`across the European Union.
`the EU. The derogation for spinach is currently being
`On 2 April 2002 the European Commission
`reviewed.72
`amended EC Regulation No. 194/97 (already
`Nevertheless, no official method has been published
`amended with some periphrasis from EC Regulation
`No. 864/199970 and 466/200171) and adopted EC
`in EU legislation and nitrate levels in vegetables are
`Regulation No. 563/2002.72 The maximum levels set
`generally assayed by modifying the protocols used for
`other foods.
`by this Regulation are summarized in Table 5. The
`Limits to maximum levels of nitrate for trade in
`limits vary according to season, with higher nitrate
`other vegetables are set in some European countries
`levels permitted in crops grown in winter compared
`(Table 6). For potato, several countries have put
`with those grown in the summer. Lower limits are fixed
`forward the proposal of ‘guidelines’ for nitrate content
`for open-grown lettuce than for lettuce grown under
`(in Germany, for instance, only tubers with less than
`glass, and in order to allow effective control the limits
`−1 fresh matter (fm) are accepted), while
`200 mg kg
`set for open-grown lettuce should apply also to lettuce
`−1
`in Poland there is a maximum limit of 183 mg kg
`grown under glass in the absence of precise labelling.
`fm.73
`Lower limits are fixed for ‘iceberg’ than other types of
`Rocket and other Italian export vegetable (e.g.
`lettuce.
`potato) sales contracts include very strict clauses,
`The differences between nitrate levels in different
`for instance with Switzerland and Germany. Namely,
`varieties have been most extensively studied in
`nitrate content for rocket is required not to exceed
`relation to lettuce where open leaf varieties generally
`−1 fm, which is a very strict threshold
`2.5–4.0 g kg
`have higher nitrate concentrations than tight-headed
`varieties such as iceberg.32
`that is difficult to respect on account of the high
`accumulation of nitrate in rocket, even when reduced
`EC Regulation No. 563/2002 states that ‘in some
`amounts of nitrate are used in its cultivation.74
`regions nitrate levels are reported to be frequently
`No nitrate standards for vegetables have been
`higher than those set in the Annex of Regulation
`introduced in the USA.
`In China, a suggested
`(EC) No 466/2001, although the general trend shows
`−1
`that the levels of nitrate in lettuce are decreasing’.72
`maximum level of nitrate in vegetables of 3100 mg kg
`has been established.75
`The levels of nitrate in spinach show no clear
`−1 fm) in lettuce and spinach according to European Commission Regulation (EC) No.Table 5. Maximum levels (limits) for the nitrate (mg kg
`
`
`563/200272
`
`Product
`
`Fresh spinacha (Spinacia oleracea L.)
`
`Preserved, deep-frozen or frozen spinach
`Fresh lettuce (Lactuca sativa L.) (protected and
`open-grown lettuce) excluding ‘iceberg’ type
`
`‘Iceberg’ type lettuces
`
`Harvest period
`
`Harvested 1 November to 31 March
`Harvested 1 April to 31 October
`
`Harvested 1 October to 31 March:
`—lettuce grown under cover
`—grown in the open air
`Harvested 1 April to 30 September:
`—lettuce grown under cover
`—lettuce grown in the open air
`Lettuce grown under cover
`Lettuce grown in the open air
`
`NO3
`
`3000
`2500
`2000
`
`4500
`4000
`3500
`2500
`
`2500
`2000
`
`a The maximum levels for fresh spinach do not apply for fresh spinach subject to processing and which is directly transported in bulk from field to
`processing plant.
`
`14
`
`J Sci Food Agric 86:10–17 (2006)
`
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`
`

`

`−1 fm) to trade various vegetables in some European countries (after Santamaria33)
`Table 6. Maximum levels (limits) of NO3 (mg kg
`
`Nitrate in vegetables
`
`Vegetable
`
`Carrot
`Red beetroot
`Endive (summer)
`Indivia (winter)
`Cabbage
`Radish
`Celery (green)
`Celery (white)
`Lamb’s lettuce
`
`Austria
`
`Belgium
`
`Germany
`
`Netherlands
`
`Switzerland
`
`1500
`4500
`2500
`3500
`1500
`
`2000
`2000
`
`5000
`4000
`3500
`
`3000
`
`2500
`
`3500
`2500
`3500
`
`3500
`2500
`2500
`
`3500
`
`the European Commission
`On 7 April 2004,
`established the maximum permitted level for nitrate
`in baby foods and processed cereal-based foods for
`−1 on an ‘as
`infants and young children of 200 mg kg
`sold’ basis.76
`
`CONCLUSIONS
`Although current epidemiological data provide con-
`flicting evidence regarding the potential
`long-term
`health risks of nitrate levels encountered in the diet,
`it is widely accepted that the reduction of dietary
`nitrate is a desirable preventive measure. The max-
`imum allowable nitrate levels in vegetables should
`not exceed levels that reflect good agricultural prac-
`tices.
`A reduction in nitrate content can, however,
`represent added value for vegetable products (already
`rich in carotenoids, vitamins C and E, selenium,
`dietary fibre, plant sterols, glucosinolates and indoles,
`isothiocyanates, flavonoids, phenols, etc.).
`
`REFERENCES
`1 Walker R, Nitrates, nitrites and N-nitrosocompounds: a review
`of the occurrence in food and diet and the toxicological
`implications. Food Addit Contam 7:717–768 (1990).
`2 Gangolli SD, van den Brandt P, Feron V, Janzowsky C, Koe-
`man J, Speijers G, Speigelhalder B, Walker R and Winsh-
`nok J, Assessment of nitrate, nitrite, and N-nitroso com-
`pounds. Eur J Pharmacol Environ Toxicol Pharmacol Sect
`292:1–38 (1994).
`3 Speijers GJA, Nitrate, in Toxicological evaluation of certain food
`additives and contaminants
`in food, ed by World Health
`Organization, Food Additives Series 35, Geneva, pp 325–360
`(1996).
`4 Speijers GJA and van den Brandt PA, Nitrate (and poten-
`tial endogenous formation of N-nitroso compounds). [Online].
`WHO Food Additives Series 50 (2003). Available:
`http://www.inchem.org/documents/jecfa/jecmono/v50je06.
`htm [21 July 2004].
`5 Mensinga TT, Speijers GJA and Meulenbelt J, Health implica-
`tions of exposure to environmental nitrogenous compounds.
`Toxicol Rev 22:41–51 (2003).
`6 Spiegelhalder B, Eisenbrand G and Preussmann R, Influence of
`dietary nitrate on nitrite content of human saliva: possible
`relevance to in vivo formation of N-nitroso compounds. Food
`Cosmet Toxicol 14:545–548 (1976).
`7 Pannala AS, Mani AR, Spencer JPE, Skinner V, Bruckdor-
`fer KR, Moore KP and Rice-Evans CA, The effect of dietary
`nitrate on salivary, plasma, and urinary nitrate metabolism in
`humans. Free Rad Biol Med 34:576–584 (2003).
`
`8 Speijers GJA, Nitrite (and potential endogenous formation of
`N-nitroso compounds), in Toxicological evaluation of certain
`food additives and contaminants in food, ed by World Health
`Organization, Food Additives Series 35, Geneva, pp 269–323
`(1996).
`9 Speijers GJA and van den Brandt PA, Nitrite (and poten-
`tial endogenous formation of N-nitroso compounds). [Online].
`WHO Food Additives Series 50 (2003). Available:
`http://www.inchem.org/documents/jecfa/jecmono/v50je05.
`htm [21 July 2004].
`10 Lijinsky W, N-Nitroso compounds in the diet. Mutat Res
`443:129–138 (1999).
`11 Knobeloch L, Salna B, Hogan A, Postle J and Anderson H, Blue
`babies and nitrate-contaminated well water. Environ Health
`Perspect 108:675–678 (2000).
`12 McKnight GM, Duncan CW, Leifert C and Golden MH,
`Dietary nitrate in man: friend or foe? Br J Nutr 81:349–358
`(1999).
`13 Vittozzi L, Toxicology of nitrates and nitrites. Food Addit Contam
`9:579–585 (1992).
`14 Magee PN and Barnes JM, Some toxic properties of dimethyl-
`nitrosamine. Br J Ind Med 11:167–174 (1954).
`15 Hill MJ, Nitrate toxicity: myth or reality? Br J Nutr 81:343–344
`(1999).
`16 Beresford SA, Is nitrate in drinking water associated with gastric
`cancer in the urban UK? Int J Epidemiol 14:57–63 (1985).
`17 Forman D, Al-Dabbagh A and Doll EC, Nitrate, nitrite and
`gastric cancer in Great Britain. Nature 313:620–625 (1985).
`18 Steinmetz KA and Potter JD, Vegetables, fruit and cancer. I.
`Epidemiology. Cancer Causes Control 2:325–357 (1991).
`19 Chow CK and Hong CB, Dietary vitamin E and selenium and
`toxicity of nitrite and nitrate. Toxicology 180:195–207 (2002).
`20 Vermeer ITM, Pachen DMFA, Dallinga JW, Kleinjans JCS and
`van Maanen JMS, Volatile N-nitrosamine formation after
`intake of nitrate at the ADI level in combination with an
`amine-rich diet. Environ Health Perspect 106:459–463 (1998).
`21 Van Maanen JMS, van Dijk A, Mulder K, de Baets MH,
`Menheere PCA, van der Heide D, Mertens PLJM and
`Kleinjans JCS, Consumption of drinking water with high
`nitrate levels causes hypertrophy of the thyroid. Toxicol Lett
`72:365–374 (1994).
`22 Parslow RC, McKinney PA, Law GR, Staines A, Williams R
`and Bodansky HJ, Incidence of childhood diabetes mellitus
`in Yorkshire, Northern England, is associated with nitrate
`in drinking water: an ecological analysis. Diabetologia
`40:550–556 (1997).
`23 McKinney PA, Paslow R and Bodansky HJ, Nitrate exposure
`and childhood diabetes, in Managing the risks of nitrates to
`humans and the environment, ed by Wilson WS, Ball AS and
`Hinton RH, Royal Society of Chemistry, Cambridge, UK,
`pp 327–339 (1999).
`24 Addiscott T and Benjamin N, 2000. Are you taking your nitrate?
`Food Sci Techn Today 14:59–61 (2000).
`25 Duncan C, Dougall H,
`Johnston P, Greens S, Brogan R,
`Leifert C, Smith L, Golden M and Benjamin N, Chemical
`
`J Sci Food Agric 86:10–17 (2006)
`
`15
`
`Page 6 of 8
`
`

`

`P Santamaria
`
`generation of nitric oxide in the mouth from the enterosali-
`vary circulation of the dietary nitrate. Nature Med 1:546–551
`(1995).
`26 Dykhuizin RS, Frazer R, Duncan C, Smith CC, Golden M,
`Benjamin N and Leifert C, Antimicrobial effect of acidified
`nitrate on gut pathogens: importance of dietary nitrate in host
`defence. Antimicrob Agents Chemother 40:1422–1425 (1996).
`27 L’hirondel J and L’hirondel J-L, Nitrate and man: toxic, harmless
`or beneficial? CABI, Wallingford, UK, p 168 (2002).
`28 Boink A and Speijers GJA, Health effects of nitrates and nitrites,
`a review. Acta Hortic 563:29–36 (2001).
`29 Auerswald H, Peters P, Br ¨uckner B, Krumbein A and Kuchen-
`buch R, Sensory analysis and instrumental measurements of
`short-term stored tomatoes (Lycopersicon esculentum Mill.).
`Postharvest Biol Techn 15:323–334 (1999).
`30 SCF (Scientific Committee on Food), Opinion on nitrate and
`nitrite, expressed on 19 October 1990 (26th series), ed by
`European Commission, Brussels, pp 23–32 (1992).
`31 SCF (Scientific Committee on Food), Opinion on nitrate and
`nitrite, expressed on 22 September 1995 (Annex 4 to Document
`III/5611/95), ed by European Commission, Brussels, p 20
`(1995).
`32 SCF (Scientific Committee on Food), Assessment of dietary
`intake of nitrates by the population in the European Union,
`as a consequence of the consumption of vegetables, in Reports
`on tasks for scientific cooperation: report of experts participating
`in Task 3.2.3, ed by European Commission, Brussels, p 34
`(1997).
`33 Santamaria P, Contributo degli ortaggi all’assunzione gior-
`naliera di nitrato, nitrito e nitrosammine. Industrie Alimentari
`36:1329–1334 (1997).
`34 Hambridge T, Nitrate and nitrite: intake assessment. [Online].
`WHO Food Additives Series 50 (2003). Available:
`http://www.inchem.org/documents/jecfa/jecmono/v50je07.
`htm [21 July 2004].
`35 Dejonckheere W, Steurbaut W, Drieghe S, Verstraeten R and
`Braeckman H, Nitrate in food commodities of vegetable origin
`and the total diet in Belgium (1992–1993). Microbyol Aliment
`Nutr 12:359–370 (1994).
`36 Dich J, J¨arvinen R, Knekt P and Penttil¨a PL, Dietary intakes of
`nitrate, nitrite and NDMA in the Finnish mobile clinic health
`examination survey. Food Addit Contam 13:541–552 (1996).
`37 Corn´ee J, Lairon D, Velema J, Guyader M and Berthezene P,
`An estimate of nitrate, nitrite and N-nitrosodimethylamine
`concentrations in French food products or food groups. Sci
`Aliments 12:155–197 (1992).
`in der
`38 Selenka F and Brand-Grimm D, Nitrat und nitrit
`Ern¨ahrung des Meuschen. Kalkulation der mittleren
`Tagesonfuahme und Absch¨atzung der Schawankungsbreite.
`Zentralbl Bakteriol Hyg I Abt Orig B 162:449–466 (1976).
`39 CSS (Consiglio Superiore Sanit`a), Commissione ‘Nitriti, nitrati e
`nitrosamine’. Documento conclusivo, Rome, p 154 (1980).
`40 Borawska M, Markiewica R and Wikowska A, Nitrate and
`nitrite content in daily hospital diets during the winter season:
`comparison of analytical and calculation methods. Eur J Clin
`Nutr 41:489–493 (1998).
`41 ACAPV (Administraci´on de la Communidad Aut´onoma
`del Pa´ıs Vasco), Food chemical surveillance in the Basque
`Country: 1990–1995, Vitoria-Gasteiz: Servicio Central de
`publicaciones del Gobierno Vasco (1997).
`42 Jagerstad M and Nilsson R, Intake of nitrate and nitrite of some
`Swedish consumers as measured by the duplicate portion
`technique, in Proc Sec Symp Nitrite Meat Prod, Zeist, ed by
`Jagerstad M and Nilsson R, pp 283–287 (1976).
`43 Ellen G, Egmond E, van Loon JW, Sahertian ET and Tolsma K,
`Dietary intakes of some essential trace elements, nitrate, nitrite
`and N-nitrosamines, by Dutch adults: estimated via a 24-
`hour duplicate portion study. Food Addit Contam 7:207–221
`(1990).
`44 Knight TM, Forman D, Al-Dabbagh SA and Doll R, Estima-
`tion of dietary intake of nitrate and nitrite in Great Britain.
`Food Chem Toxicol 25:277–285 (198