A systematic review of salicylates in foods: Estimated daily intake of a Scottish population

Abstract

Several studies suggest that natural salicylates in plant-based foods may benefit health. However, large variation in published values of the salicylate content of foods means that relating dietary intakes to disease risk is problematical. Consequently, we have systematically reviewed the available literature using prescribed selection criteria. By combining these literature values with in-house analysis, we have constructed a food composition database describing median salicylate values for 27 different types of fruits, 21 vegetables, 28 herbs, spices and condiments, 2 soups and 11 beverages. Application of a validated food frequency questionnaire estimated median dietary intakes of 4.42 (range 2.90-6.27) and 3.16 (2.35-4.89) mg/day for Scottish males and females, respectively. Major dietary sources of salicylates were alcoholic beverages (22%), herbs and spices (17%), fruits (16%), non-alcoholic beverages including fruit juices (13%), tomato-based sauces (12%) and vegetables (9%). Application of the database to populations with differing dietary habits and disease risk profiles may provide further evidence for the role of dietary salicylates in the prevention of chronic diseases.

Full text

REVIEW
A systematic review of salicylates in foods: Estimated
daily intake of a Scottish population
Adrian Wood
1
, Gwen Baxter
2
, Frank Thies
1
, Janet Kyle
1
and Garry Duthie
3
1
School of Medicine and Dentistry, Division of Applied Medicine, University of Aberdeen, Foresterhill, Aberdeen,
Scotland, UK
2
Research and Development, Dumfries and Galloway Royal Infirmary, Dumfries, Scotland, UK
3
Molecular Nutrition Group, Rowett Institute of Nutrition and Health, Aberdeen, Scotland, UK
Received: August 28, 2010
Revised: November 26, 2010
Accepted: December 15, 2010
Several studies suggest that natural salicylates in plant-based foods may benefit health.
However, large variation in published values of the salicylate content of foods means that
relating dietary intakes to disease risk is problematical. Consequently, we have systematically
reviewed the available literature using prescribed selection criteria. By combining these
literature values with in-house analysis, we have constructed a food composition database
describing median salicylate values for 27 different types of fruits, 21 vegetables, 28 herbs,
spices and condiments, 2 soups and 11 beverages. Application of a validated food frequency
questionnaire estimated median dietary intakes of 4.42 (range 2.90–6.27) and 3.16 (2.35–4.89)
mg/day for Scottish males and females, respectively. Major dietary sources of salicylates were
alcoholic beverages (22%), herbs and spices (17%), fruits (16%), non-alcoholic beverages
including fruit juices (13%), tomato-based sauces (12%) and vegetables (9%). Application of
the database to populations with differing dietary habits and disease risk profiles may provide
further evidence for the role of dietary salicylates in the prevention of chronic diseases.
Keywords:
Dietary intakes / Food composition / Salicylic acid
1 Introduction
Associations between human dietary patterns and risk of
chronic diseases are well documented. For example, high
dietary intakes of fruits and vegetables are associated with
reduced risk of developing heart disease and several
common types of cancer [1, 2]. Numerous epidemiological
and laboratory studies have suggested protective effects for a
variety of nutritionally essential plant-based dietary compo-
nents, such as fibre, antioxidant vitamins and trace elements
[3]. However, plants also contain more than 100 000
secondary metabolites ranging from structurally simple
alkaloids to more complex polyphenols and steroids. Many
such non-nutritive compounds exert biological activities in
mammalian systems that may have impact on health and
disease risk [4].
There is a growing interest in the role of salicylic acid
(2-hydroxybenzoic acid) (Fig. 1) as a dietary component with
beneficial effects on human health. Potential anti-inflam-
matory, anti-atherogenic and anti-neoplastic mechanisms in
human cells include the inhibition of cyclo-oxygenase 2
transcription, the stimulation of apoptosis, moderation of
DNA mismatch repair and stimulation of antioxidant
activity [5]. Moreover, several intervention studies indicate
that regular intake of acetylsalicylic acid (aspirin) decreases
the risk of developing cancer [6], rapid deacetylation
following consumption indicating that salicylic acid is the
biologically active component [7]. Salicylic acid and its salts
and esters are abundant in the plant kingdom functioning
as hormonal mediators of local and systemically acquired
resistance to pathogens and environmental stress [8].
They are therefore likely to be present in plant products of
dietary relevance such as fruits, vegetables, herbs and
spices [9]. This has led to the suggestion that the recognised
Correspondence: Professor Garry Duthie, Rowett Institute of
Nutrition and Health, University of Aberdeen, Greenburn Road,
Aberdeen AB21 9SB, Scotland, UK
E-mail: G.Duthie@abdn.ac.uk
Fax: 144-1224-716687
&2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.mnf-journal.com
Mol. Nutr. Food Res. 2011, 55, S7–S14 S7DOI 10.1002/mnfr.201000408

effects of plant-based diets on lowering disease risk may
be attributable, at least in part, to their salicylic acid content
[10, 11].
It is unclear whether sufficient salicylic acid can be
obtained from dietary sources to exert disease preventative
activity, estimated daily intakes ranging from 0.4 to 200
mg/day have been reported [9, 12, 13]. Such a difference
may be ascribed to the disparate information available on
the salicylic acid content of foods confounding estimation of
dietary intakes. Consequently, we set out to (i) construct a
comprehensive database on salicylate levels in plant-based
foods through both in-house analytical determinations and
rigorous systematic examination of available literature and
(ii) estimate dietary salicylate intake in a healthy Scottish
population. It is intended that the food composition data-
base can be used in population studies exploring dietary
salicylate intakes and disease risk.
2 Materials and methods
To ensure as comprehensive a database as possible, data
from the literature were critically and systematically eval-
uated and then augmented with additional values from in-
house analyses of foods commonly consumed in the UK.
2.1 Critical appraisal of available literature
The method of systematic review and subsequent accep-
tance or rejection of data followed the procedures previously
employed in the construction of a flavonoid food database
[14] using the selection criteria based on the Royal Society of
Chemistry food composition tables [15–18]. In brief, these
were (i) food items had to be randomly selected and
purchased from various commercial outlets during different
seasons of the year, (ii) food samples were prepared using
normal domestic practices, (iii) optimized sample extraction
and hydrolysis conditions were clearly described or cited and
(iv) salicylate determination was based on modern techni-
ques of high-pressure liquid chromatography and MS with
validation and quality assurance measures summarised.
Using this approach, the bibliography databases CAB
abstracts, BIDS and Medline were searched using the
keywords ‘‘salicylic acid, salicylates, food and diet.’’ Data
from nine publications [9, 12, 13, 19–23] satisfied the
selection criteria and were used in the construction of the
salicylate food composition database.
2.2 Analysis of salicylate in foods
Information on commonly consumed food items in northeast
Scotland was obtained from a previous survey [18]. The total
salicylate content of the edible portions of 19 fruits, 20
vegetables, 7 spices and 6 juices purchased from local
supermarkets were determined using high-performance
liquid chromatography (HPLC) with electrochemical detec-
tion as previously described [19, 20]. Six items of the same
food were homogenised together to minimise individual
variation within each food type. Duplicate portions (1.0 g fruit
and vegetables, 0.05 g spices and 0.5mL liquids) of homo-
genised foods were suspended in 3mL of 2.5mol/L sodium
hydroxide for 24 h at room temperature. Hydrochloric acid
(1 mL of 5.3 mol/L) was then used to adjust the mixtures
so that they contained a final concentration of 0.1 mol/L
HCl. Following addition of EDTA (final concentration
100 mmol/L), 4-methyl salicylic acid (internal standard, final
concentration of 2.0 mmol/L), vortexing (15 min) and centri-
fugation (3000 rpm, 10 min, 41C), the organic phases were
dried under oxygen free nitrogen and reconstituted in 0.5mL
of 30 mmol/L citrate (pH 3.8) containing 5% methanol.
Eluted substances were detected electrochemically at an
oxidation potential of 11.1V using a previously described
four-step program [19]. The presence of salicylic acid was
confirmed by peak disappearance following addition of sali-
cylate hydroxylase and by MS [19]. Intra-assay and inter-assay
coefficients of variation (CV) were 3 and 4% respectively.
2.3 Database construction
Data for total salicylates from the literature and the in-house
analysis were combined and total salicylates for 27 different
types of fruits, 21 vegetables, 28 herbs, spices and condi-
ments, 2 soups and 11 beverages were calculated as median
values to accommodate non-normal distribution of the
range of values available for each food item.
2.4 Estimating dietary salicylate intake
Dietary intake was assessed by applying the salicylate data-
base to the Scottish Collaborative Group (SCG) semi-quan-
titative Food Frequency Questionnaire (FFQ) version 6.5
[18], consisting of a list of 170 food items, and a supple-
mental questionnaire of similar format incorporating spices
and recipes. One hundred and sixteen healthy men, mean
age 31 years (range 19–72) and 121 healthy women, mean
age 31 years (range 17–64) from Aberdeen, Scotland, UK
completed the questionnaires. For each item, participants
were asked to report their average use over the preceding
three months for a specified serving size of each food and
beverage. Nine pre-specified frequency responses were
possible, ranging from rarely or never eaten to eaten
every day. Individual salicylate intakes were calculated by
Figure 1. Molecular structure of salicylic acid.
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multiplying the frequency of each food or beverage
consumed by the salicylate content of the specified portion
size and then summing the contributions from all foods and
beverages. The salicylate contents of 19 composite dishes
(e.g. pizzas and spaghetti bolognaise) were also calculated
from standard recipes using the values for individual
ingredients from the database with adjustment for weight
lost through cooking [24–32]. Median daily total salicylic acid
intakes were adjusted for energy intake. Dietary investiga-
tions were approved by the local research ethics committee
and informed consent was obtained.
3 Results
3.1 Total salicylate content of foods
Electrochemical determination following separation by
HPLC confirmed the presence of salicylates in a range of
plant-based food items readily available to the UK consumer
(Table 1). Herbs and spices were particularly rich sources
whereas salicylates were absent in some vegetables such as
aubergines, broccoli and courgettes.
Combining the values from the in-house analysis with
those from the systematic assessment of the literature
resulted in a dietary database containing the median sali-
cylate content of 27 different types of fruits, 21 vegetables,
28 herbs, spices and condiments, 2 soups and 11 beverages
(Table 2). The salicylate content ranged from 0 to 33.59
mg/kg in fruits, 0 to 6.01 mg/kg in vegetables, 5.74 to
450 mg/kg in spices and 0.10 to 4.06 mg/kg in juices. Esti-
mated salicylate contents of standard recipes [24–32] (Table
3) ranged from 0 mg/kg (oil and lemon dressing) to 8.5 mg/
kg (tomato chutney). Raisins were particularly rich sources
of salicylates (0.98–66.2 mg/kg), a likely relative concentra-
tion effect of water loss by the drying process.
3.2 Estimated daily intakes and main food sources
Estimated medial total salicylate intakes were 4.42 and
3.16 mg/day for males and females, respectively. Following
adjustment for energy, this gender difference was no longer
apparent (Table 4). Primary food sources of salicylates
(Fig. 2) were alcoholic beverages (22%), herbs and spices
(17%), fruits (16%), non-alcoholic beverages including fruit
juices (13%), tomato-based sauces (12%) and vegetables
(9%). Salicylate intake was significantly and positively
associated (po0.01) with intakes of fibre, potassium, vita-
min C and alcohol (data not shown).
4 Discussion
Food composition databases provide essential information
for research on the health effects of nutrients, nutritional
surveillance, clinical dietetic practice and food formulation
and processing. Compositional information on potentially
bioactive phytochemicals in foods is generally lacking
although several databases for polyphenols in foods are
now under construction [33]. The present study provides
the first comprehensive and systematic assessment of
the salicylate content of commonly consumed foods and
is the first estimation of the dietary intake of salicylates
by a Scottish population. The database can be updated
and estimates of intake improved as further literature
that satisfies the systematic selection criteria becomes
available.
A particular strength of the database is only accepting
salicylate values obtained using gas or LC with alkaline or
acid hydrolysis, compound validation by MS and stated
quality assurance procedures. Values obtained by older, less
specific and colorimetric procedures were excluded as being
potentially artefactually high. However, a limitation is the
Table 1. Total salicylate content of foods purchased from local
Scottish retailers as determined by HPLC with
electrochemical detection
Food item Salicylates
(mg/kg)
Food item Salicylates
(mg/kg)
Fruits Vegetables
Banana 0.34 Asparagus 1.29
Blackberries 0.81 Aubergine 0.0
Blueberries 0.57 Broccoli 0.0
Gala melon 0.62 Cabbage
green
0.0
Grapefruit 0.44 Carrots 0.16
Green apple 0.55 Cauliflower 0.01
Kiwi fruit 0.31 Celery 0.04
Lime 0.0 Courgette 0.0
Mango 0.03 Cucumber 0.02
Nectarine 3.29 Green bean 0.07
Orange 0.11 Green pepper 0.01
Peach 0.12 Lettuce
(iceberg)
0.05
Pear 0.23 Mange tout 0.20
Plum 0.01 Mushroom
(button)
0.13
Raspberry 0.09 Onion (white) 0.80
Red grape 0.02 Potato 0.02
Strawberry 0.61 Red pepper 0.09
White grape 0.02 Swede 0.07
Yellow
melon
0.11 Tomato 0.13
Yellow pepper 0.09
Juices Spices
Apple 0.83 Black cumin 25.05
Cranberry 0.99 Cumin 29.76
Grapefruit 0.10 Chat masala 5.74
Orange 0.68 Cinnamon 0.78
Pineapple 4.06 Garam masala 12.85
Tomato 1.32 Paprika 28.25
Turmeric 20.88
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Table 2. The total salicylate database: median values calculated from combining in-house determinations with systematically reviewed
literature values
Food item (n) State Median (mg/kg) Range (mg/kg) References
Fruits
Apple (5) Fresh 0.55 o0.02–5.9 [9, 12, 21, 22], Table 1
Apricot (3) Tinned 0.10 0.03–25.8 [9, 12, 22]
Banana (3) Fresh 0.40 0.34–18.6 [9, 21], Table 1
Blackberry (3) Fresh 0.81 0.07–18.6 [9, 23], Table 1
Black chokeberry (1) Fresh 1.20 1.2 [23]
Blueberry (3) Fresh 0.57 0.33–27.80 [9, 23], Table 1
Bramble (1) Fresh 8.30 8.3 [23]
Cherry (2) Fresh 4.43 0.36–8.5 [9, 12]
Crowberry (1) Fresh 2.80 2.8 [23]
Grapes red (2) Fresh 4.71 0.02–9.4 [9], Table 1
Grapes white (4) Fresh 0.04 0.02–0.6 [12, 21, 22], Table 1
Grapefruit (3) Fresh 0.44 0.2–6.8 [9, 21], Table 1
Kiwi fruit (3) Fresh 0.31 o0.2–3.2 [9, 21], Table 1
Lemon (2) Fresh 2.50 1.8–3.2 [9, 21]
Lime (1) Fresh 0 0 Table 1
Mango (2) Fresh 0.57 0.03–1.1 [9], Table 1
Melon gala (1) Fresh 0.62 0.62 Table 1
Melon honeydew (1) Fresh 0.11 0.11 Table 1
Nectarine (5) Fresh 0.87 0.04–4.9 [9, 12, 21, 22], Table 1
Orange (5) Fresh 0.11 o0.02–23.9 [9, 12, 21, 22], Table 1
Peach (2) Fresh 2.96 0.12–5.8 [9], Table 1
Pear (3) Fresh 1.46 o0.2–2.7 [9, 21], Table 1
Plum (3) Fresh 0.50 0.01–2.1 [9, 21], Table 1
Raspberries (3) Fresh 0.90 0.09–51.4 [9, 23], Table 1
Raisins (2) Fresh 33.59 0.98–66.2 [9, 12]
Sorbus (1) Fresh 0.28 0.28 [22]
Strawberry (4) Fresh 0.63 0.04–13.6 [9, 12, 22], Table 1
Vegetables
Asparagus (2) Fresh 1.35 1.29–1.4 [9], Table 1
Aubergine (2) Fresh 4.40 0–8.8 [9], Table 1
Broccoli (2) Fresh 3.25 0–6.5 [9], Table 1
Cabbage-green (2) Fresh 0 0 [9], Table 1
Carrot (3) Fresh 0.50 0.16–2.3 [9, 21], Table 1
Cauliflower (2) Fresh 0.80 0.01–1.6 [23], Table 1
Celery (2) Fresh 0.02 0–0.04 [9], Table1
Courgette (1) Fresh 0 0 Table 1
Cucumber (4) Fresh 0.24 0.02–7.8 [9, 12, 21], Table 1
Green beans (2) Fresh 0.59 0.07–1.1 [9], Table 1
Lettuce (2) Fresh 0.02 0–0.05 [9], Table 1
Mange tout (1) Fresh 0.20 0.2 Table 1
Mushroom (2) Fresh 1.27 0.13–2.4 [9], Table 1
Onion (2) Fresh 1.20 0.8–1.6 [9], Table 1
Peas frozen (2) Fresh 0.35 0.3–0.4 [9, 21]
Peppers-green (2) Fresh 6.01 0.01–12 [9], Table 1
Peppers-red (1) Fresh 0.1 0.1 Table 1
Pepper-yellow (1) Fresh 0.1 0.1 Table 1
Potato (2) Fresh 0.01 0–0.02 [9], Table 1
Swede (2) Fresh 0.04 0–0.07 [9], Table 1
Tomato (5) Fresh 0.36 0.05-1.3 [9, 12, 21, 23], Table 1
Herbs, spices and condiments
Asafoetida (1) Dried 38 38 [20]
Black cumin (1) Dried 25.05 25.05 Table 1
Cardamom black (2) Dried 173.5 77–270 [9, 20]
Cardamom green (1) Dried 132 132 [20]
Chat masala (1) Dried 5.74 5.74 Table 1
Chilli powder (3) Dried 13 o0.2–1466 [9, 20]
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lack of information on how locality, varietal and growing
conditions and the effects of processing and storage affect
the salicylate content of foods. For example, the salicylate
content of five brands of orange juice ranged from 0.47 to
3.01 mg/L. Such potential confounding affects have been
minimised by the computation of single, median salicylate
values for each food item. This may more likely reflect the
intake of a population exposed to a diverse range of products
over the longer term. In addition to seasonal and varietal
influences on salicylate contents of primary products, the
database would benefit from direct analysis of commonly
consumed meals. Calculated daily intakes included standard
recipes but no information is available on the salicylate
content of processed foods where some forms may be used
as flavouring agents or preservatives [34].
Estimated medial salicylate intakes of 4.42 and 3.16 mg/
day for males and females respectively are comparable with
Table 2. Continued
Food item (n) State Median (mg/kg) Range (mg/kg) References
Cinnamon (5) Dried 23.8 0.78–642 [9, 12, 20, 21], Table 1
Cloves (2) Dried 41.2 25–57.4 [9, 20]
Coriander (2) Fresh 14.5 2–27 [9, 20]
Cumin (3) Dried 450 29.8–16294 [9, 20], Table 1
Curry powder (3) Dried 15.2 5.55–2180 [9, 12, 21]
Fennel (2) Dried 14 8–20 [9, 20]
Fenugreek (2) Dried 61.5 1–122 [9, 20]
Garam masala (2) Dried 340.42 12.85–668 [9], Table 1
Garlic (3) Fresh 1 o0.2–56 [9, 19, 20]
Ginger (3) Fresh 35 o0.2–45 [9, 20, 21]
Honey (3) Liquid 0.66 o0.2–39 [9, 12, 21]
Mint (2) Fresh 54.2 14.4–94 [9, 21]
Mixed herbs (2) Dried 289.15 22.3–556 [9, 21]
Nutmeg (2) Dried 26.09 24–28.18 [9], Table 1
Oregano (3) Dried 26 19.9–660 [9, 12, 21]
Paprika – hot (5) Dried 28.25 2.98–2030 [9, 12, 20, 21], Table1
Pepper – black (4) Dried 33.85 3.05–90 [9, 12, 20, 21]
Tamarind (1) Fresh 96 96 [20]
Turmeric (4) Dried 392.44 17–3505 [9, 12, 20], Table 1
Thyme (3) Dried 28.6 12.8–1830 [9, 12, 21]
Malt vinegar (2) Liquid 0.03 0–0.05 [9, 21]
White vinegar (2) Liquid 6.73 0.15–13.3 [9, 21]
Soups
Lentil (2) Tinned, liquid 0.21 0.12–0.3 [19]
Tomato (3) Tinned, liquid 0.022 0.005–0.034 [19]
Drinks
Coffee-instant (3) Freeze dried, liquid 1.8 0.37–6.8 [9, 12, 21]
Tea (3) Tea bag, liquid 1.06 0.42–34.5 [9, 12, 21]
Beer (2) Liquid 1.63 0.06–3.2 [9, 21]
White wine (8) Liquid 0.44 0.01–12.9 [21, 23]
Red wine (13) Liquid 0.50 0–2.58 [12, 21, 23]
Apple juice (3) Liquid 0.83 0.73–3.81 Table 1
Cranberry juice (2) Liquid 0.99 0.91–1.07 Table 1
Grapefruit juice (1) Liquid 0.10 Table 1
Orange juice (5) Liquid 0.68 0.47–3.01 Table 1
Pineapple juice (1) Liquid 4.06 Table 1
Tomato juice (1) Liquid 1.32 Table 1
Table 3. Estimated total salicylate content of some standard
recipe dishes
Recipe dish Total salicylates
(mg/kg)
Bolognaise sauce 3.2
Pizza, tomato 0.7
Flan, cheese onion and potato 0.5
Flan, cheese and mushroom 0.2
Pancakes, savoury, stuffed with
vegetables
4.2
Nut roast 3.2
Dressing, oil and lemon 0.0
Chutney, tomato 8.5
Cornish pastie 4.9
Vegetable korma 7.3
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estimated intakes in a Scottish population of other phenolic
compounds including types of flavonols, flavones, flavo-
nones and proanthocyanins [35]. Fruits and vegetables are
major sources of salicylates accounting for approximately
25% of total intake. Fruits and vegetables are also rich
sources of fibre, vitamin C and potassium and, therefore,
significant associations between intakes of these nutrients
and salicylates are not unexpected. Spices also account for a
considerable proportion of total salicylate intake (14% in
males and 10% in females). Consequently, populations that
incorporate substantial amounts of spices in foods may have
markedly higher daily intakes of salicylates. Indeed, it has
been suggested that the low incidence of colorectal cancer
among Indian populations may be ascribed in part to high
exposure to dietary salicylates throughout life from spice
consumption [36]. In contrast, any potential cancer preven-
tative affects of dietary salicylates [37] in Scots may be
negated by the substantial proportion derived from bevera-
ges containing alcohol (22%), a recognised pro-carcinogenic
risk factor [38].
Serum and urinary salicylate concentrations of vegetar-
ians are higher than omnivores and overlap with individuals
who regularly take low-dose aspirin [39, 40]; this suggests
substantial absorption of salicylates from ingested plant-
based foods. Such serum concentrations are sufficient to
inhibit PGHS-2 mRNA synthesis and promoter activity
in vitro [41, 42] thus preventing the conversion of arachi-
donic acid to potentially tumour-promoting cyclic prosta-
noids. The Scottish population has a habitually low intake of
fruits and vegetables [43] and salicylate intakes in the
present study, therefore, may be insufficient to exert disease
preventative effects. Application of the database to popula-
tions with differing dietary habits and disease risk profiles
may provide further evidence for the role of dietary salicy-
lates in the prevention of chronic diseases.
A. W. was funded by the Food Standards Agency (UK)
Scholarship Scheme. G. D. is grateful for funding from the
Scottish Government. This paper is dedicated to the late John
Paterson.
The authors have declared no conflict of interest.
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