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The overall content of salicylic acid and salicylates in food available on the European market Paulina Katarzyna K#szycka, Micha# Szkop, and Danuta Gajewska J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.7b04313 • Publication Date (Web): 28 Nov 2017 Downloaded from http://pubs.acs.org on November 30, 2017

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Journal of Agricultural and Food Chemistry

Manuscript ID jf-2017-043134

The Overall Content of Salicylic Acid and Salicylates in Food Available on the European Market Paulina K. Kęszycka1, Michał Szkop2, Danuta Gajewska1* 1

Department of Dietetics, Faculty of Human Nutrition and Consumer Sciences, Warsaw

University of Life Sciences –SGGW, Nowoursynowska 159, 02-776 Warsaw, Poland 2

Department of Biochemistry, Faculty of Agriculture and Biology, Warsaw University of Life

Sciences – SGGW, Nowoursynowska 159, 02-776 Warsaw, Poland

*Corresponding Author: Danuta Gajewska Department of Dietetics, Faculty of Human Nutrition and Consumer Sciences, Warsaw University of Life Sciences – SGGW, Nowoursynowska 159, 02-776 Warsaw, Poland Tel: +48 22 593 70 21, e-mail: [email protected]

1 ACS Paragon Plus Environment


1

Abstract

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The study aimed to determine the salicylates content in 112 products available on the

3

European market. Quantitative determination of free and conjugated forms of salicylic acid

4

(SA) in food was performed using reversed phase high-performance liquid chromatography

5

(RP-HPLC) with fluorescence detection. The salicylates contents ranged from 0 to 1675.79

6

(µg/100 g). The results of this study confirm the presence of salicylates in food products, as

7

well as a broad content diversity of these compounds depending on the species, variety and

8

method of processing of food items. The results can be very helpful for nutritionists,

9

dieticians in planning low-salicylates or high-salicylates diets.

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Keywords Salicylates, Salicylic acid, Non-allergic salicylates hypersensitivity, Low-

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salicylate diet

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INTRODUCTION

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Salicylic acid (C7H6O3, 2-hydroxybenzoic acid) and its various derivatives are

16

naturally present in plants and are commonly referred to as salicylates. In medicine, a

17

commercially available acetylsalicylic acid (AspirinTM) is widely used as an analgesic,

18

antipyretic, anti-inflammatory, antiplatelet, vasoprotective and antineoplastic agent.1-3 Aspirin

19

has also been associated with a reduced risk of colorectal cancers and other types of cancer

20

including oesophagus, stomach, ovary, breast and lung cancer.4-6 Several studies have shown

21

that plants can synthesise salicylic acid (SA), and that the latter plays a very important role in

22

plants’ defence against pathogens.7 SA is also involved in the regulation of plants’ response to

23

stress, such as high or low temperature, salts or oxidative conditions. In termogenic plants, SA

24

is the natural trigger of heat production.8-12

25

The chemical analysis of food products has proven that salicylates are also found in

26

food, and their main sources are vegetables, fruits, herbs and spices.13-16 The results depicted

27

in the literature are very different from each other and do not allow to unambiguously

28

determine which products have a low or high salicylates content.

29

The precise data regarding the salicylates content in foods is important, especially for

30

patients with a non-allergic salicylate hypersensitivity, who should limit the intake of these

31

substances.17, 18 Some authors have reported that 2.5% Europeans may suffer from salicylate

32

sensitivity.19, 20 In addition, knowledge on salicylates content in foods allows to arrange a

33

high-salicylate diet, which in turn may have positive, anti-inflammatory effects on the health

34

of people with tolerance for these compounds. Morgan (2005) has found that salicylates

35

present in a diet rich in fruits and vegetables are largely responsible for the positive effects of

36

these foods on the human health. He proposed to classify salicylates as vitamin S. However, it

37

is not well understood whether naturally-occurring salicylates have the same benefits for

38

humans as aspirin.21



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The most frequently cited study on the salicylates content in food was conducted by

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Swain et al. in 1985. It should be noted, however, that this study was carried out more than 30

41

years ago, and that the salicylates content in food largely depends on the manner of its

42

production, which for the last 30 years has been subjected to great intensification. In addition,

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these studies did not cover products consumed commonly in significant quantities in Europe,

44

such as pickled products, or several varieties of fruits and vegetables.

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The aim of this study was to determine the content of free and bound forms of SA in

46

food products available on the European market, including fruits, vegetables, cereals, meat,

47

legumes, dairy products and beverages. To the best of our knowledge, there is still lacking

48

data on the database on salicylates content in food available on the European market.

49

Although previous studies confirmed the fact that salicylates can be found in foods, reports on

50

the naturally-occurring salicylates in food products are often contradictory and significantly

51

differ from each other. The results of our research indicate the necessity of verifying the

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opinion on the salicylates content in foods, which have so far been considered as salicylates

53

free.

54 55

MATERIALS AND METHODS

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Chemicals

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Salicylic acid was obtained from Sigma-Aldrich Inc. (St. Louis, MO, USA). Potassium

58

dihydrogen phosphate and dipotassium hydrogen phosphate were obtained from POCH SA

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(Gliwice, Poland). HPLC-grade acetonitrile and ethyl acetate were purchased from Roth

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(Karlsruhe, Germany). All aqueous solutions were prepared with ultra-pure Milli-Q water.

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HPLC eluents were filtrated before use.

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Analytical equipment


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The HPLC system was composed of a binary pump (Model 1525, Waters Corporation,

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Milford, MA, USA), a fluorimetric detector (Model 474, Waters), an autosampler (Model

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717plus, Waters) and a personal computer with Breeze data acquisition and integration

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software (Waters). Chromatographic separations were carried out at ambient temperature on a

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C8 column (Symmetry 4.6 × 150 mm, 5 µm, Waters) fitted with a C8 guard column

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(Symmetry 3.9 × 20 mm, 5 µm, Waters) using gradient elution.

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Food selection and initial processing

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Our strategy for food selection consisted in including a range of food products that are

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known to be consumed in large amounts in Poland and were, or were not, earlier reported to

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have a salicylates content. For this purpose, we selected and purchased 112 products,

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including 38 vegetables (fresh and processed) 30 fruits (fresh and processed), 12 kinds of

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meat, milk and dairy products, 14 different cereal products, 10 beverages and 8 food products

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classified as others.

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Each cultivar of fresh Polish fruits and vegetables was purchased between June and

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November 2014, directly from four different manufacturers, located in the Masovian district

78

in Poland. A minimum of 500 g or 10 individual units for smaller products (e.g. berries,

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cherries), and 4 individual units for larger fruits and vegetables (e.g. apple, pear, tomato,

80

potato, carrots) were collected. Imported fruits were purchased in 4 supermarkets, following

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the same procedure. The composite sample for each species was made from 500 g of

82

individual small fruits or vegetables, or 4 bigger units, randomly selected from the purchased

83

products. Immediately after the purchase, fresh products were cleaned, the inedible parts were

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discarded, and in some cases, the products were subjected to a thermal treatment. Other

85

products were purchased in four supermarkets in Warsaw (in amount of a minimum of 100 g

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for each product). For dry products (grains, legumes, flours, candy, yeast), a composite

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sample was produced by carefully mixing and grinding the primary items from 4 purchased



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samples. Meat products were cut in equally shaped small pieces, then composited. Canned

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food products were drained and dried food products were composited. All fresh and canned

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products were freeze-dried with a freeze dryer Labconco 2.5, at a temperature of −40 °C and

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under a pressure of 0.100 mBa. The freeze-dried samples were homogenized, placed in plastic

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tubes and stored at −80 °C to prevent the loss of salicylates. All liquid products (oil, soy milk,

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milk, soda, juices, yogurt, tea, cereal coffee) were directly subjected to extraction. Tea and

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other hot beverages were prepared as infusion (2 g of tea brewed for 2 min in 200 mL of

95

boiling water). Cereal coffee was prepared by adding 4 g of instant coffee to 200 mL of hot

96

water.

97 98 99

All analyses were done in three replications, using sixty milligram weights of dry food products and 1 mL of liquid products for each individual run. All data was collected and entered into an Excel©Microsoft. Descriptive statistics

100

were undertaken and the means and SD of four replications of the salicylates content were

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reported for each food product. For practical reasons, we expressed the content of salicylates

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in µg per 100 g of fresh weight for solid food products, or in µg per 100 mL for liquid food

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products. The calculation of the salicylates content in µg per 100 g of fresh weight for solid

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food products was based on the difference of the products’ weight prior to, and after the

105

lyophilization process.

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Sample clean up and SA quantitation

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The sample clean up procedure and the overall methodology of free SA and free +

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bound SA determination in foods has been previously developed in our laboratory and

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recently published in the form of the methodological paper.22 The developed method has been

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validated in terms of linearity and range, LOD, LOQ, accuracy (recovery) and precision

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(repeatability). In brief, the sample clean up procedure comprised three extraction steps,

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namely initial extraction, extraction by ethyl acetate and back extraction to the aqueous phase.


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The developed procedure relied on the physiochemical properties of SA, which partition

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coefficient between aqueous and organic phase changes significantly in acidic and alkaline

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pH. For total salicylates (i.e. free + bound SA) content determination, the samples were

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additionally subjected to exhaustive acidic hydrolysis. This step was aimed to release SA

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from its glycoside and ester forms, the most abundant known SA derivatives present in plant

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tissues.23 The recovery rates of SA for established sample preparation procedure were not

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lower than 85%, while RSD values for intra-day and inter-day precisions were not higher than

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6%. The quantitation of SA was performed using HPLC with fluorescence detection on the

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basis of external standard calibration. The instrumental LOD and LOQ values were 0.02 and

122

0.07 ng, respectively. The method LOD values were approximately 0.001 µg mL−1 for liquid

123

products and 0.021 µg g−1 of dry weight for solid products, while method LOQ values were

124

approximately 0.004 µg mL−1 for liquid products and 0.074 µg g−1 of dry weight for solid

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products.

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RESULTS

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The contents of free SA and total salicylates (free SA plus bound SA) in analyzed food

128

products are listed in the Tables from 1 to 5. Salicylates content varied considerably

129

depending on the food species and the processing method. The amount of salicylates in

130

vegetables ranged from below the LOQ (champignon) to over 1600 µg/100 g in lentils. Most

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vegetables (76%) contained less than 100 µg/100 g of salicylates. Small amounts of

132

salicylates were detected in courgette, eggplant, lettuce and onion, as well as in white

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cabbage, olives and red bell pepper. Surprisingly, raw cauliflower had a very high content of

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salicylates – 544.16 µg/100 g of product. Legumes and pickled products (cabbage and

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cucumbers) contained also relatively large amounts of salicylates. Pickled and marinated

136

vegetables contained more salicylates than their fresh counterparts (Table 1). Among all

137

analyzed fruits, the highest content of salicylates was found in watermelon, strawberries and



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plums. No salicylates were detected in the three kinds of Polish apple, two varieties of sweet

139

apples (Golden delicious and Idared), and one variety of sour apples (Antonówka). Polish

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pear varieties did not contain salicylates (Table 2). Among dairy and meat products, only

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cottage cheese and powdered milk contained considerable amounts of salicylates. Raw meat

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had a very low or low level of salicylates. No salicylates were found in eggs (Table 3). Most

143

cereals contained considerable amounts of salicylates. The highest level of salicylates among

144

all cereals was found in buckwheat (flour and roasted groats). Small amounts of salicylates

145

were detected in wheat, while no salicylates were found in millet (Table 4). Several

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beverages, especially black and green tea, as well as cereal coffee, contained very large

147

amounts of salicylates. No salicylates were found in olive oil and in rapeseed oil, which is

148

most commonly used in Poland. A very high content of salicylates was found in yeast (Table

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5).

150

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It was observed that the salicylates content changed as the product was subjected to

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the processing methods. Peeled vegetables and fruits contained less salicylates than unpeeled

152

products (tomato, cucumber, eggplant, nectarines). Similarly, cooking had a significant

153

impact on the salicylates content in foodstuffs. Vegetables boiled in water contained far less

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salicylates than raw vegetables (beans, broccoli, cauliflower) (Table 6). In contrast, pickled

155

and marinated products contained higher amounts of salicylates in comparison with fresh

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vegetables (fermented cabbage and cucumber).

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DISCUSSION

159

To the best of our knowledge, the present paper is the first so comprehensive database

160

on salicylates content in food available on the Polish and European markets. Previous studies

161

confirmed the fact that salicylates can be found in foods and that plant foods are one of the

162

best sources of these compounds. However, reports on the naturally-occurring salicylates in


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food products are often contradictory and significantly differ from each other.13-16, 24 The level

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of dietary salicylates may depend on several factors including food production techniques

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(conventional versus organic); the geographic origin and the growing condition; plant

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varieties; the age of the plant (younger versus older); the part of the plant (leaves versus

167

roots); seasonal variation; time of food storage; cooking or processing methods. 7, 25-28

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Furthermore, data related to bioavailability of salicylates from diet is limited and not

169

conclusive. Most studies have used urinary salicylates excretion as an indicator of dietary

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salicylates intake, and have established that bioavailability of salicylates remains low.24,29,30

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Cruz et al. (1999) reported that capsaicin can reduce the bioavailability of salicylates in the

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blood stream (among rats and humans), especially when ingested for a while before

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salicylates. They emphasized that a long-term regular consumption of capsaicin from chili

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pepper reduces the salicylates bioavailability more than a single ingestion.31

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The results of the present study confirm the large discrepancies regarding the

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salicylates content in foods and indicate the need for further research, where the varieties of

177

vegetables and fruits as well as the method of growing the plants are taken into consideration.

178

One of the first studies conducted by Robertson and Kermode in 1981, using the

179

spectrofluorimetric technique, reported that the salicylates content in vegetables ranged from

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2 µg/100 g for cabbage to 10 µg/100 g for corn. 32 The most comprehensive listing of

181

salicylates contents for food products was published by Swain and colleagues.13,17 They

182

examined the salicylates content in 333 products, including 86 samples of vegetables.

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According to this study, fresh vegetables can provide up to 1900 µg of salicylates in 100 g of

184

product. Subsequent studies have shown that the salicylates content is probably much lower

185

than the one shown in Swain’s study. In 1996, Venema et al. determined the salicylates

186

content in 31 products using HPLC with fluorescence detection. They found very low

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contents of salicylates (which ranged from 0 to 1 mg/kg) in fruits and vegetables, and



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moderate contents of salicylates (from 3 to 28 mg/kg) in herbs and spices.24 Scotter et al.

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(2007) determined the salicylates content in 76 food products using gas chromatography-mass

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spectrometry. The salicylates content in vegetables did not exceed 11 µg/100 g product.14

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Wood et al. (2011) examined 52 foods using HPLC with electrochemical detection. The

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salicylates content in vegetables was up to 129 µg per 100 g of the product (for asparagus).

193

Interestingly, the salicylates content in the cauliflower, which in our study was one of the

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highest of all vegetables, was of only 1 µg/100 g.15 The most recent studies by Malakar et al.

195

(2017) described the content of salicylates in 112 common Australian food products, hence

196

contributing to the existing data on dietary salicylates.16

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In our study, considerable differences with available data were noted for cauliflower

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and cereals. We found high content of salicylates in some cereals like brown and white rice,

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as well as pseudocereals, like buckwheat. Similar data with existing literature was observed

200

for eggs, meats and oils.

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The salicylates content in food products is influenced by the processing methods, such

202

as peeling, heating and fermentation. However, the manner of processing can either reduce or

203

increase the content of salicylates in foodstuff. We found a lower content of salicylates in

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vegetables that are boiled in water. The mechanisms affecting the salicylates content during

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conventional boiling are related to the fact that SA is a volatile compound and during heating,

206

sublimes and evaporates.23,26

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Moreover, peeled fruits and vegetables were characterized by a lower salicylates

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content than unpeeled vegetables, which indicates a high concentration of salicylates in the

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skin. On the other hand, the tomato paste had a higher salicylates content than fresh tomatoes.

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Swain (1988) demonstrated that the greater the concentration of the food is while reducing the

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amount of water in the product, the higher the salicylates content of the product will be.17 The

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higher content of salicylates in pickled and marinated products may result from the SA


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synthesis by bacteria and/or the addition of herbs and spices during the food processing

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technology, as the latter are a good source of salicylates.17, 33

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Information about the exact content of salicylates in the diet is essential, as some

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studies indicate the dose dependent effect of salicylates.The western diet can provide from 10

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mg to 200 mg of salicylates in one day.13, 15 Other authors however suggest that the

218

consumption of salicylates is much lower. Janssen et al. (1997) stated that the daily intake of

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salicylates could be 10 times smaller than the one stated by Swain (1985), and contested

220

whether such low salicylates contents in foods may decrease the risk of diseases.34 Similarly,

221

Scotter et al. (2007) estimated the total daily intake of salicylates to be of 3.16 mg for women

222

and 4.42 mg for men.14 The intake of natural salicylates in Poland ranged from 1.16 mg/day to

223

15.9 mg/d. The main source of salicylates were fruits (39.97% of total salicylates), vegetables

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(31.82%), non-alcoholic beverages (10.72%), spices (6.86%) and alcohol (5.68%).35

225

To determine the actual intake of salicylates in the western diet and their possible

226

impact on the prevention of diseases, further research is needed. However, it can be assumed

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that for some individuals, even small amounts of salicylates can cause non-allergic food

228

hypersensitivity. Therefore, the precise estimation of salicylates contents in foods appears to

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be deliberate and can be helpful in preparing the diet for this group of patients. Sommer et al.

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(2016) proposed the low-salicylates diet as a novel treatment adjunct to the management of

231

aspirin-exacerbated respiratory diseases.36

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Based on our own experience with adults suffering from diagnosed salicylates

233

hypersensitivity, a personalised diet is associated with the reduction of such symptoms as

234

urticaria, eczema, sinusitis and gastrointestinal symptoms (unpublished data). The low-

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salicylates diet is perceived as very difficult for patients, due to the elimination of different

236

products, including fruits, vegetables, herbs, spices and legumes. Without any doubt,

237

improper elimination of food products from the diet can be harmful. Nevertheless, in our



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opinion, dietary modification under the control of a dietitian specialized in allergy and food

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intolerance is safe, and can improve the quality of patients life. Scientific evidence is however

240

needed in order to consider a low-salicylates diet as a routine part of the management.

241 242

CONFLICT OF INTEREST

243

The authors declare no competing financial interest.

244 245

FUNDING SOURCES

246

We thank the Faculty of Human Nutrition and Consumer Sciences of the Warsaw University

247

of Life Sciences for funding.

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Table 1. Free SA and total salicylates content in vegetables Food

Type

Brand name

Bean

Florpak Green beans Vespa

Country of origin Poland Poland

Yellow beans Unidor

Poland

Beetroot

a

b

State

Free SA (µg/100 g)

SD

raw seeds

107.88

b

2.19

Free + bound SAa (µg/100 g) 131.21

1.53

SD

fresh

6.57

0.50

71.04

0.64

cooked

4.78

0.00

38.08

1.65

fresh

8.80

0.65

136.58

2.25 2.30

cooked

5.82

0.13

57.94

fresh

13.38

0.64

87.98

3.12

180l,13–2693k,16

fresh

5.85

0.26

96.26

1.30

Overall Content of Salicylic Acid and Salicylates in Food Available on

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