screening of mycotoxin multicontamination in medicinal and aromatic herbs sampled in spain

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Short CommunicationReceived: 2 September 2008 Revised: 10 April 2009 Accepted: 20 April 2009 Published online in Wiley Interscience: 5 June 2009

(www.interscience.wiley.com) DOI 10.1002/jsfa.3647

Screening of mycotoxin multicontaminationin medicinal and aromatic herbs sampled inSpainLiliana Santos, Sonia Marın, Vicente Sanchis and Antonio J. Ramos∗

Abstract

BACKGROUND: The aim of this study was to screen the multicontamination by mycotoxins in a wide variety of aromatic and/ormedicinal herb samples collected in Spain. Mycotoxins studied were aflatoxins (AFs), ochratoxin A (OTA), zearalenone (ZEA),deoxynivalenol (DON), T-2 toxin (T-2), citrinin and fumonisins (FBs). Mycotoxins were analysed by ELISA after a clean-up stepwith multifunctional columns (AFs, ZEA, DON, FBs and T-2) or polyamide column (citrinin).

RESULTS: Of the 84 samples analysed 99% were contaminated with T-2, 98% with ZEA, 96% with AFs, 63% with OTA, 62% withDON, 61% with citrinin and 13% with FBs. Nearly 87% of samples contained four or more mycotoxins simultaneously, beingAFs, T-2 and ZEA the mycotoxins co-existing in almost every sample. 100% of the samples in our study were multicontaminated.

CONCLUSION: This study shows that this kind of commodity could be an important source of mycotoxin contamination and, ingeneral, this contamination is not limited to only one group of mycotoxins. Mycotoxin contamination on artichoke immatureflorets, boldus leaves, burdock leaves, dandelion plant, frangula bark, ginkgo leaves, lemon verbena leaves, olive leaves, redtea leaves, ribgrass leaves, St Mary’s thistle seeds, spearmint leaves, star anise fruit, vervain and white tea leaves has beendescribed for the first time. Finally, this is the first report on DON and T-2 presence in herbs. No study of this kind has beenpreviously developed in Spain.c© 2009 Society of Chemical Industry

Keywords: mycotoxins; co-occurrence; ELISA; herbs

INTRODUCTIONMycotoxins are fungal secondary metabolites commonly presentin feeds and foods. Human exposure occurs mainly by ingestion ofmycotoxin-contaminated products and can lead to serious healthproblems, including immunosupression and even carcinogenesis.The most important mycotoxins are aflatoxins (AFs), ochratoxinA (OTA), zearalenone (ZEA), deoxynivalenol (DON), T-2 toxin andfumonisins (FBs). AFs are a group of mycotoxins produced by somefungi of the genus Aspergillus section Flavi (especially A. flavus,A. parasiticus, A. nomius). OTA is mainly produced by Penicilliumverrucosum,Aspergillusochraceus and Aspergilluscarbonarius, whileZEA, FBs, DON and T-2 toxin are produced by species of thegenus Fusarium. Citrinin is produced mainly by Penicillium citrinum,Penicillium expansum and Penicillium verrucosum.

There is an increasing concern for mycotoxin contamination infoods and feeds, because they can be found in a wide range ofcommodities including cereals, spices, dried fruits, apple products,wine and coffee. Previous studies1 have demonstrated that herbaldrugs are susceptible to mycotoxin contamination. For AFs, OTA,DON, ZEA and FBs there are legal limits established by Europeanlegislation,2,3 but there is no official legislation for mycotoxincontamination of aromatic and/or medicinal herbs. The EuropeanPharmacopeia establishes that aflatoxin B1 (AFB1) should be testedin herbal drugs but does not give any application limit.4 In theEuropean Union (EU), OTA legislation and levels for spices andliquorice are currently being considered.2

The most studied mycotoxins in herbs have been AFs5 – 7 andOTA,8 – 10 followed by FBs.11,12 There are only a few studiesof simultaneous occurrence of mycotoxins in herbs.13 – 16 Thepresence of AFs, OTA, ZEA, FBs and trichothecenes in the samesamples of herbs were studied by Patel et al.17

Usually, aromatic and/or medicinal herbs have a diverse fungalinfection. Fungal contamination may occur preharvest or as a resultof poor production practices. The treatments used for reducingmicrobial load (irradiation or steam treatment) may not be suitablefor mycotoxins destruction, if present.

Nowadays, the consumption of medicinal and aromatic herbs isincreasing, either for their therapeutic or natural properties, whichmay lead to an increase in the intake of mycotoxins. In 2003,8% of Spain’s adult population took herbal supplements18 andaccording to WHO, in Europe over 50% of the population haveused complementary or alternative medicine at least once.19

The objective of this study was to screen the multicontaminationby mycotoxins (AFs, OTA, ZEA, DON, T-2, citrinin and FBs) in a widevariety of aromatic and/or medicinal herbs sold in Spain.

∗ Correspondence to: Antonio J. Ramos, Av. Alcalde Rovira Roure 191, 25198Lleida, Spain. E-mail: [email protected]

Food Technology Department, University of Lleida, XaRTA-UTPV, Av. AlcaldeRovira Roure 191, 25198 Lleida, Spain

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Screening of mycotoxin multicontamination in medicinal and aromatic herbs www.soci.org

EXPERIMENTALSamplesEighty-four medicinal and/or aromatic herb samples (500 gapprox., two different samples for each kind of herb) werepurchased from herbal stores and a herbal distributor company inLleida province, Spain. For the sampling plan, European RegulationNo. 401/2006, laying down the methods of sampling and analysisfor the official control of the levels of mycotoxins in foodstuffs atthe retail stage,20 was followed. Table 1 shows the common andscientific names of the sampled herbs. Each herb sampled wasmilled to a powder using a Romer Analytical Sampling Mill (RAS

Mill; Romer Labs, Tull, Austria) and kept at −20 ◦C until analysis.

Mycotoxins determinationSample extraction was carried out on clean-up columns. Themanufacturer’s instructions were followed except that the mod-ifying extraction solution volumes were modified (between 50and 150 mL for 25 g of ground herb) according to absorbingcapacity of the samples. Extract clean-up was carried out usingmultifunctional columns for AFs+ZEA (Romer Labs MycoSep

226 Afla-Zon+; Tulln, Austria), DON+T-2 toxin (Romer LabsMycoSep 227 Trich+) and FBs (Romer Labs MycoSep 211 Fum)or polyamide columns for citrinin (ChromabondPA, 6 mL, 1000 g;Macherey-Nagel, Duren, Germany). The clean-up was always car-ried out following the manufacturer’s instructions. Briefly, for AF,ZEA, DON and T-2 clean-up, 50 mL acetonitrile–water (84–16) wasadded to 12.5 g of samples and blended for 30 min. The super-natant was filtered and 8 mL were transfered to different glasstubes (for ZEA was necessary to acidify with 80 µL acetic acid).All 8 mL were pushed through MycoSep 226 AflaZon+ (for AFand ZEA) or MycoSep 227 Trich+ (for DON and T-2). An aliquotof 1 mL was removed and evaporated to dryness. Evaporatedextracts were redissolved in 100 µL methanol–water (70–30) and600 µL buffer for AF, ZEA and T-2, and 1 mL of water for DON,before analysis by ELISA.

For FBs clean-up, 50 mL acetonitrile–water (50–50) were addedto 12.5g of sample and was blended for 30 min. Supernatantwas filtered and adjusted to a pH of 6–9. An aliquot of 3 mLof extract was mixed with 8 mL methanol–water (3–1) andwas applied to the column. The column was washed with 8 mLmethanol–water (3–1) and with 3 mL of methanol. The elution wasmade with 10 mL methanol–acetic acid (99–1) and the eluate wasevaporated to dryness. The evaporated extract was redissolved in1 mL methanol–water (0.7–13.3), before analysis by ELISA.

For citrinin clean-up, 10 g of sample were extracted with 50 mLdichloromethane and 5 mL 0.5 mol L−1 phosphoric acid, shaken for45 min, and then filtered. The column was conditioned twice with5 mL dichloromethane. An aliquot of 25 mL extract was passedslowly through the column. The column was sequentially washedwith 5 mL dichloromethane, 5 mL methanol, and 5 mL 2% formicacid in methanol. Citrinin was eluted with 5 mL 20% formic acidin methanol. The eluate was concentrated almost to dryness ina rotary vacuum evaporator at 50–55 ◦C. Evaporated extract wasredissolved in 1 mL methanol–water (0.7–13.3), before analysisby ELISA.

OTA extraction was developed following the instructions of theELISA kit and no prior column clean-up was needed. Briefly, 2 gof sample was weighed into a centrifugal screw cap vial, 5 mL of1 mol L−1 HCl were added and shaken for 5 min. Ten millilitres ofdichloromethane were added, vigorously shaken for 15 min andcentrifuged for 15 min (3500×g at 15 ◦C). The upper aqueous layer

was removed completely up to the sample cake and discarded.The entire dichloromethane extract was filtered by using a paperfilter to separate the sample cake and the filtered extract wascollected in a new centrifuge screw cap vial. An equivalent volumeof 0.13 mol L−1 sodium hydrogen carbonate buffer, pH 8.1 wasadded, vigorously shaken for 15 min. An aliquot of 100 µL of theupper aqueous phase was diluted with 400 µL of 0.13 mol L−1

sodium hydrogen carbonate buffer (pH 8.1) before analysis byELISA.

For the quantitative analysis of mycotoxins competitive en-zyme immunoassay kits from R-Biopharm AG (Darmstadt, Ger-many) were used (RIDASCREEN Aflatoxin Total, RIDASCREEN

FAST Citrinin, RIDASCREEN DON, RIDASCREEN Fumonisin,RIDASCREEN Ochratoxin A, RIDASCREEN T-2 Toxin andRIDASCREEN Zearalenone). The instructions given by the man-ufacturer for the development of the tests were strictly followed.

Table 1. Sample common names and scientific names

Scientific name Common name

Althea officinalis Marshmallow root

Arctium sp. Burdock root

Arctostaphylos uva-ursi Bearberry leaves

Cassia angustifolia Senna leaves

Citrus aurantium Orange flower

Crataegusoxyacantha/monogyna

Hawthorn

Cynara scolymus Artichoke immature florets

Equisetium arvense Horsetail

Eucalyptus sp. Eucalyptus leaves

Foeniculum vulgare Fennel fruit

Ginkgo biloba Ginkgo leaves

Glycyrrhiza glabra Liquorice root

Harpagophytum procumbers Devils claw root

Hypericum perforatum St John’s worth flowered top

Illicium verum Star anise fruit

Lippia citriodora Lemon verbena leaves

Matricaria chamomilla Chamomile flower

Melissa officinalis Lemon balm leaves

Mentha pulegium Penny royal flowered top

Mentha sp. Spearmint leaves

Mentha piperita Peppermint leaves

Olea europaea Olive leaves

Panax ginseng Ginseng root

Passiflora incarnata Incarnata passion-flower plant

Peumus boldus Boldus leaves

Pimpinella anisum Green anise fruit

Plantago lanceolata Ribgrass leaves

Rhamnus frangula Frangula bark

Rheum officinalis Rhubarb stem

Rosmarinus officinalis Rosemary leaves

Salvia officinalis Sage leaves

Sambucus nigra Elder flower

Silybum marianum St Mary’s thistle seeds

Taraxacum officinale Dandelion plant

Thea sinesis Black, white, green or red tea leaves

Tilia cordata Lime tree flower

Urtica dioica Common nettle

Valeriana officinalis Valerian root

Verbena officinalis Vervain

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The results of the analyses were obtained spectrophotometricallyat 450 nm using a SEAC SIRIO S (Florence, Italy) microtitrespectrophotometer. Mycotoxin concentrations in the sam-ples were calculated by using Ridasoft Win version 1.38program.

The ELISA kit limits of detection (LOD) were 0.025 µg kg−1 forOTA, 83 µg kg−1 for FBs, 1.4 µg kg−1 for AFs, 0.14 µg kg−1 ZEA,0.28 µg kg−1 for T-2, 14.80 µg kg−1 for DON and 16.5 µg kg−1 forcitrinin. The LOD was calculated based on the limits of detectiongiven by the kits and the dilution factor of the method, consideringclean-up procedure and the ELISA kit protocol.

Sample preparation was carried out in a separate area fromthe analytical laboratory; a protective mask was used to preventinhalation or an allergic response from the dust, and gloves wereused to avoid skin contact with the herb extracts.

RESULTS AND DISCUSSIONThis study has been designed to screen a relatively high number ofdifferent medicinal or aromatic herbs, some of them never studiedbefore, for mycotoxin multicontamination, in order to determineif mycotoxins could be a problem in such a wide variety ofcommodities. Of the 84 samples analysed 99% were contaminatedwith T-2 toxin, 98% with ZEA, 96% with AFs, 63% with OTA, 62%with DON, 61% with citrinin and 13% with FBs (Figs 1 and 2).Figure 3 shows that no sample was free from mycotoxins andthat at least two mycotoxins occurred simultaneously. Nearly 87%of samples contained four or more mycotoxins simultaneously,being AFs, T-2 toxin and ZEA the mycotoxins co-existing in almostevery sample.

Although, nowadays, in the EU there are no legal limits forthe studied mycotoxins in herbs (and moreover, citrinin and T-2 have no legal limit established for any foodstuff), in somecases the amount of mycotoxins found was extremely highcompared to legal limits given to other foodstuffs. For instance,853.44 µg kg−1 of total AFs were found in a red tea leaves sampleand 5.24 µg g−1 of DON was detected in a sample of bearberryleaves. The higher amounts found for the other mycotoxinswere 647 µg kg−1 of FBs in liquorice root, 354.84 µg kg−1 ofcitrinin in ginkgo leaves, 256.9 µg kg−1 of T-2 in ribgrass leaves,44.1 µg kg−1 of ZEA in frangula bark and 17.3 µg kg−1 of OTA insage leaves.

Previous studies developed by other authors found AFB1 inliquorice root in a mean concentration that range from 170to 590 µg kg−1,5,13 and in rhubarb in a level of 48 µg kg−1,21

while in senna leaves, elder flower, lemon balm leaves no AFscontamination was found.22,23 OTA has been found in samplesof liquorice root with mean concentration 50 µg kg−1,13 or in arange of 0.3–252.8 µg kg−1,9,24 but elder flower and lemon balmleaves were OTA negatives.22 Samples of ginseng root analysedby HPLC showed ZEA concentrations of 11.7 and 6.13 µg kg−1,25

but ZEA was not found in elder flower and lemon balm leaves.22

With regard to FBs, there are studies that found fumonisin B1

(FB1) in concentrations ranging from 80 to 280 µg kg−1 in samplesof black tea and from 20 to 70 µg kg−1 in chamomile samples.Fumonisin B2 (FB2) was not detected in any of these samples.11

Other authors did not detect FB1 and FB2 in any samples ofblack and green tea, chamomile, lime, sage, senna, fennel andliquorice.12

All the samples in our study were multicontaminated. Table 2shows the top five herbs regarding mycotoxin contamination(both samples showed contamination with 6 or 7 different

Figure 1. Distribution of Fusarium mycotoxin contamination in thesamples.

mycotoxins). Both samples of sage and one of chamomile weremulticontaminated with the seven mycotoxins studied. Moreover,sage samples showed high AFs levels (23.8 and 25.2 µg kg−1,respectively) and OTA levels of 17.3 and 1.1 µg kg−1. Table 3 showssamples where mycotoxin contamination has been describedfor first time. Red tea leaves, rhubarb stem, spearmint leaves,ginkgo leaves and boldus leaves had both samples analysedcontaminated with all mycotoxins studied except FBs (Tables 2and 3). All these samples had high levels of AFs, ranging from16.6 to 853.4 µg kg−1, with red tea being the most contaminated.Also, ginkgo leaves had one of the highest levels of citrinin found(298.7 and 354.8 µg kg−1). From these samples rhubarb stem was

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Figure 2. Distribution of Penicillium and Aspergillus mycotoxin contamina-tion in the samples.

Figure 3. Distribution of the number of multicontaminated samples.

the most contaminated with OTA (13.9 µg kg−1). Star anise fruit,incarnate passion-flower plant and ribgrass leaves samples weremulticontaminated with AFs, DON, ZEA, FBs and T-2 toxin. Staranise fruit and passion flower had high AFs contamination with94.8 and 104.2 µg kg−1 in star anise and 67.5 and 23.5 µg kg−1

in passion flower. Ribgrass leaves had the highest level of T-2(256.9 µg kg−1) in one of the samples.

Despite the small number of samples, this study shows thataromatic and/or medicinal herbs contamination by mycotoxinsusually never occurs just for one mycotoxin. The existenceof multicontamination is evident, bearing in mind that theconditions which make possible fungal contamination and growth,and mycotoxin production, are the same for different kindsof mycotoxigenic moulds. In some cases, the co-occurrence ofdifferent mycotoxins in a food could lead to additive or synergiceffects.26 The combined intake of mycotoxins could lead to higherrisk to human health.

Some aromatic and/or medicinal herbs can be taken directlyand others undergo thermal treatment with boiling water to maketea or infusions, thus degradation or diffusion of mycotoxin to thebrew may vary. A similar thing happens, for example, in coffee,where depending on the brewing processes, an OTA reductionbetween 14.5 to 49.8% could occur.27

Mycotoxin concentration values were sometimes very differentbetween samples. This difference could be explained by theorigin of the samples. This study clearly shows that this kind ofcommodity could be a major source of mycotoxin contaminationand, in general, this contamination is not limited to only onegroup of mycotoxins. For a more detailed study it is important toincrease the number of samples of each herb. Also, mycotoxincontamination in natural samples is not homogeneous andsampling schemes must be made based in the EU regulation.28

EU official sampling and testing methods are available onlyfor few mycotoxins and commodities which are normally notapplicable to herbal herbs drugs without thorough adaptationand validation.28,29

This work is the first of its kind in Spain. Mycotoxin contaminationon artichoke immature florets, boldus leaves, burdock leaves,dandelion plant, frangula bark, ginkgo leaves, lemon verbenaleaves, olive leaves, red tea leaves, ribgrass leaves, St Mary’s thistleseeds, spearmint leaves, star anise fruit, vervain and white tealeaves has been described for the first time. Finally, this is the firstreport on the presence of DON and T-2 in herbs.

The common consumption of multicontaminated herbs, al-though with low contamination levels, could lead to the appear-ance of some chronic diseases. Perhaps one approach to solvingthis problem could be to elaborate a specific regulation for myco-toxin contamination in herbs, pointing out the co-occurrence ofmycotoxins in this kind of commodity.

CONCLUSIONSFrom our results, mycotoxin contamination in herbal drugs hasbeen confirmed. Moreover, multicontamination has demonstratedto be present in all analysed samples. This screening shows thatsome of the samples analysed were contaminated to alarminglevels.

Since the presence of mycotoxins in this kind of commodity hasbeen demonstrated to be a real problem, it would be interestingto carry out a study to determine at which stages of the herbprocessing the mycotoxin contamination occurs.

ACKNOWLEDGEMENTSThe authors are grateful to the Spanish (Project AGL2007-66416-C05-03) and Catalonian (XaRTA – Reference Network on FoodTechnology) Government for their financial support. We thank A.van Ginkel for her collaboration in the collection of herb samplesand her valuable technical advice.


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Table 2. Top five multicontamined samples

No. Sample OTA (µg kg−1) FBs (µg kg−1) AFs (µg kg−1) ZEA (µg kg−1) T-2 (µg kg−1) DON (µg kg−1) Citrinin (µg kg−1)

20 Sage leaves 1.1 130.0 23.8 5.2 0.6 83.6 273.2

75 Sage leaves 17.3 133.3 25.2 4.7 2.5 102.2 51.6

47 Chamomile flower 0.8 90.0 35.8 7.3 8.3 123.4 49.3

29 Chamomile flower 1.0 <LOD 161.0 12.5 3.5 191.5 31.7

39 Valerian root 1.8 <LOD 6.2 1.0 13.3 64.7 20.5

64 Valerian root 0.8 96.7 15.8 4.3 10.5 38.8 <LOD

6 Senna leaves 3.1 86.7 434.3 7.1 2.4 20.5 <LOD

10 Senna leaves 4.2 <LOD 207.9 8.4 3.0 35.2 68.6

30 Rhubarb 2.1 <LOD 35.7 3.1 3.0 241.8 42.2

60 Rhubarb 13.9 <LOD 71.2 24.4 23.0 58.4 42.9

Table 3. First time described mycotoxin contaminated herbs

No. Samples OTA (µg kg−1) FBs (µg kg−1) AFs (µg kg−1) ZEA (µg kg−1) T-2 (µg kg−1) DON (µg kg−1) Citrinin (µg kg−1)

31 Artichoke <LOD <LOD 10.7 7.2 17.8 165.0 29.8

45 Artichoke 5.0 <LOD 12.1 7.8 29.8 200.2 <LOD

36 Boldus 1.6 <LOD 86.6 10.3 21.9 223.1 62.7

71 Boldus 1.2 <LOD 32.2 7.0 26.7 343.5 15.7

34 Burdock root <LOD <LOD 2.6 <LOD 0.6 <LOD 25.8

72 Burdock root <LOD <LOD 10.3 10.9 1.2 <LOD <LOD

37 Dandelion <LOD <LOD 11.8 4.2 1.9 66.5 96.0

61 Dandelion 10.6 <LOD 21.7 17.0 2.7 36.0 21.6

81 Frangula 1.5 <LOD 64.7 44.1 12.6 60.9 38.4

8 Frangula 4.2 <LOD 32.1 1.5 <LOD <LOD 26.7

11 Ginkgo 1.1 <LOD 23.3 9.1 19.1 63.4 354.8

46 Ginkgo 0.8 <LOD 23.0 9.4 29.4 134.1 298.7

74 Lemon verbena 1.5 <LOD 31.1 6.4 18.9 119.4 29.6

22 Lemon verbena <LOD <LOD 37.7 14.0 28.6 143.7 79.1

7 Olive leaves <LOD <LOD 77.6 9.3 3.5 149.9 <LOD

62 Olive leaves 1.3 <LOD 58.0 42.7 3.0 127.2 14.9

58 Red tea 4.0 <LOD 853.4 11.2 40.6 179.9 18.0

59 Red tea 3.7 <LOD 801.1 4.5 42.8 149.1 22.3

38 Ribgrass 0.9 <LOD 12.6 7.7 12.3 <LOD <LOD

70 Ribgrass 1.1 <LOD 16.1 1.6 256.9 <LOD <LOD

54 Spearmint 1.1 <LOD 29.7 9.3 4.9 91.1 41.0

66 Spearmint 1.4 <LOD 16.6 2.1 3.9 46.9 43.3

33 St Mary’s thistle <LOD 236.7 10.9 1.6 17.5 <LOD <LOD

32 St Mary’s thistle <LOD <LOD 11.5 3.5 35.6 <LOD <LOD

25 Star anise <LOD 140.0 94.8 2.2 40.6 321.2 <LOD

28 Star anise <LOD 146.7 104.2 10.1 60.5 275.2 <LOD

26 Vervain <LOD <LOD 48.9 4.8 20.4 <LOD <LOD

40 Vervain 1.1 <LOD 104.5 9.5 4.7 60.0 31.2

55 White tea 4.9 <LOD 254.0 11.2 42.8 184.4 <LOD

51 White tea 3.7 <LOD 94.2 8.3 34.5 259.1 19.7

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screening of mycotoxin multicontamination in medicinal and aromatic herbs sampled in spain

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