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Aflatoxins in selected Thai commoditiesNatthasit Tansakul a b , Sasithorn Limsuwan c , Josef Böhm b , Manfred Hollmann b &Ebrahim Razzazi-Fazeli da Department of Pharmacology, Faculty of Veterinary Medicine , Kasetsart University ,Bangkok , Thailandb Institute of Animal Nutrition , University of Veterinary Medicine Vienna , Vienna , Austriac Molecular Phytopathology and Mycotoxin Research, Department of Crop Sciences ,Göttingen University , Göttingen , Germanyd VetCore Facility for Research, VetOMICS , University of Veterinary Medicine Vienna ,Vienna , AustriaAccepted author version posted online: 12 Jun 2013.Published online: 16 Jul 2013.

To cite this article: Natthasit Tansakul , Sasithorn Limsuwan , Josef Böhm , Manfred Hollmann & Ebrahim Razzazi-Fazeli ,Food Additives & Contaminants: Part B (2013): Aflatoxins in selected Thai commodities, Food Additives & Contaminants: PartB: Surveillance, DOI: 10.1080/19393210.2013.812148

To link to this article: http://dx.doi.org/10.1080/19393210.2013.812148

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Aflatoxins in selected Thai commodities

Natthasit Tansakula,b*, Sasithorn Limsuwanc, Josef Böhmb, Manfred Hollmannb and Ebrahim Razzazi-Fazelid

aDepartment of Pharmacology, Faculty of Veterinary Medicine, Kasetsart University, Bangkok, Thailand; bInstitute of Animal Nutrition,University of Veterinary Medicine Vienna, Vienna, Austria; cMolecular Phytopathology and Mycotoxin Research, Department of CropSciences, Göttingen University, Göttingen, Germany; dVetCore Facility for Research, VetOMICS, University of Veterinary MedicineVienna, Vienna, Austria

(Received 1 January 2013; final version received 3 June 2013)

Aflatoxin (AF) B1, B2, G1 and G2 were determined in 120 samples of selected Thai commodities including unpolishedrice, unpolished glutinous rice, chilli powder, whole dried chilli pods and raw peanut. The mean concentrations of the totalAFs for analysed samples were 0.16, 25.43, 14.18, 6.62 and 1.43 µg kg−1 with positive incidences of 4%, 20%, 97%, 37%and 30%, respectively. Quantitative analysis was performed using HPLC equipped with post-column derivatisation andfluorescence detection. Sample clean-up was carried out using immunoaffinity columns for selective enrichment of AFs.The method was validated by using certified reference material, which showed recoveries over 85%. The limit of detections(LODs) and limit of quantifications (LOQs) were in a range between 0.01–0.11 µg kg−1 and 0.03–0.38 µg kg−1,respectively. The results clearly demonstrated that AFs were detectable in different matrices. Chilli powder was found tohave the highest level of AFs contamination followed by chilli pods, peanut and rice, respectively. However, among theselected commodities, unpolished rice contained only trace levels of AFB1 and AFB2. With regard to the fact that AFs are anatural contaminant in commodities, this report calls to attention the regular monitoring and effective control of foodcommodities to prevent health hazards.

Keywords: aflatoxins; rice; chilli; peanut; HPLC

Introduction

Unavoidable mycotoxin contamination in food commod-ities is of global concern as they are one of the mostharmful fungal metabolites to human and animal health.Aflatoxins are a group of toxic metabolites producedmainly by the fungi Aspergillus flavus and Aspergillusparasiticus growing on a variety of agricultural productsduring environmentally favourable conditions, particularlyin the tropical zone. The four major aflatoxin analoguesare aflatoxin B1 (AFB1), B2 (AFB2), G1 (AFG1) andG2 (AFG2). AFB1 is classified as carcinogen class 1A(International Agency for Research on Cancer 1993). TheEU food law has set maximum limits of 2 µg kg−1 forAFB1 and 4 µg kg−1 for total AFs in peanut and cereals.Maximum levels in spices are 5 µg kg−1 for AFB1 and10 µg kg−1 for the sum of AFs (European Commission2010).

Rice (Oryza sativa L.), a tropical grain, is one of thestaple food crops in the world. Rice and rice products arealso used as feed ingredient in animal production. Worldrice production was forecasted to be about 476 milliontons (on a milled basis) in 2011–2012 and Thailand is oneof the major rice exporters in the world. It was estimatedthat the mean unpolished rice consumption by the Thaipopulation was 25.60 g/person/day. The occurrence ofmycotoxins in rice has been reviewed by Tanaka et al.

(2007). Aflatoxins were found worldwide in rice samplesin the Philippines (Sales & Yoshizawa 2005), China (Liuet al. 2006), Vietnam (Nguyen et al. 2007), India (Reddyet al. 2009), Sweden (Fredlund et al. 2009), Austria (Reiteret al. 2010), Germany (Reinhold & Reinhardt 2011) andCanada (Bansal et al. 2011). In addition, glutinous rice,known as sticky rice, is a kind of rice mostly consumed asa main dish and also preferred to serve as a desert or sweetbetween meals in some regions of Asia. However, onlyfew studies are available on aflatoxin contamination inunpolished rice and unpolished glutinous rice.

Chilli, Capsicum genus of plants, is ranked secondafter black pepper among the world spices (Iqbal et al.2010). Aspergillus spp. was found to be a predominantfungal infection in chilli (Reddy et al. 2001). AFs con-tamination in several kinds of spices has been reportedelsewhere (Cho et al. 2008; Reinhold & Reinhardt 2011).Among monitoring of spices in the Irish market, chillipowder was found to be contaminated with AFs (range0.35–27.50 µg kg−1) in higher concentrations than others(O’Riordan & Wilkinson 2008). In other former surveys,AFs have also been detected in the chillies in Portugal(Martins et al. 2001), India (Reddy et al. 2001), Pakistan(Iqbal et al. 2010) and Spain (Santos et al. 2010).Although most countries in the world have no specificlegal limits on AFs for spices, the current study provides

*Corresponding author. Email: natthasitt@yahoo.com

Food Additives & Contaminants: Part B, 2013http://dx.doi.org/10.1080/19393210.2013.812148

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data on AFs contamination in chilli with regard to the EUguidelines for AFs level in spices.

High incidences and levels of AFs contamination inpeanut has widely been reported for decades, that is, inJapan (Tabata et al. 1993), the Philippines (Ali et al.1999), Malaysia (Sulaiman et al. 2007) and more recentlyin Sudan (Elzupir et al. 2011). During 1967–1987, therewere reports on peanut contaminated with AFs inThailand. Since then, a limited number of scientific reportson the incidence and levels of AFs in peanut in Thailandhave been recorded (Waenlor & Wiwanitkit 2003).Countries in tropical zones suffer from AFs contaminationin peanut as a cause of liver cancer (Liu & Wu 2010).Therefore, surveillance programmes on AFs in peanut area necessity.

Thailand, located in a tropical zone with suitable con-ditions for AFs biosynthesis, is one of the major agricul-tural food exporters in the world. Thus far, there are fewreports on AFs in rice, chilli and peanut from Thailand(Waenlor & Wiwanitkit 2003; Tanaka et al. 2007). Thepresent study aims to investigate the contamination of AFscontent in selected Thai commodities using a selective andsensitive method.

Materials and methods

Samples

In total, 120 samples including 25 unpolished rice, 10unpolished glutinous rice, 30 chilli powder, 30 wholedried chilli pods and 25 raw peanut samples were ran-domly collected from either retail fresh markets or moderntrade department stores in the central region of Thailand.Sample sizes ranged between 0.5 and 1 kg. After mixingwell, each sample was divided into 100 g subsamples,from which portions were taken to collect a final 100 gsample. The pooled 100 g sample was finely ground and10 g was taken for analysis. Unpolished rice and unpol-ished glutinous rice originated from Thailand (withoutmixing of white milled rice), but the original source ofchilli and peanut were not declared. All samples wereground and sieved at 1 mm diameter, except for peanut.Thereafter, they were labelled and put into polyethylenebags and placed at –20°C pending analysis.

Chemical and reagents

A mixed aflatoxin standard was purchased fromSupelco™ (Bellefonte, PA, USA), containing 1.026,0.297, 1.054 and 0.302 µg ml−1 AFB1, AFB2, AFG1and AFG2, respectively. HPLC grade solvents (acetoni-trile and methanol) were purchased from Fisher Scientific(Essex, UK). Purified water was produced by a UPW2system (F&L, Vienna, Austria). Sample clean-up wasperformed using AflaClean™ immunoaffinity columns

(IACs) (LC Tech™, Dorffen, Germany). The chilli pow-der certified reference material (CRM, reference numberT04132) was purchased from FAPAS™ (Food AnalysisPerformance Assessment Scheme, The Food andEnvironment Research Agency, Sand Hutton, YorkYO41 1LZ, UK).

HPLC conditions

The HPLC system consisted of a pump (LC9A, Shimadzu,Tokyo, Japan) connected to an autosampler equipped witha 100-µL injection loop (AS-2000™, Merck-Hitachi,Tokyo, Japan). A guard column (20 × 4 mm) was placedbefore the analytical column (250 × 4 mm), both filled withLichrospher 100_RP 18E 5 µm (Bischoff chromatographyLeonberg, Germany). Analysis was run at a flow rate of1 ml min−1 by an isocratic mobile phase using a mixture ofwater/methanol/acetonitrile (62:22:16, v/v/v) where119 mg/L of potassium bromide (KBr) and 350 µl/L 4 MHNO3 were added. The analytical column oven (Jetstream2 plus, TECHLAB, Erkerode, Germany) temperature wasset at 50°C. Detection was carried out by a fluorescencedetector (Waters 474, MA, USA) coupled with a Kobracell(R-Biopharm Rhône LTD, Glasgow, UK) to achieve signalenhancement. Excitation and emission wavelengths were365 and 440 nm, respectively. Chromatograms were dis-played with a Stratos™ LC software (PolymerLaboratories, Version 4.5, Shropshire, UK).

Sample preparation

Briefly, 30 ml of acetonitrile/water (60:40, v/v) was addedto 10 g sample, using a 100 ml Schott-Duran™ glasscontainer. After stirring well with a magnetic bar for30 min, the matrix was filtrated through a paper filterand transferred into a polypropylene test tube. For clean-up, IACs were allowed to stand at room temperature for30 min prior to starting the clean-up protocol. Meanwhile,3 ml of the extracted solution was diluted with 30 ml PBSexcept for chilli, where a PBS/Tween-20 (96:4, v/v) solu-tion was applied. The diluted samples were flushedthrough an IAC column with a flow rate of one drop persecond. After washing two times with 30 ml PBS and10 ml of distilled water, respectively, the sample waseluted two times with 1 ml methanol. Each eluate wasput into a glass test tube and allowed to dry under a gentlenitrogen stream. The sample was reconstituted with a 1-mlmobile phase and put in an autosampler vial.

Analytical procedure

Standard curves were constructed daily by duplicate injec-tion of five concentrations in a range of 0.5–15 ng ml−1

using mixed AFB1, AFB2, AFG1 and AFG2 solutions.

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Linear regression provided correlation coefficients (R2)above 0.997 for all curves. The limit of detection (LOD)and limit of quantification (LOQ) were determined bytaking the signal-to-noise ratios of 3:1 and 10:1,respectively, using spiked mixed standard AFB1, AFB2,AFG1 and AFG2 concentrations of 10.2, 2.9, 10.5 and3.0 ng ml−1, into blank matrices (n = 3). Repeatability andreproducibility were obtained by three replicates of eachfortified matrices in three different days. To control theperformance method, certified material reference of chilli(AFB1 and AFB2) was applied.

Results and discussion

Validation of the method

Table 1 summarises the validation results of AFs analysis indifferent matrices. High recoveries at the spike levels forAFs contents, particularly aflatoxin B series in all matriceswere noted. O’Riordan and Wilkinson (2009) found thatusing a mixture of methanol/water (80/20; v/v) as an extrac-tion solvent for AFs in chilli may provide better recoveries.Low LOD and LOQ values indicated high sensitivity.According to the specifications of the certified referencematerial, mean level of AFs in the chilli CRM should be8.84–22.73 µg kg−1 with a standard deviation of 3.52 forAFB1 and 0.42–1.07 µg kg−1 with a standard deviation of0.16 for AFB2. The method provided z-scores < 2, which issatisfactory. According to the EU food regulation(European Commission 2006), recoveries in the concentra-tion range of 1–10 µg kg−1 are acceptable when between 70and 110% and RSD should be less than 20%. The applied

method in this study showed satisfactory results, except inthe case of AFG2 in chilli.

Occurrence of aflatoxins in rice samples

In Table 2, the occurrence of AFs in unpolished Thai riceis presented, which clearly shows the low incidence ofAFs in Thai rice. This is in agreement with previousreports, where only low content of AFs was detected ina few rice samples (Sales & Yoshizawa 2005; Reiter et al.2010). As reported by Fredlund et al. (2009), AFB1 wasdetected in 71% basmati rice samples and in 20% jasminerice samples. In this case, it was also detected in high fibrecontent in jasmine rice (unpolished Thai rice) sold at theSwedish market. The authors reported AF levels between0.1 and 50.7 µg kg−1. In 2010, AFs were found in morethan 70% of the 22 analysed basmati rice samples inGermany with a mean concentration of 1.53 µg kg−1

(Reinhold & Reinhardt 2011). In Canada, two yearsstudy of AFs contamination in rice reported mean valuesof 0.34–0.39 µg kg−1 in AFB1 (with a maximum level of7.14 µg kg−1). These authors also reported AFs contam-ination in black and red rice exported from Thailand(Bansal et al. 2011).

In the current study, only trace amounts of AFB1 andAFB2 in one sample unpolished rice was noted. Higherconcentrations were found in unpolished glutinous ricethan unpolished rice. In contrast, no AFG1 and AFG2were detected in both unpolished rice and glutinous ricesamples. This is in contrast to a former report ofJankhaikhot (2005) who found only AFG1 in unpolishedrice of Thailand. It may indicate the vast diversity ofaflatoxin-producing fungal species and environmentalconditions for AFs production in Thailand (Erhlich et al.2007). Due to processing and rice composition, unpol-ished rice is more prone to be contaminated with AFsthan polished rice (Jankhaikhot 2005). Nevertheless, AFsconcentrations in unpolished rice samples did not exceedEU regulations, except for one sample of unpolished glu-tinous rice.

Occurrence of aflatoxins in chilli samples

In Table 3, contamination in chilli powder and wholedried chilli pods is shown. Out of 30 chilli powder andchilli pods samples, 29 and 11, respectively, were con-taminated with AFs. Among positive chilli tested samplesin this study, there were 16 samples of chilli powder and1 sample of chilli pods contaminated with AFs higherthan the acceptable limit of 5/10 μg kg−1 for AFB1/sumAFs as prescribed by the EU (European Commission2010). This finding confirms previous studies of inci-dences with high levels of AFs in chilli powder samples,like 93 µg kg−1 (Paterson 2007), 27.50 µg kg−1

(O’Riordan & Wilkinson 2008) and 32.20 µg kg−1

Table 1. Validated values of AFs in the different matrices.

MatrixLOD

(µg kg−1)LOQ

(µg kg−1)

Meanrecovery(%)

(n = 3)

RSD (%)

Intra-day(n = 3)

Inter-day(n = 3)

RiceAFB1 0.01 0.03 106.8 4.4 4.9AFB2 0.01 0.05 94.2 3.8 3.5AFG1 0.01 0.03 103.9 2.8 5.1AFG2 0.04 0.13 71.5 5.3 1.3ChilliAFB1 0.01 0.04 84.5 4.5 1.3AFB2 0.03 0.11 71.8 6.0 0.4AFG1 0.01 0.05 76.6 6.4 3.3AFG2 0.11 0.38 41.6 7.4 3.5Chilli (CRM)AFB1 0.01 0.04 92.9 2.9 1.6AFB2 0.03 0.11 93.6 7.5 2.2PeanutAFB1 0.01 0.04 87.3 2.1 2.4AFB2 0.01 0.03 91.7 3.2 4.1AFG1 0.01 0.03 81.2 4.1 5.9AFG2 0.06 0.19 71.9 3.4 2.7

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(Iqbal et al. 2010). The occurrence of AFs contaminationin chilli powder was approximately three times higherthan in pod samples. Additionally, our results showedlower incidence of AFs content in chilli pods whencompared to a study in India (Reddy et al. 2001).Bircan (2005) stated that chilli powder is a suitable sub-strate for AFs production. However, natural compoundssuch as capsanthin and capsaicin may have an effect onAFs biosynthesis (Santos et al. 2010). With regard toTable 3, AFB1 is the prominent toxin found in bothkinds of chilli samples, whereas no AFG2 could befound, which is similar to a Brazilian paprika study,where AFB1 was detected most, without any AFG2 con-tamination (Shundo et al. 2009). In a Spanish report,AFG2 and AFB2 were found in red paprika at similarlevels and frequencies (Hierro et al. 2008).

Occurrence of aflatoxins in peanut samples

As presented in Table 4, raw peanut samples were con-taminated with AFs at a maximum of 7.39 µg kg−1. Onlyone sample exceeded the EU limits for aflatoxins in

peanut. AFG1 was found at trace levels in two samples(6.7%) in contrast to recently published data, where AFG1was the most frequently detected (43%) with a maximumlevel of 401 µg kg−1 (Elzupir et al. 2011). Peanut isclassified as a high-risk cancer-causing food (EuropeanFeed Safety Authority. 2007) and consumption of peanuthas been of global concern as a high risk factor ofHepatocellular carcinoma (Liu & Wu 2010). Accordingto a former review (Waenlor & Wiwanitkit 2003) thehighest rate of AFs contamination among other foodswas peanut (36.6%). However, no AFs in raw peanutswere found above the EU limits in this survey, whereascommercially processed and ground roasted peanuts canbe contaminated with AFs.

Conclusion

In this limited survey of aflatoxins in different agriculturalcommodities, major focus was on rice as it is the mostimportant food consumed in Thailand. Other Thai foodingredients such as chilli and peanut were also analysed.According to the results, unpolished rice appears to be less

Table 3. Occurrence of AFs in chilli powder and whole dried chilli pods.

Positive Averagea Mina MaxaTotal AFs

Sample (n) (µg kg−1) (µg kg−1) (µg kg−1) Averagea Mina Maxa

Chilli powder (n = 30)AFB1 29 13.03 0.51 46.28 14.18 0.14 52.4AFB2 26 1.27 0.09 6.12AFG1 2 0.08 0.07 0.1AFG2 0 <0.11 – –Chilli pods (n = 30)AFB1 11 6.09 0.1 53.62 6.62 0.1 58.3AFB2 4 1.44 0.12 4.67AFG1 0 <0.01 – –AFG2 0 <0.11 – –

Note: aCalculated by positive samples where AFs content > LOQ.

Table 2. Occurrence of AFs in unpolished rice and unpolished glutinous rice.

Sample Positive Averagea Mina MaxaTotal AFs

(unpolished) (n) (µg kg−1) (µg kg−1) (µg kg−1) Averagea Mina Maxa

Rice (n = 25)AFB1 1 0.11 – – 0.16 – –AFB2 1 0.05 – –AFG1 0 <0.01 – –AFG2 0 <0.04 – –Glutinous rice (n = 10)AFB1 2 18.35 0.06 36.64 25.43 0.06 50.79AFB2 1 14.15 – –AFG1 0 <0.01 – –AFG2 0 <0.04 – –

Note: aCalculated by positive samples where AFs content > LOQ.

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contaminated with a trace amount of AFs. However,unpolished glutinous rice needs further investigation as itshowed higher levels of AFs than unpolished rice. Asexpected, AFs were found at higher levels in chilli powderrather than in whole dried chilli pods. Furthermore, AFswere detected at relatively low level in peanut samples.This study confirmed that AFB1 is a prominent toxin inthe analysed samples. As AFs pose a serious health hazardto the consumer, monitoring and effectiveness of its con-trol on high-risk foods is required.

AcknowledgementsThe Technology Grant Southeast Asia (6 months post-doctoralscholarship by OeAD), financed by the Austrian FederalMinistry for Science and Research (BMWF) in the frame of theASEA UNINET, Austria, is acknowledged.

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Note: aCalculated by positive samples where AFs content > LOQ.

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