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obiology 119 (2007) 59–66www.elsevier.com/locate/ijfoodmicro

International Journal of Food Micr

Mycotoxins in rice

Kenji Tanaka a,⁎, Yuki Sago b, Yazhi Zheng b, Hiroyuki Nakagawa b, Masayo Kushiro b

a Agriculture, Forestry and Fisheries Technical Information Society, Sixth Floor, Milling Building, 15-6, Kabuto-cho, Nihonbashi, Chuo-ku, Tokyo 103-0026 Japanb National Food Research Institute, 2-1-12 Kannondai, Tsukuba, Ibaraki 305-8642 Japan

Abstract

Mycotoxin contamination in rice is usually lower as in wheat or corn. However, there are some reports that rice has been contaminated withmycotoxins such as aflatoxin B1, B2, G1, G2 (AFS), citrinin, deoxynivalenol (DON), fumonisin B1, B2, B3 (FMS), fusarenon-X (Fus.-X),nivalenol (NIV), ochratoxin A (OTA), sterigmatocystin (STE), and zearalenone. Rice in Japan is preserved in warehouses where moisture contentand temperature are regulated. Therefore, mycotoxin contamination from post harvest fungal growth occurs very seldom. Trichothecenes,aflatoxins, and STE in rice were recently analyzed in our laboratory. In 1998, a typhoon struck before rice harvesting in Japan, and the unpolishedrice was found to be stained brown. Samples were collected and analyzed for the presence of trichothecenes. Mycotoxins DON, Fus.-X, and NIVwere detected and confirmed with GC-MS. The quantity of trichothecenes was determined using GC-ECD. STE is a carcinogenic mycotoxinproduced by Aspergillus versicolor and some other fungi. STE contamination of rice was studied in our laboratory since 1973. GC-MS, LC-MS,LC-MS/MS, and LC-UV methods for STE determination were examined, giving good results for the LC-UV method using a photo diode arraydetector. Different techniques for the extraction of STE from rice were also studied. Finally, brown rice was ground, and the ground rice wasextracted with acetonitrile-water. An Autoprep MF-A 1000 column was used to clean up AFS and STE. The cleaned-up extract was analyzed withHPLC-UV. Forty-eight brown rice samples were analyzed, and none of them were contaminated with STE. These rice samples were also analyzedfor AFS and FMS, and none of the samples were contaminated. The Ministry of Agriculture, Forestry and Fisheries in Japan is making theappropriate Institutes develop analytical methods for mycotoxins and survey mycotoxin contamination on rice as well as wheat, corn, and someother cereals.© 2007 Elsevier B.V. All rights reserved.

Keywords: Mycotoxins; Rice; Deoxynivalenol; Fusarenon-X; Nivalenol; Sterigmatocystin

1. Introduction

Mycotoxin contamination is less commonly reported for ricethan for many other cereals. However, contamination by luteos-kyrin (Shibata and Kitagawa, 1956), islanditoxin (Marumo andSumiki, 1955), and cyclochlorotine (Sato and Tatsuno, 1968) hasbeen reported on imported rice since the 2nd World War. There isalso a report by Sugimoto et al. (1977) detailing the contaminationof domestic rice with OTA, citrinin and sterigmatocystin. Norizukiet al. reported that commercial rice in Egypt was contaminatedwithaflatoxins (Norizuki et al., 1987). Weidenboerner also reported

⁎ Corresponding author. Tel.: +81 3 3667 8931; fax: +81 3 3667 8933.E-mail address: kjtanaka@afftis.or.jp (K. Tanaka).

0168-1605/$ - see front matter © 2007 Elsevier B.V. All rights reserved.doi:10.1016/j.ijfoodmicro.2007.08.002

some mycotoxins were found in rice (Weidenboerner, 2000). Thisdata are listed in Table 1. After the 2nd World War, rice wasimported into Japan, as food was limited. Some rice was infectedwith fungi. The Japanese Government stopped the distribution ofthis rice. Japanese people were safe from these mycotoxins fromthat time on.

Sugita-Konishi et al. (2006) reported natural contamination ofaflatoxins and ochratoxin A (OTA) in retail rice in 2004 and2005. Aflatoxins were not detected in 53 samples. The limit ofquantification was 0.1 μg/kg. No OTAwas detected in 50 retailrice samples. The limit of quantification was 0.1 μg/kg. TheMinistry of Agriculture, Forestry and Fisheries reportedanalytical results of mycotoxins contamination on severalcereals on May 23, 2006 (Press release from MAFF in Japan,2006). In this report, no OTA was detected in 98 rice samples.The limit of quantification was 0.0003 mg/kg.

60 K. Tanaka et al. / International Journal of Food Microbiology 119 (2007) 59–66

1.1. Trichothecene determination

According to Manabe and Tsuruta (1991), the majority offungal species are, mesophytes (optimal growth temperature:

Table 1Mycotoxin contamination in rice (Weidenboerner, 2000)

Incidence Conc. range Mea

Afl. B1 2/52⁎ 26–38 μg/kg 321/1

6/8 b2.5–15 μg/kg4/4⁎ b2.5–12.5 μg/kg7/364 37 μg/kg 209/9 ≦600 μg/kg b1–

Total 1/182 98Afl. B2 1/52⁎

1/11/4⁎ 1.8 μg/kg

Afl. G1 1/52⁎2/84 73.1–77.5 μg/kg 75.3

Afl. G2 3/84 3.7–96.3 μg/kg 45.6Aflatoxin(no specification)

3/15⁎ ≦38 μg/kg 1617/82⁎ ≦43 μg/kg 121/6⁎ ≦3 μg/kg 33/10⁎ ≦18 μg/kg 15

Aflatoxin(AFB1,AFB2,AFG1,AFG2)

13/30 22–317 μg AFB1/kg,15–125 μg AFB2/kg,14–107 μg AFG1/kg,20–98 μgAFG2/kg ,

Nc/4⁎ 0.1–2.4 μg/kgAflatoxin(no specification)

14/20 2–19 μg/kg 7.912/80⁎ tr–430 μg/kg23/81⁎ 30–1130 μg/kg32/43⁎ 30–130 μg/kg1/2316/72 ≦33 μg/kg 16

Citrinin 4/30 49–92 μg/kg2/2 700–1130 μg/kg

Deoxynivalenol 1/1⁎

Nc/4⁎ 4–6 μg/kgNc/4⁎ 4–7 μg/kg

Fumonisin B1 8/20 ≦4300 μg/kgFumonisin B2 6/20 ≦1200 μg/kgFumonisin B3 5/20 ≦600 μg/kgFumonisins (FB1, FB2) 1/4⁎ 28 μg/kgNivalenol 2/9 22

1/1⁎

Nc/4⁎ 4–11 μg/kgOchratoxin A 1/3⁎

2/36 ≦0.3 μg/kg2/32 8–25 μg/kg 16.52/15 1.7–2.4 μg/kg8/15 ≦1.0 μg/kg1/various food samples2/2⁎ 230–430 μg/kg

Sterigmatocystin 3/30 108–157 μg/kg2/nc 50–450 μg/kg?/?⁎ 3800–4300 μg/kg12/37 ≦16,300 μg/kg1/4⁎

Zearalenone 1/91/1⁎

3/42⁎ N200 μg/kg

Nc: not counted.

22–35 °C) that are capable of growing temperatures between 5and 45 °C, and therefore, in the temperate climate of Japan andin the tropical/subtropical climate, the prevailing temperaturesatisfy the growth conditions for a wide variety of mycelium

n conc. (μg/kg) Conc. (μg/kg) Contry Condition

Brasil ⁎Polished8 Egypt28 Italy

NepalNepal ⁎ParboiledThailand

2 Thailand5 USA15 Brasil ⁎Polished2 Egypt

Nepal ⁎Parboiled20 Brasil ⁎Polished

MalaysiaMalaysiaPhilippines ⁎Rice brandPhilippines ⁎MilledPhilippines ⁎PopPhilippines ⁎RoughIndia

UK ⁎Basmati riceGambiaIndia ⁎Cyclone-affectedIndia ⁎Cyclone-affectedIndia ⁎Parboiled

1000 MozambiquePhilippinesIndiaJapan

90 Papua New Guinea ⁎ImportedUK ⁎Basmati riceUK ⁎Chinese riceUSAUSAUSAUK ⁎Basmati riceNepal

63 Papua New Guinea ⁎ImportedUK ⁎Basmati rice

533 Egypt ⁎Rice germGermanyIndiaIndonesiaItaly

50 JapanJapan ⁎DeterioratedIndiaJapanJapan ⁎MoldyJapan

49 UK ⁎Chinese rice8 Nepal

3060 Papua New Guinea ⁎ImportedUruguay ⁎And by-products

Fig. 1. TIC and mass spectrum of STE by GC-MS.

61K. Tanaka et al. / International Journal of Food Microbiology 119 (2007) 59–66

62 K. Tanaka et al. / International Journal of Food Microbiology 119 (2007) 59–66

fungi. According to them, the required level of water activity inthe commercial distribution of harvested grains is considered tobe 0.65–0.70 or below.

Rice in Japan is now preserved in warehouses wheremoisture content is 13–14% (Minamisawa, 2006). Thesevalues mean 0.65–0.70 of water activity levels. The humidityof warehouse is controlled from 70% to 75%. The temperatureof warehouse is controlled less than 15 °C. Therefore, postharvest mycotoxin contamination seldom occurs in Japan.Manabe et al. (1973) developed analytical method for STE in1973 and found that contamination in stored rice in Japan in1975 (Manabe and Tsuruta, 1975). Trichothecenes, aflatoxins,and STE in rice were recently analyzed in our laboratory. In1998, a typhoon struck before rice harvesting in Japan, and theunpolished rice was found to be stained brown. Samples werecollected and analyzed for the presence of trichothecenes usingGC-MS (Tanaka et al., 2004).

Mass spectra of the trimethylsilylated extract werecompared with the spectra of the trimethylsilylated DON,

Fig. 2. Calibration curve

Fus.-X and NIV standards. The results suggest that thelodged and water damaged domestic Japanese rice wascontaminated with DON, Fus.-X and NIV. The quantity oftrichothecenes was determined using GC-ECD. DON andNIV were detected in rice sample in some area of Japan at theconcentration of 0.1 μg/g and 0.2 μg/g, respectively. DON,Fus.-X, and NIV were detected in rice sample in another areaof Japan at the concentration of 2.9 μg/g, 1.9 μg/g and2.2 μg/g, respectively.

Contamination with DON and NIV is frequently reportedfor wheat and barley, and contamination of rice with DON isalso recorded in the literature. From the results of a jointFAO-WHO Expert Committee on Food Additives, at theFifty-sixth meeting in Geneva, 6–15 February 2001, de-oxynivalenol was found to be a frequent contaminant ofcereal grains such as oats (834 samples, 68% positive), barley(1662 samples, 59% positive), wheat (11,444 samples, 57%positive), rye (295 samples, 49% positive), maize (5349samples, 41% positive) and rice (154 samples, 27% positive)

of STE by GC-MS.

Fig. 3. MS chromatogram and MS spectrum by LC-MS of STE.

Fig. 4. TIC and mass spectrum of STE by MS-MS.

63K. Tanaka et al. / International Journal of Food Microbiology 119 (2007) 59–66

Table 2LC-MS conditions to analyze STE

LC/MS: Shimadzu LC-MS2010AColumn: Ascentis ™ C18(2.1 mm I.D.×150 mm)Mobile phase A: Water containing 0.1%(v/v) acetic acidMobile phase B: Acetonitrile containing 0.1%(v/v) acetic acidTime program: 5%B (0–2 min)→95%B (17–22 min)→5%B (23–33 min)Flow rate: 0.2 ml/minInjection volume: 2 μlColumn temperature: 40 °CProbe voltage: ±4.0 kV (APPI-positive/negative mix mode)Probe temperature: 300 °CCDL temperature: 200 °CBlock heater temperature: 200 °CNebulizing gas (N2 gas) flow: 2.5 L/minCDL voltage: +30 V (negative mode), −30 V (positive mode)Q-array DC voltage: scan modeQ-array RF voltage: scan modeScan range: m/z 100–900 (1 s/scan)

Table 4LC-UV conditions to analyze STE

Analysis of sterigmatocystin by Agilent HPLCHPLC: Agilent 1100 SeriesColumn: Lichrospher 100 RP-18(e) (4.0 mm (i.d.)×250 mm)Column temperature: 25 °CDetector: photodiode array detector, wavelength 330 nmInjection volume: 20 μlMobile phase: A solution was methanol–water (52:48), and B solution wasmethanol–water (90+10). Condition; 52% of methanol till 12 min., gradientfrom 52% of methanol to 90% till 20 min., 90% of methanol till 25 min.,gradient from 90% of methanol to 52% till 26 min. and 40% methanol till40 min.

Flow rate: 0.5 ml/minSample was dissolved in 65% aqueous methanol.

64 K. Tanaka et al. / International Journal of Food Microbiology 119 (2007) 59–66

(Evaluation of certain mycotoxins, 2002). Desjardins et al.(2000) reported that trichothecenes such as DON, Fus.-X andNIV were not detected in Nepalese rice. Al-Julaifi and Al-Falih (2001) reported that they could not detect trichothe-cenes (DON+NIV+Fus.-X+diacetoxyscirpenol +neosola-niol+HT-2 toxin+and T-2 toxin) in rice during 1997–2000in Saudi Arabia. Suprasert (2000) reported that rice inThailand was contaminated with DON but at acceptablelevels compared with the 1 ppm limit set in the USA. Abbaset al. (2000) reported detection of DON and zearalenone onrice in the southern United States. Fusarium toxin analysis ofrice marketed in an area of southwest Germany and detectedDON and 3-Ac-DON, but not Fus.-X or NIV (Schollenbergeret al., 1999). DON and NIV contamination in rice wasrecently reported by Yoshizawa and Tanaka (unpublisheddata). As far as we know, Fus.-X contamination of rice hasnot previously been reported. Although the trichothecenesDON, Fus.-X, and NIV were detected in the water-damagedrice, we should point out that the rice analyzed in this study isnot representative of the quality of rice that is currentlydistributed in Japan.

1.2. Sterigmatocystin determination

STE is a carcinogenic mycotoxin produced by Aspergillusversicolor and some other fungi. STE contamination of ricewas studied in our laboratory in 1973.Many analytical methodshave been reported, but some of them are rather old. Therefore,our laboratory again studied STE analytical methods. A GC-

Table 3MS /MS conditions to analyze STE

Ionization: ESI(+)Cone Voltage: 90–130 V, Desolvation temp : 600 °C, Collision energy : 47–53 V

Monitoring ion: STE 325(M+H) /281

MS system, an LC-MS system, an LC-MS/MS system, and anHPLC system (Agilent) were studied.

GC/MS conditions were measured using a HP (nowAgilent) 6890N GC-MS series. A HP 6890N series was usedas a gas chromatograph and MS 5973 was used as a masschromatograph. A 30 m×0.25 mm i.d. HP-5MS column (J &W Scientific, Folson, CA, USA) with film thickness of0.25 μm was used. The column temperature was maintained at50 °C for 1 min, then increased by 30.0 °C/min to 300 °C, andmaintained at 300 °C for 5 min. The injection port temperaturewas set at 250 °C with an interface temperature of 310 °C. Theflow rate of He gas was 53.7 ml/min. Acetone solution of STEwas injected into GC-MS and analyzed. TIC and MS spectrumwere shown in Fig. 1. Calibration curve was shown in Fig. 2.Linearity was obtained within 10–40 ng. Detection limit was10 ng.

LC-MS analysis was made by Shimadzu LC-MS 2010A.The conditions were shown in Table 2. Four points 0 ng/2 μlmethanol solution of STE was injected and analyzed. Resultswere shown in Fig. 3. Small amount less than 4.0 ng of STE wasnot detectable. Sensitivity was not so high.

For the confirmation of STE, tandem mass spectrometry ABI4000QTrap (Applied Biosystems, USA) was used. STEmethanolsolution was injected directly into MS/MS and the mass spectrawere analyzed. MS/MS conditions were listed in Table 3. Resultswere shown in Fig. 4. These results were obtained when 0.40 ng/10 μl of methanol solution of STE was analyzed. Small amountless than 0.40 ng of STE was not detectable. Sensitivity ofdetections was not so high.

STE were analyzed by LC-UV. LC-UV conditions werelisted in Table 4. Zero point 2 ng of STE was detected withDAD detector. Comparing GC-MS analysis, LC-MS analysis,MS/MS analysis and LC-UV analysis, LC-UV analysis wasmost sensitive to detect STE.

Some extractions were also studied. Brown rice wasground, and the ground rice was extracted with acetonitrile-water (85+15). MycoSep #226 column and Autoprep MF-A1000 column are used to clean up aflatoxins (AFS). Thesecolumns were applied to clean up STE. When 2 ng/μl of STEwas applied on to these columns, recovery of STE in the caseof MycoSep #226 was 72% and one in the case of Autoprep

Table 5Risk management of mycotoxins on various agricultural commodities in Japan in 2005

Mycotoxins Agriculturalcommodity

Initial work Investigation and determination of draft of measurementsconcerning risk management

Execution ofmeasurementof riskmanagement

Verification andsurveillanceof validityof leftcolumn(includingrevision)

Note

Collectionof dataandanalysis

Preparationof riskprofile

Preliminarystudy

Researchon actualconditions

Investigationof draftof measurementsconcerning riskmanagement

Developmentof riskreduction skill

Request forriskassessment

Determinationof measurementof riskmanagement

Deoxynivalenol Wheat 3⁎ 2⁎ – 3⁎ 4⁎ 3⁎ 1⁎ 3⁎ 3⁎ 2⁎ Tentative tolerance limit(1.1 ppm in May, 2002)

Barley 3⁎ 2⁎ – 3⁎ 3⁎ 1⁎

Rice 3⁎ 2⁎ 4⁎(MHW⁎1)Nivalenol Wheat 3⁎ 2⁎ – 3⁎ 1⁎ Toxicological

experiments is beingperformed in MHW

Barley 3⁎ 2⁎ – 3⁎ 1⁎

Rice 3⁎ 2⁎ 4⁎(MHW⁎1) 3⁎

Patulin Apple(apple juice)

3⁎ 2⁎ 4⁎ 3⁎ 2⁎ 3⁎ 4⁎ Standard value underFood Sanitation Law(0.050 ppm/December,2003)

Aflatoxin B1,B2, G1, G2

Rice 3⁎ 2⁎ – 3⁎(MHW⁎1)Others(note)

3⁎ 2⁎ – 3⁎(MHW⁎1) Buckwheat, corn,peanut, sesame oil(including importedone)

Ochratoxin A Rice 3⁎ 2⁎ – 3⁎

Wheat 3⁎ 2⁎ 4⁎ 3⁎

Others(note)

3⁎ 2⁎ 3⁎(MHW⁎1) Buckwheat, corn,raisin, coffee, beer,wine, oatmeal (includingimported one)

Zealalenone Rice 3⁎ 2⁎ 3⁎

Wheat 3⁎ 2⁎ 3⁎

Fumonisin Rice 3⁎ 2⁎ – 3⁎(MHW⁎1)Wheat andbarley

3⁎ 2⁎ – 3⁎(MHW⁎1)

T-2 toxin(HT-2 toxin)

Rice 3⁎ 2⁎ 4⁎

Wheat 3⁎ 2⁎ 3⁎

Sterigmatocystin Rice 3⁎ 2⁎ 4⁎

Citrinin Rice 3⁎ 2⁎ 4⁎

Othermycotoxins

Rice 3⁎ 2⁎

Wheat andbarley

3⁎ 2⁎

Others 3⁎ 2⁎

4⁎: Completed work in the past, 3⁎: Present operating work, 2⁎: Should be urgently operated work, 1⁎: Should be urgently investegated work, –: Non-planed work.⁎1MHW: Ministry of Health and Welfare. 65

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MF-A 1000 was 103%. Therefore, Autoprep MF-A 1000column was used to clean up STE. The cleaned-up extract wasanalyzed with an HPLC system (Agilent). Forty-eight brownrice samples harvested in 2005 were analyzed, and none ofthem were contaminated with STE. These rice samples werealso analyzed for AFS and FMS, and none of the samples werecontaminated.

1.3. Risk management of mycotoxins on various agriculturalcommodities in Japan in 2005

The Ministry of Agriculture, Forestry and Fisheries inJapan is making the appropriate Institutes develop analyticalmethods for mycotoxins and survey mycotoxins contamina-tion in rice as well as in wheat, corn, and some other cereals.Risk management of mycotoxins on various agriculturalcommodities in Japan in 2005 is listed in Table 5. Furtherdevelopment of risk management will be performed in thenear future.

Acknowledgements

Table 1 was quoted from Dr. Weidenboerner’s book(Weidenboerner, 2000). We thank him. We thank Dr. YoshikoSugita-Konishi in National Institute of Health Sciences in Japanand Dr. Masaru Manabe in Japan Soy Sauce Research Institute,who gave us the valuable information on the contamination ofmycotoxins in rice. This work was supported by a grant-in-aid(Development of Evaluation and Management Methods forSupply of Safe, Reliable and Functional Food and Farm Produce)from the Ministry of Agriculture, Forestry and Fisheries, Japan.

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