Mycotoxin Research

, Volume 29, Issue 2, pp 89–96 | Cite as

A preliminary survey on the occurrence of mycotoxigenic fungi and mycotoxins contaminating red rice at consumer level in Selangor, Malaysia

  • Nik Iskandar Putra Samsudin
  • Noorlidah Abdullah
Original Paper


Red rice is a fermented product of Monascus spp. It is widely consumed by Malaysian Chinese who believe in its pharmacological properties. The traditional method of red rice preparation disregards safety regulation and renders red rice susceptible to fungal infestation and mycotoxin contamination. A preliminary study was undertaken aiming to determine the occurrence of mycotoxigenic fungi and mycotoxins contamination on red rice at consumer level in Selangor, Malaysia. Fifty red rice samples were obtained and subjected to fungal isolation, enumeration, and identification. Citrinin, aflatoxin, and ochratoxin-A were quantitated by ELISA based on the presence of predominant causal fungi. Fungal loads of 1.4 × 104 to 2.1 × 106 CFU/g exceeded Malaysian limits. Monascus spp. as starter fungi were present in 50 samples (100 %), followed by Penicillium chrysogenum (62 %), Aspergillus niger (54 %), and Aspergillus flavus (44 %). Citrinin was present in 100 % samples (0.23–20.65 mg/kg), aflatoxin in 92 % samples (0.61–77.33 μg/kg) and Ochratoxin-A in 100 % samples (0.23–2.48 μg/kg); 100 % citrinin and 76.09 % aflatoxin exceeded Malaysian limits. The presence of mycotoxigenic fungi served as an indicator of mycotoxins contamination and might imply improper production, handling, transportation, and storage of red rice. Further confirmatory analysis (e.g., HPLC) is required to verify the mycotoxins level in red rice samples and to validate the safety status of red rice.


Monascus purpureus Citrinin Aflatoxin Ochratoxin-A Chinese red rice 


Red rice is traditionally prepared by fermenting normal rice grain with a fungal starter from the genus Monascus, notably M. purpureus, M. pilosus, or M. ruber. Red rice has been a mainstay in traditional Chinese medicine (TCM) for thousands of years and has been included by the Chinese in their daily dietary intake based on its purported medicinal properties, such as anti-hypertensive (Hsieh and Tai 2003), anti-diabetic (Shi and Pan 2010), and its ability to regulate blood circulation (Wu and Zhang 1991).

However, traditionally fermented red rice does not usually abide by the formal safety and health inspection with respect to production, transportation, or storage. This in turn might lead to microbial infestation and subsequent mycotoxin contamination. Common genera of storage contaminants, such as Aspergillus, Penicillium, and Fusarium, are always associated with mycotoxins production. Furthermore, the safety status for red rice fungal starter (Monascus spp.) has always raised concern, and much debate about its natural ability to produce citrinin (Li et al. 2003) as a result of metabolism (secondary metabolite). Citrinin (CIT) is a known naturally occurring contaminant in stored food commodities such as corn, wheat, barley, and rice (CAST 2003). Toxicity studies showed that this mycotoxin is mainly nephrotoxic (toxic to kidney) (Betina 1989). Poor and ill-supervised preparation and storage will subject the red rice to chronic and deteriorated conditions which in turn will render the red rice unsuitable for human consumption. Like other foodstuffs, red rice in storage has a high risk of contamination by detrimental microorganisms (especially fungi from the genera Aspergillus and Penicillium) which might produce hazard for human consumption and, subsequently, to human health, such as in the formation of aflatoxins (AFs) and ochratoxin-A (OTA).

In Malaysia in 2010, the state Selangor holds the largest population, at 5.4 million. Of this number, 27.8 % are Malaysian Chinese (Department of Statistics 2011). Most of the Malaysian Chinese in Selangor still adhere to their customary and traditional belief in traditional Chinese medicine (TCM) on a daily basis, including the consumption of red rice as a health supplement. With such a close proximity of the Chinese community to red rice, it is thus pivotal to increase public awareness and knowledge on what they consume as health supplements. Regretfully, at present, the authority still faces the age-old complication which is the lack of comprehensive surveys and monitoring programmes, resulting in poor documentation on the health and clinical status of red rice. Hence, in the present investigation, the objectives are two-fold; (1) to determine the occurrence of mycotoxigenic fungi, and (2) to evaluate the mycotoxins contaminating red rice marketed throughout the state of Selangor, Malaysia.

Materials and methods

Samples collection

A total of 50 red rice samples were obtained from traditional Chinese medicine shops in nine districts of Selangor, Malaysia. Samples (100 g) were collected in sterile bottles, labeled, and taken to laboratory for prompt examination. Storage conditions of samples (cold, room) were recorded.

Fungal isolation

Direct plating was employed in fungal isolation from red rice samples with Czapek Dox (CD) as the solid medium. CD agar was obtained commercially and prepared according to manufacturer’s instruction. Two grams from each of the red rice sample were sprinkled onto CD agar in triplicate and incubated at 25 °C for 7 days. At the end of incubation, fungal colonies that had appeared were recorded and re-isolated for identification.

Fungal enumeration

Dilution plating was employed in fungal enumeration from red rice samples with Dichloran Rose Bengal Chloramphenicol (DRBC) as the solid medium. DRBC agar was also obtained commercially and prepared according to the manufacturer’s instruction. Ten grams from each of the red rice sample were added to 90 mL sterile 0.1 % peptone water and homogenized for 5 min to obtain a 10−1 stock solution, from which 10−2, 10−3, and 10−4 dilutions were achieved by serial dilution, and a 0.1-mL aliquot of each dilution was spread onto DRBC agar in triplicate and incubated in the dark at 25 °C for 7 days. At the end of incubation, agar plates with 10–100 colony-forming units (CFU) were used for fungal enumeration, and results were expressed as CFU per gram (CFU/g). The isolation frequency of each genus was also calculated.

Fungal identification

Taxonomic identification of mycotoxigenic food fungi (Aspergillus, Penicillium) was carried out by means of micro- and macro-morphological observation based on published manuals: Aspergillus (Raper and Fennel 1977), Penicillium (Ramirez 1982), and Monascus (Hawksworth and Pitt 1983).

Mycotoxins analyses

Quantification of CIT, AFs, and OTA were carried out based on the presence of predominant causal fungi in red rice samples. Quantification of mycotoxins was done by enzyme-linked immuno-sorbent assay (ELISA). Prior to quantification, immuno-affinity (IA) clean-up was performed to reduce the intense red colouration of samples. ELISA kits and IA columns were obtained from RIDASCREEN® (R-Biopharm, Germany). The percentage of recovery and detection limits were provided by the manufacturer in the certification enclosed with the kits: for CIT, approximately 80 % recovery and 15 μg/kg (alumina powder) detection limit; for AFs, approximately 85 % recovery and 250 ng/kg (sepharose gel) detection limit; for OTA, approximately 100 % recovery and 250 ng/kg (sepharose gel) detection limit. Sample clean-up was according to the manufacturer’s instructions involving grinding, extraction, homogenization, filtration (Whatman No. 1 filter paper), and dilution of samples: for CIT, a 5 g sample in 12.5 mL 70 % methanol was homogenized for 3 min at 150 rpm, and diluted (1 mL in 9 mL deionised water); for AFs, a 5 g sample in 25 mL 70 % methanol was homogenized for 10 min at 150 rpm, and diluted (5 mL in 15 mL deionised water); for OTA, a 10 g sample in 20 mL 60 % acetonitrile was homogenized for 20 min at 150 rpm. The filtrate of each mycotoxin extraction was passed through respective clean-up columns at a slow rate (1 drop/s) to ensure thorough clean-up. Purified samples were subjected to ELISA quantification. Microtiter wells coated with antibodies against respective antigens (CIT, AFs, OTA) were added with 50 μL of purified samples. Enzyme conjugate, enzyme substrate (urea peroxide), and chromogen (tetramethylbenzidine) were added to complete the ELISA procedure. The stop solution added changed the solution from blue to yellow which was measured photometrically at 450 nm. Samples were covered from direct light during incubation.

Statistical analyses

Results obtained were analyzed (mean, correlation, regression, independent sample t test) by using Statistical Package for Social Sciences (SPSS v.16.0; New York, USA). Dependent variables such as mycotoxigenic fungal count and mycotoxins were reported in CFU/g, mg/kg, and μg/kg, respectively. A p value < 0.05 was accepted as significant.

Results and discussion

Red rice at consumer level in Selangor, Malaysia

The sampling region in this study were the nine (9) administrative districts in the state of Selangor, Malaysia. In Selangor, red rice is normally sold at traditional Chinese medicines shops. Sampling carried out during January–December 2009 found that these shops thrive successfully within the Malaysian Chinese community with three to ten shops operating even within a small municipal sub-district which might indicate a high demand of the rice among the said community. It was learnt that red rice is included in daily intakes by the Malaysian Chinese (to sprinkle on fried meat, chicken or pork; to use as fermentation starter for Chinese red wine; or just as colorant in soups or vegetables).

Fungal contamination of red rice

Variations in storage condition were noted during red rice sampling in Selangor. Some shops stored the rice in a bare condition without packaging and placed it inside wooden drawers alongside other herbs, while some stored the rice in packaging. Some stored the rice in a refrigerator while others only at room temperature. Some shops were equipped with air-conditioning systems while others operated in an open-air surrounding. Variations of storage condition might have impacts on the fungal contamination of red rice. Figure 1 depicts fungal contamination of red rice samples by isolation frequency. Starter fungi (Monascus spp.) were present in all 50 samples (100 %), followed by Penicillium chrysogenum (62 %), Aspergillus niger (54 %), and A. flavus (44 %). For starter fungi, M. purpureus (58 %) and M. pilosus (42 %) were identified.
Fig. 1

Fungal contaminants in red rice samples

Figure 2 depicts the fungal distribution according to storage temperatures (room and cold) and fungal load. All 50 samples (100 %) were above the permissible limit set by Malaysian Ministry of Health of not more than 5.0 × 102 CFU/g (NPCB 1999), and slightly above the limit set by the International Commission for Microbiological Specification of Foods of 102 to 105 (Elliot 1980). Fungal loads were in the range of 1.4 × 104 to 2.1 × 106 CFU/g.
Fig. 2

Fungal distribution by storage temperatures and fungal load

From all 50 samples, 100 % of fungal growth detected was from the red rice starters, Monascus spp. with relatively high additions of fungi from other genera (Aspergillus, Penicillium) as shown in Fig. 2. Being the fungal starters, Monascus spp. were on the red rice as early as the start of fermentation and remained viable upon storage irrespective of the storage conditions. Unlike a freezing temperature (−20 °C) which inhibits all normal types of microbial growth, cold temperature (4 °C) does not; it merely slows down the growth rate. As such, there should be no difference between fungal loads of both storage conditions as confirmed by independent samples t tests which gave no significant difference (p = 0.069; >0.05) between fungal counts on red rice samples stored at cold and room temperatures. In other words, storage temperatures (cold or room) did not affect the viability of Monascus spp. This finding in turn might suggest that traditional post-processing techniques of red rice (outdoor- or indoor-drying) did not eliminate resistant Monascus spores. At this point, the viability of Monascus spores is of health concern. Increased viability of the spores tends to spoil the red rice if the rice is subjected to improper storage conditions, rendering the rice as unfit for human consumption. However, a larger sample size (n > 50) should be analyzed to further establish the effect of storage temperatures on fungal growth on red rice.

High readings of fungal counts (1.4 × 104 to 2.1 × 106 CFU/g) as shown in Fig. 2 were noted from all samples. This occurrence might be attributed to poor manufacturing practice (open-air surroundings, lack of use of packaging). In 2006, Fuat and co-workers conducted a mycoflora test on several poly-herbal products from Malaysia. They found that the fungal count reading was safely within the permissible limits because of the use of air-tight packaging (Fuat et al. 2006). This finding would be true in the case of red rice samples obtained in this study, where most samples were stored in bare (unpacked) conditions and gave fungal count readings that werer well above the permissible limits.

Mycotoxigenic fungi in red rice

As shown in Fig. 1, Penicillium chrysogenum (62 %), Aspergillus niger (54 %), and A. flavus (44 %) were isolated from red rice samples. Penicilli and Aspergilli are among the most well-known food-related fungi and are always treated with caution by reason of their mycotoxigenic nature (Filternborg et al. 1996). High frequencies of these fungal contaminants in red rice samples might be attributed to their being air-borne, and readily contaminating foods in storage. Open-air surroundings of shops selling red rice and a lack in the use of packaging only served in increasing the risk of air-borne fungal contamination. Similar works with high frequencies of Aspergilli and Penicillii and subsequent mycotoxins contamination were also reported in stored cocoa beans (Sanchez-Hervas et al. 2008), maize grains (Janardhana et al. 1999), and rice grains (Reddy et al. 2009). However, according to Beuchat (2003), the presence of mycotoxigenic fungi in foods may not guarantee the presence of mycotoxin. The absence of mycotoxigenic fungi may also not guarantee absence of mycotoxin in that food, since the growth followed by the death of mycotoxigenic fungi may occur at any point before the food is analyzed. Therefore, further quantification on mycotoxins was carried out to verify their presence in red rice.

Mycotoxins in red rice

Table 1 summarizes the n, n positive, minimum, maximum, mean, and standard deviation of CIT, AFs, and OTA quantitated from 50 red rice samples.
Table 1

Summary of mycotoxins quantitation in red rice samples



n Positive



Mean ± SD



50 (50 above limit)

0.23 mg/kg

20.65 mg/kg

4.03 ± 4.62 mg/kg



46 (35 above limit)

0.61 μg/kg

77.33 μg/kg

14.72 ± 16.24 μg/kg



50 (0 above limit)

0.23 μg/kg

2.48 μg/kg

0.90 ± 0.57 μg/kg

Citrinin in red rice

In the present study, the mycotoxins quantified were compared against the level stipulated in the Malaysian Food Regulation (Food Regulation 1985) and European Union (FAO 2003). CIT quantified in this study was categorized under the ‘Other mycotoxins’ section of less than 5 μg/kg and red rice was categorised under the ‘Other foods’ section in the Malaysian Food Regulation. The highest amount of CIT was at 20.65 mg/kg, and lowest at 0.23 mg/kg. This result is also in accordance with the levels of CIT found in red rice and red rice products reported by several researchers, as tabulated in Table 2. Levels of CIT found in red rice samples obtained in the present study are shown in Fig. 3.
Table 2

Levels of citrinin in red rice and red rice products


Citrinin level


Red rice

14.3 mg / kg

Kumari et al. 2009

Red rice

15.21 μg / g

Zheng et al. 2009

Red rice

2,500 mg / kg

Eisenbrand 2006

Liquid fermentation

56 mg / L

Red rice

0.28–2,458.80 mg / kg

Liu et al. 2005

Liquid fermentation

65–480 mg / L

Wang et al. 2005

Red rice

4.2–25.1 mg / kg

Shu and Lin 2002

Red rice

0.33–0.62 mg / kg

Ma et al. 2000

Red rice

0.2–17.1 mg / kg

Sabater-Vilar et al. 1999

Red rice

0.2–140 mg / kg

Xu et al. 1999

Red rice

100 mg / kg

Blanc et al. 1995

Liquid fermentation

240 mg / L

Fig. 3

Levels of CIT in red rice samples

The presence of CIT in red rice samples obtained in the present study as shown in Fig. 3 was an almost certain occurrence since Monascus spp. that were used as starters in the fermentation have been found to produce CIT at some point during metabolism (Blanc et al. 1995). The presence of Penicillium chrysogenum as an air-borne contaminant will also add to the risk of CIT contamination since it is also a known CIT producer (Ei-Banna et al. 1987).

From Fig. 3, all red rice samples (100 %) were contaminated with CIT with the majority of samples (76 %) being contaminated with CIT at less than 5 mg/kg. Although this range was quite low, it was well above the permissible limit of mycotoxins in foods which is 5.00 μg/kg. Based on the information obtained over the counter during red rice sampling, a customer might purchase 0.2–0.5 kg of red rice for average weekly consumption. Assuming the customer consumes 0.2 kg of red rice, there is a chance that he might ingest approximately 4 mg/kg of CIT which is still far above the Malaysian permissible limit.

The relationship between fungal count (CFU/g) and CIT level was analyzed by the regression method which showed a non-linear relationship (R 2 = 0.017). This finding suggested that CIT production might be independent of fungal load and that it may have been produced during the fermentation of red rice.

CIT is a potent nephrotoxin (Betina 1989). However, to date, there has been no report indicating that CIT is the main cause for kidney cancer in human. Nevertheless, based on data collected by the National Cancer Registry, Malaysian Ministry of Health, on the number of kidney cancer incidents in Malaysia, one can clearly see that there is a different trend among the major ethnic groups in Malaysia (Zainal and Nor 2011) as shown in Fig. 4. From the figure, slight fluctuations can be seen for all major ethnic groups. However, the Malaysian Chinese ethnic group remained the highest in the number of kidney cancer incidents throughout the surveyed period. According to the National Cancer Registry report, the retrieval of cancer information is a complex process because cancer is a chronic disease. The Registry believes that there are cancer cases which have not yet been notified to the registry, and this might have contributed to the lower incidence rate in the cancer report as compared to actual cases.
Fig. 4

Kidney cancer incidence by major ethnic groups in Malaysia (2002–2007)

Generally, kidney cancer is caused by many factors such as smoking, family history of kidney cancer, obesity, and exposure to carcinogen. Being a nephrotoxin, CIT poses a high risk as carcinogen. However, since there is so far no work on CIT toxicity being carried out on human subjects, one cannot simply implicate CIT as the major factor for kidney cancer. Nevertheless, the results obtained on CIT contamination of red rice samples and data collected on the high incidence of kidney cancer among the Malaysian Chinese ethnic group might be sufficient to raise awareness among red rice consumers.

Aflatoxins in red rice

As shown in Fig. 5, AFs was present in 46 samples of red rice (92 %) with a range of 0.61–77.33 μg/kg. In 4 samples (8 %), no AFs were undetected. Of the 46 contaminated samples, 35 (70 %) were quantified with AFs exceeding the Malaysian standard at 5 μg/kg (Food Regulation 1985) and the European standard at 4 μg/kg (FAO 2003).
Fig. 5

Levels of AFs in red rice samples

From 50 samples of red rice, A. flavus was present in 22 samples (44 %) but AFs were present in 46 samples (92 %). This might due to the death of A. flavus at any point in the red rice processing, or the fungus was not able to be resuscitated on agar medium on account of too few spores, but has released the AFs on the rice nevertheless. Another possibility for the low percentage of occurrence of A. flavus as compared to the high percentage of AFs was that A. flavus was inhibited by the CIT released by the starter fungi, M. purpureus and M. pilosus. As one of the mycotoxins, CIT possesses antibiotic, bacteriostatic, antifungal, and antiprotozoal properties (Berndt 1990; Bilgrami et al. 1988; Hanika et al. 1983). It may be possible that A. flavus is among the species susceptible to the antifungal effect of CIT.

As an air-borne fungus, A. flavus might have contaminated the red rice during storage. So far, there has been no work reporting on the contamination of A. flavus and AFs on red rice, although many studies have suggested that this fungus is a major storage contaminant (Schatzmayr et al. 2006; Sales and Yoshizawa 2005; Patel et al. 1996).

Ochratoxin-A in red rice

Figure 6 depicts the OTA level in red rice samples. OTA was present in all 50 red rice samples (100 %) with a range of 0.23–2.48 μg/kg. However, all readings were within the Malaysian standard at 5 μg/kg (Food Regulation 1985) and the European standard at 3 μg/kg (FAO 2003). From 50 samples of red rice, A. niger was present in only 27 samples (54 %) but OTA was present in all samples (100 %). A similar possibility of the inhibition effect of A. flavus by CIT from Monascus spp. might also occur on A. niger and thus explains the presence of lower A. niger albeit a high contamination percentage of OTA.
Fig. 6

Levels of OTA in red rice samples

It is also noteworthy that, although all red rice samples were contaminated by OTA, none of the readings exceeded either Malaysian or European standards. Low levels of OTA quantified from red rice samples may be due to the fact that A. niger is not a major producer of OTA. OTA is originally produced by A. ochraceus, hence the name (Meri et al. 2005). Even though A. niger produces OTA, it is still considered as "Generally recognized as safe" (USFDA 1998) due to the low level of OTA production.

ELISA as a semi-quantitative analysis for mycotoxins

Enzyme-linked Immunosorbent assay (ELISA) is a convenient, rapid, and reliable immunoassay technique devised to provide an alternative to the chromatography technique (Xu et al. 2006). It has been increasingly useful for mycotoxins analyses on account of its specific antigen–antibody binding technology (Yates 1986). To date, various ppb-ranged ELISA kits, either competitive or non-competitive, have been invented, made available commercially, and widely applied in laboratories for the detection of mycotoxins. Nevertheless, the binding specificity among compounds with similar chemical conformation (cross-reactivity) remains the utmost challenge in obtaining sound and irrefutable analytical results. In the present work, CIT, AFs, and OTA were analyzed by RIDASCREEN® (R-Biopharm, Germany). In the case of AFs, the specificity of the kit (which defines cross-reactivity against corresponding mycotoxins of the same class: AFB1, AFB2, AFG1, AFG2, AFM1) is given as approximately 100 %. For OTA analysis, the specificity against OTA, OTB, OTC, and OTα is also given as approximately 100 %. However, in the case of CIT, which shares almost similar chemical conformation with the various pigments synthesized by Monascus spp. through the polyketide pathway (Barber and Staunton 1979), ELISA frequently produces results that are relatively high (Xu et al. 2006). It is henceforth suggested that red rice samples should be subjected to further confirmatory analysis.

Conclusion and recommendation

The present study demonstrates that overall fungal counts on red rice samples (1.4 × 104 to 2.1 × 106 CFU/g) were considerably above the Malaysian and European standards. CIT (0.23–20.65 mg/kg) and AFs (0.61–77.33 μg/kg) quantified have also exceeded the permissible limits set by Malaysian and European standards in 50 and 35 red rice samples, respectively, while OTA (0.23–2.48 μg/kg) did not. However, semi-quantitative analysis of ELISA requires confirmatory analyses such as high performance liquid chromatography (HPLC) or thin layer chromatography (TLC) to further verify the mycotoxins level in red rice samples. Collected data nevertheless suggest that high numbers of fungal counts, the presence of mycotoxigenic fungi, and the presence of mycotoxins in red rice might collectively pose a significant health hazard towards human consumption. Traditional production of red rice should adhere to scientific inspection and clinical regulation. Toxicity studies of CIT’s nephrotoxic effect on humans should be carried out to confirm the safety and health status of red rice.



Authors extended their gratitude and recognition to staffs at Food Science Department (UPM) and Fungal Biotechnology Unit (UM) for services and information contributed to the present work. Funding was from the University of Malaya, Malaysia: Internal Research Grant, and the Ministry of Higher Education, Malaysia: Academic Training Scheme

Conflict of interest



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Copyright information

© Society for Mycotoxin Research and Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Nik Iskandar Putra Samsudin
    • 1
  • Noorlidah Abdullah
    • 2
  1. 1.Department of Food Science, Faculty of Food Science and TechnologyUniversiti Putra MalaysiaUPM SerdangMalaysia
  2. 2.Institute of Biological Science, Faculty of ScienceUniversity of MalayaFederal Territory of Kuala LumpurMalaysia

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