1Department of Food Engineering, School of Animal Science and Food Engineering, University of São Paulo, Pirassununga, Brazil;
2Department of Animal Science Engineering, College of Agriculture Luiz de Queiroz of University of Sao Paulo, Piracicaba, Brazil;
3Department of Food Science, Faculty of Food Engineering, State University of Campinas, Campinas, Brazil
This study aimed to assess the aflatoxin M1 (AFM1) levels in 72 samples of yogurt from eight processing plants in São Paulo, Brazil, and the ability of heat-killed cells of Saccharomyces cerevisiae (1010 yeast cells/g) to reduce AFM1 (0.5 µg/kg) in experimental yogurts (n = 3). Analyses were conducted by high performance liquid chromatography (HPLC). Only seven samples (9.8%) had AFM1 at a mean level of 0.071 ± 0.08 µg/kg. S. cerevisiae efficiently reduced (P < 0.05) the AFM1 levels in spiked yogurts, with a maximum reduction of 46% after 30 days of storage. Further studies should investigate potential effects of S. cerevisiae on the sensory properties of yogurts.
Key words: AFM1, decontamination, Saccharomyces cerevisiae, yeasts, yogurts
Correspondence Author: Carlos A. F. Oliveira. Av. Duque de Caxias Norte 225, Campus USP, Pirassununga, SP, Brazil, CEP 13635-900. Email: [email protected]
Received: 10 November 2021; Accepted: 30 January 2022; Published: 19 February 2022
© 2022 Codon Publications
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0). License (http://creativecommons.org/licenses/by-nc-sa/4.0/)
Aflatoxins are the most known and vastly distributed mycotoxins in food and feed products, being synthesized by fungi species from the genus Aspergillus, especially A. flavus, A. parasiticus, and A. nomius (Wochner et al., 2018). Although more than 20 types of aflatoxin have been identified, aflatoxin B1 (AFB1) is accounted as the main toxic metabolite produced by fungi in naturally contaminated cereals and other food products, as well as in animal feed. AFB1 is classified as a Group 1 carcinogen by the International Agency for Research on Cancer (2002). Feeding dairy cows with any ingredient contaminated with AFB1 can result in the further conversion of the parent composite into aflatoxin M1 (AFM1), which is excreted in urine and milk (Gonçalves et al., 2015). In milk, AFM1 is associated with casein, which persists bound to the toxin during the production of dairy products, including powdered milk, cheese, and yogurt (Campagnollo et al., 2016; Kuharic et al., 2018; Makhdoumi et al., 2021). Besides, AFM1 in milk or dairy products cannot be completely removed by regular heat treatments, like pasteurization or sterilization (Assaf et al., 2019; Campagnollo et al., 2016; Muaz et al., 2021; Ondiek et al., 2022). However, previous studies indicate that AFM1 levels in milk can be reduced by the addition of yeast cells of Saccharomyces cerevisiae, in view of the ability of this yeast species to absorb and/or inactivate AFM1 (Corassin et al., 2013).
S. cerevisiae is one of the most important yeasts used in the food industry, also being considered a GRAS (“generally recognized as safe”) organism (Van der Hoek et al., 2019). Thus, a biological approach for reducing aflatoxin based on S. cerevisiae strains that are already used in food products is an attractive alternative to reduce the AFM1 levels in yogurt and other fermented dairy products. The incorporation of nonviable cells of S. cerevisiae in Minas Frescal cheese, alone or in combination with lactic acid bacteria, resulted in up to 100% reduction of AFM1 in this type of cheese after 20 days of storage (Gonçalves et al., 2020). Furthermore, some yeast species have probiotic properties, including resistance to the acidified medium of stomach and ability to improve the gut microbiota (Souza et al., 2021). S. boulardii and Pichia kudriavzevii have been added to beverages (Paula et al., 2019) and cereal-based fermented foods (Greppi et al., 2017), respectively, to provide beneficial effects to the human host, thus opening new perspectives for the development of innovative yeast-based functional food products.
Milk and dairy products are essential segments of the human diet, being largely consumed by people of different age groups, especially the elderly and children (Campagnollo et al., 2016). Therefore, the occurrence of AFM1 in milk and milk products represents a notable hazard to human health (Gonçalves et al., 2020; Souza et al., 2020; Sumon et al., 2021). In this context, several studies revealed that human exposure to the aflatoxins may be increased through consumption of AFM1-contaminated milk and dairy products (Campagnollo et al., 2016; Gonçalves et al., 2021; Hassan and Kassaify, 2014; Makhdoumi et al., 2021; Womack et al., 2016). In Brazil, some studies regarding the occurrence of AFM1 showed high incidence of contaminated samples, ranging from 63 to 100%, and levels ranging from 0.0002 to 0.106 µg/L among different yogurt and other milk products (Gonçalves et al., 2021; Iha et al., 2011; Picinin et al., 2013). Despite these limited occurrence data, there is no information on the frequency and levels of AFM1 in yogurt collected directly from Brazilian dairy producers.
Yogurt is obtained by natural fermentation of whole or standardized milk with Lactobacillus delbruecki subsp. bulgaricus and Streptococcus thermophilus (Cruz et al., 2013). In addition, yogurt is one of the most consumed fermented milks in Brazil (Iha et al., 2011), and it is also an excellent vehicle for delivering probiotics (Cruz et al., 2013) and prebiotics (Muaz et al., 2021). Therefore, it can be hypothesized that the addition of yeasts in the manufacture of yogurts may reduce the AFM1 levels in the contaminated product. This is in accordance with the need for safe and practical decontamination methods that are acceptable to consumers and can be applied during biotechnological processes of fermented foods such as yogurts (Piotrowska et al., 2021). However, the addition of S. cerevisiae cells into yogurts to decontaminate AFM1 in the final product has never been explored. In this context, the present study aimed to determine the occurrence of AFM1 in yogurt samples collected from eight different dairy processing plants in São Paulo state, Brazil, and to evaluate the ability of S. cerevisiae to reduce the AFM1 levels in spiked yogurt with or without the addition of yeast.
Sampling procedures were carried out in eight yogurt processing plants located in the northeastern region of the state of São Paulo, Brazil. A total of 72 yogurt samples were collected (n = 9, for each plant). In each factory, nine batches of yogurt production were sampled, totaling 72 batches of yogurt evaluated in the study. All collected samples were transported to the laboratory in a thermal box with dry ice and stored at 4°C until AFM1 determination analysis.
Twelve yogurt samples (1-L bottles) from the same lot and the same manufacturer were purchased from a local supermarket and used to evaluate the ability of S. cerevisiae to reduce AFM1 in the product. All yogurt samples were formerly analyzed and considered free of AFM1 (below the detection limit of the analytical method: 0.017 μg/kg). Each yogurt sample was assigned to one treatment in a completely randomized study using a factorial arrangement of 2 × 2, corresponding to two levels of S. cerevisiae (0 and 1010 yeast cells/kg yogurt) and two levels of AFM1 (0 and 0.5 μg/kg yogurt), totaling four treatments with three repetitions per treatment. The two levels of S. cerevisiae (0 and 1010 yeast cells/kg yogurt) were selected based on previous studies on the application of this yeast for AFM1 decontamination in milk (Corassin et al., 2013) and cheese (Gonçalves et al., 2021).
The S. cerevisiae strain (categorized as a GRAS organism) used for incorporation into the yogurts was a commercially available brewer’s biological dry yeast (Fermentis K-97, SafAle, Bruggeman, Belgium) containing 1.0 × 1010 cells/g. Prior to the addition to yogurts, the cells of S. cerevisiae were submitted for inactivation in an autoclave at 121°C for 10 min, to avoid any effect on the fermentation of yogurt. The AFM1 used (Sigma-Aldrich, USA) was previously diluted in acetonitrile at 0.5 µg/mL. An aliquot of 0.5 mL of this solution was evaporated in a flask under nitrogen flow, then 0.5 kg of yogurt and 0.5 g of the heat-killed yeast cells biomass were added in the flask and mixed thoroughly for 15 min, to obtain the required levels of AFM1 and yeast in the prepared yogurts. The prepared yogurts were stored at 4°C for 30 days, and samples were collected immediately and after preparation (day 0) and at 10-day intervals.
AFM1 was extracted and purified from all yogurt samples (collected in dairy plants and artificially spiked with AFM1 and/or yeast cell biomass) using immunoaffinity columns (Aflatest WB, Vicam, Watertown, MA, USA), exactly as described by Jager et al. (2013). Final extracts from yogurt samples were injected (20 µL) into a Shimadzu 10VP liquid chromatograph (Kyoto, Japan), equipped with a 10 AXL fluorescence detector (excitation at 360 nm and emission above 440 nm). The chromatographic run was achieved using a Kinetex C18 column (Phenomenex, Torrance, CA, USA) 4.6 × 150 mm, 2.6 μm particle size, and the isocratic mobile phase consisted of methanol/water/acetonitrile (61.4:28.1:10.5, v/v/v) with a flow rate of 0.50 mL/min.
Five-point calibration curves containing AFM1 at levels from 0.1 to 1.0 μg/L were prepared using AFM1 standard prepared in acetonitrile. Integrated peak areas were linearly correlated with the concentrations. Identification of AFM1 was achieved by comparing the retention time of AFM1 peaks in the samples with the standards in the calibration curves. The limits of detection (LOD) and limits of quantification (LOQ) were calculated at a signal-to-noise ratio of 3 and 10, respectively, being 0.017 and 0.055 μg/kg, respectively. The analytical method was previously validated with contaminated yogurt samples at levels of 0.2 and 0.5 μg/kg (n = 3, for each concentration), which resulted in AFM1 recovery rates in yogurt samples ranging from 72 to 93% (Jager et al., 2013).
The pH was determined in yogurt samples artificially spiked with AFM1 and/or yeast cell biomass as described by AOAC (2019).
The General Linear Model of SAS (2004) was approached as the statistical analysis of AFM1 binding assays, while a level of P < 0.05 was considered as significant.
AFM1 was detected in seven samples (9.8 %) of yogurt manufactured in dairy plants at São Paulo state, with a range of 0.017 to 0.130 µg/kg (Table 1). While no regulation for the levels of AFM1 in yogurt was established in Brazil, none of the analyzed samples presented levels higher than the Brazilian limit for milk (0.50 µg/L) (ANVISA, 2011). As AFM1 is frequent in dairy foods produced worldwide, many countries proposed some regulatory limits for AFM1 in milk and dairy products, with limits varying from 0.05 to 0.5 µg/kg (Iha et al., 2011). Studies have described the occurrence of AFM1 in yogurt worldwide, although the frequency is high; in most studies, the reported levels of AFM1 were considered low (Muaz et al., 2021; Souza et al., 2020).
Table 1. Aflatoxin M1 (AFM1) levels in yogurt manufactured in dairy plants at São Paulo, Brazil.
|Range of AFM1 level (µg/kg)||Number of samples||%|
aLOD: Limit of detection (0.017 μg/kg).
The number of the contaminated samples (n = 7) and the mean level of AFM1 (0.051 ± 0.13 µg/kg) reported in the present study were similar to those reported by Cano-Sancho et al. (2010), who evaluated the occurrence of AFM1 in 72 samples of yogurt marketed in Spain and detected a low incidence of AFM1, 2.8% (n = 2), and low levels of AFM1, ranging from 0.04 to 0.052 µg/kg. However, in Iran, Fallah (2010) and Nilchian and Rahumi (2012) reported a higher incidence of AFM1 in yogurt, about 66.1% (n = 45) and 35% (n = 14), respectively. However, both studies reported ranges for AFM1 of 0.015 to 0.119 µg/kg, and 0.011 to 0.116 µg/kg, respectively. Analogous to Iran, in Pakistan, Iqbal et al. (2013) reported a higher incidence of AFM1, 33.3% (n = 32), than in the present study and low levels of AFM1 (0.019 to 0.053 µg/kg) in the evaluated yogurt samples. In Turkey, as well as in Pakistan, Ertas et al. (2011) and Kocasari et al. (2012) reported a high incidence of AFM1 in the samples, 56% (n = 28) and 44.4% (n = 20), and low levels of AFM1 0.002 µg/kg at 0.078 and 0.05 to 0.36 µg/kg, respectively. In Qatar, Hassan et al. (2018), despite reporting a high incidence of 76% (n = 16), the levels of AFM1 detected in the yogurt samples were less than 0.05 µg/L.
Several reports indicate that the occurrence of AFM1 in milk and dairy products strongly depended on several factors, including lactation stage, feed quality, season/climate, animal breed, and milk production performance beside the used technique for AFM1 assessment (Hassan et al., 2018; Iqbal et al., 2017; Makhdoumi et al., 2021; Shahbazi et al., 2017). Considering the findings from studies conducted in Spain, Iran, Pakistan, Turkey, Qatar, and Brazil, the incidences of AFM1 in yogurt are greater than that noted in the present study (Makhdoumi et al., 2021; Muaz et al., 2021; Souza et al., 2020; Sumon et al., 2021). However, the levels in the aforementioned studies were overall low, similar to our data, thus indicating low exposure to AFM1 through intake of these products. Although in our study a limited number of samples was screened, the results indicate that milk received for the manufacture of yogurt in the dairy plants evaluated have low incidence and levels of AFM1. These findings stress the need for control measures to avoid fungi growth and AFB1 formation in dairy farms to prevent milk contamination with AFM1 (Gonçalves et al., 2017). Good agricultural practices, which include the use of pest-resistant crops, proper cultivation practices, proper use of fertilizers, irrigation, and crop rotation, are essential tools to prevent and control mycotoxins in dairy farms (Gonçalves et al., 2015).
The pH of the yogurt, stored at 4°C, was not affected (P > 0.05) by using S. cerevisiae in any of the evaluated treatments, during the entire period (from days 0 to 30) of the study (Table 2).
Table 2. pH values of yogurts prepared with or without the addition of heat-killed cells of yeast and aflatoxin M1 during 30 days of storage.
|Yeasta (cells/kg)||AFM1 (µg/kg)||pH|
|Day 0||Day 10||Day 20||Day 30||Meanb|
|0||0||4.01||4.14||4.03||4.05||4.06 ± 0.06|
|1010||0||4.35||4.34||4.28||4.3||4.32 ± 0.03|
|0||0.5||4.03||4.01||3.95||3.99||4.00 ± 0.03|
|1010||0.5||4.92||4.34||4.19||4.24||4.42 ± 0.34|
aCommercially available brewer’s biological dry yeast (Fermentis K-97, SafAle, Bruggeman, Belgium) containing 1.0 × 1010 yeast cells/g.
bValues were expressed as mean ± standard deviation of samples analyzed in triplicate.
No significant differences were found between means in rows or columns (P > 0.05).
As expected, AFM1 concentrations in nonspiked yogurts were below the LOD of the analytical method (0.017 μg/kg). The mean levels of AFM1 in spiked yogurts ranged from 0.27 ± 0.03 to 0.50 ± 0,01 µg AFM1/kg during 30 days of storage (Table 3). In our study, in the treatment without S. cerevisiae, a percentage reduction of 10% in AFM1 after 30 days was noted, which can be associated with the natural function of lactic acid bacteria in raw and pasteurized milk used in the processing of yogurt (Franciosi et al., 2009). Another explanation for the observed reduction in AFM1 can be correlated with the low pH value. Corroborating with our study, Govaris et al. (2002) reported the stability of AFM1 in yogurt artificially contaminated with concentrations of 0.05 and 0.1 µg/L, during storage for 4 weeks, at 4°C, at two pH levels (4.0 and 4.6). Their findings demonstrated that at a pH of 4.6, no significant change in AFM1 levels was observed. However, AFM1 showed a significant decrease after the third and fourth weeks of storage. The authors quoted that the reduction of AFM1 could be a function of the low pH.
Table 3. Mean aflatoxin M1 (AFM1) levels and percentage reductions (R) in spiked yogurts prepared with or without heat-killed cells of yeast during 30 days of storage.
|Aflatoxin M1 in yogurt during storage|
|Day 0||Day 10||Day 20||Day 30|
|% (R)c||Mean level (µg/kg)||% (R)||Mean level (µg/kg)||% (R)||Mean level (µg/kg)||% (R)|
|0||0.5||0.50 ± 0.01||0.0||0.49 ± 0.03||2.0||0.48 ± 0.02||4.0||0.45 ± 0.01||10.0|
|1010||0.5||0.46 ± 0.01||8.0||0.38 ± 0.01||24.0||0.32 ± 0.01||36.0||0.27 ± 0.03||46.0|
aCommercially available brewer’s biological dry yeast (Fermentis K-97, SafAle, Bruggeman, Belgium) containing 1.0 × 1010 yeast cells/g.
bValues are expressed as mean ± SD of samples analyzed in triplicate.
cCumulative reduction percentages of AFM1 in relation to the initial concentration of AFM1 in spiked yogurts.
dLOD: Limit of detection (0.017 μg/kg).
The effect of S. cerevisiae in reducing AFM1 was highlighted by the findings of our study. There was an 8% reduction in AFM1 in yogurt on day 0, followed by an increase in reduction on day 10 (24%), continuing the reduction on day 20 (36%), and at day 30, the percentage of AFM1 decreased, reaching a reduction of 46%. There is only one previous study that assessed the effect of S. cerevisiae on the removal of aflatoxin M1 in yogurt. In a similar study to ours, Karazhiyan et al. (2016) reported AFM1 reduction percentages much higher than ours, when they evaluated the ability of S. cerevisiae (viable, treated with acid, heat, and ultrasound) to bind to AFM1 in yogurt over time (days 1, 7, 14, and 21 after manufacture). Among the treated yeasts, the one with the highest binding capacity to AFM1 was treated with acid (76.46%). Yeasts treated with heat (76.39%) and ultrasound (74.20%) also showed high percentages of reduction. An important advantage of using S. cerevisiae as the AFM1 binder in yogurts is the overall acceptance of this yeast without restrictions in the food industry, considering its classification as a GRAS organism (Van der Hoek et al., 2019). Besides, the low costs of adding S. cerevisiae biomass in yogurts provide a viable alternative to the dairy industry to reduce the AFM1 contamination in the product during the storage period. In this regard, further investigations are recommended to evaluate the involved mechanisms in the process of mycotoxin reduction by S. cerevisiae. In addition, the associated factors with the stability of the sequestration of toxins, such as the concentration of yeasts, acidity, and type of initial culture, should be considered (Karazhiyan et al., 2016).
The limited survey performed in the present study indicates that milk received for the manufacture of yogurt in the dairy plants evaluated have low incidence (9.8%) and levels (mean: 0.071 ± 0.08 µg/kg) of AFM1. The addition of S. cerevisiae biomass in yogurts containing 0.5 µg/kg of AFM1 reduced its concentration to 0.27 µg/kg after 30 days of storage, thus providing a 46% decrease of AFM1 in the period. Results of this trial indicate that the incorporation of S. cerevisiae could efficiently decrease the AFM1 levels in yogurt. Further studies are required to examine the involved mechanisms in the process of aflatoxin reduction by S. cerevisiae. In addition, the associated factors with the stability of the sequestration of toxins, such as the concentration of yeasts, acidity, and type of initial culture, should be considered.
This research was funded by São Paulo Research of Foundation, FAPESP (grant number 2017/20081-6), by the Brazilian National Council for Scientific and Technological Development, CNPq (Grant # 302195/2018-1), and by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) – Finance Code 001.
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