Elsevier

Food Chemistry

Volume 312, 15 May 2020, 126034
Food Chemistry

Mycotoxins in maize harvested in Republic of Serbia in the period 2012–2015. Part 1: Regulated mycotoxins and its derivatives

https://doi.org/10.1016/j.foodchem.2019.126034Get rights and content

Highlights

  • LC–MS/MS was applied for analysis of maize samples from Northern Serbia (2012–2015).

  • Weather conditions had significant effect on the occurrence of 20 mycotoxins.

  • AFs were the most dominant in maize samples collected from very hot and dry years.

  • DON, ZEA and its derivatives occurred with high prevalence in samples from 2014.

  • FUMs were detected with very high prevalence (76%–100%) in samples from each year.

Abstract

The main objective of this study was to apply a liquid chromatography–tandem mass spectrometric method to investigate the presence of 20 mycotoxins in 204 maize samples harvested in Northern Serbia in the period 2012–2015, including seasons with extreme drought (2012), hot and dry conditions (2013 and 2015) and extreme precipitation (2014). Between 2 and 20 mycotoxins contaminated examined samples. In samples collected from each year, all of six examined fumonisins were detected with very high prevalence (from 76% to 100%). Aflatoxin B1 was detected in 94% and 90% maize samples from 2012 and 2015, respectively. In samples from year 2014, deoxynivalenol, zearalenone and its derivatives were detected in 100% of samples. Furthermore, ochratoxin A (25%) was the most predominant in samples from 2012. The obtained results indicate that changes in weather conditions, recorded in the period of four years, had significant influence on the occurrence of examined mycotoxins in maize.

Introduction

Maize represents one of the most widely used staple food and feed ingredients in the world. It is well known that consumption of maize provides significant amounts of nutrients, vitamins and minerals, and also frequent consumption of maize may have several health benefits on human and animal organism. In Republic of Serbia, maize is mostly used for animal feeding (80%), while the remaining amount is mainly intended for human consumption and food industry. About 40% of total planted area of field crops in Serbia is covered with maize; while around 70% of the total maize production in Serbia is located Northern Serbia. With the approximate amount of 6.5 million tons per year, Serbia is one of the largest maize producers in Europe. The overall amount of produced maize in Serbia is higher than domestic consumption; therefore a considerable fraction of produced maize is exported to European Union, neighboring as well as to Mediterranean countries, with a tendency to expand the market to China and Indonesia. An annual amount of 1.5 million tons of exported maize classified Serbia among leader countries for maize exports in Europe, as well as in the whole world (Maslac, 2018). Although, in the past decade, maize represents one of the most significant agricultural product and export items of Serbia, maize yield as well as maize quality and safety highly depend on weather conditions during the maize growing season (April–September). Maslac (2018) reported that only about 7–9% of arable land in Serbia is irrigated. This fact should be considered with a great attention due to the recent increases of air temperature by 1.4 °C as well as number of tropical days for 50% during maize growing seasons in Serbia (Matović, Gregorić, & Glamočlija, 2013).

Beside influence on maize yield, weather conditions during maize growing season represent factor with the very strong influence on the occurrence of mycotoxins in maize. Mycotoxins are secondary metabolites which are very often produced by toxigenic fungi in response to stress caused by environmental extremes (Medina, Rodríguez, & Magan, 2015). Furthermore, besides weather conditions, fungal infection and subsequent synthesis of mycotoxins also depend on agronomic factors (type of hybrid, soil, tillage, and previous crop), biological factors (susceptible crops), storage conditions (temperature, humidity, handling, presence of insects, rodents and birds), as well as storage time (Pepeljnjak & Šegvć, 2004). More than 400 mycotoxins are currently identified worldwide, but the most important groups of mycotoxins that are of major health concern for humans and animals are: aflatoxins (AFs), ochratoxin A (OTA), deoxynivalenol (DON), zearalenone (ZEA) and fumonisins (FUMs); due to their teratogenic, nephrotoxic, hepatotoxic, neurotoxic, mutagenic immunosuppressive characteristics, etc. (Creppy, 2002, Eriksen and Pettersson, 2004)

The International Agency for research on Cancer classified AFs (AFB1, AFG1, AFB2, AFG2, AFM1) in the first group as human carcinogens, while fumonisin B1 (FB1) and OTA belong to the group 2B as possible carcinogenic compound to humans. Based on limited data and evidence in humans and animals, DON and ZEA are classified in group 3 (IARC, 2012).

AFs are a group of mycotoxins produced by Aspergillus (A.) species, particularly A. flavus, A. parasiticus and A. nomius. Among the approximately twenty AFs identified, five of them occur naturally and they are significant contaminants of a wide variety of food and feed: AFB1, AFB2, AFG1, AFG2, and AFM1 (Creppy, 2002). AFB1 is highly toxic, classified as the most potent naturally occurring chemical liver carcinogen known (IARC, 2012).

Ochratoxins are a group of mycotoxins that includes at least nine different compounds. OTA is the most prevalent and toxic compound of the group. Ochratoxin B (OTB) is the non-chlorinated ester of OTA, which could be transformed to OTA even though at a low level. OTA and OTB often co-exist in food raw materials, easily transforming to each other under special environment conditions (El Khoury & Atoui, 2010).

DON belongs to the type B trichothecenes and their occurrence is primarily associated with Fusarium (F.) graminearum and F. culmorum. Occurrence of those fungus and DON in cereals is characteristic for regions with lower air temperature and higher amount of precipitation. Although DON is among the least toxic of the trichothecenes, it is the most frequently detected one throughout the world, and its occurrence is considered to be an indicator of the possible presence of other, more toxic trichothecenes (Eriksen & Pettersson, 2004). DON very often co-occurs in cereals with its acetylated derivatives 3-acetyl deoxynivalenol (3-ADON) and 15-acetyl deoxynivalenol (15-ADON). In the recent years deoxynivalenol-3 glucoside (DON-3G), a so called masked form of DON is frequently detected in some cereals and cereal derived products (Maresca, 2013).

ZEA is produced by numerous Fusarium species, including F. roseum, F. tricinctum, F. sporotrichioides, F. oxysporum and F. moniliforme. In comparison to many other mycotoxins, ZEA has a lower acute toxicity. However, ZEA is a powerful estrogen, with hormonal activity exceeding that of most other naturally occurring non-steroidal oestrogens. Alpha zearalenol (α-ZOL) and beta zearalenol (β-ZOL) are reductive metabolites of ZEA, which are very often formed in plant and fungal metabolism. Whereas β-ZOL is less toxic than ZEA, α-ZOL possesses an about 10-fold higher estrogenicity than ZEA. Under microbial activity ZEA could be transformed to a zearalenone-sulfate (ZEA-S) (Zinedine, Soriano, Molto, & Manes, 2007).

So far, about sixteen different FUMs have been isolated and identified. The predominant mycotoxin is FB1, produced by F. verticillioides and F. proliferatum, followed by FB2, FB3, FB4, FA1 and FA2. FB1 is considered to be the most toxic of these compounds (Butkeraitis et al., 2004). The endophytic nature of the fumonisin-producing maize pathogen F. verticillioides, resulted in natural occurrence of FUMs in maize and maize derived products worldwide. High prevalence of FUMs in maize have been noticed in many countries all over the world (Lino, Silva, Pena, & Silveira, 2006), and this is the reason why, from the past decades until today, there is constant tendency to minimize their occurrence in maize.

Previously published studies, related to the presence of mycotoxins in maize from Serbia, were mainly restricted to investigation of presence of one or a few mycotoxins. Previous studies reported high presence of AFs (Kos et al., 2018, Kos et al., 2013), and DON (Kos et al., 2017) in Serbian maize samples. Based on these reports it could be noticed that in the recent years human population as well as livestock in Serbia were exposed to high risk of certain mycotoxins. Furthermore, considering that in the recent years Serbia was faced with climate changes, and that maize and maize derived products are consumed almost on a daily basis, the primary aim of this work was to investigate the influence of weather conditions recorded in four different years (2012–2015) on the occurrence of the following 20 fungal metabolites: aflatoxins (AFB1, AFB2, AFG1, AFG2, AFM1), ochratoxins (OTA, OTB), fumonisins (FB1, FB2, FB3, FB4, FA1, FA2), ZEA, ZEA-S, α-ZOL, β-ZOL, DON, DON-3G, and 15-ADON. To the best of author’s knowledge, this study represents the first report from Serbia, as well as from neighboring countries, related to the occurrence of all regulated mycotoxins and its derivatives in maize samples collected in four different years.

Section snippets

Samples

A total of two hundred and four (n = 204) maize samples were collected in the period of four years, 2012–2015. Every year after harvest, 51 maize samples were collected from the Northern Serbia (Autonomous Province of Vojvodina). Most commercial maize hybrids, currently grown in Northern Serbia, were included in this study. Maize samples were selected to be representative for every investigated year, which means that maize samples were systematically taken from the entire investigated area.

In

Occurrence of mycotoxins in maize samples

Results for the analysis of 20 fungal metabolites in 204 maize samples collected in the Northern Serbia in the period of four years (2012–2015) are shown in the Table 2. From the obtained results it could be noticed that significant differences exist in mycotoxins occurrence as well as in the range of determined concentrations in samples originated from different years. In the recent years, many authors indicated that weather conditions (especially air temperature and amount of precipitation)

Conclusion

Considering the findings of the present study it could be noticed that among 20 examined fungal metabolites, 20, 17, 13, and 17 were detected in maize samples collected from 2012, 2013, 2014 and 2015 years, respectively. Furthermore, the obtained results indicate that recorded differences in weather conditions in investigated period of four years had a great influence on the presence or absence of certain mycotoxins in maize. On the one hand, conditions of extreme and prolonged drought in 2012

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This paper is a result of the research conducted within Projects DS-2016-0059, “Faces of changing climate in Danube region: occurrence of mycotoxins in maize and suggesting the mitigation strategy” financed by funds of Multilateral Scientific and Technological Cooperation Projects in the Danube Region; European Union’s Horizon 2020 research and innovation program under grant agreement no. 692195 (MultiCoop); and Projects TR 31029 and III 46001 funding from the Ministry of Education, Science and

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