Mycotoxins in grains and concentrates for ruminants

Mycotoxins in grains and concentrates for ruminants

INTRODUCTION

Mycotoxin-producing fungi thrive on animal and human feedstuffs, utilizing them as their growth medium. These fungi generate mycotoxins, which are secondary metabolites characterized by their low molecular weight and high toxicity (Zain, 2011). Grains and plant-based concentrates, in particular, serve as optimal substrates for their proliferation (Yiannikouris and Jouany, 2002).

Fungal colonization of grains can occur either before or after harvesting.

EFFECTS IN RUMINANTS

In general, animals are exposed to mycotoxin intoxication based on the type of feed they consume, whether it be grains or concentrates. Ruminants are more resistant to the toxic effects of mycotoxins compared to monogastrics, and this increased resistance is attributed to the ruminal microbiota, which degrades and inactivates these metabolites(Fink-Gremmels, 2008). Nevertheless, numerous toxic effects associated with the consumption of mycotoxin-contaminated food are still described.

Fusarium fungi are widespread and often contaminate crops during their development, especially when conditions of humidity and temperature are favorable.

Several species within this genus produce mycotoxins that can cause intoxications in both ruminants and humans, as well as other animals (Zinedine et al., 2007). The main toxins produced by this genus of fungi are fumonisins, trichothecenes, and zearalenone.

Fumonisins are of significant concern as they interfere with sphingolipid metabolism (Marasas, 1995). The most important fumonisin, fumonisin B1, has been linked to esophageal cancer in humans (EFSA, 2005). The International Agency for Research on Cancer (IARC) considers it a possible human carcinogen (Group 2B).

Among animals, fumonisins have been subject to more comprehensive investigation in swine and equines. Ruminants, notably beef cattle, seem to exhibit greater resistance to their adverse effects. Nevertheless, it is well-documented that fumonisins are minimally metabolized in the rumen, leading to hepatotoxic and nephrotoxic consequences, as well as detrimental impacts on feed intake and production in dairy cows (Smith, 2012).

Trichothecenes like deoxynivalenol (DON) and T-2 toxin undergo metabolic transformation in the rumen, resulting in the production of considerably less harmful metabolites. As a result, they are unlikely to induce substantial disruptions in ruminant animals, although it’s worth noting that the available information on this subject is limited, as highlighted by (Eriksen and Pettersson in 2004).

Zearalenone has a three-dimensional molecular configuration similar to estradiol, enabling it to occupy estradiol receptors, stimulating them and acting as an endocrine disruptor in males and females of various animal species (D’Mello et al., 1999; Haschek et al., 2002).

Meanwhile, fungal species belonging to the Aspergillus and Penicillium genera primarily proliferate during storage. Aspergillus spp. is notably recognized for its capacity to generate potent toxins such as aflatoxins and ochratoxins, as outlined by (Navale et al., 2021).

Aflatoxins exhibit hepatotoxic, immunosuppressive, mutagenic, teratogenic, and carcinogenic properties across various species, including humans, according to (Zain ,2011). Among these toxins, aflatoxin B1 stands out as the most potent naturally occurring carcinogen known, as noted by (Coppock et al., 2018).

In ruminants, the effects can range from acute to chronic, contingent on the dose and duration of exposure. Chronic intoxication is particularly concerning for public health in dairy cows, given that both aflatoxin B1 and its milk-derived metabolite, M1, are carcinogenic in humans (IARC, 1993; IARC, 2002) and also contribute to immunosuppression in nursing calves.

Ochratoxins, produced by several Penicillium species, possess nephrotoxic and immunosuppressive properties, as detailed by Perrone and Susca in 2017. Ochratoxin A, while highly potent, rarely exerts negative effects on ruminants, as it is converted into less active compounds within the rumen by protozoa, as reported by (Mobashar et al.,2010).

Table 1 provides a summary of the primary effects observed as a result of mycotoxin consumption in ruminants, based on a review by Gallo and co-authors in 2015. It underscores the relatively limited and inconclusive knowledge available on the topic.

Table 1. Key effects of mycotoxin exposure in ruminants observed in experimental or field studies (summarized from Gallo et al., 2015)

INITIATION OF CONTAMINATION AND ENVIRONMENTAL CONDITIONS FOR DEVELOPMENT

The growth of fungi and subsequent mycotoxin production is not constant but contingent on environmental factors, including humidity and temperature. Generally, elevated temperature and humidity conditions promote both fungal growth and mycotoxin production.

In this context, events associated with climate change appear to be altering patterns of mycotoxicosis outbreaks, causing them to manifest in regions where they were previously uncommon, as observed by (Tolosa et al., 2021).

The contamination of grains with fungi (and consequently mycotoxin levels) is not uniform, with some areas within batches, silos, or storage facilities showing higher contamination levels than others, forming “accumulation hotspots” according to the Food Safety Authority of Ireland in 2009. Even grains within the same batch can exhibit variation, as highlighted by(Tittlemier et al., 2022).

In the case of humid sorghum grains stored in bags, García and Santos et al. (2020)reported a beneficial effect of storage time. If storage occurs under suitable conditions, the sustained low pH over time reduces the concentration of condensed tannins (which can be potential protectors against fungal contamination in the grain but hinder ruminal fermentation) and reduces fungal contamination.

According to this study, storing grains in bags for 180 days would be optimal for enhancing ruminal fermentation of hard-to-digest grains and reducing contamination. As reported by García and Santos et al. (2022), in sorghum grain silos, the relative abundance of Fusarium decreased after 30 days of storage, and in grains with high tannin content, Aspergillus spp. decreased.

These findings open up a new perspective on the potential advantages of using grains with high tannin content to produce silage, at least in environments with a high risk of fungal contamination.

Within this framework, the following guidance is provided concerning food: the identification and measurement of mycotoxin-producing fungi and the assessment of mycotoxin levels. Armed with this data, steps can be implemented to reduce the likelihood of contamination in food meant for both human and animal consumption.

IDENTIFICATION & QUANTIFICATION

Historically, the identification and quantification of toxigenic fungi contaminating food have been carried out through isolation and morphological identification based on their phenotypic characteristics. In these methods, the developed colonies of isolated food cultures are counted and transferred to specific media for identification under a microscope based on their micro and macro-morphological characteristics according to conventional identification keys for the main fungal genera.

These methods allow the identification of isolates at the species level by amplifying and sequencing different genes (Ward et al., 2002; O’Donnell et al., 2004) or by amplification with specific primers (Nicolaisen et al., 2009; Scauflaire et al., 2012).

To determine and quantify mycotoxin concentrations in food, various immunoassay and chromatographic methods can be employed (Diaz and Smith, 2005). Chromatographic techniques such as thin-layer chromatography (TLC), high-performance liquid chromatography (HPLC), ultra-high-performance liquid chromatography (UHPLC), and liquid chromatography-mass spectrometry (LC-MS).

The latter method, LC-MS, is widely used due to its potential for evaluating large quantities of samples and simultaneously detecting various mycotoxins (Krska et al., 2008). Another methodology currently in use is a combined and integrated rapid immunochromatographic technique.

This method combines antibodies on a single membrane strip, allowing the detection of various analytes in just minutes. It requires a portable lateral flow chromatography device that enables the determination of a wide range of mycotoxin concentrations on-site.

CONTROL + PREVENTION

To control and prevent the contamination of food by toxigenic fungi and mycotoxins, it is essential to initiate management practices in the field. This encompasses considerations such as the choice of crops, crop varieties, weed control, irrigation, and crop rotation (Edwards, 2004). Given that climatic conditions are beyond control and significantly impact fungal and mycotoxin development, field-level measures may not always be entirely effective, necessitating intervention during harvesting and storage.

During harvest, grain damage should be avoided, as it predisposes to fungal contamination and mycotoxins. In storage, it may be possible to control humidity and temperature to reduce the risk of contamination (Shapira & Paster, 2004). Acidic environments and low water activity are effective ways to control and inhibit bacterial growth. However, fungi can grow under a broader range of physicochemical conditions than most bacteria.