Mycotoxins in ruminant production:Part 3: Modes of action and applied outcomes
There are a significant number of studies that demonstrate a wide range of negative and potentially costly consequences of mycotoxin exposure in ruminants.
By Cathy Bandyk, PhD, PASThe low priority often allotted to mycotoxin management in ruminant livestock production is likely due in large part to inadequate research and understanding. A limited number of studies in the 1980’s and 90’s (DiCostanzo et al., 1996) affirmed tolerance of DON at up to 21 dietary ppm for feedlot cattle, and suggested a maximum of 5 ppm zearalenone to avoid reproductive issues in heifers and cows. But there are relatively few recent studies that are directly applicable to field conditions, or that contribute to understanding of the systemic effects of various toxins and combinations. Much of the work to date has involved small sample sizes, limited replicates, and short (often very short) durations. Many focus on single toxins and few outcomes.
There are, however, a significant number of studies that demonstrate a wide range of negative and potentially costly consequences of mycotoxin exposure in ruminants.
Modes of Action. Reductions in dry matter intake have been reported in dairy cows, beef cattle, goats, and lambs exposed to dietary mycotoxins (Edington et al., 1994; Whitlow and Hagler, 2007; Gallo et al., 2015; Huang et al., 2018; Custodio et al., 2020; Wu et al., 2022). Lower intakes, combined with impaired rumen function and gut absorptive capacity (Fink-Gremmels, 2008) compromise the supply of nutrients available for production and maintenance (including immune defenses). Mycotoxin-induced damage sustained by the liver (Osweiler et al., 1993; Sulzberger et al., 2017; Jiang et al., 2021) and kidney (Custodio et al., 2020) would also be expected to limit performance and efficiency.
The negative effects of mycotoxins on ruminant immune function have been demonstrated both in vitro and in dairy cows and feeder calves. When bovine macrophages were exposed to several Penicillium mycotoxins, at levels that had previously been determined to cause 25% inhibition of cell proliferation (Oh et al., 2015), cytokine gene expression related to inflammatory and cell-mediated immune response was altered such that host resistance to intracellular pathogens was impaired. Some of the toxins tested also impacted phagocytosis, and/or ability to deal with oxidative stress.
Feeding 75 μg of AFB1 per kg DM to mid-lactation Holstein cows for just 5 days reduced red blood cell count and hemoglobin concentrations (Ogunade et al., 2016). Blood and milk from dairy cows consuming naturally-occurring aflatoxins had lowered phagocytic activity and killing capacity (Mozafari et al., 2017). And when fumonisin-contaminated corn screenings were fed to feeder calves for 31 days, lymphocyte blastogenesis and liver function were impaired (Osweiler et al., 1993).
Some mycotoxins primarily impact endocrine and exocrine functions, leading to reproductive problems and inefficiencies (Jiang et al., 2021). Zearalenone, for example, can bind to estrogen receptor sites and cause estrogenic effects; co-exposure with ochratoxin exacerbates these issues (Dogan and Dal, 2022). Some of the emerging mycotoxins have been similarly implicated (Chiminelli et al., 2022). However, the negative influences of mycotoxins on reproduction are not limited to stimulation of estrogen receptors (Yousef, 2017).
As an example, graded levels of zearalenone or zearalenone derivatives induced dose-dependent delays in maturation of bovine oocytes as well as chromatin abnormalities (Minervini et al., 2001). The authors suggested these disruptions were due to non-estrogenic impacts of toxin exposure.
Male fertility and genetic contributions can also be impacted by mycotoxins. In vitro exposure of semen to AFB1 alters viability, mitochondrial membrane potential, acrosome and DNA integrity, and fewer fertilized oocytes surviving to the four-cell stage (Komsky-Elbaz et al., 2020). Proteomic analysis further revealed differential expression of proteins associated with processes and cellular pathways involved in spermatozoa function, fertilization competence, and embryonic development. In all, the researchers identified 345 genes that were genetically altered in blastocysts exposed to the aflatoxin, indicating likely deleterious effects on offspring.
Detrimental impactts specific to the mammary gland have also been identified in dairy cows. Elevated somatic cell counts, indicative of impaired udder health, have been linked to elevated mycotoxin levels in feed (Penagos-Tabares et al., 2023). Disruptions in mammary gland homeostasis and immune defenses can be induced by several Fusarium toxins (Xu et al., 2023). These authors reported that in vitro exposure to DON, enniatin B and beauvericin induced cell death, altered paracellular permeability, and resulted in changes in gene expression related to immune function in bovine mammary epithelium.
Liquid chromatography with tandem mass spectrometry (LC-MS/MS) evaluation of milk demonstrated consequential alterations in metabolomic pathways when late-lactation Holsteins were fed mycotoxin-infected corn meal and cottonseed (Wu et al., 2022). The observed changes in key small molecule metabolites indicated significant impacts on amino acid, carbohydrate, and mammary energy metabolism.
Production-level outcomes. While there is value in understanding the metabolic impacts that mycotoxins exert on livestock, this information is only of practical importance if economically important production measures are affected.
Performance results are not consistent across the literature (perhaps due to the research issues discussed above), but a summary of 50 ruminant animal experiments and field trials showed at least one negative response in 80% of the reports (Gallo et al., 2015).
Milk yield and components have been tracked relative to mycotoxin exposure in numerous studies. Aflatoxin added to the diet of limit-fed Holsteins in late lactation reduced milk fat yield from 1.63 to 1.47 lb/hd/day, and milk protein yield from 1.43 to 1.36 lb/hd/day (Queiroz et al., 2012). Milk yield, milk fat, and milk protein were all reduced, dependent on toxin feeding rate and combinations, in late lactation cows receiving moldy feeds (Wu et al., 2022). And Ogunade et al. (2016) reported milk yield of 57.2 lb/day for cows fed AFB1 vs. 62.7 lb (P = 0.08) for the control group. FCM yield also tended to be lower when the aflatoxin was added to the diet.
Mycotoxin exposure has reduced both weight gains and feed efficiency in growing and finishing ruminants. When aflatoxin was added to the diet of growing lambs at 2.5 ppm, dry matter intake decreased by 46%, and daily gains dropped from 1.14 to 0.33 lb. The gain:feed ratio went from 0.13 to 0.07 (Edrington et al., 1994). The addition of exogenous mycotoxin contamination to the diet of Nellore bulls being finished in drylot reduced daily gains from 3.76 to 3.45 lb; at the end of the 97-day feeding period, the control animals were 32 lb heavier. The bulls consuming the additional mycotoxins also had reduced dressing percent, leading to a 30.8 lb difference in hot carcass weight (Custodio et al., 2020). Karls et al. (2020) evaluated performance of growing and finishing steers fed diets naturally contaminated with mycotoxins, including relatively high levels of DON and ZER, with or without a commercial binder. Without a negative control, the differences seen between the two treatment groups represents the minimum effect being exerted by the toxins. Gains during the growing phase were 2.97 lb/day with the binder vs 2.77 without. During the finishing phase, gains averaged 4.55 lb/day with the binder vs 4.18 without. Dry matter intake was similar on the finishing diet, suggesting the greater performance was due to improved feed use efficiency. In fact, finish phase F:G was 6.25 vs 6.83 (P=o.o6) with and without mycotoxin remediation.
A recent review of the reproductive impacts of ZEN on dairy cows (Dogan and Dal, 2022) summarized negative outcomes that have been reported with ZEN exposure: infertility, early embryonic loss, abortions, hyperestrogenism in heifers, and suppression of key hormones. Resulting failure or delay in getting cows rebred represents a significant cost to both dairy and beef cow/calf producers.
A growing body of research, combined with increased consideration of mycotoxins when troubleshooting on-farm issues, is painting a clearer picture of the losses attributable to mycotoxins, as well as the biologic explanations behind them. The logical response has been development of a range of products developed as mycotoxin management or remediation tools. The final article in this series will review available options.
References available upon request.
Part 3 of a 4 part series. The final article in this series will review available mitigation strategies.
