Dietary Mycotoxin Exposure: Emerging Risks to Human Health

A special issue of Toxins (ISSN 2072-6651). This special issue belongs to the section "Mycotoxins".

Deadline for manuscript submissions: closed (31 May 2019) | Viewed by 59162

Special Issue Editors


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Guest Editor
Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD 21205, USA
Interests: aflatoxins and mycotoxins in human health; environmental health sciences; chemical carcinogenesis; environmental carcinogenesis; chemoprevention; cancer prevention and control

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Guest Editor
Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD 21205, USA
Interests: cancer prevention; cancer biology; nutrition; environmental exposures; biomarkers; public health

Special Issue Information

Dear Colleagues,

Worldwide, the ingestion of mycotoxins from contaminated foodstuffs imposes a significant burden to human health. Some of these impacts, such as the role of aflatoxins in the etiology of liver cancer, are strongly supported by decades of basic and epidemiological evidence. While interrogation of such established relationships is warranted and continues to yield new insight, emerging risks from dietary exposure to mycotoxins have received less attention. Greater understanding of the full spectrum of their effects is necessary to target prevention efforts and improve the health of vulnerable populations.

This Special Issue of Toxins invites articles that address risks to human health presented by dietary mycotoxin exposure, with particular interest in: a) novel or emerging associations between dietary exposures and disease states; b) novel biomarkers or analytical techniques for assessment of mycotoxin exposure, metabolism, or related disease risk; c) impacts on under-represented populations; or d) novel sources of dietary exposure in populations with high rates of mycotoxin-associated disease(s).

Given the abundance of existing literature on the subject of aflatoxins and liver carcinogenesis, such papers must be sufficiently novel to obtain consideration, and will preferably address one or more of the above topics of interest. As the focus of this Special Issue is on human health, papers concerning mycology, contamination surveillance, agriculture, or other endpoints not directly related to human exposure or health outcomes are outside of the scope. Econometric research is welcome, provided the analysis specifically concerns the influence of mycotoxin exposure on human health. Experimental work in animal models is welcome, but preference will be given to studies demonstrating outcomes or mechanisms readily translatable to human health.

We look forward to reviewing original research or review articles, which will shed needed light on the myriad impacts of dietary mycotoxin exposure to human health around the world.

Prof. Dr. John D. Groopman
Dr. Joshua W. Smith
Guest Editors

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Keywords

  • Mycotoxins
  • environmental exposure
  • diet
  • toxicology
  • public health

Published Papers (9 papers)

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Research

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12 pages, 1933 KiB  
Article
Aflatoxin Exposure from Milk in Rural Kenya and the Contribution to the Risk of Liver Cancer
by Anima J. Sirma, Kohei Makita, Delia Grace Randolph, Daniel Senerwa and Johanna F. Lindahl
Toxins 2019, 11(8), 469; https://doi.org/10.3390/toxins11080469 - 10 Aug 2019
Cited by 15 | Viewed by 4623
Abstract
Milk is an important commodity in Kenya; the country has the largest dairy herd and highest per capita milk consumption in East Africa. As such, hazards in milk are of concern. Aflatoxin M1 (AFM1) is a toxic metabolite of aflatoxin [...] Read more.
Milk is an important commodity in Kenya; the country has the largest dairy herd and highest per capita milk consumption in East Africa. As such, hazards in milk are of concern. Aflatoxin M1 (AFM1) is a toxic metabolite of aflatoxin B1 (AFB1) excreted in milk by lactating animals after ingesting AFB1-contaminated feeds. This metabolite is injurious to human health, but there is little information on the risk to human health posed by AFM1 in milk in rural Kenya. To fill this gap, a quantitative risk assessment (QRA) applying probabilistic statistical tools to quantify risks was conducted. This assessed the risk of liver cancer posed by AFM1 in milk, assuming 10-fold lower carcinogenicity than AFB1. Data from four agro–ecological zones in Kenya (semi-arid, temperate, sub-humid and humid) were used. We estimated that people were exposed to between 0.3 and 1 ng AFM1 per kg body weight per day through the consumption of milk. The annual incidence rates of cancer attributed to the consumption of AFM1 in milk were 3.5 × 10−3 (95% CI: 3 × 10−3–3.9 × 10−3), 2.9 × 10−3 (95% CI: 2.5 × 10−3–3.3 × 10−3), 1.4 × 10−3 (95% CI: 1.2 × 10−3–1.5 × 10−3) and 2.7 × 10−3 (95% CI: 2.3 × 10−3–3 × 10−3) cancers per 100,000 in adult females, adult males, children 6–18 years old, and in children less than five years old, respectively. Our results show that aflatoxin exposure from milk contributes relatively little to the incidence of liver cancer. Nonetheless, risk managers should take action based on cumulative exposure from all sources of aflatoxins. Full article
(This article belongs to the Special Issue Dietary Mycotoxin Exposure: Emerging Risks to Human Health)
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9 pages, 1267 KiB  
Article
Assessing Aflatoxin Exposure Risk from Peanuts and Peanut Products Imported to Taiwan
by Keng-Wen Lien, Xin Wang, Min-Hsiung Pan and Min-Pei Ling
Toxins 2019, 11(2), 80; https://doi.org/10.3390/toxins11020080 - 01 Feb 2019
Cited by 28 | Viewed by 6112
Abstract
Aflatoxins are highly toxic and cause disease in livestock and humans. In order to assess Taiwan population exposure to aflatoxin from peanuts and peanut products, a total of 1089 samples of peanut candy, peanut butter, and peanuts etc. were collected in the period [...] Read more.
Aflatoxins are highly toxic and cause disease in livestock and humans. In order to assess Taiwan population exposure to aflatoxin from peanuts and peanut products, a total of 1089 samples of peanut candy, peanut butter, and peanuts etc. were collected in the period from 2011 to 2017 and analyzed using a liquid chromatography/tandem mass spectrometer. The overall mean contamination levels of aflatoxin in peanuts and peanut products were 2.40 μg/kg of aflatoxin B1, 0.41 μg/kg of aflatoxin B2, 0.19 μg/kg of aflatoxin G1, and 0.03 μg/kg of aflatoxin G2. We use margin of exposure (MOE) as a tool to improve food safety management. According to MOE levels of aflatoxins in peanuts and peanut products from China, Indonesia, Thailand, the United States, and the Philippines were above the safe lower limit of 10,000, indicating an absence of public health or safety risk for the majority of the population. However, products from Vietnam were under the MOE safe lower limit, suggesting that regulatory actions must be continued to avoid excessive consumer exposure. Full article
(This article belongs to the Special Issue Dietary Mycotoxin Exposure: Emerging Risks to Human Health)
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14 pages, 3019 KiB  
Article
Autophagy and Apoptosis Interact to Modulate T-2 Toxin-Induced Toxicity in Liver Cells
by Jing Wu, Yu Zhou, Zhihang Yuan, Jine Yi, Jingshu Chen, Naidong Wang and Yanan Tian
Toxins 2019, 11(1), 45; https://doi.org/10.3390/toxins11010045 - 15 Jan 2019
Cited by 50 | Viewed by 5275
Abstract
T-2 toxin is a mycotoxin generated by Fusarium species which has been shown to be highly toxic to human and animals. T-2 toxin induces apoptosis in various tissues/organs. Apoptosis and autophagy are two closely interconnected processes, which are important for maintaining physiological homeostasis [...] Read more.
T-2 toxin is a mycotoxin generated by Fusarium species which has been shown to be highly toxic to human and animals. T-2 toxin induces apoptosis in various tissues/organs. Apoptosis and autophagy are two closely interconnected processes, which are important for maintaining physiological homeostasis as well as pathogenesis. Here, for the first time, we demonstrated that T-2 toxins induce autophagy in human liver cells (L02). We demonstrated that T-2 toxin induce acidic vesicular organelles formation, concomitant with the alterations in p62/SQSTM1 and LC3-phosphatidylethanolamine conjugate (LC3-II) and the enhancement of the autophagic flux. Using mRFP-GFP-LC3 by lentiviral transduction, we showed T-2 toxin-mediated lysosomal fusion and the formation of autophagosomes in L02 cells. The formation of autophagosomes was further confirmed by transmission electron microcopy. While T-2 toxin induced both autophagy and apoptosis, autophagy appears to be a leading event in the response to T-2 toxin treatment, reflecting its protective role in cells against cellular damage. Activating autophagy by rapamycin (RAPA) inhibited apoptosis, while suppressing autophagy by chloroquine greatly enhanced the T-2 toxin-induced apoptosis, suggesting the crosstalk between autophagy and apoptosis. Taken together, these results indicate that autophagy plays a role in protecting cells from T-2 toxin-induced apoptosis suggesting that autophagy may be manipulated for the alleviation of toxic responses induced by T-2 toxin. Full article
(This article belongs to the Special Issue Dietary Mycotoxin Exposure: Emerging Risks to Human Health)
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18 pages, 1203 KiB  
Article
Occurrence and Quantitative Risk Assessment of Twelve Mycotoxins in Eggs and Chicken Tissues in China
by Lan Wang, Qiaoyan Zhang, Zheng Yan, Yanglan Tan, Runyue Zhu, Dianzhen Yu, Hua Yang and Aibo Wu
Toxins 2018, 10(11), 477; https://doi.org/10.3390/toxins10110477 - 16 Nov 2018
Cited by 36 | Viewed by 4356
Abstract
Aflatoxins (AFs), deoxynivalenols (DONs), and zearalenones (ZENs) are common mycotoxins that contaminate feedstuff, causing contamination of poultry products. In our study, these mycotoxins were quantified in 152 egg samples collected from markets in Jiangsu (JS), Zhejiang (ZJ), and Shanghai (SH) and in 70 [...] Read more.
Aflatoxins (AFs), deoxynivalenols (DONs), and zearalenones (ZENs) are common mycotoxins that contaminate feedstuff, causing contamination of poultry products. In our study, these mycotoxins were quantified in 152 egg samples collected from markets in Jiangsu (JS), Zhejiang (ZJ), and Shanghai (SH) and in 70 chicken tissue samples (liver, heart, and gizzard) from ZJ in China. The main mycotoxins observed in egg samples were DON, 15-AcDON, and ZEN, although only ZEN family mycotoxins (ZEN, α-ZEL, β-ZEL, and α-ZAL) were detected in chicken tissues. Furthermore, for the first time, we assessed the health risks of exposure of three populations (children, adults, and elder adults) to DONs (DON, 3-AcDON, and 15-AcDON) and ZEN in eggs (from three different areas) and to ZEN in chicken tissues. We show that the mean dietary intake (DI) values and the 97.5th percentile DI values of DON and ZEN through egg ingestion were lower than the provisional maximum tolerable daily intake (PMTDI) (1 μg/kg body weight (BW)/day) for the three populations in the three geographical areas studied. However, eggs contaminated with high levels of DONs and ZEN contributed to a large proportion of the PMTDI of these mycotoxins, especially in children and elder adults. Although ZEN was highly detected in the chicken tissues, no significant health risk was observed. Full article
(This article belongs to the Special Issue Dietary Mycotoxin Exposure: Emerging Risks to Human Health)
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15 pages, 290 KiB  
Article
A Risk Assessment of Aflatoxin M1 Exposure in Low and Mid-Income Dairy Consumers in Kenya
by Sara Ahlberg, Delia Grace, Gideon Kiarie, Yumi Kirino and Johanna Lindahl
Toxins 2018, 10(9), 348; https://doi.org/10.3390/toxins10090348 - 29 Aug 2018
Cited by 43 | Viewed by 5422
Abstract
Aflatoxin M1 (AFM1), a human carcinogen, is found in milk products and may have potentially severe health impacts on milk consumers. We assessed the risk of cancer and stunting as a result of AFM1 consumption in Nairobi, Kenya, using [...] Read more.
Aflatoxin M1 (AFM1), a human carcinogen, is found in milk products and may have potentially severe health impacts on milk consumers. We assessed the risk of cancer and stunting as a result of AFM1 consumption in Nairobi, Kenya, using worst case assumptions of toxicity and data from previous studies. Almost all (99.5%) milk was contaminated with AFM1. Cancer risk caused by AFM1 was lower among consumers purchasing from formal markets (0.003 cases per 100,000) than for low-income consumers (0.006 cases per 100,000) purchasing from informal markets. Overall cancer risk (0.004 cases per 100,000) from AFM1 alone was low. Stunting is multifactorial, but assuming only AFM1 consumption was the determinant, consumption of milk contaminated with AFM1 levels found in this study could contribute to 2.1% of children below three years in middle-income families, and 2.4% in low-income families, being stunted. Overall, 2.7% of children could hypothetically be stunted due to AFM1 exposure from milk. Based on our results AFM1 levels found in milk could contribute to an average of −0.340 height for age z-score reduction in growth. The exposure to AFM1 from milk is 46 ng/day on average, but children bear higher exposure of 3.5 ng/kg bodyweight (bw)/day compared to adults, at 0.8 ng/kg bw/day. Our paper shows that concern over aflatoxins in milk in Nairobi is disproportionate if only risk of cancer is considered, but that the effect on stunting children might be much more significant from a public health perspective; however, there is still insufficient data on the health effects of AFM1. Full article
(This article belongs to the Special Issue Dietary Mycotoxin Exposure: Emerging Risks to Human Health)
18 pages, 901 KiB  
Article
Exposure Assessment to Mycotoxins in a Portuguese Fresh Bread Dough Company by Using a Multi-Biomarker Approach
by Susana Viegas, Ricardo Assunção, Carla Nunes, Bernd Osteresch, Magdalena Twarużek, Robert Kosicki, Jan Grajewski, Carla Martins, Paula Alvito, Ana Almeida and Carla Viegas
Toxins 2018, 10(9), 342; https://doi.org/10.3390/toxins10090342 - 23 Aug 2018
Cited by 32 | Viewed by 4421
Abstract
Mycotoxins are toxic mold metabolites that can persist in environment long after the fungi species responsible for their production disappear. Critical workplace for mycotoxins presence has already been studied and nowadays it is possible to recognize that exposure to mycotoxins through inhalation occurs [...] Read more.
Mycotoxins are toxic mold metabolites that can persist in environment long after the fungi species responsible for their production disappear. Critical workplace for mycotoxins presence has already been studied and nowadays it is possible to recognize that exposure to mycotoxins through inhalation occurs due to their presence in dust. This study aimed to assess occupational co-exposure to multiple mycotoxins in a fresh bread dough company, an occupational setting not studied until now. Occupational exposure assessment to mycotoxins was done using a LC-MS/MS urinary multi-biomarker approach. Twenty-one workers and nineteen individuals that were used as controls participated in the study. Workers/controls (spot-urine) and environment (settled dust) samples were collected and analyzed. Concerning workers group, DON-GlcA, and OTA were the most prevalent biomarkers (>LOD), 66% and 90.5%, respectively. In the control group, OTA was also one of the most detected (68%) followed by CIT (58%) and DON-GlcA (58%). DON was the mycotoxin measured in high amounts in the settled dust sample (58.2 ng/g). Both workers and controls are exposed to several mycotoxins simultaneously. The workers group, due to their high contact with flour dust, revealed a higher exposure to DON. Considering these results, risk management measures must be applied including specific and adequate health surveillance programs in order to avoid exposure and consequently the associated health consequences. Full article
(This article belongs to the Special Issue Dietary Mycotoxin Exposure: Emerging Risks to Human Health)
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13 pages, 791 KiB  
Article
Evaluation of Mycotoxin Residues on Ready-to-Eat Food by Chromatographic Methods Coupled to Mass Spectrometry in Tandem
by Dionisia Carballo, Guillermina Font, Emilia Ferrer and Houda Berrada
Toxins 2018, 10(6), 243; https://doi.org/10.3390/toxins10060243 - 15 Jun 2018
Cited by 37 | Viewed by 4685
Abstract
Simultaneous determination of twenty-seven mycotoxins in ready-to-eat food samples using “Quick Easy Cheap Rough and Safe” (QuEChERS) extraction and chromatographic methods coupled to mass spectrometry in tandem is described in this study. Mycotoxins included in this survey were aflatoxins (B1, B [...] Read more.
Simultaneous determination of twenty-seven mycotoxins in ready-to-eat food samples using “Quick Easy Cheap Rough and Safe” (QuEChERS) extraction and chromatographic methods coupled to mass spectrometry in tandem is described in this study. Mycotoxins included in this survey were aflatoxins (B1, B2, G1, G2), enniatins (A, A1, B, B1), beauvericin (BEA), fumonisins (FB1, FB2), sterigmatocystin (STG), deoxynivalenol (DON), 3-acetyl-deoxynivalenol (3-ADON), 15-acetyl-deoxynivalenol (15-ADON), nivalenol (NIV), neosolaniol (NEO), diacetoxyscirpenol (DAS), fusarenon-X (FUS-X), zearalenone (ZEA), α-zearalanol (αZAL), β-zearalenone (βZAL), α-zearalenol (αZOL), β-zearalenol (βzol), T2, and HT-2 toxin. The method showed satisfactory extraction results with recoveries ranging from 63 to 119% for the different food matrix samples. Limits of detection (LODS) and quantification (LOQs) were between 0.15–1.5 µg/kg and 0.5–5 µg/kg, respectively. The method was successfully applied to the analysis of 25 ready-to-eat food samples. Results showed presence of deoxynivalenol at 36% of samples (2.61–21.59 µg/kg), enniatin B at 20% of samples (9.83–86.32 µg/kg), HT-2 toxin at 16% of samples (9.06–34.43 µg/kg), and aflatoxin G2 at 4% of samples (2.84 µg/kg). Mycotoxins were detected mainly in ready-to-eat food samples prepared with cereals, vegetables, and legumes, even at levels below those often obtained from raw food. Full article
(This article belongs to the Special Issue Dietary Mycotoxin Exposure: Emerging Risks to Human Health)
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Review

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21 pages, 786 KiB  
Review
Updates on the Effect of Mycotoxins on Male Reproductive Efficiency in Mammals
by Diala El. Khoury, Salma Fayjaloun, Marc Nassar, Joseph Sahakian and Pauline Y. Aad
Toxins 2019, 11(9), 515; https://doi.org/10.3390/toxins11090515 - 03 Sep 2019
Cited by 41 | Viewed by 6372
Abstract
Mycotoxins are ubiquitous and unavoidable harmful fungal products with the ability to cause disease in both animals and humans, and are found in almost all types of foods, with a greater prevalence in hot humid environments. These mycotoxins vary greatly in structure and [...] Read more.
Mycotoxins are ubiquitous and unavoidable harmful fungal products with the ability to cause disease in both animals and humans, and are found in almost all types of foods, with a greater prevalence in hot humid environments. These mycotoxins vary greatly in structure and biochemical effects; therefore, by better understanding the toxicological and pathological aspects of mycotoxins, we can be better equipped to fight the diseases, as well as the biological and economic devastations, they induce. Multiple studies point to the association between a recent increase in male infertility and the increased occurrence of these mycotoxins in the environment. Furthermore, understanding how mycotoxins may induce an accumulation of epimutations during parental lifetimes can shed light on their implications with respect to fertility and reproductive efficiency. By acknowledging the diversity of mycotoxin molecular function and mode of action, this review aims to address the current limited knowledge on the effects of these chemicals on spermatogenesis and the various endocrine and epigenetics patterns associated with their disruptions. Full article
(This article belongs to the Special Issue Dietary Mycotoxin Exposure: Emerging Risks to Human Health)
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19 pages, 1957 KiB  
Review
Aflatoxin B1 and M1: Biological Properties and Their Involvement in Cancer Development
by Silvia Marchese, Andrea Polo, Andrea Ariano, Salvatore Velotto, Susan Costantini and Lorella Severino
Toxins 2018, 10(6), 214; https://doi.org/10.3390/toxins10060214 - 24 May 2018
Cited by 327 | Viewed by 17096
Abstract
Aflatoxins are fungal metabolites found in feeds and foods. When the ruminants eat feedstuffs containing Aflatoxin B1 (AFB1), this toxin is metabolized and Aflatoxin M1 (AFM1) is excreted in milk. International Agency for Research on Cancer (IARC) classified AFB1 and AFM1 as human [...] Read more.
Aflatoxins are fungal metabolites found in feeds and foods. When the ruminants eat feedstuffs containing Aflatoxin B1 (AFB1), this toxin is metabolized and Aflatoxin M1 (AFM1) is excreted in milk. International Agency for Research on Cancer (IARC) classified AFB1 and AFM1 as human carcinogens belonging to Group 1 and Group 2B, respectively, with the formation of DNA adducts. In the last years, some epidemiological studies were conducted on cancer patients aimed to evaluate the effects of AFB1 and AFM1 exposure on cancer cells in order to verify the correlation between toxin exposure and cancer cell proliferation and invasion. In this review, we summarize the activation pathways of AFB1 and AFM1 and the data already reported in literature about their correlation with cancer development and progression. Moreover, considering that few data are still reported about what genes/proteins/miRNAs can be used as damage markers due to AFB1 and AFM1 exposure, we performed a bioinformatic analysis based on interaction network and miRNA predictions to identify a panel of genes/proteins/miRNAs that can be used as targets in further studies for evaluating the effects of the damages induced by AFB1 and AFM1 and their capacity to induce cancer initiation. Full article
(This article belongs to the Special Issue Dietary Mycotoxin Exposure: Emerging Risks to Human Health)
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