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Martin Weidenbörner Mycotoxins in Animal Products - Milk and Milk Products, and Meat Mycotoxins in Animal Products Martin Weidenbörner Mycotoxins in Animal Products Milk and Milk Products, and Meat Martin Weidenbörner Bonn, Germany ISBN 978-3-030-30918-3 ISBN 978-3-030-30919-0 (eBook) https://doi.org/10.1007/978-3-030-30919-0 © Springer Nature Switzerland AG 2019 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland Holger Hindorf Preface Mycotoxins in Animal Products—Milk and Milk Products, and Meat (Volume III) deals with mycotoxin contamination of foodstuffs of animal origin. Although not mentioned in the title of the book, mycotoxin contamination of, e.g., aquatic foodstuff, egg, fish, and seafood, as well as edible insects, is also listed. Nut butters and sesame butter are mentioned in Mycotoxins in Animal Products—Milk and Milk Products, and Meat as well as in Mycotoxins in Plants and Plant Products— Cocoa, Coffee, Fruits and Fruit Products, Medicinal Plants, Nuts, Spices, Wine because their ingredients are of both animal and plant origin. This is also true for a few other articles dealing with animal and plant products already mentioned in Mycotoxins in Plants and Plant Products—Cereals and Cereal Products or in Volume II. Human breast milk is a very important foodstuff but listed separately behind all other items in the chapter “Mycotoxin Contamination of Animal Products as well as Human Breast Milk” because it is of human origin but not an animal product. Since mankind has existed, the need for foodstuff has been indispensable. But food supplies can be attacked by microorganisms. If suitable conditions prevail, microorganisms can grow and subsequently spoil the foodstuff. Of these organisms, filamentous fungi are of special interest. Once they grow, they not only spoil the foodstuff but can also contaminate it with mycotoxins. The presence of these invisible mycotoxins in foodstuff is undesirable and can cause serious problems. High levels of mycotoxins can even cause death shortly after exposure, whereas low levels of mycotoxins can cause disorders in various organs and/or impair immunity. In the end, mycotoxins are a cost factor in human health. In contrast to bacterial contamination of foodstuff, the enhanced contamination by fungi becomes more apparent. Each consumer knows about the appearance of moldy foodstuff, and the awareness of the public concerning the health hazard of foodstuffs is great. Furthermore, consumers demand high-quality foodstuff. As a prerequisite for producing such foodstuff, the food industry as a whole must be aware of fungi and their corresponding mycotoxins. In this case, the third volume, Mycotoxins in Animal Products—Milk and Milk Products, and Meat, gives excellent information about the main mycotoxins occurring in foodstuff of animal origin. Mycotoxin contamination in foodstuff of animal origin is often represented by metabolites of the Aspergillus flavus group, the aflatoxins, predominantly aflatoxin M (AFM), which frequently occurs in different types of milk and dairy 1 1 products. Next to AFM ochratoxin A (OTA, Aspergillus spp. and Penicillium spp.) is often found in animal foodstuff, 1 especially in pigs. Mycotoxins like patulin (PAT) and penicillic acid (PA, Aspergillus spp. and Penicillium spp.), mycophenolic acid (MA) and roquefortine C (ROQ C, Penicillium spp.), sterigmatocystin (STG, Aspergillus spp.), and zearalenone (ZEA, Fusarium spp.) appeared to a lesser extent. The occurrence of mycotoxins, such as fumonisin/s, depsipeptides (e.g., beauvericin (BEA) and enniatins), trichothecenes (Fusarium spp.), penitrem A (PEA, Penicillium spp.), and Alternaria toxins, is normally rare in foodstuff of animal origin. Specialists of these mycotoxin-producing fungi can also grow during foodstuff is preserved, e.g., in a refrigerator. All these mycotoxins can be very harmful to humans when ingested. In the early 1960s, mycotoxin research started with the discovery of aflatoxins in peanut meal causing turkey X disease. In the same decade, monohydroxylated AFM (a possible human carcinogen), a metabolization product of AFB produced 1 1 in the animal’s rumen, in milk was first reported. In many kinds of milk and cheese, AFM is the main mycotoxin. If 1 feedstuff is contaminated by aflatoxin, there is a high probability that AFM occurred in the milk and the corresponding 1 dairy products. Depending on various factors like nutritional and physical status of the animal, up to ~6% of the AFB 1 ingested with the feed is transformed by the liver (cytochrome 450) to AFM. Because of the water-soluble hydroxyl group, 1 AFM can easily be excreted through, e.g., the milk (indirect contamination). AFM is not completely inactivated by heat. 1 1 Therefore, it occurs not only in raw milk but also in pasteurized and sterilized milk samples. Its presence in human breast milk is a result of aflatoxin/s contamination of foodstuffs. Together with AFM, OTA is the most common mycotoxin in 1 human breast milk. But in contrast to AFM, this mycotoxin predominates in kidneys and blood of pigs due to the 1 consumption of ochratoxin A-contaminated feedstuffs. vii viii Preface During the manufacture of cheese, maximum concentrations of AFM arise due to the high affinity of AFM to the 1 1 casein fraction. AFB and AFG occur only to a minor extent. AFM concentration in the corresponding cheese can be four 1 1 1 times higher than that in cheese milk. However, in yogurt AFM concentration is lowered by different factors such as low 1 pH and formation of organic acids or lactic acid bacteria. For the protection of consumers, the EU has set a limit of 0.050 μg AFM1/kg milk. During cheese manufacture, direct contamination (intentional or accidental) of cheeses such as Camembert and Roquefort with molds is typical. Although selected strains of P. camemberti (cyclopiazonic acid, CPA) and P. roqueforti (mycophenolic acid and roquefortine C) are used as ripening cultures, they may produce the aforementioned mycotoxins. However, these metabolites exhibit only lower toxicity and occur in low to very low levels. CPA is also one of the few mycotoxins which is considered to transfer into milk. In cheese citrinin (CIT) is often associated with OTA, but not frequently found in this kind of foodstuff. In comparison with cereals and their products, the intake of ochratoxin A from cheese seems to be negligible. If A. versicolor is growing on the cheese’s surface, STG contamination may be a result of that postcontamination. Aflatoxin/s, citrinin, penitrem A, roquefortine C, and sterigmatocystin are stable in cheese. In contrast patulin, penicillic acid, and PR toxin which can be transformed to, e.g., PR imine or PR amide do not persist. Whereas zearalenone could be detected in different animal products, other mycotoxins such as the fumonisins, enniatins, trichothecenes, or Alternaria toxins play only a minor role in the contamination of foodstuffs of animal origin. This book provides a basic overview of the most well-known mycotoxins in animal products. Their degree of contamination and the range of concentration of mycotoxins, as well as the mean of the positive samples (as far as possible), are shown in each case. These basic information are intended for readers interested in this topic. Mycotoxin-contaminated foodstuffs are listed in alphabetical order. Terms with brackets followed single items. All types of butter, cheese, milk, and sausage are listed together to get a quicker overview about mycotoxins involved in the corresponding foodstuffs. This was done as far as possible. Data of more than 160 new publications are added to Volume III. In the end, data of more than 560 articles have been considered in the book. Each item contains the relevant information as far as possible. The present book is the last of three volumes, dealing with the mycotoxin contamination of plants and plant products as well as of animal origin. For detailed information, the more interested reader is referred to the points “Co-contamination” and “Further contamination.” Co-contaminations of a sample with two or more mycotoxins are listed as described in the corresponding article. If “For detailed information see the article” occurs behind “Co-contamination,” the corresponding publication dealt with this co-contamination mostly from a general point of view. All entries contain the point “Further contamination,” which gives additional information about mycotoxin contamination of foodstuff of animal origin. Moreover, if “see also …” is written at the end of “Further contamination,” a look into Chapter 2: Further Mycotoxins and Microbial Metabolites (e.g. Chicken gizzard, zearalenone, literature326), is appropriate. Here, the remaining mycotoxins/microbial metabolites of an animal product are listed. Finally, the book contains plenty of information if totally utilized. The book also shows whether a food of animal origin is predisposed to mycotoxin contamination, documented by the number of different mycotoxins and the number of citations for the corresponding food item. This was done as far as possible for each case of mycotoxin contamination. Documenting this, more than 560 publications have been used which are all available at German libraries. The main part of the book represents Chapter 1: Mycotoxin Contamination of Animal Products as well as Human Breast Milk. It discusses in detail mycotoxin contamination of animal products and human breast milk. This is followed by Chapter 2: Further Mycotoxins and Microbial Metabolites, Chapter 3: Mycotoxins and Their Animal Product Spectrum as well as Human Breast Milk, Chapter 4: Animal Products as well as Human Breast Milk and Their Mycotoxins, and Chapter 5: Mycotoxin Contamination in Conventional and Organic Animal Products. This chapter lists articles with their index numbers which compare mycotoxin contamination in conventional and organic production. Chapter 6 documenting the Numerical and Alphabetical Bibliography follows. The chief publications considered are in English language. Articles in other languages have been chosen only if comprehensive summaries or tables, listing detailed results, were provided in English. Articles that unequivocally describe mycotoxin contamination of animal products (already apparent in the title) have been selected. There are exceptions, however. Also, the most cited publications that satisfied the aforementioned requirements have been considered for the book. Determination methods of mycotoxins are quite beyond the scope of this book (see the title of the book). The focus is on natural mycotoxin contamination of animal products as well as human breast milk. Publications containing data about mycotoxins due to artificial contamination (infected by direct fungal inoculation) have not been included in this volume. Except for a few articles, the publications cited are mainly dealing with natural mycotoxin contamination of marketed animal products. Mycotoxins in Animals and Animal Products—Milk and Milk Products, and Meat will provide more information and contribute to the transparency of animal products consumed by humans in relation to mycotoxin contamination. It is a suitable reference text for mycotoxin contamination in this kind of foodstuff. Preface ix This fundamental book is especially written for scientists and researchers who are interested in mycotoxin contamination of foodstuff of animal products for human consumption and will be especially suitable for those working in food microbiology, food technology, and the food industry (e.g., food producers, supervisors of food, food traders), as well as ministries, offices, and departments of farming and environmental regulation at national and international levels, bureaus, associations, agricultural bodies, mycologists, mycotoxicologists, toxicologists, biologists, chemists, biochemists, plant pathologists, supervisors in food quality control, lawyers and experts in food law, students of the respective fields, and other interested groups. Bonn, Germany Martin Weidenbörner How to Handle the Book The different mycotoxins in foodstuffs of animal origin are classified by the fungal genera which produce them. However, also other fungal genera may be able to produce a special mycotoxin, but only main producers or relevant species interesting for this book are chosen. For a quick overview, each mycotoxin can furthermore be looked up for its presence in animal products as well as human breast milk at the end of the book (Chapter 3: Mycotoxins and Their Animal Product Spectrum as well as Human Breast Milk) (Tables 1–5) and vice versa (Chapter 4: Animal Products as well as Human Breast Milk and Their Mycotoxins). In Chapter 1: “Mycotoxin Contamination of Animal Products as well as Human Breast Milk (Volume III),” mycotoxins are arranged as follows: Alternaria Toxins Altenuene (ALT), alternariol methyl ether (AME), tenuazonic acid (TA) Aspergillus Toxins Aflatoxin/s: Aflatoxin B (AFB), aflatoxin B (AFB), aflatoxin G (AFG), aflatoxin G (AFG), aflatoxin M (AFM), 1 1 2 2 1 1 2 2 1 1 aflatoxin M (AFM), aflatoxin/s (AF/AFS) 2 2 Other Aspergillus Toxins: Sterigmatocystin (STG) Aspergillus and Penicillium Toxins Citrinin (CIT), cyclopiazonic acid (CPA), ochratoxin A (OTA), ochratoxin B (OTB), patulin (PAT), penicillic acid (PA) Fusarium Toxins Depsipeptides: Beauvericin (BEA), enniatin A (ENA), enniatin A (ENA), enniatin B (ENB), enniatin B (ENB) 1 1 1 1 Fumonisin/s: Fumonisin B (FB) 1 1 Type A Trichothecenes: HT-2 toxin (HT-2), neosolaniol (NEO), T-2 toxin (T-2) Type B Trichothecenes: Deoxynivalenol (DON), 3-acetyldeoxynivalenol (3-AcDON), 15-acetyldeoxynivalenol (15-AcDON), Fusarenon-X (FUS-X), nivalenol (NIV) Other Fusarium Toxins: Zearalenone (ZEA) Penicillium Toxins Isofumigaclavine A (IFC A), isofumigaclavine B (IFC B), mycophenolic acid (MA), penitrem A (PEA), roquefortine C (ROQ C) Each declaration of mycotoxin contamination of animal products as well as human breast milk comprises seven main information: Incidence: 3/7 = 3 positives for aflatoxin contamination in relation to 7 investigated Concentration range: minimum and maximum residue values or only the maximum residue value Ø Concentration: Ø mycotoxin contamination for the positive samples (as far as possible) Sample origin: location, where the sample/s come/s from (as far as possible) Sample year: in which month/year the sample was collected/investigated (as far as possible) Country: origin of publication Literature number: Italy43 xi xii How to Handle the Book Usually, the highest mycotoxin value or the lowest and the highest value of mycotoxin contamination is given. In general, mean values of the mycotoxin-positive samples are stated. The presented concentrations (measuring units) occur always in μg/kg or μg/l. If a variant of a trial should not be listed, “no contamination” was determined. In some cases, a variant may be stated although mycotoxin concentration has not been detected. In this case “no contamination” is written. Each entry is marked with an index number, which is located behind the name of the involved country/countries where the publication has been carried out. This index number stands for the article where the presented results can be checked. It occurs again in the numerical bibliography. The index number refers to the title of the corresponding article. In the alphabetical bibliography, the literature is additionally arranged according to the author’s first name of publication. Behind each literature arranged alphabetically, there is a number in brackets giving information about the position of the literature in the numerical bibliography, e.g., (43) in the alphabetical bibliography denotes the 43rd position in the numerical bibliography. To easily find further mycotoxin-contaminated animal or animal products as well as human breast milk in an entry, the reader has to keep in mind the following scheme: “Further contamination”: Cheese (goat cheese), AFM, literature43 1 – Title of item: Cheese (goat cheese) – Mycotoxin: AFM 1 – Index number: literature43 With these facts, further contaminated/co-contaminated animal products presented in the original publication can be found in this book. Moreover, all mycotoxins, contaminating the same animal product (listed in “Further contamination”), are quoted in this book. Additionally, the corresponding data in “Further contamination” are marked with an index number. This number can be related to the article, which is presented in the numerical bibliography.

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