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Chemical Hazards from Poultry Meat: Cooking, Digestion

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Chemical Hazards from Poultry Meat: Cooking, Digestion Chemical hazards from poultry meat: cooking, digestion, absorption and toxicity Thesis submitted to University do Porto, in partial fulfilment of requirements for the PhD degree in Sustainable Chemistry Maria Madalena Costa Sobral Under the supervision of: Associate Professor Isabel Maria Pinto Leite Viegas Oliveira Ferreira And the co-supervision of: Doctor Miguel Ângelo Rodrigues Pinto de Faria Doctor Sara Cristina da Silva Cunha Porto May, 2020 ©AUTHORIZED THE COMPREHENSIVE REPRODUCTION OF THIS THESIS ONLY FOR RESEARCH PURPOSES THROUGH A WRITTEN DECLARATION OF THE INTERESTED PART THAT IS COMMITTED TO SUCH PLEDGES This work was supported by Fundação para a Ciência e Tecnologia (FCT) through PhD grant (PD/DB/114581/2016), by FEDER - Fundo Europeu de Desenvolvimento Regional funds through the COMPETE 2020 - Operational Programme for Competitiveness and Internationalisation (POCI), and by the DIETImpact project (PTDC/SAU-NUT/30322/2017 and POCI-01-0145-FEDER-030322). It was also supported by UID/QUI/50006/2013 and UID/QUI/50006/2019. iii The experimental work presented in this thesis was undertaken under the PhD Programme in Sustainable Chemistry (REQUIMTE), hosted by University of Porto, Nova Lisbon University, and University of Aveiro. The experimental work was mainly performed in the Laboratory of Bromatology and Hydrology, Department of Chemical Sciences, Faculty of Pharmacy, University of Porto (Portugal). iv AGRADECIMENTOS No culminar desta etapa gostaria de agradecer a todas as pessoas que de algum modo contribuíram durante o meu percurso académico ao longo destes anos. Em primeiro lugar quero expressar toda a minha gratidão à Professora Isabel por ter aceitado ser minha orientadora, tornando possível este doutoramento. Agradeço toda a ajuda, orientação, dedicação, pronta disponibilidade em todas as etapas, e acima de tudo por ter acreditado em mim. Quero agradecer também ao Doutor Miguel e à Doutora Sara, pela co-orientação, por todo o apoio ao longo destes anos, pelas sugestões e discussões científicas no decorrer dos trabalhos, mas acima de tudo pelos conhecimentos transmitidos. À Professora Susana por todo o apoio, discussões de trabalho, e transmissão de conhecimento que ajudaram a enriquecer esta tese. Às minhas meninas, muito obrigada por me terem acolhido no vosso grupo, por todas as conversas científicas e pessoais, pela boa disposição, e por todos os nossos almoços e “catraiadas” para celebrar os nossos sucessos! De uma forma geral, agradeço a todos os colegas de laboratório de Bromatologia e Hidrologia pelo auxílio em todas as atividades desenvolvidas. Me gustaría agradecer a Toñi y Roberto por haberme recibido en vuestro laboratorio en la Universidad de Almería. También a los demás miembros del grupo de Química Analítica de Contaminantes. Muchas gracias por la integración en el grupo, por la simpatía, por toda la ayuda, disponibilidad y conocimiento compartido. Los meses que estuve ahí me dejaron buenas memorias y enseñanzas muy importantes para mí, tanto profesionalmente como personalmente. ¡Muchas gracias a todos! Não há palavras suficientes para agradecer aos pilares da minha vida, os meus pais e irmão, pelo apoio incondicional, paciência, compreensão e por se orgulharem sempre de mim. Ao meu companheiro, pelo ser fantástico e inigualável que é, pelo incansável apoio, carinho, amizade, compreensão e sobretudo pela calma e serenidade que sempre me transmite nos momentos menos bons. Muito obrigada por seres o meu porto seguro e por me ajudares cada dia a ser uma pessoa melhor. Um sentido obrigada a todos! v ABSTRACT Poultry meat is rich in valuable nutrients, such as high-quality proteins, vitamins, minerals, and polyunsaturated fatty acids. Chicken is one of the most consumed poultry meat worldwide with its production and supply raising over the years, which has also increased the occurrence of chemical hazards as cocciodiostats and antibiotic residues, used to fight infections in animals, as well as mycotoxins that can enter the food chain via fungal infection of crops and consequent carry-over to humans. The cooking of meat can also contribute to the formation of deleterious compounds due to oxidation of nutrients. Some culinary practices, such as herbs addition, marinades, or roasting bags have been tested to avoid formation of hazardous substances during cooking while keeping the nutritional value of meat. Nonetheless, there is no information concerning their impact on mycotoxins or antibiotics, nor on lipid and protein oxidation of poultry meat. Thus, this thesis aimed to evaluate: i) the influence of adding ingredients (oregano/beer) on lipid and protein oxidation after cooking (oven/microwave) and in vitro digestion of chicken meat. Therefore, five oxidation markers - malondialdehyde (MDA), 4-hydroxy-2- nonenal (HNE), hexanal (HEX), carbonyls, and Schiff bases – as well as free amino acids and total fatty acids content were measured; ii) moreover, the stability of 14 antibacterial and coccidiostats drugs (ACDs) during cooking and in vitro digestion was also ascertained concerning the addition of oregano and/or beer, and, iii) the behaviour of 10 prevalent mycotoxins was also evaluated during cooking and digestion of chicken, with/without roasting bags and/or commercial mixture of herbs. As the amount of compounds present in cooked meat does not directly reflect the actual amount available for absorption and toxicity, in vitro digestion studies, using the INFOGEST protocol, were also performed for all chemical hazards. Moreover, the natural co-occurrence of mycotoxins and the lack of information on their absorptive and toxicological behaviour when in combination has instigated the evaluation of the transport of four prevalent mycotoxins - aflatoxin B1 (AFB1), deoxynivalenol (DON), fumonisin B1 (FB1), and ochratoxin A (OTA), - isolated and in mixture, across gastric NCI- N87 and intestinal Caco-2 monolayers, as well as their binary toxicological interactions to determine the combinations as additive, antagonistic or synergistic concerning toxicity using as models the Caco-2 (intestinal) and HepG2 (hepatic) cells. As to results, oregano prevented MDA, HEX, and HNE formation, while beer seemed not to influence their formation. The ACDs were stable during cooking, except amoxicillin, chlortetracycline and tylosin (reductions >50%), being molecular rearrangement and dechlorination reactions the most probable transformations derived from cooking. Adding vii oregano did not benefit their reductions. Mycotoxins were reduced up to 60% by cooking in the presence of herbs; the roasting bags did not confer any advantage. After in vitro digestion, MDA, carbonyls, and Schiff bases increased, regardless of the culinary practice, while HNE and HEX values were reduced. ACDs exhibited maximum bioaccessibility of 60% for all compounds probably due to drug-bile salts interaction suggesting that the bioaccessibility prediction must not be based only on ACDs determination in the free form. In the case of mycotoxins, they exhibited the highest bioaccessibility in digested samples cooked with herbs. However, despite their higher bioaccessibility, as cooking with herbs highly reduced their contents, the exposure to these mycotoxins after digestion is lower in samples with added herbs. Besides the increase of oxidation markers, their lowest contents were observed after cooking with oregano, thus, it should be recommended as a mitigation strategy to avoid the formation of oxidation products during cooking, as well as diminishing their formation during in vitro digestion. Herbs also showed to be an effective strategy to reduce mycotoxins in meat, while in the case of ACDs oregano’s influence was not clear. Moreover, more strategies to reduce ACDs and mycotoxins should be the subject of future research together with more accurate methodologies to assess their bioaccessibility. Concerning gastrointestinal transport assays of mycotoxins, different absorptive patterns on both epithelia were found between molecules isolated or in mixture highlighting that their co-ocurrence and consequent co-exposure considerably impacts human absorption and toxicity. When evaluating the cytotoxicity of combined mycotoxins, synergism or antagonism effects on both Caco-2 and HepG2 cells were observed. Synergistic strengths as high as a dose reduction index of 10 for AFB1-DON were observed in hepatic cells. Taken together our findings indicate that the toxicological effects differ regarding the type of mycotoxins used for combinations and the stronger synergistic effect was observed for DON containing mixtures in both cells. Therefore, even though DON has not been classified as to its carcinogenicity to humans, this mycotoxin may present a serious threat to health, mainly when co-occurring in the environment. Keywords: lipid oxidation products, protein oxidation, antibiotics, mycotoxins, in vitro digestion, in vitro absorption, combined cytotoxicity viii RESUMO A carne de aves é nutricionalmente importante, sendo rica em proteínas, vitaminas, minerais e ácidos gordos poliinsaturados. O frango é uma das carnes de aves mais consumidas em todo o mundo, no entanto a sua elevada produção e fornecimento ao longo dos anos aumentou a ocorrência de riscos químicos como resíduos de antibióticos, utilizados no combate a infecções em animais, e micotoxinas que podem entrar na cadeia alimentar através de infecção fúngica das culturas e consequente transferência para o homem. O processo de cocção da carne também pode contribuir para a formação de compostos
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