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08 Festivals et lieux

Viegas, C.1, 3 / Rodrigues, P.2 / Garcia, F.2 / Monteiro, L.2 / Caetano, L. A.1,3 / Viegas, S.1, 4

Resumo

O fornecimento de ração é fundamental para todos os sistemas de produção animal e qualquer fator que afete este sistema é um potencial problema para a produção. A contaminação fúngica pode ocorrer em qualquer fase da cadeia de produção e é em grande parte dependente de fatores ambientais, podendo a contaminação deste ambiente ocupacional ter consequências na saúde dos trabalhadores. Foi realizada pesquisa bibliográfica de artigos focando contaminação fúngica e por micotoxinas na cadeia de produção de rações. A secção Flavi do género Aspergillus e o complexo Fusarium graminearum foram os mais reportados nos artigos consultados. Em relação às micotoxinas, a Zearalenona (ZEA) e Deoxynivalenol (DON) foram as mais referidas. No entanto, Aflatoxina B1 é também referida e destacada na literatura devido ao fato de ser o agente carcinogénico de origem natural mais potente.

Palavras-chave: produção de ração; contaminação fúngica; contaminação por micotoxinas; exposição ocupacional.

Abstract

Feed supply is central to all animal production systems and any factor that affects the safety of the feed supply chain is a significant constraint to production. Fungal contamination from feed processing industry may result in health problems for workers. Scientific papers available on online databases reporting fungi and mycotoxins contamination in feed production chain were analysed. Aspergillus section Flavi and Fusarium graminearum complex were the most frequent fungi reported as feed contaminants. Regarding mycotoxins, Zearalenone (ZEA) and Deoxynivalenol (DON) were the most reported. However, Aflatoxin B1 is also highlighted since is the most potent naturally occurring carcinogen.

Keywords: feed production; fungi contamination; mycotoxins contamination; occupational exposure.

1. Theory

Feed is commonly colonised by some species of fungi that are able to produce few different mycotoxins, which can be hazardous to animal and human health (Frisvad and Lund 1993). Mycotoxins production is dependent on feed fungal contamination, the agronomic practices, the feed composition and harvesting, handling and storage conditions applied (Bryden, 2012). Contamination may occur at any stage of the feed production chain, being largely dependent on environmental factors, especially moisture and temperature (Figure 1) (Milani, 2013). Regarding mycotoxins, it is possible, in some occasions that workers are exposed to high levels of airborne mycotoxins during certain operations and this can be more harmful than oral exposure (Mayer et al., 2008). Additionally, exposure to multiple mycotoxins can also occur, potentially leading to adverse health effects (Degen, 2011).

Although food and feed contaminated by mycotoxins have been reported, only a few number of studies examined the consequences of exposure to mycotoxins in occupational settings (Halstensen, 2008).

1 Environment and Health Research Group (GIAS) Escola Superior de Tecnologia da Saúde de Lisboa, ESTeSL,

Instituto Politécnico de Lisboa, Av. D. João II, Lote 4.69.01, 1990-096 Lisboa, Portugal.

2Escola Superior de Tecnologia da Saúde de Lisboa, ESTeSL, Instituto Politécnico de Lisboa, Lisbon, Portugal. 3Research Institute for Medicines (iMed.ULisboa), Faculty of Pharmacy, University of Lisbon, Lisbon, Portugal

4 Centro de Investigação em Saúde Pública, Escola Nacional de Saúde Pública, New University of Lisbon, Lisbon,

  Figure 1. Feed production chain 

The aim of this study is to claim attention for the occupational exposure to fungi and mycotoxins occurring in the feed production setting through the collection of scientific papers about this topic.

2. Methodology

Extensive search was performed to identify reports on contamination by fungi and mycotoxin in the different stages of feed production and the consequent effects on the health of workers. Scientific papers, available on online databases, were analyzed reporting fungi and mycotoxins contamination in feed production chain, since the pre-harvest stage to the final product. Literature research was performed using the databases PubMed, Google Scholar and Scielo, from January 2016 to May 2016.

The following key words were used: “feed production”, “feed contamination”, “fungi contamination”, “mycotoxins”, “feed production exposure”, and “mycotoxins effects”, and, as a result, we have found seventy-five scientific papers. Either English or Portuguese written articles presenting findings regarding feed contamination with fungi and mycotoxins and/or occupational exposure in feed production were selected for further analyses.

3. Evidence

Seventy-five scientific papers were analyzed. Two main stages of the feed supply chain were identified as crucial when studying contamination, namely: pre-harvest and post- harvest/storage. The articles analysed reported the existence of contamination in 5 different raw materials used to produce the feed (Soya, Oat, Wheat, Maize and Barley) (Almeida et al. 2011). Concerning fungal contamination, many species of filamentous fungi from Aspergillus genus were described as feed contaminants in the analyzed scientific articles (Scarpati et al. 2014), being the Aspergillus section Flavi the most reported (Varga, 2009). In addition, Fusarium graminearum complex was also reported as a frequent raw material contaminant (Martins et al., 2008) (Table 1).

Concerning mycotoxins contamination, 6 different groups where identified: Aflatoxins (AF), Deoxynivalenol (DON) Zearalenone (ZEA), Ochratoxin (OTA), Nivalenol (NIV) and Fumonisins (Dorn et al., 2011; Baranyi et al. 2015), being the most reported ZEA and DON, each one by 8 different studies (Table 1). Zearalenone was reported in both stages (pre and post-harvest), being present in all the raw materials studied (Almeida et al. 2011). Deoxynivalenol contamination was observed worldwide in cereal crops, being wheat, maize and barley most frequently affected (EFSA, 2004). The same mycotoxin was also one of the most reported in the post-harvest stage, corroborating the frequent observed contamination in silages (Rodrigues and Naehrer 2012).

Although not the most reported, Aflatoxins (B1, B2, G1 and G2) are considered to be the group of mycotoxins of greatest concern from a global perspective (Sweeney and Dobson, 1998). They are primarily produced by Aspergillus flavus, A. parasiticus and in rare cases, by A. nomius (Ertas et al., 2008) all belonging to Aspergillus section Flavi. AFB1, the most abundant and most toxic aflatoxin (EFSA, 2004), is often referred to as the most potent naturally occurring carcinogen (Sweeney and Dobson, 1998). It is classified as a Group 1 human carcinogen by the International Agency for Research on Cancer (IARC) (IARC, 1993).

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Table 1. Fungi and mycotoxins contamination reported on feed production chain. AF- Aflatoxin; AFB1/B2/G1/G2- Aflatoxin B1/B2/G1/G2; ZEA- Zealarenone; DON- Deoxylivalenol; OTA- Ochratoxin A;

NIV- Nivalenol; FB- Fumonisin B complex.

When raw materials are handled in feed production, clouds of fragments of grain, inorganic soil particles and associated organic contaminants are dispersed in the air, including viable and non-viable microorganisms and their components, such as mycotoxins (Swan et al. 1998). It is difficult to define the precise effects of grain dust on the workers respiratory system due to the diverse composition of the grain dust and exposure frequency, duration and intensity (Swan et al. 1998).

Constituents of grain dust generated during pre-harvest stage are different from those in dust generated when stored grain is handled. In the pre-harvest stage raw materials becomes colonized by a different range of microorganisms depending on the conditions of the site where the crop is, especially water content, oxygen availability and temperature. In the post-harvest stage, if the grain is stored dry microorganisms present at harvest may survive but do not proliferate. If the water content of the grain is greater, some spores may germinate and grow, including Aspergillus spp. (Dosman et al., 1980). Consequently, the resuspension of particles

Step / stage Raw Material Fungi/ Mycotoxin reported Study Aspergillus flavus;

Trametes versicolor/ AF Scarpati et al. 2014 ZEA Pleadin et al. 2015 Aspergillus flavus, nomius,

pseudonomius and

parasiticus/ AF B1, B2, G1 and G2

Baranyi et al. 2015

DON Van der Fels-Klerx et al. 2013

Maize

DON; ZEA; FB; NIV Dorn, B., et al. 2011 ZEA Pleadin et al. 2015 Aspergillus flavus, nomius,

pseudonomius and

parasiticus/ AF B1, B2, G1 and G2

Baranyi et al. 2015 Wheat

DON Van der Fels-Klerx et al. 2013

Pre-harvest

Barley ZEA Pleadin et al. 2015

AF; OTA; ZEA Ibáñez-Vea et al. 2012 ZEA; FB Manova et al. 2009 AFB1; OTA; DON; ZEA; FB Tabuc et al. 2011 Barley

Fusarium graminearum/DON Martins et al. 2008 DON; ZEA Pleadin et al. 2012 FB1; FB2; ZEA; OTA Domijan et al. 2005 ZEA; FB Manova et al. 2009 AFB1; OTA; DON; ZEA; FB Tabuc et al. 2011 Aspergillus flavus;

Trametes versicolor / AF Scarpati et al. 2014 DON; ZEA; FB1 Goertz et al. 2010 Maize

AF; OTA; FB; ZEA; DON Grajewski et al. 2012 ZEA; FB Manova et al. 2009 AFB1; OTA; DON; ZEA; FB Tabuc et al. 2011 Wheat

DON; ZEA Stanciu et al. 2015. Oat AFB1; OTA; DON; ZEA; FB Tabuc et al. 2011 Post- Harvest / Storage

during the whole process of grain treatment, and later feed production, influence and can promote the inhalation of bioaerosols.

Fungi and mycotoxin contamination can occur at any stage in the feed production chain and applying Hazard Analysis Critical Control Points (HACCP) could be an effective approach to reduce contamination throughout the whole process. Additionally, preventing exposure to particles during all the process can avoid exposure to the other contaminants (fungi and mycotoxins) since particles acts as carriers for workers respiratory system (Viegas et al., 2015). Applying this approach successfully can reduce fungal and mycotoxin contamination in all the chain sectors, reducing also workers exposure, with the added benefit of increasing production efficiency (Aldred and Magan, 2004).

It should be noted that due to climate changes, mycotoxin risk assessment should include a wider concept of risk evaluation, including emerging risks since new mycotoxins could arise for new dominant fungus making the occurrence of new mycotoxins or mycotoxins not yet considered as a new potential occupational exposure threat (Viegas et al., 2016). Future studies are crucial to better understand how contamination of feed by fungi and mycotoxins occurs and how we can control and eliminate contamination in order to guarantee workers and animal health.

4. References

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Almeida, I., Martins, H. M., Santos, S., Costa, J. M., & Bernardo, F. (2011). Co-occurrence of mycotoxins in swine feed produced in Portugal. Mycotoxin research, 27: 177-181.

Baranyi, N., Despot, D. J., Palágyi, A., Kiss, N., Kocsubé, S., Szekeres, A. & Varga, J. (2015). Identification of Aspergillus species in Central Europe able to produce G-type aflatoxins. Acta Biologica Hungarica, 66: 339-347.

Bryden, W. L. (2012). Mycotoxin contamination of the feed supply chain: Implications for animal productivity and feed security. Animal Feed Science and Technology, 173, 134- 158.

Opinion of the Scientific Panel on Contaminants in the Food Chain on a request from the Commission related to Aflatoxin B1 as undesirable substance in animal feed. EFSA J. 2004, 39: 1–27.

Degen, G. (2011). Tools for investigating workplace-related risks from mycotoxin exposure. World Mycotoxin Journal, 4: 315-327.

Domijan, A. M., Peraica, M., Jurjević, Ž. Ivić, D., & Cvjetković, B. (2005). Fumonisin B1, fumonisin B2, zearalenone and ochratoxin A contamination of maize in Croatia. Food additives and contaminants, 22:677-680.

Dorn, B., Forrer, H. R., Jenny, E., Wettstein, F. E., Bucheli, T. D., & Vogelgsang, S. (2011). Fusarium species complex and mycotoxins in grain maize from maize hybrid trials and from grower’s fields. Journal of applied microbiology, 111: 693-706.

Dosman, J. A. & Cotton, D. J. (1980). Occupational pulmonary disease: focus on grain dust and health. Academic Press, Inc., 111 Fifth Avenue, New York, NY 10003, USA.

Ertas, N., Gonulalan, Z., Yildirim, Y. & Karadal, F. (2011) A survey of concentration of aflatoxin M1 in dairy products marketed in Turkey. Food Control, 22: 1956–1959

Frisvad, J. C. & Lund F (1993) Toxin and secondary metabolite production by Penicillium species growing in stored cereals. Scudamore K(ed) Occurrence and significance of mycotoxins. Central Science Laboratory, Slough, UK, 146–171.

Goertz, A., Zuehlke, S., Spiteller, M., Steiner, U., Dehne, H. W., Waalwijk, C. & Oerke, E. C. (2010). Fusarium species and mycotoxin profiles on commercial maize hybrids in Germany. European Journal of Plant Pathology, 128: 101-111.

Grajewski, J., Błajet Kosicka, A., Twarużek, M. & Kosicki, R. (2012). Occurrence of mycotoxins in Polish animal feed in years 2006–2009. Journal of animal physiology and animal nutrition, 96: 870-877.

Halstensen, A. S. (2008). Species-specific fungal DNA in airborne dust as surrogate for occupational mycotoxin exposure? International journal of molecular sciences, 9: 2543- 2558.

IARC. (1993) Some Naturally Occurring Substances: Food Items and Constituents, Heterocyclic Aromatic Amines and Mycotoxins—Fumonisin B1. IARC Monogr. Eval. Carcinog. Risks Hum, 56: 245–395.

Ibáñez-Vea, M., González-Peñas, E., Lizarraga, E. & De Cerain, A. L. (2012). Co-occurrence of aflatoxins, ochratoxin A and zearalenone in barley from a northern region of Spain. Food chemistry, 132: 35-42.

Manova, R. & Mladenova, R. (2009). Incidence of zearalenone and fumonisins in Bulgarian cereal production. Food control, 20: 362-365.

Mayer, S., Engelhart, S., Kolk, A., & Blome, H. (2008). The significance of mycotoxins in the framework of assessing workplace related risks. Mycotoxin research, 24: 151-164.

Martins, H. M., Marques, M., Almeida, I., Guerra, M. M. & Bernardo, F. (2008). Mycotoxins in feedstuffs in Portugal: an overview. Mycotoxin research, 24:19-23.

Milani, J. M. (2013). Ecological conditions affecting mycotoxin production in cereals: a review. Veterinarni Medicina, 58, 405-411.

Pleadin, J., Sokolović, M., Perši, N., Zadravec, M., Jaki, V., & Vulić, A. (2012). Contamination of maize with deoxynivalenol and zearalenone in Croatia. Food Control, 28: 94-98.

Pleadin, J., Mihaljević, Ž. Barbir, T., Vulić, A., Kmetič, I., Zadravec, M., & Mitak, M. (2015). Natural incidence of zearalenone in Croatian pig feed, urine and meat in 2014. Food Additives & Contaminants: Part B, 8:277-283.

Rodrigues, I., & Naehrer, K. (2012). Prevalence of mycotoxins in feedstuffs and feed surveyed worldwide in 2009 and 2010. Phytopathologia Mediterranea,51, 175-192.

Scarpati, M., Bello, C., Pietricola, C., Zaccaria, M., Bertocchi, L., Angelucci, A. & Reverberi, M. (2014). Aflatoxin control in maize by Trametes versicolor. Toxins, 6, 3426-3437.

Stanciu, O., Banc, R., Cozma, A., Filip, L., Miere, D., Mañes, J. & Loghin, F. (2015). Occurence of Fusarium Mycotoxins in Wheat from Europe–A Review. Acta Universitatis Cibiniensis. Series E: Food Technology, 19: 35-60.

Swan, J. R. & Crook, B. (1998). Airborne microorganisms associated with grain handling. Annals of Agricultural and Environmental Medicine, 5(1): 7-15.

Sweeney, M.J. & Dobson, A.D.W. (1998) Mycotoxin production by Aspergillus, Fusarium and Penicillium species. Int. J. Food Microbiol. 43: 141–158.

Tabuc, C., Taranu, I. & Calin, L. (2011). Survey of mould and mycotoxin contamination of cereals in South-Eastern Romania in 2008–2010. Archiva Zootechnica, 14: 25.

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Viegas, C., Meneses, M., & Viegas, S. (2016). Climate changes influence in occupational exposure to fungi and mycotoxins. Occupational Safety and Hygiene IV.

Viegas, C.; Pinheiro, C.; Sabino, R.; Viegas, S.; Brandão, J.; Veríssimo, C.; editors. Environmental mycology in public health: fungi and mycotoxins risk assessment and management. Academic Press; 2015.

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