Hostname: page-component-848d4c4894-tn8tq Total loading time: 0 Render date: 2024-06-28T22:04:31.608Z Has data issue: false hasContentIssue false

Study of the effects of PR toxin, mycophenolic acid and roquefortine C on in vitro gas production parameters and their stability in the rumen environment

Published online by Cambridge University Press:  01 May 2014

A. GALLO*
Affiliation:
Feed and Food Science and Nutrition Institute, Faculty of Agricultural, Food and Environmental Sciences, Università Cattolica del Sacro Cuore, Via Emilia Parmense 84, 29122 Piacenza, Italy
G. GIUBERTI
Affiliation:
Feed and Food Science and Nutrition Institute, Faculty of Agricultural, Food and Environmental Sciences, Università Cattolica del Sacro Cuore, Via Emilia Parmense 84, 29122 Piacenza, Italy
T. BERTUZZI
Affiliation:
Feed and Food Science and Nutrition Institute, Faculty of Agricultural, Food and Environmental Sciences, Università Cattolica del Sacro Cuore, Via Emilia Parmense 84, 29122 Piacenza, Italy
M. MOSCHINI
Affiliation:
Feed and Food Science and Nutrition Institute, Faculty of Agricultural, Food and Environmental Sciences, Università Cattolica del Sacro Cuore, Via Emilia Parmense 84, 29122 Piacenza, Italy
F. MASOERO
Affiliation:
Feed and Food Science and Nutrition Institute, Faculty of Agricultural, Food and Environmental Sciences, Università Cattolica del Sacro Cuore, Via Emilia Parmense 84, 29122 Piacenza, Italy
*
*To whom all correspondence should be addressed. Email: antonio.gallo@unicatt.it

Summary

Moulds belonging to Penicillium section roqueforti are common contaminants of feedstuffs and produce several mycotoxins that can cause health hazards when ingested by farm animals. Among these, PR toxin (PR), mycophenolic acid (MY) and roquefortine C (RC) have been frequently detected in forages, particularly silages. The aims of the current trials were to study the effects of the presence of pure mycotoxins on in vitro rumen fermentation parameters and to assess their stability in the rumen environment. Two successive in vitro gas production experiments were carried out: a central composite design with four replications of central point (CCD) and a completely randomized design with a fully factorial arrangement of treatments (FFD). In CCD, the effects of PR, MY and RC concentrations in diluted rumen fluid (i.e. 0·01, 0·30, 1·01, 1·71 and 2·00 μg of each mycotoxin/ml) were tested. Gas volume produced after 48 h of incubation (Vf) decreased linearly as concentrations of RC and MY in diluted rumen fluid increased, with marginal effects similar for two mycotoxins, being respectively −14·6 and −13·4 ml/g organic matter (OM) for each 1·0 μg/ml of increment in mycotoxin concentration. Similarly, total volatile fatty acid (VFA) production decreased quadratically as concentrations of RC and MY increased, with marginal effects about two times higher for MY than RC, being −4·22 and −2·62 mmol/l for each 1·0 μg/ml of increment in mycotoxin concentration. With respect to maximum Vf (i.e. 410·6 ml/g OM) and VFA (98·06 mmol/l) values estimated by the model, decreases of 13·6 and 15·2% were obtained when incubating the highest RC and MY concentrations, respectively. The PR did not interfere with rumen fermentation pattern and it was not recovered after 48 h of incubation, whereas the stabilities of MY and RC in rumen fluid were similar and on average equal to about 50%. On the basis of CCD results, a second experiment (FFD) was carried out in which only effects of MY and RC concentrations (i.e. 0, 0·67, 1·33 and 2·00 μg of each mycotoxin/ml of diluted rumen fluid) were tested. Data from FFD showed Vf decreased linearly when concentrations of MY and RC increased, with marginal effect two-folds higher for MY than for RC (−11·1 ml/g OM and −6·7 ml/g OM, respectively). Similar marginal effects of MY and RC in decreasing VFA production were recorded: −2·38 and −2·86 mmol/l for each 1·0 μg/ml of increment in mycotoxin concentration, respectively. At the highest RC and MY tested concentrations, Vf and VFA decreased by 8·7 and 10·7%, respectively, over maximum estimated values. In FFD, the average amounts of MY and RC recovered in rumen fluid after 48 h of incubation were 79·0 and 40·6%, respectively. In conclusion, the MY and RC from standards interfered with rumen microorganisms at relatively low levels and were partially stable in the rumen environment after 48 h of incubation. These findings suggested that MY and RC could interfere with digestive processes and might represent a potential risk for ruminants fed diets containing feeds contaminated by mycotoxins produced by P. roqueforti.

Type
Animal Research Papers
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

AOAC (Association of Official Analytical Chemists) (1995). Official Methods of Analysis, 15th edn, Arlington, VA, USA: AOAC.Google Scholar
Auerbach, H., Oldenburg, E. & Weissbach, F. (1998). Incidence of Penicillium roqueforti and roquefortine C in silages. Journal of the Science of Food & Agriculture 76, 565572.Google Scholar
Berthiller, F., Crews, C., Dall'Asta, C., De Saeger, S., Haesaert, G., Karlovsky, P., Oswald, I. P., Seefelder, W., Speijers, G. & Stroka, J. (2013). Masked mycotoxins: a review. Molecular Nutrition and Food Research 57, 165186.Google Scholar
Bertuzzi, T., Rastelli, S., Mulazzi, A. & Pietri, A. (2012). Evaluation and improvement of extraction methods for the analysis of aflatoxins B1, B2, G1 and G2 from naturally contaminated maize. Food Analytical Methods 5, 512519.CrossRefGoogle Scholar
Borreani, G., Tabacco, E., Antoniazzi, S. & Cavallarin, L. (2005). Zearalenone contamination in farm maize silage. Italian Journal of Animal Science 4 (Suppl. 2), 162165.CrossRefGoogle Scholar
Boundra, H. & Morgavi, D. P. (2005). Mycotoxin risk evaluation in feeds contaminated by Aspergillus fumigatus . Animal Feed Science and Technology 120, 113123.CrossRefGoogle Scholar
Council for Agricultural Science and Technology (CAST) (2003). Mycotoxins: Risks in Plant, Animal and Human Systems. Ames, Iowa, USA: CAST.Google Scholar
D'Mello, J. P. F. & Macdonald, A. M. C. (1997). Mycotoxins. Animal Feed Science and Technology 69, 155166.Google Scholar
Driehuis, F. (2013). Silage and the safety and quality of dairy foods: a review. Agricultural and Food Science 22, 1634.Google Scholar
Driehuis, F., Spanjer, M. C., Scholten, J. M. & te Giffel, M. C. (2008 a). Occurrence of mycotoxins in maize, grass and wheat silage for dairy cattle in Netherlands. Food Additives and Contaminants Part B 1, 4150.CrossRefGoogle ScholarPubMed
Driehuis, F., Spanjer, M. C., Scholten, J. M. & te Giffel, M. C. (2008 b). Occurrence of mycotoxins in feedstuffs of dairy cows and estimation of total dietary intakes. Journal of Dairy Science 91, 42614271.CrossRefGoogle ScholarPubMed
European Commission (1986). Council directive of 24 November 1986 on the approximation of laws, regulations and administrative provisions of the member states regarding the protection of animals used for experimental and other scientific purposes. Official Journal of the European Communities L358, 128.Google Scholar
European Commission (2002). Commission decision of 12 August 2002 implementing council directive 96/23/EC concerning the performance of analytical methods and the interpretation of results. Official Journal of the European Communities L221, 836.Google Scholar
Fink-Gremmels, J. (2008 a). The role of mycotoxins in the health and performance of dairy cows. The Veterinary Journal 176, 8492.Google Scholar
Fink-Gremmels, J. (2008 b). Mycotoxins in cattle feeds and carry-over to dairy milk: a review. Food Additives and Contaminants: Part A 25, 172180.Google Scholar
Frisvad, J. C. & Samson, R. A. (2004). Polyphasic taxonomy of Penicillium subgenus Penicillium. A guide to identification of the food and air-borne terverticillate Penicillia and their mycotoxins. Studies in Mycology 49, 1174.Google Scholar
Gallo, A. & Masoero, F. (2010). In vitro models to evaluate the capacity of different sequestering agents to adsorb aflatoxins. Italian Journal of Animal Science 9, 109116.Google Scholar
Gallo, A., Masoero, F., Bertuzzi, T., Piva, G. & Pietri, A. (2010). Effect of the inclusion of adsorbents on aflatoxin B-1 quantification in animal feedstuffs. Food Additives and Contaminants – Part A 27, 5463.CrossRefGoogle ScholarPubMed
Gallo, A., Moschini, M., Cerioli, C. & Masoero, F. (2013). Use of principal component analysis to classify forages and predict their calculated energy content. Animal 7, 930939.Google Scholar
Giuberti, G., Gallo, A., Masoero, F., Ferraretto, L. F., Hoffman, P. C. & Shaver, R. D. (2014). Factors affecting starch utilization in large animal food production system: a review. Starch/Stärke 66, 7290.Google Scholar
Harvey, R. B., Edrington, T. S., Kubena, L. F., Elissalde, M. H., Corrier, D. E. & Rottinghaus, G. E. (1995). Effect of aflatoxin and diacetoxyscirpenol in ewe lambs. Bulletin of Environmental Contamination and Toxicology 54, 325330.Google Scholar
Jeong, J. S., Lee, J. H., Simizu, Y., Tazaki, H., Itabashi, H. & Kimura, N. (2010). Effects of the Fusarium mycotoxin deoxynivalenol on in vitro rumn fermentation. Animal Feed Science and Technology 162, 144148.Google Scholar
Jiang, Y. H., Yang, H. J. & Lund, P. (2012). Effect of aflatoxin B1 on in vitro ruminal fermentation of rations high in alfalfa hay or ryegrass hay. Animal Feed Science and Technology 175, 8589.Google Scholar
Masoero, F., Gallo, A., Zanfi, C., Giuberti, G. & Spanghero, M. (2010). Chemical composition and rumen degradability of three corn hybrids treated with insecticides against the European corn borer (Ostrinia nubilalis). Animal Feed Science and Technology 155, 2532.CrossRefGoogle Scholar
Menke, K. H. & Steingass, H. (1988). Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Animal Research and Development 28, 755.Google Scholar
Mohr, A. I., Lorenz, I., Baum, B., Hewicker-Trautwein, M., Pfaffl, M., Dzidić, A., Meyer, H. H., Bauer, J. & Meyer, K. (2007). Influence of oral application of mycophenolic acid on the clinical health status of sheep. Journal of Veterinary Medicine Series A: Physiology, Pathology, Clinical Medicine 54, 7681.Google Scholar
Morgavi, D. P., Boudra, H., Jouany, J. P. & Michalet-Doreau, B. (2004). Effect and stability of gliotoxin, an Aspergillus fumigatus toxin, on in vitro rumen fermentation. Food Additives and Contaminants 21, 871878.Google Scholar
Moschini, M., Gallo, A., Piva, G. & Masoero, F. (2008). The effects of rumen fluid on the in vitro aflatoxin binding capacity of different sequestering agents and in vivo release of the sequestered toxin. Animal Feed Science and Technology 147, 292309.CrossRefGoogle Scholar
Müller, H. M. & Amend, R. (1997). Formation and disappearance of mycophenolic acid, patulin, penicillic acid and PR toxin in maize silage inoculated with Penicillium roqueforti . Archiv für Tierernaehrung 50, 213225.Google Scholar
Niderkorn, V., Morgavi, D. P., Pujos, E., Tissandier, A. & Boudra, H. (2007). Screening of fermentative bacteria for their ability to bind and biotransform deoxynivalenol, zearalenone and fumonisins in an in vitro simulated corn silage model. Food Additives and Contaminants 24, 406415.CrossRefGoogle Scholar
Nielsen, K. F., Sumarah, M. W., Frisvad, J. C. & Miller, D. J. (2006). Production of metabolites from the Penicillium roqueforti complex. Journal of Agricultural and Food Chemistry 54, 37563763.Google Scholar
NRC (2001). Nutrient Requirements of Dairy Cattle, 7th revision edn, Washington, D.C.: National Academy Press.Google Scholar
Nout, M. J. R., Bouwmeester, H. M., Haaksma, J. & Van Dijk, H. (1993). Fungal growth in silages of sugarbeet press pulp and maize. Journal of Agricultural Science, Cambridge 121, 323326.Google Scholar
Pedrosa, K. & Griessler, K. (2009). Toxicity, occurrence and negative effects of PR toxin – the hidden enemy. International Dairy Topics 9, 79.Google Scholar
Pereyra, C. M., Alonso, V. A., Rosa, C. A. R., Chiacchiera, S. M., Dalcero, A. M. & Cavaglieri, L. R. (2008). Gliotoxin natural incidence and toxigenicity of Aspergillus fumigatus isolated from corn silage and ready dairy cattle feed. World Mycotoxin Journal 1, 457462.Google Scholar
Pietri, A. & Bertuzzi, T. (2012). Simple phosphate buffer extraction for the determination of fumonisins in masa, maize, and derived products. Food Analytical Methods 5, 10881096.CrossRefGoogle Scholar
Pietri, A., Battilani, P., Gualla, A. & Bertuzzi, T. (2012). Mycotoxin levels in maize produced in northern Italy in 2008 as influenced by growing location and FAO class of hybrid. World Mycotoxin Journal 5, 409418.CrossRefGoogle Scholar
Rasmussen, R. R., Storm, I. M. L. D., Rasmussen, P. H., Smedsgaard, J. & Nielsen, K. F. (2010). Multi-mycotoxin analysis of maize silage by LC-MS/MS. Analytical and Bioanalytical Chemistry 397, 765776.CrossRefGoogle ScholarPubMed
Rasmussen, R. R., Rasmussen, P. H., Larsen, T. O., Bladt, T. T. & Binderup, M. L. (2011). In vitro cytotoxicity of fungi spoiling maize silage. Food and Chemical Toxicology 49, 3144.Google Scholar
Richard, E., Heutte, N., Sage, L., Pottier, D., Bouchart, V., Lebailly, P. & Garon, D. (2007). Toxigenic fungi and mycotoxins in mature corn silage. Food and Chemical Toxicology 45, 24202425.Google Scholar
SAS Institute Inc. (2003). SAS/SAT Guide for Personal Computers, version 9.13. Cary, NC, USA: SAS Institute Inc.Google Scholar
Scudamore, K. A. & Livesey, C. T. (1998). Occurrence and significance of mycotoxins in forage crops and silage: a review. Journal of the Science of Food & Agriculture 77, 117.3.0.CO;2-4>CrossRefGoogle Scholar
Storm, I. M. L. D., Sørensen, M. L., Jens, L., Rasmussen, R. R., Nielsen, K. F. & Thrane, U. (2008). Mycotoxins in silage. Stewart Postharvest Review 4, 112.Google Scholar
Storm, I. M. L. D., Kristensen, N. B., Raun, B. M. L., Smedsgaard, J. & Thrane, U. (2010). Dynamics in the microbiology of maize silage during whole-season storage. Journal of Applied Microbiology 109, 10171026.Google Scholar
St-Pierre, N. R. & Weiss, W. P. (2009). Technical note: designing and analyzing quantitative factorial experiments. Journal of Dairy Science 92, 45814588.CrossRefGoogle ScholarPubMed
Tapia, M. O., Stern, M. D., Koski, R. L., Bach, A. & Murphy, M. J. (2002). Effects of patulin on rumen fermentation in continuous culture fermenters. Animal Feed Science and Technology 97, 239246.Google Scholar
Van Soest, P. J., Robertson, J. B. & Lewis, B. A. (1991). Methods of dietary fiber, neutral detergent fiber and non-polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 35833597.CrossRefGoogle Scholar
Westlake, K., Mackie, R. I. & Dutton, M. F. (1989). In vitro metabolism of mycotoxins by bacterial protozoal and ovine ruminal fluid preparations. Animal Feed Science and Technology 25, 169178.Google Scholar
Whitlow, L. W. & Hagler, W. M. (2010). Mold and Mycotoxin Issues in Dairy Cattle: Effects, Prevention and Treatment. Greensboro, NC, USA: North Carolina A&T State University Cooperative Extension. Available online from: http://www.extension.org/pages/11768/mold-and-mycotoxin-issues-in-dairy-cattle:-effects-prevention-and-treatment (accessed 30 January 2013).Google Scholar
Yu, W., Yu, F. Y., Undersander, D. J. & Chu, F. S. (1999). Immunoassays of selected mycotoxins in hay, silage and mixed feed. Food and Agricultural Immunology 11, 307319.Google Scholar