Mycological and enzymatic studies on fresh beef meat sold in Taiz City, Yemen
Keywords:
Fresh meat, Food spoilage, Protease, Lipase
Abstract
The mycological analysis of 30 fresh beef meat samples on Czapek’s agar at 7º and 28ºC revealed that, heavily contamination with moulds was observed especially at 28ºC. A total of 234 and 400 colonies ⁄ 450 g meat were collected on both temperatures, respectively. Sixty-seven species belonging to 20 genera were identified. Members of Aspergillus, Mucor, Penicillium and Trichoderma were the most prevalent fungi. At 7°C was highly spoilage by yeasts fungi, while filamentous fungi predominated at 28°C. The ability of the common fungal isolates to produce protease and lipase enzymes revealed that most of them were positive. Among 152 isolates tested, 103 (67.8%) and 96 (63.2%) could respectively produce these enzymes. Because the deteriorative effects of the above fungi, food should be frequently and routinely analyzed. Also, it is essential to store the meat at lower temperature immediately after slaughtering and during transport and storage to reduce or prevent mould growth.
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References
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14. Martín A, Juan JC, Felix N, Maria JB, Miguel AA. Contribution of a selected fungal population to proteolysis on dry-cured ham. Int J Food Microbiol. 2004; 94: 55-66.
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30. Pitt JI. The genus Penicillium and its telemorphic states. Eupenicillium and Talaromyces. Academic Press, London, 1979.
31. Moubasher AH. Soil fungi in Qatar and other Arab countries. Scientific and Applied Research Center. University of Qatar, Doha, Qatar, 1993.
32. Domsch KH, Gams W, Anderson T-H. Compendium of soil fungi. 2nd edn, IHW-Verlag, Eching, 2007.
33. Paterson RRM, Bridge PD. Biochemical techniques for filamentous fungi. Int. Mycol. Instit. CAB international, Surrey, 1994; 21.
34. Ullman V, Blasins G. A simple medium for the detection of different lipolytic activity of microorganisms. Zentrabl Bakteriol J Hyg. 1974; 229: 264-267.
35. Farghaly RM, Gherbawy YAMH, Yosef MS. Contamination of meat stored in home refrigerators in Qena (Egypt). Czech Mycol. 2004; 56: 53-62.
36. Sørensen LM, Jacobsen T, Nielsen PV, Frisvad JC, Koch AG. Mycobiota in the processing areas of two different meat products. Int J Food Microbiol. 2008; 124(1): 58-64.
37. Omorodion NJPN, Odu NN. Microbiological quality of meats sold in Port Harcaurt Metropolis, Nigeria. Nat Sci. 2014; 12(2): 58-62.
38. Asefa DT, Kure CF, Gjerde RO, Omer MK, Langsrud S, Nesbakken T, Skaar I. Fungal growth pattern, sources and factors of mould contamination in a dry-cured meat production facility. Int J Food Microbiol. 2010; 140: 131-135.
39. Pal M, Bagi AS. Fungi isolated from lymph nodes of buffaloes. Mycoses. 1989; 32(11): 578-580.
40. Robert AS, Ellen SH, Jens CF, Oli F. Introduction to food-borne fungi. Centraalbureau Voor Schimmel Cultures Baarn Delft, 1995.
41. Youssef BM, Mahrous SR, Aziz NH. Effect of gamma irradiation on aflatoxin B1 production by Aspergillus flavus in ground beef stored at 5C. J Food Safety. 1999; 19(4): 231-239.
42. Tawakkol W, Khafaga NI. Fungal contamination of meat and its environment with special reference to the strains producing aflatoxins, ochratoxins, proteinase and lipase enzymes. New Egypt J Microbiol. 2007; 17(2): 1-14.
43. Battilani P, Pietri A, Giorni P, Formenti S, Bertuzzi T, Toscani T, et al. Penicillium populations in dry-cured ham manufacturing plants. J Food Prot. 2007; 70: 975-980.
44. Nielsen DS, Jacbsen T, Jesperson L, Koch AG, Arneborg N. Occurrence and growth of yeasts in processed meat products-implications for potential spoilage. Meat Sci. 2008; 80(3): 919-926.
45. Ahmed KE, Abdel-Sater MA. Mycological quality of Laban Rayeb sold in Assiut City. Assiut Vet Med J. 2003; 49(99): 75-77.
46. El-Diasty EM, Salem RM. Incidence of lipolytic and proteolytic fungi in some milk products and their public health significance. J Appl Sci Res. 2007; 3(12): 1684-1688.
47. Ghatass ZF, Soliman MM, Mohamed MM. Dielectric technique for quality control of beef meat in the range 10 kHz - 1 MHz. Am Euras J Sci Res. 2008; 3(1): 62-69.
48. Djamel C, Ali T, Nelly C. Acid protease production by isolated species of Penicillium. Eur J Sci Res. 2009; 25(3): 469-477.
49. Saleem A, El-Said AHM. Proteolytic activity of beef luncheon fungi as affected by incorporation of some food preservatives. Acta Microbiol Immunol Hung. 2009; 56(4): 417-426.
50. Nasser AL, El-Shanawany AA, Barakat A. Ecological and physiological studies on fungi associated with camel hairs from Saudi Arabia. 8th Con. 15-17. Fac. Vet. Med. Assiut Univ. Egypt, 1998.
51. Aravindan R, Anbumathi P, Viruthagiri T. Lipase applications in food industry. Ind J Biotechnol. 2007; 6: 141-158.
52. Griebeler N, Polloni A, Remonatto D, Arbter F, Vardanega R, Cechet J, et al. Isolation and screening of lipase-producing fungi with hydrolytic activity. Food Bioprocess Technol. 2011; 4(4): 578-586.
53. Nwuche CO, Ogbonna JC. Isolation of lipase producing fungi from palm oil mill effluent (pome) dump sites at Nsukka. Braz Arch Biol Technol. 2011; 54(1): 113-116.
54. Rajendra BK. Extracellular lipase enzyme production by seed-borne fungi under the influence of physical factors. Int J Biol. 2011; 3(1): 94-100.
55. Shivkumar M, Bhajbhuje MNF. Biodiversity of seed borne microfungal flora in storage on cauliflower (Brassica oleracea var. botrytis) from Nagpur region. Int J Life Sci. 2014: 43-47.
56. Gayatri DA, Madhuri V. Seed mycoflora of safflower and its control by using botanicals, bio-agent and fungicides - a review. Int J Appl Biol Pharm Technol. 2014; 5(1): 208-215.
57. Ghosh PK, Saxena RK, Gupta R, Yadav RP, Davidson S. Microbial lipases: production and applications. Sci Prog. 1996; 79: 119-157.
58. Barakat A, Abdel-Sater MA. Preliminary characterization and lipolytic activity of moulds associated with raw butter. Bull Fac Sci Assiut Univ. 1999; 28(1): 112-116.
59. de Maia MMD, de Morais MMC, de Morais Jr MA, Melo EHM, de Filho JLL. Production of extracellular lipase by the phytopathogenic fungus Fusarium solani fs1. Revista Microbiol. 1999; 30: 304-309.
60. Colen G, Junqueira BG, Moraes-Santos T. Isolation and screening of alkaline lipase-producing fungi from Brazilian savanna soil. World J Microbiol Biotechnol. 2006; 22(8): 881-885.
61. Hasan S, Ahmad A, Purwar A, Khan N, Kundan R, Gupta G. Production of extracellular enzymes in the entomopathogenic fungus Verticillium lecanii. Bioinf. 2013; 9(5): 238-242.
62. Esteves AC, Saraiva M, Correia A, Alves A. Botryosphaeriales fungi produce extracellular enzymes with biotechnological potential. Can J Microbiol. 2014; 60(5): 332-342.
63. Costa-Silva TA, Souza CRF, Oliveira WP, Said S. Characterization and spray drying of lipase produced by endophytic fungus Cercospora kikuchii. Braz J Chem Eng. 2014; 31(4): 849-858.
2. Gill CO. Microbiological contamination of meat during slaughter and butchering of cattle, sheep and pigs. In: Davies A, Board R, eds. The microbiology of meat and poultry. London: Blackie Academic and Professional, 1998; 118-157.
3. Pietzsch O, Kawerau H. Salmonellen in Schweinesch 5 lachtund Zerlegebetrieben sowie Schweinehackfleisch. Vet Med Hefte. 4. Bundesgesundheitsamt, Berlin, 1984.
4. Bell RG. Distribution and sources of microbial contamination on beef carcasses. J Appl Microobiol. 1997; 82: 292-300.
5. Farber JM, Idziak ES. Attachment of psychrotrophic meat spoilage bacteria to muscle surfaces. J Food Prot. 1984; 47: 92-95.
6. Mukhopadhyay HK, Pillai RM, Pal UK, Ajay Kumar VJ. Microbial quality of fresh chevon and beef in retail outlets of Pondicherry. Tamilnadu J Vet Animal Sci. 2009; 5 (1): 33-36.
7. Draughon FA, Melton CC, Maxedon D. Microbial profiles of country-cured hams age in Stockinettes. Barrier Bags, and Paraff, 1981.
8. Nassar AM, Ismail MA. Psychrotrophic and mesophilic fungi isolated from imported frozen lean meat in Egypt. J Food Safety. 1994; 14(4): 289-295.
9. Ismail MA, Abou-Elala AH, Nassar A, Michail DG. Fungal contamination of beef carcasses and the environment in a slaughterhouse. Food Microbiol. 1995; 12: 441-445.
10. Nunez F, Rodríguez MM, Bermudez ME, Cordoba JJ, Asensio MA. Composition and toxigenic potential of the mould population on dry-cured Iberian ham. Int J Food Microbiol. 1996; 32: 185-197.
11. Ismail MA, Zaky ZM. Evaluation of the mycological status of luncheon meat with special reference to aflatoxigenic moulds and aflatoxin residues. Mycopathol. 1999; 146: 147-154.
12. Laich F, Fierro F, Martín JF. Production of penicillin by fungi growing on food products: identification of a complete penicillin gene cluster in Penicillium griseofulvum and a truncated cluster in Penicillium verrucosum. Appl Environ Microbiol. 2001; 68(3): 1211-1219.
13. Mižãkovã A, Pipovã M, Turek P. The occurrence of moulds in fermented raw meat products. Czech J Food Sci. 2002; 20: 89-94.
14. Martín A, Juan JC, Felix N, Maria JB, Miguel AA. Contribution of a selected fungal population to proteolysis on dry-cured ham. Int J Food Microbiol. 2004; 94: 55-66.
15. Elmali M, Yaman H. Microbiological quality of raw meat balls: produced and sold in the Eastern of Turkey. Pakistan J Nut. 2005; 4(4): 197-201.
16. Wang X, Ma P, Jiang D, Peng Q, Yang H. The natural microflora of Xuanwei ham and the no-mouldy ham production. J Food Eng. 2006; 77: 103-111.
17. Saleem A. Effect of some food preservatives on the lipolytic activity of beef luncheon fungi. Mycobiol. 2008; 36(3): 167-172.
18. Iacumin L, Chiesa L, Boscolo D, Manzano M, Cantoni C, Orlic S, et al. Moulds and ochratoxin A on surfaces of artisanal and industrial dry sausages. Food Microbiol. 2009; 26: 65-70.
19. Sonjak S, Ličen M, Frisvad JC, Cimerman NG. The mycobiota of three dry-cured meat products from Slovenia. Food Microbiol. 2011; 28(3): 373-376
20. Desnuelle P. In the enzymes III. Boyer PD, ed. Academic Press, New York, 1972: 575-616.
21. Macrae AR. In microbial enzymes and technology. Fogarty WM, ed. Appl Sci London, 1983: 225-250.
22. Tauro P, Kapoor KK, Yadav KS. An introduction to microbiology. 1st edn. New Age International Publisher. New Delhi, India, 1986.
23. Pitt JI, Hocking AD. Fungi and food spoilage. 3rd edn, Springer, London, New York, 2009.
24. Smith NI, Dawson VT. The bacteriostatic action of rose bengal in media used for the plate counts of fungi. Soil Sci. 1944; 58: 467-471.
25. Al-Doory Y. Laboratory medical mycology. Lea Febiger Philadelphia Kimpton Publishers, London, 1980: 357-367.
26. Raper KB, Funnell DJ. The genus Aspergillus. Williams and Wilkins, Baltimore, USA, 1965.
27. Booth C. The genus Fusarium. Kew, UK., Commonwealth Mycological Institute, 1971.
28. Ellis MB. Dematiaceous hyphomycetes. Commonwealth Mycological Institute, Kew, Surrey, England, 1971.
29. Ellis MB. More dematiaceus hyphomycetes, Commonwealth Mycological institute, Kew, Surrey, England, 1976.
30. Pitt JI. The genus Penicillium and its telemorphic states. Eupenicillium and Talaromyces. Academic Press, London, 1979.
31. Moubasher AH. Soil fungi in Qatar and other Arab countries. Scientific and Applied Research Center. University of Qatar, Doha, Qatar, 1993.
32. Domsch KH, Gams W, Anderson T-H. Compendium of soil fungi. 2nd edn, IHW-Verlag, Eching, 2007.
33. Paterson RRM, Bridge PD. Biochemical techniques for filamentous fungi. Int. Mycol. Instit. CAB international, Surrey, 1994; 21.
34. Ullman V, Blasins G. A simple medium for the detection of different lipolytic activity of microorganisms. Zentrabl Bakteriol J Hyg. 1974; 229: 264-267.
35. Farghaly RM, Gherbawy YAMH, Yosef MS. Contamination of meat stored in home refrigerators in Qena (Egypt). Czech Mycol. 2004; 56: 53-62.
36. Sørensen LM, Jacobsen T, Nielsen PV, Frisvad JC, Koch AG. Mycobiota in the processing areas of two different meat products. Int J Food Microbiol. 2008; 124(1): 58-64.
37. Omorodion NJPN, Odu NN. Microbiological quality of meats sold in Port Harcaurt Metropolis, Nigeria. Nat Sci. 2014; 12(2): 58-62.
38. Asefa DT, Kure CF, Gjerde RO, Omer MK, Langsrud S, Nesbakken T, Skaar I. Fungal growth pattern, sources and factors of mould contamination in a dry-cured meat production facility. Int J Food Microbiol. 2010; 140: 131-135.
39. Pal M, Bagi AS. Fungi isolated from lymph nodes of buffaloes. Mycoses. 1989; 32(11): 578-580.
40. Robert AS, Ellen SH, Jens CF, Oli F. Introduction to food-borne fungi. Centraalbureau Voor Schimmel Cultures Baarn Delft, 1995.
41. Youssef BM, Mahrous SR, Aziz NH. Effect of gamma irradiation on aflatoxin B1 production by Aspergillus flavus in ground beef stored at 5C. J Food Safety. 1999; 19(4): 231-239.
42. Tawakkol W, Khafaga NI. Fungal contamination of meat and its environment with special reference to the strains producing aflatoxins, ochratoxins, proteinase and lipase enzymes. New Egypt J Microbiol. 2007; 17(2): 1-14.
43. Battilani P, Pietri A, Giorni P, Formenti S, Bertuzzi T, Toscani T, et al. Penicillium populations in dry-cured ham manufacturing plants. J Food Prot. 2007; 70: 975-980.
44. Nielsen DS, Jacbsen T, Jesperson L, Koch AG, Arneborg N. Occurrence and growth of yeasts in processed meat products-implications for potential spoilage. Meat Sci. 2008; 80(3): 919-926.
45. Ahmed KE, Abdel-Sater MA. Mycological quality of Laban Rayeb sold in Assiut City. Assiut Vet Med J. 2003; 49(99): 75-77.
46. El-Diasty EM, Salem RM. Incidence of lipolytic and proteolytic fungi in some milk products and their public health significance. J Appl Sci Res. 2007; 3(12): 1684-1688.
47. Ghatass ZF, Soliman MM, Mohamed MM. Dielectric technique for quality control of beef meat in the range 10 kHz - 1 MHz. Am Euras J Sci Res. 2008; 3(1): 62-69.
48. Djamel C, Ali T, Nelly C. Acid protease production by isolated species of Penicillium. Eur J Sci Res. 2009; 25(3): 469-477.
49. Saleem A, El-Said AHM. Proteolytic activity of beef luncheon fungi as affected by incorporation of some food preservatives. Acta Microbiol Immunol Hung. 2009; 56(4): 417-426.
50. Nasser AL, El-Shanawany AA, Barakat A. Ecological and physiological studies on fungi associated with camel hairs from Saudi Arabia. 8th Con. 15-17. Fac. Vet. Med. Assiut Univ. Egypt, 1998.
51. Aravindan R, Anbumathi P, Viruthagiri T. Lipase applications in food industry. Ind J Biotechnol. 2007; 6: 141-158.
52. Griebeler N, Polloni A, Remonatto D, Arbter F, Vardanega R, Cechet J, et al. Isolation and screening of lipase-producing fungi with hydrolytic activity. Food Bioprocess Technol. 2011; 4(4): 578-586.
53. Nwuche CO, Ogbonna JC. Isolation of lipase producing fungi from palm oil mill effluent (pome) dump sites at Nsukka. Braz Arch Biol Technol. 2011; 54(1): 113-116.
54. Rajendra BK. Extracellular lipase enzyme production by seed-borne fungi under the influence of physical factors. Int J Biol. 2011; 3(1): 94-100.
55. Shivkumar M, Bhajbhuje MNF. Biodiversity of seed borne microfungal flora in storage on cauliflower (Brassica oleracea var. botrytis) from Nagpur region. Int J Life Sci. 2014: 43-47.
56. Gayatri DA, Madhuri V. Seed mycoflora of safflower and its control by using botanicals, bio-agent and fungicides - a review. Int J Appl Biol Pharm Technol. 2014; 5(1): 208-215.
57. Ghosh PK, Saxena RK, Gupta R, Yadav RP, Davidson S. Microbial lipases: production and applications. Sci Prog. 1996; 79: 119-157.
58. Barakat A, Abdel-Sater MA. Preliminary characterization and lipolytic activity of moulds associated with raw butter. Bull Fac Sci Assiut Univ. 1999; 28(1): 112-116.
59. de Maia MMD, de Morais MMC, de Morais Jr MA, Melo EHM, de Filho JLL. Production of extracellular lipase by the phytopathogenic fungus Fusarium solani fs1. Revista Microbiol. 1999; 30: 304-309.
60. Colen G, Junqueira BG, Moraes-Santos T. Isolation and screening of alkaline lipase-producing fungi from Brazilian savanna soil. World J Microbiol Biotechnol. 2006; 22(8): 881-885.
61. Hasan S, Ahmad A, Purwar A, Khan N, Kundan R, Gupta G. Production of extracellular enzymes in the entomopathogenic fungus Verticillium lecanii. Bioinf. 2013; 9(5): 238-242.
62. Esteves AC, Saraiva M, Correia A, Alves A. Botryosphaeriales fungi produce extracellular enzymes with biotechnological potential. Can J Microbiol. 2014; 60(5): 332-342.
63. Costa-Silva TA, Souza CRF, Oliveira WP, Said S. Characterization and spray drying of lipase produced by endophytic fungus Cercospora kikuchii. Braz J Chem Eng. 2014; 31(4): 849-858.
Published
2017-12-31
How to Cite
(1)
Abdel-Sater, M.; Al-Sharjabi, F.; Al-Ashwal, E. Mycological and Enzymatic Studies on Fresh Beef Meat Sold in Taiz City, Yemen. European Journal of Biological Research 2017, 7, 337-347.
Section
Research Articles
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