Rapid and sensitive method for detection of Staphylococcus aureus enterotoxin genes in milk sample

Mahantesh M Kurjogi; Basappa B Kaliwal

doi:10.7324/JABB.2018.60203

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Abstract

Staphylococcus aureus is a common microflora present on skin and mucous membrane of cattle. Despite its amiable nature, S. aureus can turn shrewd and get to be distinctly pathogenic. Staphylococcus present in the milk may produce numerous potential destructive variables, like toxins. Consequently, consumption of S. aureus contaminant milk may result in Staphylococcal food poisoning (SFP). Therefore, the present study was carried out to evaluate the presence of Se-encoding genes in S. aureus and also validate the detection of toxin genes directly from the milk sample contaminated with S. aureus using real-time polymerase chain reaction (RT-PCR). The RT-PCR results were reported as Ct values, which confirmed the presence of enterotoxin genes in the S. aureus isolates and milk samples. Application of RT-PCR for the detection of Se genes in cultures of S. aureus and also from milk samples revealed the probable onset of SFP. Therefore, the study suggests that the analysis of milk for the presence of any toxin genes should be strictly performed before reaching the consumer.

Keyword: Staphylococcus aureus Enterotoxin Mastitis Food poisoning Real-time polymerase chain reaction Milk.

Citation:

Kurjogi MM, Kaliwal BB. Rapid and sensitive method for detection of Staphylococcus aureus enterotoxin genes in milk sample. J App Biol Biotech. 2018;6(2):15-19. DOI: 10.7324/JABB.2018.60203

Copyright: Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike license.

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Reference

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2. Hokmabad RV, Mogaddam MF, Sadegh MM, Mirzaii H. Bacterial pathogens of intramammary infections in Azeri buffaloes of Iran and their antibiogram. Afr J Agric Res 2011;6:2516-21.
3. Kurjogi MM, Kaliwal BB. Prevalence and antimicrobial susceptibility of bacteria isolated from bovine mastitis. Adv Appl Sci Res 2011;2:229-35.
4. Derzelle S, Dilasser F, Duquenne M, Deperrois V. Differential temporal expression of the staphylococcal enterotoxins genes during cell growth. Food Microbiol 2009;26:896-904. https://doi.org/10.1016/j.fm.2009.06.007
5. Larkin EA, Carman RJ, Krakauer T, Stiles BG. Staphylococcus aureus: The toxic presence of a pathogen extraordinaire. Curr Med Chem 2009;16:4003-19. https://doi.org/10.2174/092986709789352321
6. Evenson ML, Hinds MW, Bernstein RS, Bergdoll MS. Estimation of human dose of staphylococcal enterotoxin A from a large outbreak of staphylococcal food poisoning involving chocolate milk. Int J Food Microbiol 1988;7:311-6. https://doi.org/10.1016/0168-1605(88)90057-8
7. Le Loir Y, Baron F, Gautier M. Staphylococcus aureus and food poisoning. Gen Mol Res 2003;2:63-76.
8. Murray RJ. Recognition and management of Staphylococcus aureus toxin-mediated disease. Intern Med J 2005;35 Suppl 2:S106-19. https://doi.org/10.1111/j.1444-0903.2005.00984.x
9. Nakayama A, Okayama A, Hashida M, Yamamoto Y, Takebe H, Ohnaka T, et al. Development of a routine laboratory direct detection system of staphylococcal enterotoxin genes. J Med Microbiol 2006;55:273-7. https://doi.org/10.1099/jmm.0.46027-0
10. Muhammad G, Athar M, Shakoor A, Khan MZ, Rahman F, Ahmad MT. Surf field mastitis test: An expensive new tool for evaluation of wholesomeness of fresh milk. Pak J Food Sci 1995;5:91-3.
11. Kurjogi MM, Kaliwal RB, Shivasharana CT, Kaliwal BB. Characterization of toxin genes in Staphylococcus aureus isolated from milk of cows with mastitis. Int J Rec Sci Res 2012;3:841-6.
12. Moore E, Arnscheidt A, Kruger A, Stromp C, Mau M. Simplified protocols for the preparation of genomic DNA from bacterial cultures. Mol Microb Ecol Man 2004;1:3-18.
13. Holmberg SD, Blake PA. Staphylococcal food poisoning in the united states. New facts and old misconceptions. JAMA 1984;251:487-9. https://doi.org/10.1001/jama.1984.03340280037024
14. Huang IY, Hughes JL, Bergdoll MS, Schantz EJ. Complete amino acid sequence of staphylococcal enterotoxin A. J Biol Chem 1987;262:7006-13.
15. Betley MJ, Mekalanos JJ. Nucleotide sequence of the Type A staphylococcal enterotoxin gene. J Bacteriol 1988;170:34-41. https://doi.org/10.1128/jb.170.1.34-41.1988
16. Johns MB Jr, Khan SA. Staphylococcal enterotoxin B gene is associated with a discrete genetic element. J Bacteriol 1988;170:4033-9. https://doi.org/10.1128/jb.170.9.4033-4039.1988
17. Sugiyama H, Hayama T. Abdominal viscera as site of emetic action for staphylococcal enterotoxin in the monkey. J Infect Dis 1965;115:330-6. https://doi.org/10.1093/infdis/115.4.330
18. Shanahan F, Denburg JA, Fox J, Bienenstock J, Befus D. Mast cell heterogeneity: Effects of neuroenteric peptides on histamine release. J Immunol 1985;135:1331-7.
19. Scheuber PH, Denzlinger C, Wilker D, Beck G, Keppler D, Hammer DK, et al. Cysteinyl leukotrienes as mediators of staphylococcal enterotoxin B in the monkey. Eur J Clin Invest 1987;17:455-9. https://doi.org/10.1111/j.1365-2362.1987.tb01142.x
20. Alber G, Scheuber PH, Reck B, Sailer-Kramer B, Hartmann A, Hammer DK, et al. Role of substance P in immediate-type skin reactions induced by staphylococcal enterotoxin B in unsensitized monkeys. J Allergy Clin Immunol 1989;84:880-5. https://doi.org/10.1016/0091-6749(89)90383-7
21. Jett M, Brinkley W, Neill R, Gemski P, Hunt R. Staphylococcus aureus enterotoxin B challenge of monkeys: Correlation of plasma levels of arachidonic acid cascade products with occurrence of illness. Infect Immun 1990;58:3494-9.
22. Kent TH. Staphylococcal enterotoxin gastroenteritis in rhesus monkeys. Am J Pathol 1966;48:387-407.
23. Sheehan DG, Jervis HR, Takeuchi A, Sprinz H. The effect of staphylococcal enterotoxin on the epithelial mucosubstance of the small intestine of rhesus monkeys. Am J Pathol 1970;60:1-18.
24. Hamad AR, Marrack P, Kappler JW. Transcytosis of staphylococcal superantigen toxins. J Exp Med 1997;185:1447-54. https://doi.org/10.1084/jem.185.8.1447
25. Rajkovic A, El-Moualij B, Uyttendaele M, Brolet P, Zorzi W, Heinen E, et al. Immunoquantitative real-time PCR for detection and quantification of Staphylococcus aureus enterotoxin B in foods. Appl Environ Microbiol 2006;72:6593-9. https://doi.org/10.1128/AEM.03068-05
26. Becker K, Friedrich AW, Lubritz G, Weilert M, Peters G, Von Eiff C, et al. Prevalence of genes encoding pyrogenic toxin superantigens and exfoliative toxins among strains of Staphylococcus aureus isolated from blood and nasal specimens. J Clin Microbiol 2003;41:1434-9. https://doi.org/10.1128/JCM.41.4.1434-1439.2003
27. Letertre C, Perelle S, Dilasser F, Fach P. Detection and genotyping by real-time PCR of the staphylococcal enterotoxin genes sea to sej. Mol Cell Probes 2003;17:139-47. https://doi.org/10.1016/S0890-8508(03)00045-8
28. Paule SM, Pasquariello AC, Thomson RB Jr. Kaul KL, Peterson LR. Real-time PCR can rapidly detect methicillin-susceptible and methicillin-resistant Staphylococcus aureus directly from positive blood culture bottles. Am J Clin Pathol 2005;124:404-7. https://doi.org/10.1309/6EA3U9V8NCLLGKQN
29. Klotz M, Opper S, Heeg K, Zimmermann S. Detection of Staphylococcus aureus enterotoxins A to D by real-time fluorescence PCR assay. J Clin Microbiol 2003;41:4683-7. https://doi.org/10.1128/JCM.41.10.4683-4687.2003
30. Asao T, Kumeda Y, Kawai T, Shibata T, Oda H, Haruki K, et al. An extensive outbreak of staphylococcal food poisoning due to low-fat milk in Japan: Estimation of enterotoxin A in the incriminated milk and powdered skim milk. Epidemiol Infect 2003;130:33-40. https://doi.org/10.1017/S0950268802007951
31. Heller LC, Davis CR, Peak KK, Wingfield D, Cannons AC, Amuso PT, et al. Comparison of methods for DNA isolation from food samples for detection of shiga toxin-producing Escherichia coli by real-time PCR. Appl Environ Microbiol 2003;69:1844-6. https://doi.org/10.1128/AEM.69.3.1844-1846.2003

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1. Fox LK, Gay JM. Contagious mastitis. Vet Clin North Am Food Anim Pract 1993;9:475-87. https://doi.org/10.1016/S0749-0720(15)30615-0

2. Hokmabad RV, Mogaddam MF, Sadegh MM, Mirzaii H. Bacterial pathogens of intramammary infections in Azeri buffaloes of Iran and their antibiogram. Afr J Agric Res 2011;6:2516-21.

3. Kurjogi MM, Kaliwal BB. Prevalence and antimicrobial susceptibility of bacteria isolated from bovine mastitis. Adv Appl Sci Res 2011;2:229-35.

4. Derzelle S, Dilasser F, Duquenne M, Deperrois V. Differential temporal expression of the staphylococcal enterotoxins genes during cell growth. Food Microbiol 2009;26:896-904. https://doi.org/10.1016/j.fm.2009.06.007

5. Larkin EA, Carman RJ, Krakauer T, Stiles BG. Staphylococcus aureus: The toxic presence of a pathogen extraordinaire. Curr Med Chem 2009;16:4003-19. https://doi.org/10.2174/092986709789352321

6. Evenson ML, Hinds MW, Bernstein RS, Bergdoll MS. Estimation of human dose of staphylococcal enterotoxin A from a large outbreak of staphylococcal food poisoning involving chocolate milk. Int J Food Microbiol 1988;7:311-6. https://doi.org/10.1016/0168-1605(88)90057-8

7. Le Loir Y, Baron F, Gautier M. Staphylococcus aureus and food poisoning. Gen Mol Res 2003;2:63-76.

8. Murray RJ. Recognition and management of Staphylococcus aureus toxin-mediated disease. Intern Med J 2005;35 Suppl 2:S106-19. https://doi.org/10.1111/j.1444-0903.2005.00984.x

9. Nakayama A, Okayama A, Hashida M, Yamamoto Y, Takebe H, Ohnaka T, et al. Development of a routine laboratory direct detection system of staphylococcal enterotoxin genes. J Med Microbiol 2006;55:273-7. https://doi.org/10.1099/jmm.0.46027-0

10. Muhammad G, Athar M, Shakoor A, Khan MZ, Rahman F, Ahmad MT. Surf field mastitis test: An expensive new tool for evaluation of wholesomeness of fresh milk. Pak J Food Sci 1995;5:91-3.

11. Kurjogi MM, Kaliwal RB, Shivasharana CT, Kaliwal BB. Characterization of toxin genes in Staphylococcus aureus isolated from milk of cows with mastitis. Int J Rec Sci Res 2012;3:841-6.

12. Moore E, Arnscheidt A, Kruger A, Stromp C, Mau M. Simplified protocols for the preparation of genomic DNA from bacterial cultures. Mol Microb Ecol Man 2004;1:3-18.

13. Holmberg SD, Blake PA. Staphylococcal food poisoning in the united states. New facts and old misconceptions. JAMA 1984;251:487-9. https://doi.org/10.1001/jama.1984.03340280037024

14. Huang IY, Hughes JL, Bergdoll MS, Schantz EJ. Complete amino acid sequence of staphylococcal enterotoxin A. J Biol Chem 1987;262:7006-13.

15. Betley MJ, Mekalanos JJ. Nucleotide sequence of the Type A staphylococcal enterotoxin gene. J Bacteriol 1988;170:34-41. https://doi.org/10.1128/jb.170.1.34-41.1988

16. Johns MB Jr, Khan SA. Staphylococcal enterotoxin B gene is associated with a discrete genetic element. J Bacteriol 1988;170:4033-9. https://doi.org/10.1128/jb.170.9.4033-4039.1988

17. Sugiyama H, Hayama T. Abdominal viscera as site of emetic action for staphylococcal enterotoxin in the monkey. J Infect Dis 1965;115:330-6. https://doi.org/10.1093/infdis/115.4.330

18. Shanahan F, Denburg JA, Fox J, Bienenstock J, Befus D. Mast cell heterogeneity: Effects of neuroenteric peptides on histamine release. J Immunol 1985;135:1331-7.

19. Scheuber PH, Denzlinger C, Wilker D, Beck G, Keppler D, Hammer DK, et al. Cysteinyl leukotrienes as mediators of staphylococcal enterotoxin B in the monkey. Eur J Clin Invest 1987;17:455-9. https://doi.org/10.1111/j.1365-2362.1987.tb01142.x

20. Alber G, Scheuber PH, Reck B, Sailer-Kramer B, Hartmann A, Hammer DK, et al. Role of substance P in immediate-type skin reactions induced by staphylococcal enterotoxin B in unsensitized monkeys. J Allergy Clin Immunol 1989;84:880-5. https://doi.org/10.1016/0091-6749(89)90383-7

21. Jett M, Brinkley W, Neill R, Gemski P, Hunt R. Staphylococcus aureus enterotoxin B challenge of monkeys: Correlation of plasma levels of arachidonic acid cascade products with occurrence of illness. Infect Immun 1990;58:3494-9.

22. Kent TH. Staphylococcal enterotoxin gastroenteritis in rhesus monkeys. Am J Pathol 1966;48:387-407.

23. Sheehan DG, Jervis HR, Takeuchi A, Sprinz H. The effect of staphylococcal enterotoxin on the epithelial mucosubstance of the small intestine of rhesus monkeys. Am J Pathol 1970;60:1-18.

24. Hamad AR, Marrack P, Kappler JW. Transcytosis of staphylococcal superantigen toxins. J Exp Med 1997;185:1447-54. https://doi.org/10.1084/jem.185.8.1447

25. Rajkovic A, El-Moualij B, Uyttendaele M, Brolet P, Zorzi W, Heinen E, et al. Immunoquantitative real-time PCR for detection and quantification of Staphylococcus aureus enterotoxin B in foods. Appl Environ Microbiol 2006;72:6593-9. https://doi.org/10.1128/AEM.03068-05

26. Becker K, Friedrich AW, Lubritz G, Weilert M, Peters G, Von Eiff C, et al. Prevalence of genes encoding pyrogenic toxin superantigens and exfoliative toxins among strains of Staphylococcus aureus isolated from blood and nasal specimens. J Clin Microbiol 2003;41:1434-9. https://doi.org/10.1128/JCM.41.4.1434-1439.2003

27. Letertre C, Perelle S, Dilasser F, Fach P. Detection and genotyping by real-time PCR of the staphylococcal enterotoxin genes sea to sej. Mol Cell Probes 2003;17:139-47. https://doi.org/10.1016/S0890-8508(03)00045-8

28. Paule SM, Pasquariello AC, Thomson RB Jr. Kaul KL, Peterson LR. Real-time PCR can rapidly detect methicillin-susceptible and methicillin-resistant Staphylococcus aureus directly from positive blood culture bottles. Am J Clin Pathol 2005;124:404-7. https://doi.org/10.1309/6EA3U9V8NCLLGKQN

29. Klotz M, Opper S, Heeg K, Zimmermann S. Detection of Staphylococcus aureus enterotoxins A to D by real-time fluorescence PCR assay. J Clin Microbiol 2003;41:4683-7. https://doi.org/10.1128/JCM.41.10.4683-4687.2003

30. Asao T, Kumeda Y, Kawai T, Shibata T, Oda H, Haruki K, et al. An extensive outbreak of staphylococcal food poisoning due to low-fat milk in Japan: Estimation of enterotoxin A in the incriminated milk and powdered skim milk. Epidemiol Infect 2003;130:33-40. https://doi.org/10.1017/S0950268802007951

31. Heller LC, Davis CR, Peak KK, Wingfield D, Cannons AC, Amuso PT, et al. Comparison of methods for DNA isolation from food samples for detection of shiga toxin-producing Escherichia coli by real-time PCR. Appl Environ Microbiol 2003;69:1844-6. https://doi.org/10.1128/AEM.69.3.1844-1846.2003