International Journal of Nutrition and Food Sciences

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Behavior of Salmonella Heidelberg in Fruit Juices

Received: 03 February 2013    Accepted:     Published: 10 March 2013
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Abstract

The aim of the study is determination of the behavior of Salmonella heidelberg under acidic conditions and variable temperatures. The growth and survival of Salmonella heidelberg (10 isolates) in fresh fruit juices including; apple (pH, 3.2-1.4), orange (pH, 5.4 –1.5), mango (pH, 5.4-2.8), guava (pH, 5.7-2.4), pineapple (pH, 5.6-2.3), and cocktail (pH, 5.7-2.3) were determined after 0, 3, 6, 9, 12, 15, 18 and 21 days of storage at 10 ºC, 0, 3, 6, 9, 12 and 15 days of storage at 25 ºC, and 0, 3, 6 and 9 days of storage at 37 ºC. Survival in fruit juices depended upon their pH, the type of strain, the type of juices and the incubation temperature. Salmonella heidelberg Survived for up to 18 d in mango, guava, pineapple and cocktail juices, orange juice for up to 15 d and apple juice for up to 12 d stored at 10 ºC. At 20 ºC, Salmonella heidelberg was survived for up to 12 d in guava, pineapple and cocktail juices, 9 d for mango juice, orange juice for up to 9 d and apple juice for up to 6 d. The shortest survival time was observed at 37 ºC for 9 d in mango, guava, pineapple, cocktail juices, 6 d for orange as well as 3 d for apple juices respectively. These findings indicated that, as temperatures of acidify fresh fruit juices (apple, orange, mango, guava, pineapple and cocktail juices, respectively) increase as Salmonella heidelberg population decrease. The author reported that, Acid foods, especially if kept at refrigeration temperatures, support survival of Salmonella heidelberg and may cause Salmonella heidelberg food poisoning.

DOI 10.11648/j.ijnfs.20130202.13
Published in International Journal of Nutrition and Food Sciences (Volume 2, Issue 2, March 2013)
Page(s) 38-44
Creative Commons

This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited.

Copyright

Copyright © The Author(s), 2024. Published by Science Publishing Group

Keywords

Salmonella heidelberg, Behavior, Fruit Juices, pH and Temperature

References
[1] Mead PS, Slutsker L, Dietz V, et al. Food-related illness and death in the United States. Emerg In-fect Dis 1999;5:607–625.
[2] Voetsch AC, Van Gilder TJ, Angulo FJ, et al. (2004). FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin. Infect. Dis., 38 Suppl 3: S127–S134.
[3] Williams, J. E. (1965). Paratyphoid and arizona infections, p. 260-328. In H. E. Biester and L. H. Schwarte [ed.], Diseases of poultry, 5th ed. The Iowa State Univ. Press, Ames.
[4] CDC. 2007. National Antimicrobial Resistance Monitoring System for Enteric Bacteria (NARMS): human isolates final report, 2003. CDC, Atlanta, GA.
[5] CDC. 2007. National Antimicrobial Resistance Monitoring System for Enteric Bacteria (NARMS): human isolates final report, 2004. CDC, Atlanta, GA.
[6] FDA. 2006. National Antimicrobial Resistance Monitoring System—Enteric Bacteria (NARMS): 2003 Executive Report. FDA, Bethesda, MD.
[7] Zhao, S., P. F. McDermott, S. Friedman, J. Abbott, S. Ayers, A. Glenn, E. Hall-Robinson, S. K. Hubert, H. Harbottle, R. D. Walker, T. M. Chiller, and D. G. White (2006). Antimicrobial resistance and genetic relatedness among Salmonella from retail foods of animal origin: NARMS retail meat surveillance. Foodborne Pathog. Dis. 3:106–117.
[8] Chittick, P., A. Sulka, R. V. Tauxe, and A. M. Fry. (2006). A summary of national reports of food-borne outbreaks of Salmonella heidelberg infections in the United States: clues for disease prevention. J. Food Prot. 69:1150–1153.
[9] Currie, A., L. MacDougall, J. Aramini, C. Gaulin, R. Ahmed, and S. Isaacs. (2005). Frozen chicken nuggets and strips and eggs are leading risk factors for Salmonella heidelberg in-fections in Cana-da. Epidemiol. Infect. 133:809–816.
[10] PHAC (Public Health Agency of Canada) (2007). Salmonella heidelberg ceftiofur related resistance in human and retail chicken isolates. Public Health Agency of Canada, Guelph, Ontario, Canada. http://www.phac-aspc.gc.ca/cipars-picra/heidelberg/pdf/heidelberg_e.pdf.
[11] Barnass, S., M. O’Mahony, P. N. Sockett, J. Garner, J. Franklin, and S. Tabaqchali. (1989). The tangible cost im-plications of a hospital outbreak of multiply-resistant Sal-monella. Epidemiol. In-fect. 103:227–234.
[12] CDC, (1986). Salmonella heidelberg outbreak at a conven-tion—New Mexico. MMWR Morb. Mortal. Wkly. Rep. 35:91.
[13] Choi, M., T. T. Yoshikawa, J. Bridge, A. Schlaifer, D. Os-terweil, D. Reid, and D. C. Norman. (1990). Salmonella outbreak in a nursing home. J. Am. Geriatr. Soc. 38:531–534.
[14] Layton, M. C., S. G. Calliste, T. M. Gomez, C. Patton, and S. Brooks (1997). A mixed foodborne outbreak with Salmonella heidelberg and Campylobacter jejuni in a nursing home. Infect. Control Hosp. Epidemiol. 18:115–121.
[15] Lyons, R. W., C. L. Samples, H. N. DeSilva, K. A. Ross, E. M. Julian, and P. J. Checko. (1980). An epidemic of resistant Salmonella in a nursery. Animal-tohuman spread. JAMA 243:546–547.
[16] Feng, P. (1992). Commercial assay systems for the detecting food borne Salmonella: a review. J. Food Prot. 55:927-934.
[17] Tietjen, M. and D. Y. C. Fung, (1995). Salmonellae and food safety. Crit. Rev. Microbiol. 21(1):53-83.
[18] Beuchat, L. R., (1995). Pathogenic microorganisms associated with fresh produce. J. Food Prot. 59:204-216.
[19] D’Aoust, J., (1997). Salmonella species, p. 135-137. In M. P. Doyle, L. R. Beuchat, and T. J. Montville (ed.), Food micro-biology: fundamentals and frontiers. American Society for Microbiol-ogy, Washington, D.C.
[20] Doyle, M. P., T. Zhao, J. Meng, and S. Zhao, (1997). E. coli O157:H7, p. 175-178. In M. P. doyle, L. R. Beuchat and T. J. Montville (ed.), Food Microbiology: fundamentals and fron-tiers. Ameri-can Society for Microbiology, Washington, D.C.
[21] Cohen, J. I., J. A. Bartlett, and G. Ralph Corey, (1987). Ex-tra-intestinal manifestations of Salmonella infections. Medicine 66:349-387.
[22] Goldberg MB, Rubin RH. (1988). The spectrum of Salmonella infection. Infect Dis Clin North Am. 1988 Sep;2(3):571-598.
[23] Rodriguez M., De Diego I., and Carmen M. M. (1998). Extraintestinal Salmonellosis in a General Hospital (1991 to 1996): Relationships between Salmonella Genomic Groups and Clinical Presentations. J. Clin. Microbiol., 36(11): 3291–3296
[24] Buchanan, R. L. and Edelson, S. G. (1996). Culturing ente-rohaemorrhagic E. coli in the presence and absence of glucose as a simple means of evaluating the acid tolerance of stationary phase cells. Appl. Environm. Microbiol., 62:4009-4013.
[25] McCarthy, J., Holbrook R. and Stephens, P. J. (1998). An improved direct plate method for the enumeration of stressed E. coli O157:H7 from food. J. Food Prot., 61:1093-1097.
[26] Jordan, K. N., Hall S. and MacClure P. J. (1999). Osmotic stress on dilution of acid injured E. coli O157:H7. Lett. Appl. Microbiol.. 28:389-393.
[27] Deng, Y., Ryu J. H. and Beuchat, L. R. (1999). Tolerance of acid-adapted and non-adapted E. coli O157:H7 cells to reduced pH as affected by type of acidulant. J. Appl. Microbiol., 86:203-210.
[28] Gomutputra , C. and Fabian, F. W. (1953). Acids and chlo-ramphenicol as sanitizing agents for meat contaminated with food-poisoning organisms. Journal of Milk and Food Tech-nology 16, 220-227.
[29] El-Safey, E. M. and Ammar M. S., (2002c). Survival and growth of E. coli O157:H7 population in acidulous pickled vegetables. 18th international ICFMH Symposium Food Micro 2002, Lille-hammer, Norway 18-23 August 2002. pp. 217.
[30] Vantarakis A, Affifi M, Kokkinos P, Tsibouxi M, Papape-tropoulou M. (2011). Occurrence of microorganisms of public health and spoilage significance in fruit juices sold in retail markets in Greece. Anaerobe. 17(6):288-291.
[31] HE and Ingham SC (1999). Combinations of Intervention Treatments Resulting in 5-Log10-Unit Reductions in Numbers of Escherichia coli O157:H7 and Salmonella typhimurium DT104 Organ-isms in Apple Cider. Appl. Environ. Microb., 65( 5): 1924–1929
[32] Noël H, Hofhuis A, De Jonge R, Heuvelink AE, De Jong A, Heck ME, De Jager C, van Pelt W. (2010). Consumption of fresh fruit juice: how a healthy food practice caused a national outbreak of Salmonella Panama gastroenteritis. Foodborne Pathog Dis. 2010 Apr;7(4):375-381.
[33] Bagamboula CF, Uyttendaele M, Debevere J. (2002). Acid tolerance of Shigella sonnei and Shigella flexneri. J. Appl. Microbiol. 93(3):479-486.
[34] El-Safey, E. M., (2001). Search for E. coli O157:H7 in Egyptian foods and dairy products. PhD. Sci. A thesis, Bot. and Microbiol. Dept., Fac. Sci., Al-Azhar Univ., Cairo, Egypt.
[35] Anderson, M. E., Huff H. E., Naumann H. D., Damare J. M., Partt M., Johnson R. and Marshall R. T., (1987a). Evaluation of an automated beef carcass washing and santizing system under production conditions. J. Food Prot. 50 : 562-566.
[36] Anderson, W. H., Wildon C. R. and Poelma P. L., (1987b). Glucuronidase assay in a rapid MPN determination for E. coli from selcted foods. J. Assoc. Off. Anol. Chem. 70 : 31-34.
[37] Dickson J. S. and Anderson, M. E. (1992). Microbiological decontamination of food animal car-casses by washing and sanitizing systems: a review. J. food prot. 55:133-140.
[38] Nicolò MS, Gioffrè A, Carnazza S, Platania G, Silvestro ID, Guglielmino SP.(2011). Viable but nonculturable state of foodborne pathogens in grapefruit juice: a study of laboratory. Foodborne Pathog. Dis., 8(1):11-17.
[39] Truong VT, Boyer RR, McKinney JM, O'Keefe SF, Williams RC. (2010). Effect of alpha-cyclodextrin-cinnamic acid in-clusion complexes on populations of Escherichia coli O157:H7 and Salmonella enterica in fruit juices. J Food Prot. 73(1):92-96.
[40] Little CL, Mitchell RT; Food Standards Agency; Local Au-thorities Coordinators of Regulatory Services; Health Pro-tection Agency (2004). Microbiological quality of pre-cut fruit, sprouted seeds, and unpasteurised fruit and vegetable juices from retail and production premises in the UK, and the application of HAACP. Commun. Dis. Public Health., 7(3):184-190.
[41] Raybaudi-Massilia RM, Mosqueda-Melgar J, Martín-Belloso O (2006). Antimicrobial activity of essential oils on Salmonella enteritidis, Escherichia coli, and Listeria innocua in fruit juices. J. Food Prot., 69(7):1579-1586.
[42] Whitney BM, Williams RC, Eifert J, Marcy J. (2007). High-pressure resistance variation of Esche-richia coli O157:H7 strains and Salmonella serovars in tryptic soy broth, distilled water, and fruit juice. J. Food Prot. 70(9):2078-2083.
[43] Mosqueda-Melgar J, Elez-Martínez P, Raybaudi-Massilia RM, Martín-Belloso O (2008a). Effects of pulsed electric fields on pathogenic microorganisms of major concern in fluid foods: a review. Crit. Rev. Food Sci. Nutr., 48(8):747-59.
[44] Mosqueda-Melgar J, Raybaudi-Massilia RM, Martín-Belloso O (2008b). Combination of high-intensity pulsed electric fields with natural antimicrobials to inactivate pathogenic microorgan-isms and extend the shelf-life of melon and wa-termelon juices. Food Microbiol. 25(3):479-491.
[45] Alvarez-Ordóñez A, Fernández A, Bernardo A, López M (2009). A comparative study of thermal and acid inactivation kinetics in fruit juices of Salmonella enterica serovar Ty-phimurium and Salmonella enterica serovar Senftenberg grown at acidic conditions. Foodborne Pathog Dis., 6(9):1147-1155.
[46] Duan J, Zhao Y. (2009). Antimicrobial efficiency of essential oil and freeze-thaw treatments against Escherichia coli O157:H7 and Salmonella enterica Ser. Enteritidis in straw-berry juice. J. Food Sci., 74(3):M131-137.
[47] McClure, P. J. and Hall, S. (2000). Survival of E. coli O157:H7 in foods. J. Appli. Microbiol. Sympo. Suppl., 88:61S-70S.
[48] Wong E, Vaillant F, Pérez A. (2010). Osmosonication of blackberry juice: impact on selected pathogens, spoilage microorganisms, and main quality parameters. J Food Sci., 75(7):M468-474.
[49] Lee SY, Sagong HG, Ryu S, Kang DH. (2012). Effect of continuous ohmic heating to inactivate Escherichia coli O157:H7, Salmonella typhimurium and Listeria monocyto-genes in orange juice and tomato juice. J Appl Microbiol. 2012 Apr;112(4):723-731.
[50] USDA. National Antimicrobial Resistance Monitoring System for Enteric Bacteria (NARMS). USDA, Washington, DC. http://www.ars.usda.gov/Main/docs.htm?docid_6750&page_4.
Author Information
  • Faculty of Science, Al-Azhar University. Assuit branch, P.O. 71542, .Assuit. EGYPT; on Secondment to College of Applied Medical Science, Majmaah University, AlMajmaah, 11952, Pox. 1816, KSA

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    El-Safey Mohamed El-Safey. (2013). Behavior of Salmonella Heidelberg in Fruit Juices. International Journal of Nutrition and Food Sciences, 2(2), 38-44. https://doi.org/10.11648/j.ijnfs.20130202.13

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    El-Safey Mohamed El-Safey. Behavior of Salmonella Heidelberg in Fruit Juices. Int. J. Nutr. Food Sci. 2013, 2(2), 38-44. doi: 10.11648/j.ijnfs.20130202.13

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    AMA Style

    El-Safey Mohamed El-Safey. Behavior of Salmonella Heidelberg in Fruit Juices. Int J Nutr Food Sci. 2013;2(2):38-44. doi: 10.11648/j.ijnfs.20130202.13

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  • @article{10.11648/j.ijnfs.20130202.13,
      author = {El-Safey Mohamed El-Safey},
      title = {Behavior of Salmonella Heidelberg in Fruit Juices},
      journal = {International Journal of Nutrition and Food Sciences},
      volume = {2},
      number = {2},
      pages = {38-44},
      doi = {10.11648/j.ijnfs.20130202.13},
      url = {https://doi.org/10.11648/j.ijnfs.20130202.13},
      eprint = {https://download.sciencepg.com/pdf/10.11648.j.ijnfs.20130202.13},
      abstract = {The aim of the study is determination of the behavior of Salmonella heidelberg under acidic conditions and variable temperatures. The growth and survival of Salmonella heidelberg (10 isolates) in fresh fruit juices including; apple (pH, 3.2-1.4), orange (pH, 5.4 –1.5), mango (pH, 5.4-2.8), guava (pH, 5.7-2.4), pineapple (pH, 5.6-2.3), and cocktail (pH, 5.7-2.3) were determined after 0, 3, 6, 9, 12, 15, 18 and 21 days of storage at 10 ºC, 0, 3, 6, 9, 12 and 15 days of storage at 25 ºC, and 0, 3, 6 and 9 days of storage at 37 ºC. Survival in fruit juices depended upon their pH, the type of strain, the type of juices and the incubation temperature. Salmonella heidelberg Survived for up to 18 d in mango, guava, pineapple and cocktail juices, orange juice for up to 15 d and apple juice for up to 12 d stored at 10 ºC. At 20 ºC, Salmonella heidelberg was survived for up to 12 d in guava, pineapple and cocktail juices, 9 d for mango juice, orange juice for up to 9 d and apple juice for up to 6 d. The shortest survival time was observed at 37 ºC for 9 d in mango, guava, pineapple, cocktail juices, 6 d for orange as well as 3 d for apple juices respectively. These findings indicated that, as temperatures of acidify fresh fruit juices (apple, orange, mango, guava, pineapple and cocktail juices, respectively) increase as Salmonella heidelberg population decrease. The author reported that, Acid foods, especially if kept at refrigeration temperatures, support survival of Salmonella heidelberg and may cause Salmonella heidelberg food poisoning.},
     year = {2013}
    }
    

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  • TY  - JOUR
    T1  - Behavior of Salmonella Heidelberg in Fruit Juices
    AU  - El-Safey Mohamed El-Safey
    Y1  - 2013/03/10
    PY  - 2013
    N1  - https://doi.org/10.11648/j.ijnfs.20130202.13
    DO  - 10.11648/j.ijnfs.20130202.13
    T2  - International Journal of Nutrition and Food Sciences
    JF  - International Journal of Nutrition and Food Sciences
    JO  - International Journal of Nutrition and Food Sciences
    SP  - 38
    EP  - 44
    PB  - Science Publishing Group
    SN  - 2327-2716
    UR  - https://doi.org/10.11648/j.ijnfs.20130202.13
    AB  - The aim of the study is determination of the behavior of Salmonella heidelberg under acidic conditions and variable temperatures. The growth and survival of Salmonella heidelberg (10 isolates) in fresh fruit juices including; apple (pH, 3.2-1.4), orange (pH, 5.4 –1.5), mango (pH, 5.4-2.8), guava (pH, 5.7-2.4), pineapple (pH, 5.6-2.3), and cocktail (pH, 5.7-2.3) were determined after 0, 3, 6, 9, 12, 15, 18 and 21 days of storage at 10 ºC, 0, 3, 6, 9, 12 and 15 days of storage at 25 ºC, and 0, 3, 6 and 9 days of storage at 37 ºC. Survival in fruit juices depended upon their pH, the type of strain, the type of juices and the incubation temperature. Salmonella heidelberg Survived for up to 18 d in mango, guava, pineapple and cocktail juices, orange juice for up to 15 d and apple juice for up to 12 d stored at 10 ºC. At 20 ºC, Salmonella heidelberg was survived for up to 12 d in guava, pineapple and cocktail juices, 9 d for mango juice, orange juice for up to 9 d and apple juice for up to 6 d. The shortest survival time was observed at 37 ºC for 9 d in mango, guava, pineapple, cocktail juices, 6 d for orange as well as 3 d for apple juices respectively. These findings indicated that, as temperatures of acidify fresh fruit juices (apple, orange, mango, guava, pineapple and cocktail juices, respectively) increase as Salmonella heidelberg population decrease. The author reported that, Acid foods, especially if kept at refrigeration temperatures, support survival of Salmonella heidelberg and may cause Salmonella heidelberg food poisoning.
    VL  - 2
    IS  - 2
    ER  - 

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