Survival kinetics of Listeria monocytogenes on chickpeas, sesame seeds, pine nuts, and black pepper as affected by relative humidity storage conditions

Autoři: Joelle K. Salazar aff001;  Vidya Natarajan aff001;  Diana Stewart aff001;  Quincy Suehr aff001;  Tanvi Mhetras aff002;  Lauren J. Gonsalves aff001;  Mary Lou Tortorello aff001
Působiště autorů: Division of Food Processing Science and Technology, U. S. Food and Drug Administration, Bedford Park, Illinois, United States of America aff001;  Institute for Food Safety and Health, Illinois Institute of Technology, Bedford Park, Illinois, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226362


Nuts and seeds have been increasingly associated with recalls due to contamination with Listeria monocytogenes. Storage of these food commodities occurs at various relative humidity (RH) conditions for months or years. The objective of this study was to assess L. monocytogenes survival on four commodities representing dried legumes, seeds, and spices categories: chickpeas, sesame seeds, pine nuts, and black pepper kernels. Inoculated products at 10 log CFU/g were stored for 180 days (6 months) at 25°C and different relative humidity (RH) levels: 25% (low), 45% (ambient), and 75% (high). After 180 days at 25% RH, L. monocytogenes populations decreased to 2.67–6.59 log CFU/g; the highest survival of the pathogen was observed on pine nuts and sesame seeds with decay rates of -0.014± 0.001 log CFU/g per d. Significantly greater population reductions on all products were observed during storage at 45 and 75% RH. At 45% RH, L. monocytogenes levels decreased to 1.90–6.36 log CFU/g. On chickpeas and black pepper stored at 75% RH, the pathogen population decreased to below the limit of enumeration (1 log CFU/g) yet were still detected via enrichments. The lowest survival of L. monocytogenes occurred at 75% RH on black pepper with a decay rate of -0.058±0.003 log CFU/g per d. Overall, regardless of RH level, the ability of the products to support survival of the pathogen may be expressed in the following order: pine nuts > sesame seeds > chickpeas > black pepper. The results of this study can aid in understanding how L. monocytogenes survives on dried legumes, seeds, and spices, and the data can contribute to the risk assessment of this pathogen.

Klíčová slova:

Bacterial pathogens – Fats – Humidity – Legumes – Listeria monocytogenes – Peanut – Salmonella enterica – Specimen storage


1. Harris LJ, Yada S, Beuchat LR. Outbreaks of foodborne illness associated with the consumption of tree nuts, peanuts, and sesame seeds 2018.

2. CDC. Multistate outbreak of human Salmonella Enteritidis infections linked to Turkish pine nuts 2011.

3. CDC. Multistate outbreak of Salmonella Montevideo and Salmonella Senftenberg infections linked to Wonderful Pistachios (final update) 2016.

4. CDC. Multistate outbreak of human Salmonella Montevideo infections (final update) 2010.

5. Zweifel C, Stephan R. Spices and herbs as source of Salmonella-related foodborne disease. Food Res Int. 2011;45(2):765–9.

6. FDA. Gomarco recalls limited number of Macrobars and Thrive bars because of possible health risk 2017.

7. FDA. NOW Health Group Inc. expands voluntary recall of Ellyndale Nutty Infusions because of possible health risk 2017.

8. FDA. Recall on Fewer Than 225 Ava’s Brand Organic Cashews roasted and salted 8 oz. tubs in NJ, NY, PA, and CT 2017.

9. FDA. Kroger recalls Simple Truth dry roasted macadamia nuts because of possible health risk 2017.

10. FDA. U.S. House of Thaller recalls selected pine nut hummus products because of possible health risk 2017.

11. FDA. Publix recalls cranberry nut and seed mix due to possible health risk 2016.

12. FDA. United Natural Trading LLC announces voluntary recall of walnuts 2016.

13. News Desk. Illinois firm recalls shelled walnuts for potential Listeria 2014.

14. News Desk. Walnuts recalled due to potential Listeria contamination 2014.

15. News Desk. Phoenix company announces walnut recall, names California disbributor 2014.

16. Beach C. Snacks, nuts, protein bars recalled for Listeria concerns 2016.

17. Picha D, Pyzner J. Storage hints for pecans. Louisiana State University Agricultural Center. 2013.

18. Kader AA. Chapter 2: Impact of nut postharvest handling, de-shelling, drying and storage on quality. In: Harris LJ, editor. Improving the Safety and Quality of Nuts. Cambridge, UK: Woodhead Publishing Limited; 2013.

19. Kenney SJ, Beuchat LR. Survival, growth, and thermal resistance of Listeria monocytogenes in products containing peanut and chocolate. J Food Prot. 2004;67(10):2205–11. doi: 10.4315/0362-028x-67.10.2205 15508631

20. Koseki S, Nakamura N, Shiina T. Comparison of desiccation tolerance among Listeria monocytogenes, Escherichia coli O157:H7, Salmonella enterica, and Cronobacter sakazakii in powdered infant formula. J Food Prot. 2015;78(1):104–10. doi: 10.4315/0362-028X.JFP-14-249 25581184

21. Brackett RE, Beuchat LR. Survival of Listeria monocytogenes in whole egg and egg yolk powders and in liquid whole egg. Food Microbiol. 1991;8(4):331–7.

22. Kimber MA, Kaur H, Wang L, Danyluk MD, Harris LJ. Survival of Salmonella, Escherichia coli O157:H7, and Listeria monocytogenes on inoculated almonds and pistachios stored at -19, 4, and 24 degrees C. J Food Prot. 2012;75(8):1394–403. doi: 10.4315/0362-028X.JFP-12-023 22856562

23. Brar PK, Proano LG, Friedrich LM, Harris LJ, Danyluk MD. Survival of Salmonella, Escherichia coli O157:H7, and Listeria monocytogenes on raw peanut and pecan kernels stored at -24, 4, and 22 degrees C. J Food Prot. 2015;78(2):323–32. doi: 10.4315/0362-028X.JFP-14-327 25710147

24. Blessington T, Mitcham EJ, Harris LJ. Survival of Salmonella enterica, Escherichia coli O157:H7, and Listeria monocytogenes on inoculated walnut kernels during storage. J Food Prot. 2012;75(2):245–54. doi: 10.4315/0362-028X.JFP-11-278 22289584

25. Blessington T, Theofel CG, Mitcham EJ, Harris LJ. Survival of foodborne pathogens on inshell walnuts. Int J Food Microbiol. 2013;166(3):341–8. doi: 10.1016/j.ijfoodmicro.2013.07.016 24026009

26. Farakos SM, Pouillot R, Keller SE. Salmonella Survival Kinetics on Pecans, Hazelnuts, and Pine Nuts at Various Water Activities and Temperatures. J Food Prot. 2017;80(5):879–85. doi: 10.4315/0362-028X.JFP-16-392 28414256

27. Farakos SM, Pouillot R, Anderson N, Johnson R, Son I, Van Doren J. Modeling the survival kinetics of Salmonella in tree nuts for use in risk assessment. Int J Food Microbiol. 2016;227:41–50. doi: 10.1016/j.ijfoodmicro.2016.03.014 27062527

28. Farakos SM, Frank JF, Schaffner DW. Modeling the influence of temperature, water activity and water mobility on the persistence of Salmonella in low-moisture foods. Int J Food Microbiol. 2013;166(2):280–93. doi: 10.1016/j.ijfoodmicro.2013.07.007 23973840

29. Hwang CA, Porto-Fett AC, Juneja VK, Ingham SC, Ingham BH, Luchansky JB. Modeling the survival of Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella Typhimurium during fermentation, drying, and storage of soudjouk-style fermented sausage. Int J Food Microbiol. 2009;129(3):244–52. doi: 10.1016/j.ijfoodmicro.2008.12.003 19157610

30. Fleming DW, Cochi SL, MacDonald KL, Brondum J, Hayes PS, Plikaytis BD, et al. Pasteurized milk as a vehicle of infection in an outbreak of listeriosis. N Engl J Med. 1985;312(7):404–7. doi: 10.1056/NEJM198502143120704 3918263

31. FDA. Bacteriological Analytical Manual (BAM) Chapter 10: Detection of Listeria monocytogenes in foods and environmental samples, and enumeration of Listeria monocytogenes in foods 2017.

32. Beuchat LR. Relationship of water activity to moisture content in tree nuts. J Food Sci. 1978;43:754–8.

33. Venkatachalam M, Sathe SK. Chemical composition of selected edible nut seeds. J Agric Food Chem. 2006;54(13):4705–14. doi: 10.1021/jf0606959 16787018

34. Nergiz C, Donmez I. Chemical composition and nuritive value of Pinus pinea L. seeds. Food Chem. 2004;86:365–8.

35. Martinchik AN. Nutritional value of sesame seeds. Vopr Pitan. 2011;80(3):41–3. 21842753

36. Jukanti AK, Gaur PM, Gowda CL, Chibbar RN. Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review. Br J Nutr. 2012;108 Suppl 1:S11–26.

37. Barmpalia-Davis IM, Geornaras I, Kendall PA, Sofos JN. Effect of fat content on survival of Listeria monocytogenes during simulated digestion of inoculated beef frankfurters stored at 7 degrees C. Food Microbiol. 2009;26(5):483–90. doi: 10.1016/ 19465244

Článek vyšel v časopise


2019 Číslo 12