Inactivation of Salmonella enterica and Surrogate Enterococcus faecium on Whole Black Peppercorns and Cumin Seeds Using Vacuum Steam Pasteurization

Jordan J. Newkirk; Jian Wu; Jennifer C. Acuff; Chris B. Caver; Kumar Mallikarjunan; Brian D. Wiersema; Robert C. Williams; Monica A. Ponder

doi:10.3389/fsufs.2018.00048

Inactivation of Salmonella enterica and Surrogate Enterococcus faecium on Whole Black Peppercorns and Cumin Seeds Using Vacuum Steam Pasteurization

Jordan J. Newkirk, Jian Wu, Jennifer C. Acuff, Chris B. Caver, Kumar Mallikarjunan, Brian D. Wiersema, Robert C. Williams, Monica A. Ponder

Food Science and Nutrition

Research output: Contribution to journal › Article › peer-review

22 Scopus citations

Abstract

Spices, including black pepper and cumin seeds, have been implicated in outbreaks of salmonellosis and prompted recalls of ready-to-eat products containing contaminated spices. Vacuum-assisted steam pasteurization is performed to improve the safety and quality of many low water activity products, however process parameters associated with inactivation on whole spices are not well described. The objective of this study was to determine the effectiveness of a lab-scale vacuum-assisted steam process for the inactivation of Salmonella enterica and its potential surrogate Enterococcus faecium ATCC 8459 inoculated onto the surface of whole peppercorns and cumin seeds. In addition, the effect of two inoculation preparation methods [growth on tryptic soy agar (TSA) or inclusion within a native microbiota biofilm], on the reduction of S. enterica serovars or E. faecium was compared on steam pasteurized whole black peppercorns. Spices were processed using steam under a vacuum to achieve a mean product temperature of 86.7 ± 2.8°C for different dwell times. Salmonella inoculated using the TSA-grown method, required 83 and 70 s respectively to achieve a 5-log reduction of Salmonella on peppercorns and cumin seeds. Longer time periods were needed to achieve a 5-log reduction of Salmonella when it was present in a native biofilm on whole peppercorns. Survivor estimations were best predicted by the Weibull models. The mean log reductions of E. faecium were 0.9 log CFU/g lower than Salmonella on whole black peppercorns inoculated using the TSA-grown cells (P = 0.0021). The mean log reductions of Salmonella and E. faecium prepared using the biofilm-inclusion method were not significantly different (P = 0.76). E. faecium log CFU/g reductions were not significantly different compared to Salmonella on whole cumin seeds (P = 0.42) indicating that while reductions are comparable the surrogate may not always provide a conservative indication of complete Salmonella elimination for all spices processed using vacuum-assisted steam. Highlights: - E. faecium is a surrogate for Salmonella on steam processed whole black peppercorn. - E. faecium is not a conservative surrogate for Salmonella on steam processed >85°C whole cumin.

Original language	English (US)
Article number	48
Journal	Frontiers in Sustainable Food Systems
Volume	2
DOIs	https://doi.org/10.3389/fsufs.2018.00048
State	Published - Aug 7 2018

Bibliographical note

Funding Information:
Funding for this research was provided in part by the International Life Sciences Institute of North America Committee for Food Microbiology, by the Virginia Agricultural Experiment Station and the Hatch Program of the National Institute of Food and Agriculture, U.S. Department of Agriculture. ILSI North America is a public non-profit foundation that provides a forum to advance understanding of scientific issues related to the nutritional quality and safety of the food supply by sponsoring research programs, educational seminars and workshops, and publications. ILSI North America receives support primarily from its industry membership. In addition, the American Spice Trade Association (ASTA) provided an unrestricted grant to ILSI North America for this research. ASTA is a trade association that represents the U.S. spice industry and works to ensure clean, safe spices. The opinions expressed herein are those of the authors and do not necessarily represent the views of the funding organizations.

Funding Information:
We would like to thank the U.S. Food and Drug Administration, Office of Regulatory Affairs, Arkansas Regional Lab for providing the spice-isolated strains. Special thanks to Kim Waterman, Natalie Pulido, Thomas Saunders, Brett Driver, Robert Lane, and Sandy Janwatin for providing technical assistance. Funding. Funding for this research was provided in part by the International Life Sciences Institute of North America Committee for Food Microbiology, by the Virginia Agricultural Experiment Station and the Hatch Program of the National Institute of Food and Agriculture, U.S. Department of Agriculture. ILSI North America is a public non-profit foundation that provides a forum to advance understanding of scientific issues related to the nutritional quality and safety of the food supply by sponsoring research programs, educational seminars and workshops, and publications. ILSI North America receives support primarily from its industry membership. In addition, the American Spice Trade Association (ASTA) provided an unrestricted grant to ILSI North America for this research. ASTA is a trade association that represents the U.S. spice industry and works to ensure clean, safe spices. The opinions expressed herein are those of the authors and do not necessarily represent the views of the funding organizations.

Publisher Copyright:
© Copyright © 2018 Newkirk, Wu, Acuff, Caver, Mallikarjunan, Wiersema, Williams and Ponder.

Keywords

Enterococcus faecium
Salmonella
cumin
peppercorns
steam
surrogate

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10.3389/fsufs.2018.00048

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Newkirk, J. J., Wu, J., Acuff, J. C., Caver, C. B., Mallikarjunan, K., Wiersema, B. D., Williams, R. C., & Ponder, M. A. (2018). Inactivation of Salmonella enterica and Surrogate Enterococcus faecium on Whole Black Peppercorns and Cumin Seeds Using Vacuum Steam Pasteurization. Frontiers in Sustainable Food Systems, 2, Article 48. https://doi.org/10.3389/fsufs.2018.00048

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title = "Inactivation of Salmonella enterica and Surrogate Enterococcus faecium on Whole Black Peppercorns and Cumin Seeds Using Vacuum Steam Pasteurization",

abstract = "Spices, including black pepper and cumin seeds, have been implicated in outbreaks of salmonellosis and prompted recalls of ready-to-eat products containing contaminated spices. Vacuum-assisted steam pasteurization is performed to improve the safety and quality of many low water activity products, however process parameters associated with inactivation on whole spices are not well described. The objective of this study was to determine the effectiveness of a lab-scale vacuum-assisted steam process for the inactivation of Salmonella enterica and its potential surrogate Enterococcus faecium ATCC 8459 inoculated onto the surface of whole peppercorns and cumin seeds. In addition, the effect of two inoculation preparation methods [growth on tryptic soy agar (TSA) or inclusion within a native microbiota biofilm], on the reduction of S. enterica serovars or E. faecium was compared on steam pasteurized whole black peppercorns. Spices were processed using steam under a vacuum to achieve a mean product temperature of 86.7 ± 2.8°C for different dwell times. Salmonella inoculated using the TSA-grown method, required 83 and 70 s respectively to achieve a 5-log reduction of Salmonella on peppercorns and cumin seeds. Longer time periods were needed to achieve a 5-log reduction of Salmonella when it was present in a native biofilm on whole peppercorns. Survivor estimations were best predicted by the Weibull models. The mean log reductions of E. faecium were 0.9 log CFU/g lower than Salmonella on whole black peppercorns inoculated using the TSA-grown cells (P = 0.0021). The mean log reductions of Salmonella and E. faecium prepared using the biofilm-inclusion method were not significantly different (P = 0.76). E. faecium log CFU/g reductions were not significantly different compared to Salmonella on whole cumin seeds (P = 0.42) indicating that while reductions are comparable the surrogate may not always provide a conservative indication of complete Salmonella elimination for all spices processed using vacuum-assisted steam. Highlights: - E. faecium is a surrogate for Salmonella on steam processed whole black peppercorn. - E. faecium is not a conservative surrogate for Salmonella on steam processed >85°C whole cumin.",

keywords = "Enterococcus faecium, Salmonella, cumin, peppercorns, steam, surrogate",

author = "Newkirk, {Jordan J.} and Jian Wu and Acuff, {Jennifer C.} and Caver, {Chris B.} and Kumar Mallikarjunan and Wiersema, {Brian D.} and Williams, {Robert C.} and Ponder, {Monica A.}",

note = "Funding Information: Funding for this research was provided in part by the International Life Sciences Institute of North America Committee for Food Microbiology, by the Virginia Agricultural Experiment Station and the Hatch Program of the National Institute of Food and Agriculture, U.S. Department of Agriculture. ILSI North America is a public non-profit foundation that provides a forum to advance understanding of scientific issues related to the nutritional quality and safety of the food supply by sponsoring research programs, educational seminars and workshops, and publications. ILSI North America receives support primarily from its industry membership. In addition, the American Spice Trade Association (ASTA) provided an unrestricted grant to ILSI North America for this research. ASTA is a trade association that represents the U.S. spice industry and works to ensure clean, safe spices. The opinions expressed herein are those of the authors and do not necessarily represent the views of the funding organizations. Funding Information: We would like to thank the U.S. Food and Drug Administration, Office of Regulatory Affairs, Arkansas Regional Lab for providing the spice-isolated strains. Special thanks to Kim Waterman, Natalie Pulido, Thomas Saunders, Brett Driver, Robert Lane, and Sandy Janwatin for providing technical assistance. Funding. Funding for this research was provided in part by the International Life Sciences Institute of North America Committee for Food Microbiology, by the Virginia Agricultural Experiment Station and the Hatch Program of the National Institute of Food and Agriculture, U.S. Department of Agriculture. ILSI North America is a public non-profit foundation that provides a forum to advance understanding of scientific issues related to the nutritional quality and safety of the food supply by sponsoring research programs, educational seminars and workshops, and publications. ILSI North America receives support primarily from its industry membership. In addition, the American Spice Trade Association (ASTA) provided an unrestricted grant to ILSI North America for this research. ASTA is a trade association that represents the U.S. spice industry and works to ensure clean, safe spices. The opinions expressed herein are those of the authors and do not necessarily represent the views of the funding organizations. Publisher Copyright: {\textcopyright} Copyright {\textcopyright} 2018 Newkirk, Wu, Acuff, Caver, Mallikarjunan, Wiersema, Williams and Ponder.",

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AU - Newkirk, Jordan J.

AU - Wu, Jian

AU - Acuff, Jennifer C.

AU - Caver, Chris B.

AU - Mallikarjunan, Kumar

AU - Wiersema, Brian D.

AU - Williams, Robert C.

AU - Ponder, Monica A.

N1 - Funding Information: Funding for this research was provided in part by the International Life Sciences Institute of North America Committee for Food Microbiology, by the Virginia Agricultural Experiment Station and the Hatch Program of the National Institute of Food and Agriculture, U.S. Department of Agriculture. ILSI North America is a public non-profit foundation that provides a forum to advance understanding of scientific issues related to the nutritional quality and safety of the food supply by sponsoring research programs, educational seminars and workshops, and publications. ILSI North America receives support primarily from its industry membership. In addition, the American Spice Trade Association (ASTA) provided an unrestricted grant to ILSI North America for this research. ASTA is a trade association that represents the U.S. spice industry and works to ensure clean, safe spices. The opinions expressed herein are those of the authors and do not necessarily represent the views of the funding organizations. Funding Information: We would like to thank the U.S. Food and Drug Administration, Office of Regulatory Affairs, Arkansas Regional Lab for providing the spice-isolated strains. Special thanks to Kim Waterman, Natalie Pulido, Thomas Saunders, Brett Driver, Robert Lane, and Sandy Janwatin for providing technical assistance. Funding. Funding for this research was provided in part by the International Life Sciences Institute of North America Committee for Food Microbiology, by the Virginia Agricultural Experiment Station and the Hatch Program of the National Institute of Food and Agriculture, U.S. Department of Agriculture. ILSI North America is a public non-profit foundation that provides a forum to advance understanding of scientific issues related to the nutritional quality and safety of the food supply by sponsoring research programs, educational seminars and workshops, and publications. ILSI North America receives support primarily from its industry membership. In addition, the American Spice Trade Association (ASTA) provided an unrestricted grant to ILSI North America for this research. ASTA is a trade association that represents the U.S. spice industry and works to ensure clean, safe spices. The opinions expressed herein are those of the authors and do not necessarily represent the views of the funding organizations. Publisher Copyright: © Copyright © 2018 Newkirk, Wu, Acuff, Caver, Mallikarjunan, Wiersema, Williams and Ponder.

PY - 2018/8/7

Y1 - 2018/8/7

N2 - Spices, including black pepper and cumin seeds, have been implicated in outbreaks of salmonellosis and prompted recalls of ready-to-eat products containing contaminated spices. Vacuum-assisted steam pasteurization is performed to improve the safety and quality of many low water activity products, however process parameters associated with inactivation on whole spices are not well described. The objective of this study was to determine the effectiveness of a lab-scale vacuum-assisted steam process for the inactivation of Salmonella enterica and its potential surrogate Enterococcus faecium ATCC 8459 inoculated onto the surface of whole peppercorns and cumin seeds. In addition, the effect of two inoculation preparation methods [growth on tryptic soy agar (TSA) or inclusion within a native microbiota biofilm], on the reduction of S. enterica serovars or E. faecium was compared on steam pasteurized whole black peppercorns. Spices were processed using steam under a vacuum to achieve a mean product temperature of 86.7 ± 2.8°C for different dwell times. Salmonella inoculated using the TSA-grown method, required 83 and 70 s respectively to achieve a 5-log reduction of Salmonella on peppercorns and cumin seeds. Longer time periods were needed to achieve a 5-log reduction of Salmonella when it was present in a native biofilm on whole peppercorns. Survivor estimations were best predicted by the Weibull models. The mean log reductions of E. faecium were 0.9 log CFU/g lower than Salmonella on whole black peppercorns inoculated using the TSA-grown cells (P = 0.0021). The mean log reductions of Salmonella and E. faecium prepared using the biofilm-inclusion method were not significantly different (P = 0.76). E. faecium log CFU/g reductions were not significantly different compared to Salmonella on whole cumin seeds (P = 0.42) indicating that while reductions are comparable the surrogate may not always provide a conservative indication of complete Salmonella elimination for all spices processed using vacuum-assisted steam. Highlights: - E. faecium is a surrogate for Salmonella on steam processed whole black peppercorn. - E. faecium is not a conservative surrogate for Salmonella on steam processed >85°C whole cumin.

AB - Spices, including black pepper and cumin seeds, have been implicated in outbreaks of salmonellosis and prompted recalls of ready-to-eat products containing contaminated spices. Vacuum-assisted steam pasteurization is performed to improve the safety and quality of many low water activity products, however process parameters associated with inactivation on whole spices are not well described. The objective of this study was to determine the effectiveness of a lab-scale vacuum-assisted steam process for the inactivation of Salmonella enterica and its potential surrogate Enterococcus faecium ATCC 8459 inoculated onto the surface of whole peppercorns and cumin seeds. In addition, the effect of two inoculation preparation methods [growth on tryptic soy agar (TSA) or inclusion within a native microbiota biofilm], on the reduction of S. enterica serovars or E. faecium was compared on steam pasteurized whole black peppercorns. Spices were processed using steam under a vacuum to achieve a mean product temperature of 86.7 ± 2.8°C for different dwell times. Salmonella inoculated using the TSA-grown method, required 83 and 70 s respectively to achieve a 5-log reduction of Salmonella on peppercorns and cumin seeds. Longer time periods were needed to achieve a 5-log reduction of Salmonella when it was present in a native biofilm on whole peppercorns. Survivor estimations were best predicted by the Weibull models. The mean log reductions of E. faecium were 0.9 log CFU/g lower than Salmonella on whole black peppercorns inoculated using the TSA-grown cells (P = 0.0021). The mean log reductions of Salmonella and E. faecium prepared using the biofilm-inclusion method were not significantly different (P = 0.76). E. faecium log CFU/g reductions were not significantly different compared to Salmonella on whole cumin seeds (P = 0.42) indicating that while reductions are comparable the surrogate may not always provide a conservative indication of complete Salmonella elimination for all spices processed using vacuum-assisted steam. Highlights: - E. faecium is a surrogate for Salmonella on steam processed whole black peppercorn. - E. faecium is not a conservative surrogate for Salmonella on steam processed >85°C whole cumin.

KW - Enterococcus faecium

KW - Salmonella

KW - cumin

KW - peppercorns

KW - steam

KW - surrogate

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Inactivation of Salmonella enterica and Surrogate Enterococcus faecium on Whole Black Peppercorns and Cumin Seeds Using Vacuum Steam Pasteurization

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