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Article: Rapid detection and quantitation of dipicolinic acid from Clostridium botulinum spores using mixed-mode liquid chromatography-tandem mass spectrometry

Redan, Benjamin W. / Morrissey, Travis R. / Rolfe, Catherine A. / Aguilar, Viviana L. / Skinner, Guy E. / Reddy, N. Rukma

Analytical and bioanalytical chemistry. 2022 Mar., v. 414, no. 8

2022

Abstract: Analysis of the dipicolinic acid (DPA) released from Clostridium botulinum spores during thermal processing is crucial to obtaining a mechanistic understanding of the factors involved in spore heat resistance and related food safety applications. Here, ... ...

Abstract	Analysis of the dipicolinic acid (DPA) released from Clostridium botulinum spores during thermal processing is crucial to obtaining a mechanistic understanding of the factors involved in spore heat resistance and related food safety applications. Here, we developed a novel mixed-mode liquid chromatography-tandem mass spectrometry (LC–MS/MS) method for detection of the DPA released from C. botulinum type A, nonproteolytic types B and F strains, and nonpathogenic surrogate Clostridium sporogenes PA3679 spores. DPA was retained on a mixed-mode C18/anion exchange column and was detected using electrospray ionization (ESI) positive mode within a 4-min analysis time. The intraday and interday precision (%CV) was 1.94–3.46% and 4.04–8.28%, respectively. Matrix effects were minimal across proteolytic type A Giorgio-A, nonproteolytic types QC-B and 202-F, and C. sporogenes PA3679 spore suspensions (90.1–114% of spiked DPA concentrations). DPA recovery in carrot juice and beef broth ranged from 105 to 118%, indicating limited matrix effects of these food products. Experiments that assessed the DPA released from Giorgio-A spores over the course of a 5-min thermal treatment at 108 °C found a significant correlation (R = 0.907; P < 0.05) between the log reduction of spores and amount of DPA released. This mixed-mode LC–MS/MS method provides a means for rapid detection of DPA released from C. botulinum spores during thermal processing and has the potential to be used for experiments in the field of food safety that assess the thermal resistance characteristics of various C. botulinum spore types.
Keywords	Clostridium botulinum ; Clostridium sporogenes ; analytical chemistry ; beef ; carrot juice ; electrospray ionization mass spectrometry ; food safety ; heat tolerance ; heat treatment ; liquid chromatography ; proteolysis ; rapid methods ; spores ; tandem mass spectrometry
Language	English
Dates of publication	2022-03
Size	p. 2767-2774.
Publishing place	Springer Berlin Heidelberg
Document type	Article
ISSN	1618-2642
DOI	10.1007/s00216-022-03926-7
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Rapid detection and quantitation of dipicolinic acid from Clostridium botulinum spores using mixed-mode liquid chromatography-tandem mass spectrometry.

Redan, Benjamin W / Morrissey, Travis R / Rolfe, Catherine A / Aguilar, Viviana L / Skinner, Guy E / Reddy, N Rukma

Analytical and bioanalytical chemistry

2022 Volume 414, Issue 8, Page(s) 2767–2774

Abstract	Analysis of the dipicolinic acid (DPA) released from Clostridium botulinum spores during thermal processing is crucial to obtaining a mechanistic understanding of the factors involved in spore heat resistance and related food safety applications. Here, we developed a novel mixed-mode liquid chromatography-tandem mass spectrometry (LC-MS/MS) method for detection of the DPA released from C. botulinum type A, nonproteolytic types B and F strains, and nonpathogenic surrogate Clostridium sporogenes PA3679 spores. DPA was retained on a mixed-mode C18/anion exchange column and was detected using electrospray ionization (ESI) positive mode within a 4-min analysis time. The intraday and interday precision (%CV) was 1.94-3.46% and 4.04-8.28%, respectively. Matrix effects were minimal across proteolytic type A Giorgio-A, nonproteolytic types QC-B and 202-F, and C. sporogenes PA3679 spore suspensions (90.1-114% of spiked DPA concentrations). DPA recovery in carrot juice and beef broth ranged from 105 to 118%, indicating limited matrix effects of these food products. Experiments that assessed the DPA released from Giorgio-A spores over the course of a 5-min thermal treatment at 108 °C found a significant correlation (R = 0.907; P < 0.05) between the log reduction of spores and amount of DPA released. This mixed-mode LC-MS/MS method provides a means for rapid detection of DPA released from C. botulinum spores during thermal processing and has the potential to be used for experiments in the field of food safety that assess the thermal resistance characteristics of various C. botulinum spore types.
MeSH term(s)	Chromatography, Liquid ; Clostridium botulinum/chemistry ; Hot Temperature ; Picolinic Acids/analysis ; Spores, Bacterial/chemistry ; Tandem Mass Spectrometry
Chemical Substances	Picolinic Acids ; dipicolinic acid (UE81S5CQ0G)
Language	English
Publishing date	2022-02-02
Publishing country	Germany
Document type	Journal Article
ZDB-ID	201093-8
ISSN	1618-2650 ; 0016-1152 ; 0372-7920
ISSN (online)	1618-2650
ISSN	0016-1152 ; 0372-7920
DOI	10.1007/s00216-022-03926-7
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Evidence for Bacillus cereus Spores as the Target Pathogen in Thermally Processed Extended Shelf Life Refrigerated Foods

Reddy, N. Rukma / Morrissey, Travis R. / Aguilar, Viviana L. / Schill, Kristin M. / Skinner, Guy E.

Journal of food protection. 2021 Mar., v. 84, no. 3

2021

Abstract: The microbial safety concern associated with thermally processed extended shelf life (ESL) refrigerated foods is based on adequate elimination of spore-forming pathogens such as nonproteolytic Clostridium botulinum types B, E, and F. These pathogens are ... ...

Abstract	The microbial safety concern associated with thermally processed extended shelf life (ESL) refrigerated foods is based on adequate elimination of spore-forming pathogens such as nonproteolytic Clostridium botulinum types B, E, and F. These pathogens are traditionally regarded as targets for validation of thermally processed ESL foods. However, their use for research is restricted due to their designation as select agents. In this study, the thermal resistances of spores of 10 nonproteolytic C. botulinum types B and F and seven psychrotrophic Bacillus cereus strains were evaluated in ACES (N-(2-acetamido)-2-aminoethanesulfonic acid) buffer (0.05 M, pH 7.00) and compared to determine whether any of the B. cereus strains could serve as a nonselect agent for establishing thermal processes for ESL refrigerated foods. Thermal decimal reduction times (DT-values) of both nonproteolytic C. botulinum types B and F and psychrotrophic B. cereus strains decreased as process temperature increased from 80 to 91°C, and the highest values were obtained at 80°C. All psychrotrophic B. cereus strains tested were more thermally resistant than nonproteolytic C. botulinum types B and F. DT-values of nonproteolytic C. botulinum types B and F decreased to <1.0 min at 87°C, whereas all psychrotrophic B. cereus strains had higher DT-values (i.e., 52.35 to 133.69 min) at the same temperature. Among all psychrotrophic B. cereus strains tested, BC-6A16 had the highest DT-values at any given temperature. The DT-values indicated that the psychrotrophic B. cereus strains were more thermally resistant than the nonproteolytic C. botulinum strains and therefore may be potential target pathogens for thermal process validation of ESL refrigerated foods. However, further comparative challenge studies are needed with a model food system or an ESL refrigerated food to confirm these results.
Keywords	Bacillus cereus ; extended shelf life ; food safety ; model food systems ; pH ; pathogens ; refrigeration ; temperature
Language	English
Size	p. 442-448.
Publishing place	International Association of Milk, Food, and Environmental Sanitarians.
Document type	Article
ZDB-ID	243284-5
ISSN	1944-9097 ; 0362-028X
ISSN (online)	1944-9097
ISSN	0362-028X
DOI	10.4315/JFP-20-267
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Inactivation of Salmonella, Shiga Toxin-producing E. coli, and Listeria monocytogenes in Raw Diet Pet Foods Using High-Pressure Processing.

Lee, Alvin / Maks-Warren, Nicole / Aguilar, Viviana / Piszczor, Karolina / Swicegood, Brittany / Ye, Mu / Warren, Joshua / O'Neill, Edward / Fleck, Mark / Tejayadi, Susy

Journal of food protection

2023 Volume 86, Issue 9, Page(s) 100124

Abstract: Pet food formulated with raw meat can pose health risks to pets and humans. High-pressure processing (HPP) was evaluated to achieve a 5-log reduction ofSalmonella,E. coliSTEC, andL. monocytogenesin commercial raw pet foods and maintain a 5-log reduction ... ...

Abstract	Pet food formulated with raw meat can pose health risks to pets and humans. High-pressure processing (HPP) was evaluated to achieve a 5-log reduction ofSalmonella,E. coliSTEC, andL. monocytogenesin commercial raw pet foods and maintain a 5-log reduction throughout post-HPP storage.Three formulation types that varied in the amounts of striated meat, organ meat, bone, seeds, and other ingredients (fruits, vegetables, and minor ingredients) designated as A-, S-, and R-formulations were used. Eight raw diet pet foods, consisting of three beef formulations (A-, S- and R-Beef), three chicken formulations (A-, S-, and R-Chicken), and two lamb formulations (A- and S-Lamb), were inoculated with 7 log CFU/g cocktails ofSalmonella,E. coliSTEC orL. monocytogenes, HPP at 586 MPa for 1-4 min, and stored refrigerated (4°C) or frozen (-10 to -18°C) for 21 days with microbiological analyses at various time intervals. A- formulations (20-46% meat, 42-68% organs, 0.9-1.3% seeds, and 10.7-11.1% fruits, vegetables, and minor ingredients) inoculated withSalmonellaand treated at 586 MPa for at least 2 min achieved a 5-log reduction 1 day post-HPP and maintained that inactivation level during frozen storage. A- and S-formulations inoculated withE. coliSTEC and treated at 586 MPa for at least 2 min achieved a 5-log reduction from day 6 of frozen storage. L. monocytogeneswas more HPP resistant thanSalmonellaandE. coliSTEC.S-formulations containing chicken or beef and stored frozen post-HPP had lower inactivation of L. monocytogenes compared to A-formulations containing chicken or beef. S-Lamb had higher frozen storage inactivation (5.95 ± 0.20 log CFU/g) compared to chicken (2.52 ± 0.38 log CFU/g) or beef (2.36 ± 0.48 log CFU/g). HPP coupled with frozen storage time was effective in achieving and maintaining a 5-log reduction ofSalmonellaandE. coliSTEC whileL. monocytogeneswas more resistant and requires further optimization to achieve a 5-log reduction.
MeSH term(s)	Cattle ; Animals ; Sheep ; Humans ; Food Handling ; Listeria monocytogenes ; Colony Count, Microbial ; Food Microbiology ; Diet ; Shiga-Toxigenic Escherichia coli ; Salmonella ; Shiga Toxins
Chemical Substances	Shiga Toxins
Language	English
Publishing date	2023-07-04
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	243284-5
ISSN	1944-9097 ; 0362-028X
ISSN (online)	1944-9097
ISSN	0362-028X
DOI	10.1016/j.jfp.2023.100124
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Evidence for Bacillus cereus Spores as the Target Pathogen in Thermally Processed Extended Shelf Life Refrigerated Foods.

Reddy, N Rukma / Morrissey, Travis R / Aguilar, Viviana L / Schill, Kristin M / Skinner, Guy E

Journal of food protection

2020 Volume 84, Issue 3, Page(s) 442–448

Abstract	The microbial safety concern associated with thermally processed extended shelf life (ESL) refrigerated foods is based on adequate elimination of spore-forming pathogens such as nonproteolytic Clostridium botulinum types B, E, and F. These pathogens are traditionally regarded as targets for validation of thermally processed ESL foods. However, their use for research is restricted due to their designation as select agents. In this study, the thermal resistances of spores of 10 nonproteolytic C. botulinum types B and F and seven psychrotrophic Bacillus cereus strains were evaluated in ACES (N-(2-acetamido)-2-aminoethanesulfonic acid) buffer (0.05 M, pH 7.00) and compared to determine whether any of the B. cereus strains could serve as a nonselect agent for establishing thermal processes for ESL refrigerated foods. Thermal decimal reduction times (DT-values) of both nonproteolytic C. botulinum types B and F and psychrotrophic B. cereus strains decreased as process temperature increased from 80 to 91°C, and the highest values were obtained at 80°C. All psychrotrophic B. cereus strains tested were more thermally resistant than nonproteolytic C. botulinum types B and F. DT-values of nonproteolytic C. botulinum types B and F decreased to <1.0 min at 87°C, whereas all psychrotrophic B. cereus strains had higher DT-values (i.e., 52.35 to 133.69 min) at the same temperature. Among all psychrotrophic B. cereus strains tested, BC-6A16 had the highest DT-values at any given temperature. The DT-values indicated that the psychrotrophic B. cereus strains were more thermally resistant than the nonproteolytic C. botulinum strains and therefore may be potential target pathogens for thermal process validation of ESL refrigerated foods. However, further comparative challenge studies are needed with a model food system or an ESL refrigerated food to confirm these results.
MeSH term(s)	Bacillus cereus ; Clostridium botulinum ; Food Microbiology ; Hot Temperature ; Spores, Bacterial
Language	English
Publishing date	2020-10-19
Publishing country	United States
Document type	Journal Article
ZDB-ID	243284-5
ISSN	1944-9097 ; 0362-028X
ISSN (online)	1944-9097
ISSN	0362-028X
DOI	10.4315/JFP-20-267
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: The use of High-Pressure Processing (HPP) to improve the safety and quality of raw coconut (Cocos nucifera L) water

Raghubeer, Errol V / Phan, Bick Ngoc / Onuoha, Emmanuel / Diggins, Sheylend / Aguilar, Viviana / Swanson, Sara / Lee, Alvin

International journal of food microbiology. 2020 Oct. 16, v. 331

2020

Abstract: This research investigated the use of high-pressure processing (HPP) for inactivating vegetative pathogens and spoilage microbiota in fresh unfiltered coconut water (Cocos nucifera L) from nuts obtained from Florida and frozen CW from Brazil with pH >5.0 ...

Abstract	This research investigated the use of high-pressure processing (HPP) for inactivating vegetative pathogens and spoilage microbiota in fresh unfiltered coconut water (Cocos nucifera L) from nuts obtained from Florida and frozen CW from Brazil with pH >5.0 and storage at 4 °C. Additionally, CW was evaluated to determine if it supported the growth and toxin production of Clostridium botulinum with or without the use of HPP when stored at refrigeration temperatures. Samples of fresh unfiltered CW were inoculated to 5.5 to 6.5 logs/mL with multiple strain cocktails of E. coli O157:H7, Salmonella spp. and Listeria monocytogenes and HPP at 593 MPa for 3 min at 4 °C. HPP and inoculated non-HPP controls were stored at 4 °C for 54 and 75 days for Florida CW and Brazil CW, respectively. Results of analyses showed HPP samples with <1 CFU/mL and no detection (negative/25 mL) with enrichment procedures for the 3 inoculated pathogens for all analyses. The non-HPP control samples did not show growth of the pathogens but a gradual decrease in levels to ca. 3-Logs/mL by day 54 in the fresh Florida CW and similarly in frozen Brazil CW by Day 75. Microbial spoilage of uninoculated samples was evaluated for normal spoilage microbiota through 120 days storage at 4 °C. Microbial counts remained at ca. 2-logs with no detectable signs of spoilage for HPP samples through 120 d. The non-HPP control samples spoiled within 2 weeks of storage at 4 °C with gas production, cloudiness, and off-odors. To evaluate if CW supports the growth and toxin production of C. botulinum, samples of unfiltered and filtered (0.2 μm) CW were inoculated with either proteolytic or non-proteolytic C. botulinum spores at 2 log CFU/mL that were processed at 593 MPa for 3 min and stored at 4 °C and 10 °C for 45 days. Inoculated positive and non-inoculated negative controls were prepared and stored as the HPP treated and non-HPP samples. No growth of C. botulinum or toxin production was detected in either the unfiltered or filtered CW regardless if products were HPP treated or not. All inoculated samples with C. botulinum spores were enriched at Day-45 in PYGS media to determine the viability of the inoculated spores at the end of shelf-life and screened for C. botulinum toxins. In all samples, C. botulinum toxin Types A, B and E were detected indicating spores were viable throughout the storage. Type F toxin was not detected possibly due to inherent conditions in the samples that may affected toxin screening.
Keywords	Clostridium botulinum ; Escherichia coli O157 ; Listeria monocytogenes ; Salmonella ; botulinum toxin ; coconut water ; coconuts ; food microbiology ; off odors ; pH ; proteolysis ; refrigeration ; shelf life ; spoilage ; spoilage microorganisms ; viability ; Brazil ; Florida
Language	English
Dates of publication	2020-1016
Publishing place	Elsevier B.V.
Document type	Article
Note	NAL-AP-2-clean
ZDB-ID	87122-9
ISSN	1879-3460 ; 0168-1605
ISSN (online)	1879-3460
ISSN	0168-1605
DOI	10.1016/j.ijfoodmicro.2020.108697
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: The use of High-Pressure Processing (HPP) to improve the safety and quality of raw coconut (Cocos nucifera L) water.

Raghubeer, Errol V / Phan, Bick Ngoc / Onuoha, Emmanuel / Diggins, Sheylend / Aguilar, Viviana / Swanson, Sara / Lee, Alvin

International journal of food microbiology

2020 Volume 331, Page(s) 108697

Abstract	This research investigated the use of high-pressure processing (HPP) for inactivating vegetative pathogens and spoilage microbiota in fresh unfiltered coconut water (Cocos nucifera L) from nuts obtained from Florida and frozen CW from Brazil with pH >5.0 and storage at 4 °C. Additionally, CW was evaluated to determine if it supported the growth and toxin production of Clostridium botulinum with or without the use of HPP when stored at refrigeration temperatures. Samples of fresh unfiltered CW were inoculated to 5.5 to 6.5 logs/mL with multiple strain cocktails of E. coli O157:H7, Salmonella spp. and Listeria monocytogenes and HPP at 593 MPa for 3 min at 4 °C. HPP and inoculated non-HPP controls were stored at 4 °C for 54 and 75 days for Florida CW and Brazil CW, respectively. Results of analyses showed HPP samples with <1 CFU/mL and no detection (negative/25 mL) with enrichment procedures for the 3 inoculated pathogens for all analyses. The non-HPP control samples did not show growth of the pathogens but a gradual decrease in levels to ca. 3-Logs/mL by day 54 in the fresh Florida CW and similarly in frozen Brazil CW by Day 75. Microbial spoilage of uninoculated samples was evaluated for normal spoilage microbiota through 120 days storage at 4 °C. Microbial counts remained at ca. 2-logs with no detectable signs of spoilage for HPP samples through 120 d. The non-HPP control samples spoiled within 2 weeks of storage at 4 °C with gas production, cloudiness, and off-odors. To evaluate if CW supports the growth and toxin production of C. botulinum, samples of unfiltered and filtered (0.2 μm) CW were inoculated with either proteolytic or non-proteolytic C. botulinum spores at 2 log CFU/mL that were processed at 593 MPa for 3 min and stored at 4 °C and 10 °C for 45 days. Inoculated positive and non-inoculated negative controls were prepared and stored as the HPP treated and non-HPP samples. No growth of C. botulinum or toxin production was detected in either the unfiltered or filtered CW regardless if products were HPP treated or not. All inoculated samples with C. botulinum spores were enriched at Day-45 in PYGS media to determine the viability of the inoculated spores at the end of shelf-life and screened for C. botulinum toxins. In all samples, C. botulinum toxin Types A, B and E were detected indicating spores were viable throughout the storage. Type F toxin was not detected possibly due to inherent conditions in the samples that may affected toxin screening.
MeSH term(s)	Bacteria/growth & development ; Bacteria/isolation & purification ; Bacterial Physiological Phenomena ; Brazil ; Cocos/microbiology ; Colony Count, Microbial ; Food Handling/methods ; Food Microbiology/methods ; Fruit and Vegetable Juices/microbiology ; Raw Foods/microbiology ; Temperature
Language	English
Publishing date	2020-05-29
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	87122-9
ISSN	1879-3460 ; 0168-1605
ISSN (online)	1879-3460
ISSN	0168-1605
DOI	10.1016/j.ijfoodmicro.2020.108697
Database	MEDical Literature Analysis and Retrieval System OnLINE

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