Source: UNIVERSITY OF MAINE submitted to NRP
IMPACT OF SODIUM CONCENTRATION ON MICROBIAL AND CHEMICAL SAFETY OF (SPONTANEOUSLY) FERMENTED VEGETABLES
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1015467
Grant No.
2018-67018-28115
Cumulative Award Amt.
$148,339.00
Proposal No.
2017-08044
Multistate No.
(N/A)
Project Start Date
May 15, 2018
Project End Date
May 14, 2021
Grant Year
2018
Program Code
[A1331]- Improving Food Safety
Recipient Organization
UNIVERSITY OF MAINE
(N/A)
ORONO,ME 04469
Performing Department
(N/A)
Non Technical Summary
Lactic acid bacteria (LAB)-fermented foods have gained popularity in recent years as consumers learn more about their health-related benefits. Popular LAB-fermented foods consumed in the U.S. include pickles, olives, kimchi and sauerkraut. While fermented foods offer distinct health benefits, the elevated sodium content, which inhibits the growth of pathogenic and food spoilage organisms in these products, is a significant concern. Fermented food producers are investigating reduced-salt fermentation methods while seeking to maintain products free of foodborne pathogens and spoilage organisms and with low levels of allergenic amines. Expanding knowledge of vegetable fermentation processes will enhance food safety for producers in a developing niche, particularly those who market their products to consumers supporting farm-to-table, local, and organic agriculture. The National Agricultural Statistics Service (NASS) recorded a nearly 100% increase in the number of Maine farms producing fresh cabbage in the years between 2007 and 2012 (from 59 to 115). Ensuring the safety of value-added food products will also have a positive impact on the state's agricultural economy by providing fresh vegetable producers with knowledge and resources that support value-added production. We propose to ferment sauerkraut from locally produced cabbage, with natural bacterial flora and varied sodium content to assess acidification rates and the survival of inoculated pathogenic bacteria. Other analyses to be conducted include characterization and measurement of common biogenic amines that have negative health effects, and monitoring production of the healthful bioactive gamma-Aminobutyric acid (GABA) to improve nutritive value of fermented foods and the health of consumers.
Animal Health Component
90%
Research Effort Categories
Basic
(N/A)
Applied
90%
Developmental
10%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
71214401100100%
Goals / Objectives
OBJECTIVESEnhance Food Safety *Impact of reduced sodium concentration on pathogen survival during fermentationDescribe inactivation kinetics of foodborne pathogens during spontaneous vegetable fermentationObserve survival of pathogens at low concentrations during fermentation and cold storageMeasure titratable acidity (TA)Characterize organic acid profile by UPLC (lactic, acetic and other acids)Assess effect of salt concentration on formation of BABA concentrations during fermentation (by UPLC)BA concentrations during cold storage (3 months)BA content of fresh (regionally produced) and shelf-stable (canned) sauerkrautConfirm Product Acceptability *Consumer panels to determine acceptability of reduced-sodium products* Goals can still be accomplished with the reduced funding/time.
Project Methods
EXPERIMENTAL DESIGNPhase I: Raw, shredded cabbage purchased in bulk from a local distributor (to assure material homogeneity) will be analyzed for levels of common microbial indicator populations (TPC, lactic acid bacteria, coliforms, yeast and mold). Shredded cabbage will be combined with NaCl at 1.0, 1.5, 2.0 and 2.5% (w/w). All raw cabbage fermentations will be performed in triplicate, under sanitary conditions in 1 gallon fermentation vessels with airlocks and sample ports, maintained at 19° C. Because the proposed work will rely on natural cabbage microflora, the fermentation period will likely be longer than when using a known LAB inoculant. Initial fermentation may take 2 days to begin and several weeks to complete. During active fermentation, brine samples will be harvested from each vessel approximately every 72 hours with aliquots analyzed as follows:Salt concentration, pH and titratable acidity measurement;Identification and quantification of biogenic amines and organic acids with analytical methods modified for UPLC;Enumeration of aerobic microflora (dilution and plating on trypticase soy agar), yeast and mold (dilution and plating on acidified potato dextrose agar), lactic acid bacteria (dilution and plating on DeMann Rogosa Sharpe agar), and coliforms (most probable number analysis);Presence/absence of Listeria spp., Staphylococcus aureus and Salmonella spp. by enrichment and real time PCR;Presence/ absence of botulinum neurotoxin-producing clostridia determined by multiplex PCR.When brine pH reaches 3.4 (fermentation is complete), microbiological sampling will cease and fermentation vessels will be refrigerated at 4° C for 3 months. Samples will be harvested bi-weekly during the storage period, and tested for pH, TA, OA, BA.Phase II: Sauerkraut will be prepared as described previously, in one pint batches. Fermentation jars will be inoculated, upon the start of fermentation, with approximately 106 CFU/ml of pathogen cocktail comprised of three strains of enterohemorrhagic E. coli, Staphylococcus aureus, Salmonella, or Listeria monocytogenes. This phase will provide information regarding the susceptibility of the chosen pathogens to the conditions inherent in sauerkraut fermentation, and to clarify the effect of salt concentration on pathogen survival.Brine will be sampled for microbiological plating approximately every 72 hours throughout fermentation and biweekly for up to eight weeks of subsequent refrigerated storage at 4°C. Brine analysis will include:Aerobic plate count and LAB plate count to verify normal fermentative progress in the presence of pathogens;Count inoculated pathogens via dilution and plating on selective agar medium. Dilutions will be plated using non-selective agar overlay to allow for recovery and enumeration of injured cells.Plating will be discontinued when two successive samplings fail to produce counts above the detection limit of the method utilized (10 CFU/g). The pathogenic species with highest survivability during fermentation will be utilized in the final phase of research, as described below.Consumer acceptability of the control and reduced-sodium fermented products will be determined using the standard 9-point hedonic scale to assess appearance, taste, aroma, texture, and overall liking. One hundred adults (at least 18 years old) who are interested in reduced sodium foods and who like sauerkraut will be recruited from the greater Bangor, Maine region. SIMS software (version 6, Berkeley Heights, New Jersey) will be used to create the questionnaire, assign random 3-digit codes to samples, randomize sample presentation order, and analyze results. Samples will be served in 2-ounce white china ramekins at 4?°C. Spring water will be used to cleanse palates between samples. Consumers will record their liking on Hewlett Packard Elite Pro tablets. Demographic questions including age, gender, sauerkraut purchase habits, and purchase intent questions will also be asked. R software (The R Foundation for Statistical Computing, Vienna, Austria) will calculate analysis of variance, Tukey's HSD test, and preference mapping; a probability level of p ≤ 0.05 will be used to establish significant differences.Phase III: Sauerkraut will be prepared as described previously, with shredded cabbage inoculated with pathogen cell suspensions of approximately 102 CFU/jar to simulate low level contamination likely to occur naturally.Brine will be sampled for microbiological plating every 48 hours throughout fermentation and for up to eight weeks while in refrigerated storage at 4°C. Samples will be analyzed as follows:Aerobic plate count and LAB plate count to verify normal fermentative progression in the presence of pathogens;Presence or absence of inoculated pathogen by enrichment and cultural methods, without bacterial count.DATA ANALYSIS: Data will be analyzed using the statistical software packages SPSS. Organic acids, pH, titratable acidity, and salt concentrations will be correlated with pathogen survival/growth, and production of biogenic amines (BA).

Progress 05/15/18 to 05/14/21

Outputs
Target Audience: Nothing Reported Changes/Problems:This project was extended by one year (no cost extension) with the goals of 1. Method development for a more robust analytical method for biogenic amine analysis, 2. DNA sequencing and identification of naturally-occurring LAB bacteria and 3. Publication of results. The COVID-19 pandemic of 2020-2021 made these final project goals challenging. A combination of university-imposed safety rules limiting access to research facilities and supply chain disruptions of critical chemical reagents resulted in failure to meet goals 1 and 2. A graduate thesis was published and a manuscript for peer-reviewed scientific publication is currently in preparation. What opportunities for training and professional development has the project provided?This project has provided diverse research experiences for a graduate (Master of Sciences) and several undergraduate (Bachelor of Science) food science students. This training included experience with experimental design, diverse skill development in a Biohazard II level microbiology lab, opportunities to work with advanced chromatographic instrumentation and training in sensory science. How have the results been disseminated to communities of interest?To date, results from this study have been disseminated by thesis publication (University of Maine). Findings from this project are currently in preparation for peer reviewed publication and will also be used by University of Maine Cooperative Extension Food Science specialists to advise both commercial and hobby food fermenters. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Most objectives were met and described in detail in previous progress reports (2019, 2020). Listed below are summary findings for the project. Enhanced Food Safety Pathogen Survival at Low Concentrations (Fermentation and Cold Storage) The effects of three different salt (0.5%, 1.5%, and 2.5% NaCl (w/w)) and garlic (0%, 0.5%, and 1.0% (w/w)) concentrations on bacterial pathogen (STEC,Salmonella, andL. monocytogenes) survival were evaluated. Results indicate that neither the salt or garlic concentrations tested had a significant effect on pathogen survival. Although there was a decrease inSalmonellaandL. monocytogenessurvival after storage, neither pathogen was completely eradicated in all samples. Therefore, to better ensure consumer safety, it is important for fermenters to maintain cleanliness and avoid cross-contamination during production. Biogenic amines Biogenic amine (BAs) concentrations (histamine and tyramine) in the beet kvass evaluated using high performance liquid chromatography (HPLC) were negligible, however the method developed for this assay was not ideal for the resolution of other BAs, such as gamma aminobutyric acid (gaba). As a BA, gaba is an anomaly, as it is considered a beneficial biochemical byproduct of LAB fermentation. Although we were unable to complete satisfactory method development for gaba and several other BAs, significant progress was made toward the completion of a rapid and robust analytical method for a wide variety of food matrices. Biochemical Profile HPLC analysis of the beet kvass showed that salt and garlic concentration had a significant effect on organic acid and fructose content. Specifically, beet kvass produced with garlic had significantly reduced lactic and acetic acid, glucose, and fructose content, but significantly increased ethanol levels, when compared with samples without garlic. This biochemical profile suggests that garlic favors the growth of yeast in beet kvass. These observations suggest that formula development has considerable impacts on microbial diversity in this product. Consumer Acceptability Sensory evaluation revealed that salt concentration is a significant deciding factor on overall product acceptance, with consumers generally preferring lower salt levels. Inclusion of information on the potential health benefits of the product increased panelists' interest in consuming the product, indicating that participants may be willing to compromise sensory characteristics for health benefits. Therefore, producers may formulate beet kvass with lower salt and with or without garlic, without adversely affecting product acceptability.

Publications

  • Type: Theses/Dissertations Status: Published Year Published: 2020 Citation: Hing, Abigail, "Effects of Salt and Garlic Concentration on The Microbial Safety, Biochemical Properties, and Sensory Acceptance of Spontaneously Fermented Beet Kvass" (2020). Electronic Theses and Dissertations. 3236. https://digitalcommons.library.umaine.edu/etd/3236


Progress 05/15/19 to 05/14/20

Outputs
Target Audience: Nothing Reported Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Training opportunities for this project continue to be focused on graduate and undergraduate student training encompassing a breadth of interdisiplinary skiils. As she progresses through the objectives of this project, the graduate student supported by this project has recieved extensive training in advanced microbiological techniques, analytical chemistry (high performance liquid chromatography) and sensory evaluation. An undergraduate student assisting with this project has recieved similar laboratory-related experience. How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals?Year 3 of the projectwill be dedicated to completion of 1. Anaytlical objectives:gama amino butyric acid analysis by GC/MS and identification of lactobacillus (LAB) species using Illumina MiSeq DNA sequencing; 2. Completion of publications and presentations (thesis, conference presentation andpeer-reviewed articles.

Impacts
What was accomplished under these goals? After completing the original objectives of our work with spontaneously fermented cabbage (sauerkraut), we began work with beet kvass, a little known product that has seen a recent surge in popularity among home fermentation enthusiasts. As beet root is exposed to a number of soil-born microorganisms (fermentation and pathogenic), we thought this product would present a good model for both fermentation quality and microbiological safety parameters. In the microbial safety challenge study of beet kvass, neither salt concentration (0.5%, 1.5%, and 2.5% NaCl) nor presence or concentration of garlic (0.0%, 0.5%, and 1.0%) significantly affected the survival of STEC, Salmonella, or L. monocytogenes during the fermentation of spontaneously fermented beet kvass. Additionally, our study also analyzed the survival of these pathogens after 30 days of refrigerated (4 degrees C) storage. Among the three pathogenic bacteria, STEC was the most acid resistant, with an increased resistance with higher salt concentrations during storage. Refrigerated storage did not have a significant effect on survival rate of STEC, although there was a 21% decrease in survival from day 0 (81%) to day 30 of storage (64%). These results indicate a potential risk of foodborne illness, irrespective of salt level, primarily because of the low infectious dose of STEC. In contrast, Salmonella was the least acid resistant, with a 72% (26 of 36 samples) survival rate during production, and 17% (6 of 36 samples) following storage. Complete eradication of Salmonella after refrigerated storage was observed in beet kvass prepared with 1.5% NaCl. L. monocytogenes had a survival rate of 78% (28 of 36 samples) after fermentation, and a decreased survival rate of 31% (11 of 36 samples) following storage. Overall, these results indicate that although fermented foods are typically considered safe, it is crucial to weigh the health benefits against the risks of foodborne illness as a result of their consumption. Based on this study, there is a potential risk for STEC, Salmonella, and L. monocytogenes survival during fermentation of beet kvass, regardless of low salt concentrations or garlic concentration. This finding reinforces that the production of naturally fermented beet kvass should follow proper hygiene and sanitation practices to avoid contamination of beet kvass with pathogenic bacteria that may be present in raw materials or result from cross-contamination from the environment. Though survival of all pathogens decreased after 30 days of refrigerated storage, the survival rates were still considerably high, and it is not advised that fermentation be considered a sole method to ensure product safety. Therefore, to decrease the safety risk, it is recommended to clean the red beetroot by soaking in 10% bleach solution for 10 mins and thoroughly rinse with tap water. As for the physicochemical properties of beet kvass, it was discovered that the concentration of biogenic amines was negligible and does not pose a food safety risk. The results indicate that both the salt and garlic concentration have a significant effects on organic acids, sugar, and ethanol content. The addition of garlic in beet kvass produced samples with lower lactic acid, acetic acid, glucose, and fructose content, but higher ethanol. This biochemical profile suggests that garlic favors the growth of yeast in kvass. Although not explicitly analyzed in our study, these observations demonstrate the likely effects of formulation variability on microbial diversity among the treatments. Lastly, the consumer sensory testing of beet kvass treated with 0.5% and 2.5% salt concentration, and 0% and 0.5% garlic concentration, indicated that beet kvass prepared with 1.5% salt and 0.5% garlic had the highest overall liking score of 6.12 on a 9-point hedonic scale. Salt concentration was a significant deciding factor for the overall acceptance of beet kvass. The study showed sensory preference for lower salt content in fermented beet kvass. The score is lower than benchmark (7 out of 9) for acceptable products. However, the study also indicated the inclusion of health claims increased panelists product interest, indicating participants may be willing to compromise sensory characteristics for health. Therefore, additional work assessing the health mediated effects of this modified beet kvass formulation is necessary to maximizing product marketability.

Publications


    Progress 05/15/18 to 05/14/19

    Outputs
    Target Audience:The overall goal of this project is to ascertain the safety and quality of food vegetable products fermented under low-sodium conditions. Upon completion of the project we plan to disseminate results to commercial and home producers of fermented products via cooperative extension bulletins. As the first part of this process, a scientific poster was presented at the 2018 annual meeting of the International Association of Food Protection (Salt Lake City). Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Opportunities for professional development within this project are numerous. The University of Maine Food Science Program is small, yet robust. Faculty work closely with both graduate and undergraduate students in both classroom and laboratory settings. Research laboratories often double as teaching labs and graduate students are strongly encouraged to mentor undergraduates in a research environment. As this project has microbiological and chemistry aspects, several students have been extensively trained in advanced microbiological techniques (including work with pathogenic organisms), product development and analytical chemistry (including work with high performance liquid chromatography). As the project enters year 2, students will be exposed to new instrumentation (minion) and techniques. How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals?Year 2 of the project will focus on spontaneously fermentedbeet kvass. Kvass is an ancient beverage enjoying new popularity and is of special interesst as it has not received much attention in the scientific community and is likely to contain soil-borne microorganisms (including pathogens). Research tasks are as follows: 1. Identify the lactic bacteria community in beet kvass during production and storage. 2. Determine safety (pathogenic organisms present). 3. Determine effects of garlic on lactic acid bacteria community and the biochemical components (organic acids). 4. Measure the concentrations of biogenic amines present with different treatments (salt/garlic) over time. 5. Conduct a sensory evaluation (consumer acceptance) of the product.

    Impacts
    What was accomplished under these goals? Impact of reduced sodium concentration on pathogen survival during fermentation and during cold storage: As it is one of the most popular fermented vegetable products with consumers, sauerkraut was chosen as the first low-sodium model for this study. Sauerkraut was spontaneously (natural flora) fermented at 1.0, 1.5, 2.0 and 2.5% (w/w) NaCl content and innoculated with a pathogen cocktail containing strains of Shiga toxin-producing Escherichia coli (STEC), S. aureus and L. monocytogenes. Significant increases in all pathogens were observed on day one, but all pathogens decreased as fermentation progressed. Salt concentration had no effect on pathogen survival. L. monocytogenes did not survive beyond day 6 of fermentation, but STEC and S. aureus were detectedafter fermentation was completed, but after 1 week of refrigeration (4 degrees C) no pathogens were detected. Impact of reduced sodium concentration on microbiological kinetics (microbial populations and metabolic products) Sauerkraut prepared at1, 1.5, 2.0, and 2.5% concentrations (w/w)of NaClwere prepared and allowed to ferment to a final pH of 3.7. All samples experienced significantly lower pH within 3 days and all sodium concentrations resulted in a terminal pH of 3.7 by 14 days. Lactic acid bacteria increased by 6-8 log (CFU/mL) for all salt concentrations by day 14. No fungi or coliforms were detected in any of the samples after fermentation was complete (pH=3.7) and no differences were observed in organic acid or sugar levels between salt concentrations. This indicates that reduced sodium levels in spontaneously-fermented sauerkraut do not negatively affect quality of the final product.

    Publications

    • Type: Theses/Dissertations Status: Published Year Published: 2018 Citation: Recommended Citation Khanna, Surbhi, "Effects of Salt Concentration on the Physicochemical Properties and Microbial Safety of Spontaneously Fermented Cabbage" (2019). Electronic Theses and Dissertations. 3013. https://digitalcommons.library.umaine.edu/etd/3013