Search for Author, Title, Keyword
ORIGINAL ARTICLE
Antibacterial Effect of Sea Buckthorn (Hippophae rhamnoides L.) Fruit Extract on Radish Seeds Prior to Sprouting
 
More details
Hide details
1
Institute of Fermentation Technology and Microbiology, Faculty of Biotechnology and Food Sciences, Lodz University of Technology, Wólczańska 171/173, 90-530, Łódź, Poland
 
 
Submission date: 2024-01-19
 
 
Acceptance date: 2024-04-02
 
 
Online publication date: 2024-04-18
 
 
Publication date: 2024-04-18
 
 
Corresponding author
Katarzyna Rajkowska   

Institute of Fermentation Technology and Microbiology, Faculty of Biotechnology and Food Sciences, Lodz University of Technology, Wólczańska 171/173, 90-530, Łódź, Poland
 
 
 
KEYWORDS
TOPICS
ABSTRACT
Sprouts consumption is increasing worldwide due to their nutritional and health benefits. However, they can be sources of foodborne bacterial diseases, including sprout-related outbreaks caused primarily by Shiga toxin-producing Escherichia coli and Salmonella spp. The aim of this study was to determine the efficacy of a dried sea buckthorn fruit extract in sanitization of contaminated radish seeds. The efficacy of 15-min seed treatment and 3-h soaking in the extract solution was evaluated in comparison to the treatment with 20,000 mg/L calcium hypochlorite, recommended by the U.S. Food and Drug Administration. The effect of the sea buckthorn fruit extract on radish seed germination capacity and the profile of phenolic compounds in the extract were also determined. Decontamination effect of the extract after a 15-min seed treatment ranged from 72.1% against Staphylococcus aureus to 93.0% against Listeria monocytogenes and was higher than that of active chlorine against E. coli, S. aureus and Salmonella enterica. Soaking seeds for 3 h in the extract increased the decontamination efficiency only against S. aureus (81.9%). Compared to water, after 4 days of sprouting, no significant differences were found in radish seed germination capacity and the length of roots and hypocotyls of sprouts. The sea buckthorn fruit extract had a high content of phenolic compounds, namely isorhamnetin 3-rhamnosylglucoside (12.99 mg/L), isorhamnetin 3-rutinoside (8.25 mg/L), protocatechuic acid (5.43 mg/L), isorhamnetin 3-glucoside (3.41 mg/L), and gallic acid (3.36 mg/L). The extract can be used as a substance limiting bacterial contamination of radish seeds and, as a result, sprouts, as well as a valuable source of phenolic compounds.
FUNDING
The research did not receive any external funds.
CONFLICT OF INTEREST
Authors declare no conflict of interests.
 
REFERENCES (47)
1.
Abellán, Á., Domínguez-Perles, R., Moreno, D.A., García-Viguera, C. (2019). Sorting out the value of cruciferous sprouts as sources of bioactive compounds for nutrition and health. Nutrients, 11(2), art. no. 429. https://doi.org/10.3390/nu1102....
 
2.
Allende, A., Selma, M.V., López-Gálvez, F., Villaescusa, R., Gil, M.I. (2008). Role of commercial sanitizers and washing systems on epihytic microorganisms and sensory quality of fresh-cut escarole and lettuce. Postharvest Biology and Technology, 49(1), 155–163. https://doi.org/10.1016/j.post....
 
3.
Barak, J.D., Whitehand, L.C., Charkowski, A.O. (2002). Differences in attachment of Salmonella enterica serovars and Escherichia coli O157:H7 to alfalfa sprouts. Applied and Environmental Microbiology, 68(10), 4758–4763. https://doi.org/10.1128/AEM.68....
 
4.
Beuchat, L.R., Ward, T.E., Pettigrew C.A. (2001). Comparison of chlorine and a prototype produce wash product for effectiveness in killing Salmonella and Escherichia coli O157:H7 on alfalfa seeds. Journal of Food Protection, 64(2), 52–158. https://doi.org/10.4315/0362-0....
 
5.
Bhattacharya, D., Ghosh, D., Bhattacharya, S., Sarkar, S., Karmakar, P., Koley, H., Gachhui, R. (2018). Antibacterial activity of polyphenolic fraction of Kombucha against Vibrio cholerae: targeting cell membrane. Letters in Applied Microbiology, 66(2), 145–152. https://doi.org/10.1111/lam.12....
 
6.
Centers for Disease Control and Prevention. (2023). List of multistate foodborne outbreak notices. Available at: https://www.cdc.gov/foodsafety... (accessed: 21 September 2023).
 
7.
Chaman, S., Syed, N.I.H., Danish, Z., Khan, F.Z. (2011). Phytochemical analysis, antioxidant and antibacterial effects of sea buckthorn berries. Pakistan Journal of Pharmaceutical Sciences, 24(3), 345–351.
 
8.
Charkowski, A.O., Sarreal, C.Z., Mandrell, R.E. (2001). Wrinkled alfalfa seeds harbor more aerobic bacteria and are more difficult to sanitize than smooth seeds. Journal of Food Protection, 64(9), 1292–1298. https://doi.org/10.4315/0362-0....
 
9.
Chen, A., Feng, X., Dorjsuren, B., Chimedtseren, C., Damda, T.-A., Zhang, C. (2023). Traditional food, modern food and nutritional value of Sea buckthorn (Hippophae rhamnoides L.): A review. Journal of Future Foods, 3(3), 191–205. https://doi.org/10.1016/j.jfut....
 
10.
Codex Alimentarius Commission. (2001). Report of the thirty third session of the Codex Committee on food hygiene. Annex I. Proposed draft annex for sprout production. Codex Alimentarius Commission: Geneva.
 
11.
Czyżowska, A., Wilkowska, A., Staszczak, A., Nowak, A. (2020). Characterization of phytochemicals in berry fruit wines analyzed by liquid chromatography coupled to photodiode-array detection and electrospray ionization/ion trap mass spectrometry (LC-DAD-ESI-MSn) and their antioxidant and antimicrobial activity. Foods, 9(12), art. no. 1783. https://doi.org/10.3390/foods9....
 
12.
Dadi, P.K., Ahmad, M., Ahmad, Z. (2009). Inhibition of ATPase activity of Escherichia coli ATP synthase by polyphenols. International Journal of Biological Macromolecules, 45(1), 72–79. https://doi.org/10.1016/j.ijbi....
 
13.
Ding, H., Fu, T.J., Smith, M.A. (2013). Microbial contamination in sprouts: How effective is seed disinfection treatment? Journal of Food Science, 78(4), R495–R501. https://doi.org/10.1111/1750-3....
 
14.
Efenberger-Szmechtyk, M., Nowak, A., Czyzowska, A. (2020). Plant extracts rich in polyphenols: antibacterial agents and natural preservatives for meat and meat products. Critical Reviews in Food Science and Nutrition, 61(1), 149−178. https://doi.org/10.1080/104083....
 
15.
ESSA hygiene guideline for the production of sprouts and seeds for sprouting. (2017). Official Journal of the European Union, C 220/03.
 
16.
Fay, M.L., Salazar, J.K., Ren, Y., Wu, Z., Mate, M., Khouja, B.A., Lingareddygari, P., Liggans, G. (2023). Growth kinetics of Listeria monocytogenes and Salmonella enterica on dehydrated vegetables during rehydration and subsequent storage. Foods, 12(13), art. no. 2561. https://doi.org/10.3390/foods1....
 
17.
FDA, U.S. Food and Drug Administration. (2023). Compliance with and recommendations for implementation of the standards for the growing, harvesting, packing, and holding of produce for human consumption for sprout operations: guidance for industry. Available at: https://www.fda.gov/media/1024... (accessed: 20 March 2023).
 
18.
Fleckenstein, J.M., Kuhlmann, F.M., Sheikh, A. (2021). Acute bacterial gastroenteritis. Gastroenterology Clinics of North America, 50(2), 283–304. https://doi.org/10.1016/j.gtc.....
 
19.
Fransisca, L., Park, H.K., Feng, H. (2012). E. coli O157:H7 population reduction from alfalfa seeds with malic acid and thiamine dilauryl sulfate and quality evaluation of the resulting sprouts. Journal of Food Science, 77(2), M121–M126. https://doi.org/10.1111/j.1750....
 
20.
Gamba, M., Asllanaj, E., Raguindin, P.F., Glisic, M., Franco, O.H., Minder, B., Bussler, W., Metzger, B., Kern, H., Muka, T. (2021). Nutritional and phytochemical characterization of radish (Raphanus sativus): A systematic review. Trends in Food Science & Technology, 113, 205–218. https://doi.org/10.1016/j.tifs....
 
21.
Gulcin, I. (2012). Antioxidant activity of food constituents: An overview. Archives of Toxicology, 86, 345–391. https://doi.org/10.1007/s00204....
 
22.
Guo, R., Guo, X., Li, T., Fu, X., Liu, R.H. (2017). Comparative assessment of phytochemical profiles, antioxidant and antiproliferative activities of Sea buckthorn (Hippophae rhamnoides L.) berries. Food Chemistry, 221, 997–1003. https://doi.org/10.1016/j.food....
 
23.
Ivanišová, E., Blašková, M., Terentjeva, M., Grygorieva, O., Vergun, O., Brindza, J., Kačániová, M. (2020). Biological properties of sea buckthorn (Hippophae rhamnoides L.) derived products. Acta Scientiarum Polonorum Technologia Alimentaria, 19(2), 195–205. https://doi.org/10.17306/J.AFS....
 
24.
Jaśniewska, A., Diowksz, A. (2021). Wide spectrum of active compounds in sea buckthorn (Hippophae rhamnoides) for disease prevention and food production. Antioxidants, 10(8), art. no. 1279. https://doi.org/10.3390/antiox....
 
25.
Jeong, J.H., Lee, J.W., Kim, K.S., Kim, J.-S., Han, S.N., Yu, C.Y., Lee, J.K., Kwon, Y.S., Kim, M.J. (2010). Antioxidant and antimicrobial activities of extracts from a medicinal plant, sea buckthorn. Journal of the Korean Society for Applied Biological Chemistry, 53, 33–38. https://doi.org/10.3839/jksabc....
 
26.
Kang, T.M., Cho, S.K., Park, J.Y., Song, K.B., Chung, M.S., Park, J.H. (2011). Analysis of microbial contamination of sprouts and fresh-cut salads in a market. Korean Journal of Food Science and Technology, 43(4), 490–494. https://doi.org/10.9721/KJFST.....
 
27.
Kim, C., Hung, Y.C., Brackett, R.E., Lin, C.S. (2003). Efficacy of electrolyzed oxidizing water in inactivating Salmonella on alfalfa seeds and sprouts. Journal of Food Protection, 66(2), 208–214. https://doi.org/10.4315/0362-0....
 
28.
Lang, E., Zoz, F., Iaconelli, C., Guyot, S., Alvarez-Martin, P., Beney, L., Perrier-Cornet, J.M., Gervais, P. (2016). Recovery estimation of dried foodborne pathogens is directly related to rehydration kinetics. PLoS One, 11(8), art. no. e0160844. https://doi.org/10.1371/journa....
 
29.
Mascarenhas, L.A.B., dos Santos, L.M.C., Oliveira, F.O., Rodrigues, L.A.P., Neves, P.R.F., Moreira, G.A.F., Santos, A.A.B., Lobato, G.M., Nascimento, C., Gerhardt, M., Machado, B.A.S. (2022). Evaluation of the microbial reduction efficacy and perception of use of an ozonized water spray disinfection technology. Scientific Reports, 12(1), art. no. 13019. https://doi.org/10.1038/s41598....
 
30.
Michalczyk, M., Kowalińska, J. (2009). Microbial contamination of commercially available sprouted seeds. Żywność. Nauka. Technologia. Jakość, 3(64), 32–39 (in Polish, English abstract).
 
31.
Miché, L., Balandreau, J. (2001). Effects of rice seed surface sterilization with hypochlorite on inoculated Burkholderia vietnamiensis. Applied and Environmental Microbiology, 67(7), 3046–3052. https://doi.org/10.1128/AEM.67....
 
32.
Miyahira, R.F., Antunes, A.E.C. (2021). Bacteriological safety of sprouts: A brief review. International Journal of Food Microbiology, 352, art. no. 109266. https://doi.org/10.1016/j.ijfo....
 
33.
Montville, R., Schaffner, D.W. (2004). Analysis of published sprout seed sanitization studies shows treatments are highly variable. Journal of Food Protection, 67(4), 758–765. https://doi.org/10.4315/0362-0....
 
34.
NACMCF, National Advisory Committee on Microbiological Criteria for Foods. (1999). Microbiological safety evaluations and recommendations on sprouted seeds. International Journal of Food Microbiology, 52(3), 123–153. https://doi.org/10.1016/S0168-....
 
35.
Rajkowska, K., Otlewska, A., Broncel, N., Kunicka-Styczyńska, A. (2023). Microbial diversity and bioactive compounds in dried Lycium barbarum fruits (goji): A comparative study. Molecules, 28(10), art. no. 4058. https://doi.org/10.3390/molecu....
 
36.
Sikin, A.M., Zoellner, C., Rizvi, S.S. (2013). Current intervention strategies for the microbial safety of sprouts. Journal of Food Protection, 76(12), 2099–2123. https://doi.org/10.4315/0362-0....
 
37.
Tang, Q.L., Kang, A.R., Lu, C.X. (2016). Phytochemical analysis, antibacterial activity and mode of action of the methanolic extract of Scutellaria barbata against various clinically important bacterial pathogens. International Journal of Pharmacology, 12(2), 116–125. https://doi.org/10.3923/ijp.20....
 
38.
Teleszko, M., Wojdyło, A., Rudzińska, M., Oszmiański, J., Golis, T. (2015). Analysis of lipophilic and hydrophilic bioactive compounds content in sea buckthorn (Hippophae rhamnoides L.) berries. Journal of Agricultural and Food Chemistry, 63(16), 4120−4129. https://doi.org/10.1021/acs.ja....
 
39.
Upadhyay, N.K., Kumar, M.S., Gupta, A. (2010). Antioxidant, cytoprotective and antibacterial effects of Sea buckthorn (Hippophae rhamnoides L.) leaves. Food and Chemical Toxicology, 48(12), 3443–3448. https://doi.org/10.1016/j.fct.....
 
40.
Viswanathan, P., Kaur, R. (2001). Prevalence and growth of pathogens on salad vegetables, fruits and sprouts. International Journal of Hygiene and Environmental Health, 203(3), 205–213. https://doi.org/10.1078/S1438-....
 
41.
Wang, Z., Zhao, F., Wei, P., Chai, X., Hou, G, Meng, Q. (2022). Phytochemistry, health benefits, and food applications of sea buckthorn (Hippophae rhamnoides L.): A comprehensive review. Frontiers in Nutrition, 9, art. no. 1036295. https://doi.org/10.3389/fnut.2....
 
42.
Weissinger, W.R., Beuchat, L.R. (2000). Comparison of aqueous chemical treatments to eliminate Salmonella on alfalfa seeds. Journal of Food Protection, 63(11), 1475–1482. https://doi.org/10.4315/0362-0....
 
43.
Wu, T., He, M., Zang, X., Zhou, Y., Qiu, T., Pan, S., Xu, X. (2013). A structure–activity relationship study of flavonoids as inhibitors of E. coli by membrane interaction effect. Biochimica et Biophysica Acta – Biomembranes, 1828(11), 2751–2756. https://doi.org/10.1016/j.bbam....
 
44.
Yang, B., Halttunen, T., Raimo, O., Price, K., Kallio, H. (2009). Flavonol glycosides in wild and cultivated berries of three major subspecies of Hippophae rhamnoides and changes during harvesting period. Food Chemistry, 115(2), 657−664. https://doi.org/10.1016/j.food....
 
45.
Yi, S.M., Zhu, J.L., Fu, L.L., Li, J.R. (2010). Tea polyphenols inhibit Pseudomonas aeruginosa through damage to the cell membrane. International Journal of Food Microbiology, 144(1), 111–117. https://doi.org/10.1016/j.ijfo....
 
46.
Zhang, L., Xu, S.G., Liang, W., Mei, J., Di, Y.Y., Lan, H.H., Yang, Y., Wang, W.W., Luo, Y.Y., Wang, H.Z. (2015). Antibacterial activity and mode of action of Mentha arvensis ethanol extract against multidrug-resistant Acinetobacter baumannii. Tropical Journal of Pharmaceutical Research, 14(11), 2099–2106. https://doi.org/10.4314/tjpr.v....
 
47.
Zheng, S., Bawazir, M., Dhall, A., Kim, H.E., He, L., Heo, J., Hwang, G. (2021). Implication of surface properties, bacterial motility, and hydrodynamic conditions on bacterial surface sensing and their initial adhesion. Frontiers in Bioengineering and Biotechnology, 9, art. no. 643722. https://doi.org/10.3389/fbioe.....
 
eISSN:2083-6007
ISSN:1230-0322
Journals System - logo
Scroll to top