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Toward better microbial safety of wheat sprouts: chlorophyllin-based photosensitization of seeds

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Abstract

Sprouted seeds are gaining popularity worldwide due to their high nutritional value. At the same time, they are among the most highly contaminated fresh produce and have been recognized as the primary source of food-borne pathogens, such as E. coli O157 and harmful microfungi. The antifungal and antibacterial properties of chlorophyllin-based photosensitization in vitro together with successful application of this treatment for microbial control in wheat sprouts have been investigated. First, we examined the antimicrobial efficiency of chlorophyllin (Chl, 1.5 × 10−5–5 × 10−3 M) activated in vitro by visible light (405 nm, radiant exposure: 18 J cm−2) against the food-borne pathogen Escherichia coli and plant pathogen Fusarium oxysporum. Results revealed that this treatment (1.5 × 10−5 M Chl, incubation time 1 h, 405 nm, radiant exposure: 18 J cm−2) can reduce the E. coli population by 95%. Moreover, at higher chlorophyllin concentrations (5 × 10−4–5 × 10−3 M Chl), it is possible to delay the growth of F. oxysporum by 51–74%. The decontamination of wheat seeds by chlorophyllin-based photosensitization (5 × 10−4 M Chl, 405 nm, radiant exposure: 18 J cm−2) remarkably reduced the viability of surface-attached mesophilic bacteria (~2.5log CFU g−1), E. coli (~1.5log CFU g−1) and yeasts/fungi (~1.5log CFU g−1). Moreover, SEM images confirmed that this treatment did not damage the grain surface microstructure. Most importantly, Chl-based photosensitization did not reduce the seed germination rate or seedling growth and had no impact on the visual qualities of sprouts. In conclusion, the chlorophyllin-based photosensitization treatment, being nonthermal, environmentally friendly and cost-effective, has huge potential for microbial control of highly contaminated germinated wheat sprouts and seeds used to produce sprouts, especially in organic farming.

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References

  1. A. K. Singh, J. Rehal, A. Kaur and G. Jyot, Enhancement of Attributes of Cereals by Germination and Fermentation: A Review, Crit. Rev. Food Sci. Nutr., 2015, 55, 1575–1589.

    Article  CAS  PubMed  Google Scholar 

  2. P. J. Taormina, L. R. Beuchat and L. Slutsker, Infections Associated with Eating Seed Sprouts: An International Concern, Emerging Infect. Dis., 1999, 5(5), 626–634, DOI: 10.3201/eid0505.990503.

  3. J. W. Sarah Klein, A. Tian and C. S. DeWaal, The ten riskiest foods regulated by the U.S. Food and Drug Administration. https://cspinet.org/sites/default/files/attachment/cspi_top_10_fda.pdf (accessed 28th March, 2017).

  4. T. Breuer, D. H. Benkel, R. L. Shapiro, W. N. Hall, M. M. Winnett, M. J. Linn, J. Neimann, T. J. Barrett, S. Dietrich, F. P. Downes, D.M. Toney, J. L. Pearson,H. Rolka, L. Slutsker and P. M. Griffin, A Multistate Outbreak of Escherichia coli O157:H7 Infections Linked to Alfalfa Sprouts Grown from Contaminated Seeds, Emerging Infect. Dis., 2001, 7(6), 977–982, DOI: 10.3201/eid0706.010609.

  5. A. M. Dechet, K. M. Herman, C. C. Parker, P. Taormina, J. Johanson, R. V. Tauxe and B. E. Mahon, Outbreaks Caused by Sprouts, United States, 1998–2010: Lessons Learned and Solutions Needed, Foodborne Pathog. Dis., 2014, 11(8), 635–644, DOI: 10.1089/fpd.2013.1705.

  6. L. A. King, F. Nogareda, F. X. Weill, P. Mariani-Kurkdjian, E. Loukiadis, G. Gault, N. Jourdan-DaSilva, E. Bingen, M. Mace, D. Thevenot, N. Ong, C. Castor, H. Noel, D. Van Cauteren, M. Charron, V. Vaillant, B. Aldabe, V. Goulet, G. Delmas, E. Couturier, Y. Le Strat, C. Combe, Y. Delmas, F. Terrier, B. Vendrely, P. Rolland and H. de Valk, Outbreak of Shiga toxin-producing Escherichia coli, O104:H4 associated with organic fenugreek sprouts, France, June 2011, Clin. Infect. Dis., 2012, 54, 1588–1594.

    CAS  Google Scholar 

  7. H. Uphoff, B. Hedrich, I. Strotmann, M. Arvand, G. Bettge- Weller and A. M. Hauri, A prolonged investigation of an STEC-O104 cluster in Hesse, Germany, 2011 and implications for outbreak management, J. Public Health, 2014, 22(1), 41–48, DOI: 10.1007/s10389-013-0595-2.

  8. M. Knödler, M. Berger and U. Dobrindt, Long-term survival of the Shiga toxin-producing Escherichia coli O104: H4 outbreak strain on fenugreek seeds, Food Microbiol., 2016, 59, 190–195.

    PubMed  Google Scholar 

  9. A. Wallin, Z. Luksiene, K. Zagminas and G. Surkiene, Public health and bioterrorism: renewed threat of anthrax and smallpox, Medicina, 2007, 43(4), 278–284.

    Article  PubMed  Google Scholar 

  10. A. Zahoranová, M. Henselová, D. Hudecová, B. Kaliňáková, D. Kováčik, V. Medvecká and M. Černák, Effect of Cold Atmospheric Pressure Plasma on the Wheat Seedlings Vigor and on the Inactivation of Microorganisms on the Seeds Surface, Plasma Chem. Plasma Process., 2016, 36, 397–414, DOI: 10.1007/s11090-015-9684-z.

    Article  Google Scholar 

  11. Z. Luksiene, H. Danilcenko, Z. Taraseviciene, Z. Anusevicius, A. Maroziene and H. Nivinskas, New approach to the decontamination of germinated wheat from microfungi: effects of aminolevulinic acid, Int. J. Food Microbiol., 2007, 116, 153–158, DOI: 10.1016/j. ijfoodmicro.2006.12.040.

    Article  CAS  PubMed  Google Scholar 

  12. FDA, Microbiological safety evaluations and recommendations on sprouted seed. www.fda.gov (accessed November 2018).

  13. M. Wainwright, Photodynamic antimicrobial chemotherapy, J. Antimicrob. Chemother., 1998, 42, 13–28.

    Article  CAS  PubMed  Google Scholar 

  14. N. Kashef, Y. Y. Huang and M. R. Hamblin, Advances in antimicrobial photodynamic inactivation at the nanoscale, Nanophotonics, 2017, 6(5), 853–879.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. M. R. Hamblin and T. Hasan, Photodynamic therapy: new antimicrobial approach to infectious disease, Photochem. Photobiol. Sci., 2004, 3, 436–450.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Z. Luksiene, D. Peciulyte and A. Lugauskas, Inactivation of fungi in vitro by photosensitization: preliminary results, Ann. Agric. Environ. Med., 2004, 11(2), 215–220.

    PubMed  Google Scholar 

  17. E. Alves, M. A. Faustino, M. G. Neves, A. Cunha, J. Tome and A. Almeida, An insight on bacterial cellular targets of photodynamic inactivation, Future Med. Chem., 2014, 6(2), 1–24.

    Article  Google Scholar 

  18. Z. Luksiene, in Novel Food Preservation and Microbial Assessment Techniques, ed. I. S. Boziaris, CRC Press, Boca Raton, 2014, ch. 7, pp. 184–217.

  19. N. Tortik, A. Spaeth and K. Plaetzer, Photodynamic decontamination of foodstuff from Staphylococcus aureus based on novel formulations of curcumin, Photochem. Photobiol. Sci., 2014, 13, 1402–1409.

    CAS  Google Scholar 

  20. M. R. Hamblin and G. Jori, Photodynamic inactivation of microbial pathogens: medical and environmental applications, Royal Society of Chemistry, Cambridge, 2015.

  21. M. Wainwright, T. Maisch, S. Nonell, K. Plaetzer, A. Almeida, G. P. Tegos and M. R. Hamblin, Photoantimicrobials—are we afraid of the light?, Lancet Infect. Dis., 2017, 17(2), 49–55.

    Article  Google Scholar 

  22. G. López-Carballo, P. Hernández-Muñoz, R. Gavara and M. J. Ocio, Photoactivated chlorophyllin-based gelatin films and coatings to prevent microbial contamination of food products, Int. J. Food Microbiol., 2008, 126(1–2), 65–70.

  23. E. Paskeviciute, B. Zudyte and Z. Luksiene, Towards better microbial safety of fresh produce: Chlorophyllin-based photosensitization for microbial control of foodborne pathogens on cherry tomatoes, J. Photochem. Photobiol., B, 2018, 82, 130–136.

    Article  Google Scholar 

  24. Photosynthesis: Mechanisms and Effects, ed. G. Garab, Springer Science & Business Media, Budapest, 1998, vol. 3.

  25. Z. Luksiene, I. Buchovec and E. Paskeviciute, Inactivation of several strains of Listeria monocytogenes attached to the surface of packaging material by Na-Chlorophyllin based photosensitization, J. Photochem. Photobiol., B, 2010, 101, 326–331, DOI: 10.1016/j.jphotobiol.2010.08.002.

    CAS  Google Scholar 

  26. T. Calado, A. Venancio and L. Abrunhosa, Irradiation for Mold and Mycotoxin Control: A Review, Compr. Rev. Food Sci. Food Saf., 2014, 13, 1049–1061.

    Article  CAS  Google Scholar 

  27. X. Fan, K. Sokorai, A. Weidauer, G. Gotzmann and F. H. Rögner, Comparison of gamma and electron beam irradiation in reducing populations of E. coli artificially inoculated on mung bean, clover and fenugreek seeds, and affecting germination and growth of seeds, Radiat. Phys. Chem., 2017, 130, 306–315.

    CAS  Google Scholar 

  28. L. A. Keskinen, A. Burke and B. A. Annous, Efficacy of chlorine, acidic electrolyzed water and aqueous chlorine dioxide solutions to decontaminate Escherichia coli, O157: H7 from lettuce leaves, Int. J. Food Microbiol., 2009, 132(2–3), 134–140, DOI: 10.1016/j.ijfoodmicro.2009.04.006.

  29. S. Koide, D. Shitanda, M. Note and W. Cao, Effects of mildly heated, slightly acidic electrolyzed water on the disinfection and physicochemical properties of sliced carrot, Food Control, 2011, 22(3–4), 452–456, DOI: 10.1016/j. foodcont.2010.09.025.

  30. H. A. Taha, K. A. El-Shaikh and M. M. Al-Sadi, M. M. Effect of sodium hypochlorite on Fasciola gigantica eggs and the intermediate host, Lymnaea natalensis: A scanning electron microscopy study, J. Taibah Univ. Sci., 2014, 8(2), 75–83, DOI: 10.1016/j.jtusci.2013.12.003.

  31. C. Estrela, C. R. Estrela, E. L. Barbin, J. C. E. Spanó, M. A. Marchesan and J. D. Pécora, Mechanism of action of sodium hypochlorite, Braz. Dent. J., 2002, 13(2), 113–117, DOI: 10.1590/S0103-64402002000200007.

  32. D. Kandaswamy and N. Venkateshbabu, Root canal irrigants, J. Conservative Dent., 2010, 13(4), 256–264.

    Article  Google Scholar 

  33. K. Y. Chiu and J. M. Sung, Use of ultrasonication to enhance pea seed germination andmicrobial quality of pea sprouts, Int. J. Food Sci. Technol., 2014, 49, 1699–1706, DOI: 10.1111/ijfs.12476.

    Article  CAS  Google Scholar 

  34. C. Nguyen-the and F. Carlin, The microbiology of minimally processed fresh fruits and vegetables, Crit. Rev. Food Sci. Nutr., 1994, 34, 371–401.

    Article  CAS  PubMed  Google Scholar 

  35. V. M. Gomez-Lopez, P. Ragaert, J. Devebere and F. Devlieghere, Pulsed light for food decontamination, Trends Food Sci. Technol., 2007, 18, 464–473, DOI: 10.1016/j. tifs.2007.03.010.

    Article  CAS  Google Scholar 

  36. Z. Luksiene, I. Buchovec and E. Paskeviciute, High power pulsed light for decontamination of chicken from food pathogens: a study on antimicrobial efficiency and organoleptic properties, J. Food Saf., 2011, 31, 61–68, DOI: 10.1111/j.1745-4565.2010.00267.x.

    Article  Google Scholar 

  37. Z. Luksiene, I. Buchovec, K. Kairyte, E. Paskeviciute and P. Viskelis, High-power pulsed light for microbial decontamination of some fruits and vegetables with different surfaces, J. Food Agric. Environ., 2012, 10(3&4), 162–167.

  38. Z. Luksiene, I. Buchovec and P. Viskelis, Impact of High Power Pulsed Light on Microbial Contamination, Health Promoting Components and Shelf-Life of Strawberries, Food Technol. Biotechnol., 2013, 51, 284–292.

    Google Scholar 

  39. Z. Luksiene, I. Buchovec and E. Paskeviciute, Inactivation of Bacillus cereus by Na-chlorophyllin-based photosensitization on the surface of packaging, J. Appl. Microbiol., 2010, 109, 1540–1548, DOI: 10.1111/j.1365-2672.2010.04780.x.

    CAS  PubMed  Google Scholar 

  40. Z. Luksiene and E. Paskeviciute, Novel approach to the microbial decontamination of strawberries: chlorophyllinbased photosensitization, J. Appl. Microbiol., 2011, 110(5), 1274–1283.

    Article  CAS  PubMed  Google Scholar 

  41. Z. Luksiene and E. Paskeviciute, Novel approach to decontaminate food-packaging from pathogens in non-thermal and not chemical way: chlorophyllin-based photosensitization, J. Food Process Eng., 2011, 106(2), 152–158.

    Article  CAS  Google Scholar 

  42. K. Aponiene, E. Paskeviciute, I. Reklaitis and Z. Luksiene, Reduction of microbial contamination of fruits and vegetables by hypericin-based photosensitization: comparison with other emerging antimicrobial treatments, J. Food Eng., 2015, 144, 29–35.

    Article  CAS  Google Scholar 

  43. A. Banerjee and B. Mittra, Morphological modification in wheat seedlings infected by Fusarium oxysporum, Eur. J. Plant Pathol., 2018, 152, 521–524.

    Article  Google Scholar 

  44. K. Kairyte, S. Lapinskas, V. Gudelis and Z. Luksiene, Effective inactivation of food pathogens Listeria monocytogenes and Salmonella enterica by combined treatment of hypericin-based photosensitization and high power pulsed light, J. Appl. Microbiol., 2012, 112(6), 1144–1151, DOI: 10.1111/j.1365-2672.2012.05296.x.

  45. Z. Luksiene, R. Kokstaite, P. Katauskis and V. Skakauskas, Novel Approach to Effective and Uniform Inactivation of Gram-Positive Listeria monocytogenes and Gram-Negative Salmonella enterica by Photosensitization, Food Technol. Biotechnol., 2013, 51(3), 338–344.

    CAS  Google Scholar 

  46. I. Buchovec, V. Lukseviciute, A. Marsalka, I. Reklaitis and Z. Luksiene, Effective photosensitization-based inactivation of Gram (−) food pathogens and molds using the chlorophyllin–chitosan complex: towards photoactive edible coatings to preserve strawberries, Photochem. Photobiol. Sci., 2016, 15(4), 506–516.

    Article  CAS  PubMed  Google Scholar 

  47. I. Buchovec, V. Lukseviciute, R. Kokstaite, D. Labeikyte, L. Kaziukonyte and Z. Luksiene, Inactivation of Gram (−) bacteria Salmonella enterica by chlorophyllin based photosensitization: mechanism of action and new strategies to enhance the inactivation efficiency, J. Photochem. Photobiol., B, 2017, 172, 1–10.

    CAS  Google Scholar 

  48. K. Aponiene and Z. Luksiene, Effective combination of LED-based visible light, photosensitizer and photocatalyst to combat Gram (−) bacteria, J. Photochem. Photobiol., B, 2015, 142, 257–263.

    Article  CAS  Google Scholar 

  49. L. Kordas, W. Pusz, T. Czapka and R. Kacprzyk, The Effect of Low-Temperature Plasma on Fungus Colonization of Winter Wheat Grain and Seed Quality, Pol. J. Environ. Stud., 2015, 24(1), 433–438.

    CAS  Google Scholar 

  50. D. Butscher, H. Van Loon, A. Waskow, P. R. von Rohr and M. Schuppler, Plasma inactivation of microorganisms on sprout seeds in a dielectric barrier discharge, Int. J. Food Microbiol., 2016, 238, 222–232, DOI: 10.1016/j. ijfoodmicro.2016.09.006.

    Article  CAS  PubMed  Google Scholar 

  51. S. Anžlovar, M. Likar and J. D. Koce, Antifungal potential of thyme essential oil as a preservative for storage of wheat seeds, Acta Bot. Croat., 2017, 76(1), 64–71, DOI: 10.1515/ botcro-2016-0044.

  52. P. Manas and R. Pagan, Microbial inactivation by new technologies of food preservation, J. Appl. Microbiol., 2005, 98, 1387–1399.

    Article  CAS  PubMed  Google Scholar 

  53. M. Glueck, B. Schamberger, P. Eckl and K. Plaetzer, New horizons in microbiological food safety: Photodynamic Decontamination based on a curcumin derivative, Photochem. Photobiol. Sci., 2017, 16(12), 1784–1791, DOI: 10.1039/C7PP00165G.

  54. S. Grover and A. S. Khan, Effect of ionizing radiation on some characteristics of seeds of wheat, Int. J. Sci. Technol. Res., 2014, 3(4), 32–39.

    Google Scholar 

  55. S. Choi, L. R. Beuchat, H. Kim and J. H. Ryu, Viability of sprout seeds as affected by treatment with aqueous chlorine dioxide and dry heat, and reduction of Escherichia coli, O157:H7 and Salmonella enterica on pak choi seeds by sequential treatment with chlorine dioxide, drying, and dry heat, Food Microbiol., 2016, 54, 127–132, DOI: 10.1016/j. fm.2015.10.007.

    CAS  Google Scholar 

  56. A. Mitra, Y. F. Li, T. G. Klämpfl, T. Shimizu, J. Jeon, G. E. Morfill and J. L. Zimmermann, Inactivation of Surface- Borne Microorganisms and Increased Germination of Seed Specimen by Cold Atmospheric Plasma, Food Bioprocess Technol., 2014, 7, 645–653, DOI: 10.1007/s11947-013-1126-4.

    Article  CAS  Google Scholar 

  57. A. Los, D. Ziuzina, S. Akkermans, D. Boehm, P. J. Cullen, J. Van Impe and P. Bourke, Improving microbiological safety and quality characteristics of wheat and barley by high voltage atmospheric cold plasma closed processing, Food Res. Int., 2018, 106, 509–521, DOI: 10.1016/j.foodres.2018.01.009.

    Article  CAS  PubMed  Google Scholar 

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  1. Institute of Photonics and Nanotechnology, Vilnius University, Sauletekio 10, Vilnius, Lithuania

    Bernadeta Žudyté & Živilė Lukšiené

  2. Vilnius University Institute of Computer Science, Didlaukio g. 47, Vilnius, Lithuania

    Živilė Lukšiené

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  1. Bernadeta Žudyté
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Žudyté, B., Lukšiené, Ž. Toward better microbial safety of wheat sprouts: chlorophyllin-based photosensitization of seeds. Photochem Photobiol Sci 18, 2521–2530 (2019). https://doi.org/10.1039/c9pp00157c

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