Skip to main content
Log in

Reduction of Alicyclobacillus acidoterrestris Spores on Apples by Chlorine Dioxide in Combination with Ultrasound or Shaker

  • Original Paper
  • Published:
Food and Bioprocess Technology Aims and scope Submit manuscript

Abstract

Alicyclobacillus acidoterrestris has recently become a major issue in the fruit juice industry due to its implication in the spoilage of pasteurized juices. The aim of this study was to determine the potential of combining chlorine dioxide (ClO2) with ultrasound or shaker processes to reduce A. acidoterrestris spores on the apple. Fuji apples were inoculated with a five-strain suspension of A. acidoterrestris spores and treated by ClO2, ultrasound and shaker, individually or combined. The results showed that ClO2 in combination with shaker was the most effective in reducing A. acidoterrestris spores on apples. After treatment with 200 mg/L ClO2 plus shaker (200 rpm) for 20 min, the viable spores remaining on the surface of the apple was reduced to undetectable levels (<1.7 log10 colony-forming unit (CFU)/apple). The inactivation efficiency of ClO2 was significantly decreased with the increase of pH in the range of 2.5–8.5; whereas, the alkaline condition was favorable to the spore detachment from apple surfaces. As for the artificially A. acidoterrestris-contaminated samples with spore concentrations of 3, 4, and 5 log CFU/apple, spores were reduced below the level of detection after combined treatment with ClO2 (50 mg/L, pH 2.5) and shaker (200 rpm) for 5, 10, and 20 min, respectively. This study demonstrates that the combination of ClO2 and shaker is an effective approach for controlling A. acidoterrestris spores on apples and minimizing the risk of contamination in apple juice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • American Public Health Association (APHA). (1998). Standard methods for the examination of water and wastewater. Washington, DC: American Public Health Association.

    Google Scholar 

  • Beuchat, L. R., Pettigrew, C. A., Tremblay, M. E., Roselle, B. J., & Scouten, A. J. (2004). Lethality of chlorine, chlorine dioxide, and a commercial fruit and vegetable sanitizer to vegetative cells and spores of Bacillus cereus and spores of Bacillus thuringiensis. Journal of Food Protection, 67(8), 1702–1708.

    CAS  Google Scholar 

  • Bower, C., McGuire, J., & Daeschel, M. (1996). The adhesion and detachment of bacteria and spores on food-contact surfaces. Trends in Food Science & Technology, 7(5), 152–157.

    Article  CAS  Google Scholar 

  • Brilhante de Sao Jose, J. F., de Andrade, N. J., Ramos, A. M., Dantas Vanetti, M. C., Stringheta, P. C., & Paes Chaves, J. B. (2014). Decontamination by ultrasound application in fresh fruits and vegetables. Food Control, 45, 36–50.

    Article  Google Scholar 

  • Chang, S. S. (2008). Guaiacol producing Alicyclobacillus spp: differentiation, detection, and control. PhD thesis, Washington State University, Pullman, WA, USA.

  • Chen, S. Q., Tang, Q. Y., Zhang, X. D., Zhao, G. H., Hu, X. S., Liao, X. J., Chen, F., Wu, J. H., & Xiang, H. (2006). Isolation and characterization of thermo-acidophilic endospore-forming bacteria from the concentrated apple juice-processing environment. Food Microbiology, 23(5), 439–445.

    Article  CAS  Google Scholar 

  • Danyluk, M. D., Friedrich, L. M., Jouquand, C., Goodrich-Schneider, R., Parish, M. E., & Rouseff, R. (2011). Prevalence, concentration, spoilage, and mitigation of Alicyclobacillus spp. in tropical and subtropical fruit juice concentrates. Food Microbiology, 28(3), 472–477.

    Article  CAS  Google Scholar 

  • de Oliveira, R. C., Davantel de Barros, S. T., & Gimenes, M. L. (2013). The extraction of passion fruit oil with green solvents. Journal of Food Engineering, 117(4), 458–463.

    Article  Google Scholar 

  • Food and Drug Administration (FDA), U.S. Department of Health and Human Services, & Center for Food Safety and Applied Nutrition. (1998). Guide to minimize microbial food safety hazards for fresh fruits and vegetables. Available at http://www.fda.gov/Food/GuidanceRegulation/GuidanceDocumentsRegulatoryInformation/ucm064574.htm. Accessed 26 Oct 1998.

  • Friedrich, L. M., Goodrich-Schneider, R., Parish, M. E., & Danyluk, M. D. (2009). Mitigation of Alicyclobacillus spp. spores on food contact surfaces with aqueous chlorine dioxide and hypochlorite. Food Microbiology, 26(8), 936–941.

    Article  CAS  Google Scholar 

  • Gómez-López, V. M., Rajkovic, A., Ragaert, P., Smigic, N., & Devlieghere, F. (2009). Chlorine dioxide for minimally processed produce preservation: a review. Trends in Food Science & Technology, 20(1), 17–26.

    Article  Google Scholar 

  • Gotoh, K., Harayama, K., & Handa, K. (2015). Combination effect of ultrasound and shake as a mechanical action for textile cleaning. Ultrasonics Sonochemistry, 22, 412–421.

    Article  CAS  Google Scholar 

  • Huang, J. L., Wang, L., Ren, N. Q., Liu, X. L., Sun, R. F., & Yang, G. L. (1997a). Disinfection effect of chlorine dioxide on viruses, algae and animal planktons in water. Water Research, 31(3), 455–460.

    Article  CAS  Google Scholar 

  • Huang, J. L., Wang, L., Ren, N. Q., Ma, F., & Juli. (1997b). Disinfection effect of chlorine dioxide on bacteria in water. Water Research, 31(3), 607–613.

    Article  CAS  Google Scholar 

  • Huang, T. S., Xu, C., Walker, K., West, P., Zhang, S., & Weese, J. (2006). Decontamination efficacy of combined chlorine dioxide with ultrasonication on apples and lettuce. Journal of Food Science, 71(4), 134–139.

    Article  Google Scholar 

  • Komitopoulou, E., Boziaris, I. S., Davies, E. A., Delves-Broughton, J., & Adams, M. R. (1999). Alicyclobacillus acidoterrestris in fruit juices and its control by nisin. International Journal of Food Science and Technology, 34(1), 81–85.

    Article  CAS  Google Scholar 

  • Koolman, L., Whyte, P., Meade, J., Lyng, J., & Bolton, D. (2014). A combination of chemical and ultrasonication treatments to reduce Campylobacter jejuni on raw poultry. Food and Bioprocess Technology, 7(12), 3602–3607.

    Article  CAS  Google Scholar 

  • LeChevallier, M. W., Cawthon, C. D., & Lee, R. G. (1988). Factors promoting survival of bacteria in chlorinated water supplies. Applied and Environmental Microbiology, 54(3), 649–654.

    CAS  Google Scholar 

  • Lee, S. Y., Gray, P. M., Dougherty, R. H., & Kang, D. H. (2004). The use of chlorine dioxide to control Alicyclobacillus acidoterrestris spores in aqueous suspension and on apples. International Journal of Food Microbiology, 92(2), 121–127.

    Article  CAS  Google Scholar 

  • Marriott, N. G., & Gravani, R. B. (2006). Principles of food sanitation. Springer Science & Business Media.

  • Orr, R. V., & Beuchat, L. R. (2000). Efficacy of disinfectants in killing spores of Alicyclobacillus acidoterrestris and performance of media for supporting colony development by survivors. Journal of Food Protection, 63(8), 1117–1122.

    CAS  Google Scholar 

  • Pettipher, G. L., Osmundson, M. E., & Murphy, J. M. (1997). Methods for the detection and enumeration of Alicyclobacillus acidoterrestris and investigation of growth and production of taint in fruit juice and fruit juice-containing drinks. Letters in Applied Microbiology, 24(3), 185–189.

    Article  CAS  Google Scholar 

  • Purnell, G., James, C., James, S. J., Howell, M., & Corry, J. E. L. (2014). Comparison of acidified sodium chlorite, chlorine dioxide, peroxyacetic acid and tri-sodium phosphate spray washes for decontamination of chicken carcasses. Food and Bioprocess Technology, 7(7), 2093–2101.

    Article  CAS  Google Scholar 

  • Sagong, H.-G., Lee, S.-Y., Chang, P.-S., Heu, S., Ryu, S., Choi, Y.-J., & Kang, D.-H. (2011). Combined effect of ultrasound and organic acids to reduce Escherichia coli O157:H7, Salmonella typhimurium, and Listeria monocytogenes on organic fresh lettuce. International Journal of Food Microbiology, 145(1), 287–292.

    Article  Google Scholar 

  • Smit, Y., Cameron, M., Venter, P., & Witthuhn, R. C. (2011). Alicyclobacillus spoilage and isolation—a review. Food Microbiology, 28(3), 331–349.

    Article  Google Scholar 

  • Splittstoesser, D. F., Churey, J. J., & Lee, C. Y. (1994). Growth-characteristics of aciduric sporeforming bacilli isolated from fruit juices. Journal of Food Protection, 57(12), 1080–1083.

    Google Scholar 

  • Steyn, C. E., Cameron, M., & Witthuhn, R. C. (2011). Occurrence of Alicyclobacillus in the fruit processing environment—a review. International Journal of Food Microbiology, 147(1), 1–11.

    Article  CAS  Google Scholar 

  • Wang, J., Hu, X., & Wang, Z. (2010). Kinetics models for the inactivation of Alicyclobacillus acidiphilus DSM14558T and Alicyclobacillus acidoterrestris DSM 3922T in apple juice by ultrasound. International Journal of Food Microbiology, 139(3), 177–181.

    Article  CAS  Google Scholar 

  • Wang, Z. L., Wang, J., Yue, T. L., Yuan, Y. H., Cai, R., & Niu, C. (2013). Immunomagnetic separation combined with polymerase chain reaction for the detection of Alicyclobacillus acidoterrestris in apple juice. Plos One, 8(12), e82376.

    Article  Google Scholar 

  • Wang, Z. L., Cai, R., Yuan, Y. H., Niu, C., Hu, Z. Q., & Yue, T. L. (2014). An immunomagnetic separation-real-time PCR system for the detection of Alicyclobacillus acidoterrestris in fruit products. International Journal of Food Microbiology, 175(3), 30–35.

    Article  CAS  Google Scholar 

  • Yamazaki, K., Teduka, H., & Shinano, H. (1996). Isolation and identification of Alicyclobacillus acidoterrestris from acidic beverages. Bioscience Biotechnology and Biochemistry, 60(3), 543–545.

    Article  CAS  Google Scholar 

  • Yokota, A., Fujii, T., & Goto, K. (2008). Alicyclobacillus: thermophilic acidophilic Bacilli. New York: Springer.

    Google Scholar 

  • Yuan, Y., Hu, Y., Yue, T., Chen, T., & Lo, Y. M. (2009). Effect of ultrasonic treatments on thermoacidophilic Alicyclobacillus acidoterrestris in apple juice. Journal of Food Processing and Preservation, 33(3), 370–383.

    Article  Google Scholar 

  • Yue, T. L., Geng, Y. L., Yuan, Y. H., & Guo, C. X. (2013). Isolation and identification of thermo-acidophilic bacteria from apple storehouses in China. Transactions of the Chinese Society for Agricultural Machinery, 44(7), 187–193.

    CAS  Google Scholar 

  • Zhang, J. B., Yue, T. L., & Yuan, Y. H. (2013). Alicyclobacillus contamination in the production line of kiwi products in China. Plos One, 8(7), e67704.

    Article  CAS  Google Scholar 

  • Zhou, B., Feng, H., & Pearlstein, A. J. (2012). Continuous-flow ultrasonic washing system for fresh produce surface decontamination. Innovative Food Science & Emerging Technologies, 16, 427–435.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The research was supported by the Science and Technology Research and Development Program of Shaanxi Province, China (2014K13-15), the National Natural Science Foundation of China (31371814), and the Basic Research Program of Science and Technology (2013FY113400).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tianli Yue.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cai, R., Yuan, Y., Wang, Z. et al. Reduction of Alicyclobacillus acidoterrestris Spores on Apples by Chlorine Dioxide in Combination with Ultrasound or Shaker. Food Bioprocess Technol 8, 2409–2417 (2015). https://doi.org/10.1007/s11947-015-1594-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11947-015-1594-9

Keywords

Navigation