Skip to main content
Log in

Effect of Ultrasound Combined with Ozone Water Pretreatment on the Bacterial Communities and the Physicochemical Properties of Red Swamp Crayfish Meat (Procambarus clarkii)

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

Abstract

The objective of this research was to investigate the impact of ultrasound cleaning (U) combined with ozone water cleaning (O3) on the bacterial communities and physicochemical properties of red swamp crayfish. After single-factor experiments, 600 W and 45 min for U and 13.28 mg/L and 20 min for O3 were selected as optimal parameters. The combination of ultrasound followed by ozone water cleaning (U/O3) showed the better total viable count (TVC) reduction effect in crayfish than ozone water cleaning followed by ultrasound cleaning (O3/U) and simultaneous ozone water and ultrasound cleaning (U+O3). As expected, U/O3 significantly reduced the relative abundance of Pseudoalteromonadaceae, Fusobacteriaceae, and Plesiomonas_shigelloides, and increased the cleanness of crayfish. Compared with the control (samples cleaned with water), the samples subjected to U/O3 treatment led to the myofibril separations of tail meat and an increase (P < 0.05) in the pH, myofibril fragments index (MFI), and thiobarbituric acid–reactive substance (TBARS) content. However, no significant influence (P > 0.05) was found on the physical and sensory qualities, including the expressible moisture, cooking loss, springiness, overall appearance, odor, taste, and integrity of tail meat. Therefore, U/O3 could be a potential cleaning method for crayfish in the food industry.

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

Similar content being viewed by others

References

  • Alarcon-Rojo, A. D., Janacua, H., Rodriguez, J. C., Paniwnyk, L., & Mason, T. J. (2015). Power ultrasound in meat processing. Meat Sci., 107, 86–93.

    Article  PubMed  CAS  Google Scholar 

  • Anastácio, P. M., Frias, A. F., & Marques, J. C. (1999). CRISP (crayfish and rice integrated system of production) 1. Modelling rice (Oryza sativa) growth and production. Ecological Modelling., 123(1), 17–28.

    Article  Google Scholar 

  • Aponte, M., Anastasio, A., Marrone, R., Mercogliano, R., Peruzy, M. F., & Murru, N. (2018). Impact of gaseous ozone coupled to passive refrigeration system to maximize shelf-life and quality of four different fresh fish products. Lwt., 93, 412–419.

    Article  CAS  Google Scholar 

  • Bader, H., & Hoigné, J. (1981). Deternination of ozone in water by the indigo method. Water Research., 15(4), 449–456.

    Article  CAS  Google Scholar 

  • Bahuaud, D., Morkore, T., Langsrud, O., Sinnes, K., Veiseth, E., Ofstad, R., & Thomassen, M. S. (2008). Effects of -1.5 degrees C super-chilling on quality of Atlantic salmon (Salmo salar) pre-rigor fillets: cathepsin activity, muscle histology, texture and liquid leakage. Food Chemistry., 111(2), 329–339.

    Article  PubMed  CAS  Google Scholar 

  • Behera, B. K., Bera, A. K., Paria, P., Das, A., Parida, P. K., Kumari, S., Bhowmick, S., & Das, B. K. (2018). Identification and pathogenicity of Plesiomonas shigelloides in silver carp. Aquaculture., 493, 314–318.

    Article  CAS  Google Scholar 

  • Cassani, L., Tomadoni, B., Ponce, A., Agüero, M. V., & Moreira, M. R. (2017). Combined use of ultrasound and vanillin to improve quality parameters and safety of strawberry juice enriched with prebiotic fibers. Food and Bioprocess Technology., 10(8), 1454–1465.

    Article  CAS  Google Scholar 

  • Chen, X., Chen, Y., Yang, Q., Kong, H., Yu, F., Han, D., Zheng, S., Cui, D., & Li, L. (2013). Plesiomonas shigelloides infection in southeast China. PLoS One., 8(11), e77877.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen, L., Feng, X. C., Zhang, Y. Y., Liu, X. B., Zhang, W. G., Li, C. B., Ullah, N., Xu, X. L., & Zhou, G. H. (2015). Effects of ultrasonic processing on caspase-3, calpain expression and myofibrillar structure of chicken during post-mortem ageing. Food Chem., 177, 280–287.

    Article  PubMed  CAS  Google Scholar 

  • Chitravathi, K., Chauhan, O. P., Raju, P. S., & Madhukar, N. (2015). Efficacy of aqueous ozone and chlorine in combination with passive modified atmosphere packaging on the postharvest shelf-life extension of green chillies (Capsicum annuum L.). Food and Bioprocess Technology., 8(6), 1386–1392.

    Article  CAS  Google Scholar 

  • Contigiani, E. V., Jaramillo-Sánchez, G., Castro, M. A., Gómez, P. L., & Alzamora, S. M. (2018). Postharvest quality of strawberry fruit (Fragaria x Ananassa Duch cv. Albion) as affected by ozone washing: fungal spoilage, mechanical properties, and structure. Food and Bioprocess Technology., 11(9), 1639–1650.

    Article  CAS  Google Scholar 

  • Crapo, C., Himelbloom, B., Vitt, S., & Pedersen, L. (2004). Ozone efficacy as a bactericide in seafood processing. Journal of Aquatic Food Product Technology., 13(1), 111–123.

    Article  CAS  Google Scholar 

  • Crowe, K. M., Skonberg, D., Bushway, A., & Baxter, S. (2012). Application of ozone sprays as a strategy to improve the microbial safety and quality of salmon fillets. Food Control., 25(2), 464–468.

    Article  CAS  Google Scholar 

  • Culler, R. D., Parrishjr, F. C., Smith, G. C., & Cross, H. R. (1978). Relationship of myofibril fragmentation index to certain chemical, physical and sensory characteristics of bovine longissimus muscle. J Food Sci., 43(4), 1177–1180.

    Article  CAS  Google Scholar 

  • Edgar, R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods., 10(10), 996–998.

    Article  PubMed  CAS  Google Scholar 

  • Fadrosh, D. W., Ma, B., Gajer, P., Sengamalay, N., Ott, S., Brotman, R. M., & Ravel, J. (2014). An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome, 2(6). https://doi.org/10.1186/2049-2618-2042-2046.

  • Fan, K., Zhang, M., & Jiang, F. (2019). Ultrasound treatment to modified atmospheric packaged fresh-cut cucumber: influence on microbial inhibition and storage quality. Ultrason Sonochem., 54, 162–170.

    Article  PubMed  CAS  Google Scholar 

  • Farouk, M. M., Wieliczko, K. J., & Merts, I. (2003). Ultra-fast freezing and low storage temperatures are not necessary to maintain the functional properties of manufacturing beef. Meat Sci., 66(1), 171–179.

    Article  Google Scholar 

  • Feng, L., Jiang, T., Wang, Y., & Li, J. (2012). Effects of tea polyphenol coating combined with ozone water washing on the storage quality of black sea bream (Sparus macrocephalus). Food Chem., 135(4), 2915–2921.

    Article  PubMed  CAS  Google Scholar 

  • Foster, G., Ross, H. M., Naylor, R. D., Collins, M. D., Ramos, C. P., Garayzabal, F. F., & Reid, R. J. (1995). Cetobacterium ceti gen. nov., sp. nov., a new Gram-negative obligate anaerobe from sea mammals. Letters in Applied Microbiology., 21(3), 202–206.

    Article  PubMed  CAS  Google Scholar 

  • Fuyan, Z. (1987). Discussion on determination method of thiobarbituric acid value in salted fish products. Chinese Journal of Public Health., 6(4), 247–249.

    Google Scholar 

  • Gao, S., Lewis, G. D., Ashokkumar, M., & Hemar, Y. (2014). Inactivation of microorganisms by low-frequency high-power ultrasound. Ultrason Sonochem., 21(1), 446–453.

    Article  PubMed  CAS  Google Scholar 

  • Gómez-López, V. M., Gil, M. I., Allende, A., Blancke, J., Schouteten, L., & Selma, M. V. (2014). Disinfection capacity of high-power ultrasound against E. coli O157:H7 in process water of the fresh-cut industry. Food and Bioprocess Technology., 7(12), 3390–3397.

    Article  Google Scholar 

  • Gonçalves, A. A., & Lira Santos, T. C. (2019). Improving quality and shelf-life of whole chilled Pacific white shrimp (Litopenaeus vannamei) by ozone technology combined with modified atmosphere packaging. Lwt., 99, 568–575.

    Article  CAS  Google Scholar 

  • Gornall, A. G., Bardawill, C. J., & David, M. M. (1949). Determination of serum proteins by means of the biuret reaction. Journal of Biological Chemistry., 177(2), 751–766.

    PubMed  CAS  Google Scholar 

  • Herrera, F. C., Santos, J. A., Otero, A., & Garcia-Lopez, M. L. (2006). Occurrence of Plesiomonas shigelloides in displayed portions of saltwater fish determined by a PCR assay based on the hugA gene. Int J Food Microbiol., 108(2), 233–238.

    Article  PubMed  CAS  Google Scholar 

  • Higuera-Barraza, O. A., Torres-Arreola, W., Ezquerra-Brauer, J. M., Cinco-Moroyoqui, F. J., Rodriguez Figueroa, J. C., & Marquez-Rios, E. (2017). Effect of pulsed ultrasound on the physicochemical characteristics and emulsifying properties of squid (Dosidicus gigas) mantle proteins. Ultrason Sonochem., 38, 829–834.

    Article  PubMed  CAS  Google Scholar 

  • Honikel, K. O. (1998). Reference methods for the assessment of physical characteristic of meat. Meat Science 61 (2002) 257–265, 49(4), 447–457.

    Article  PubMed  CAS  Google Scholar 

  • Hou, D., Huang, Z., Zeng, S., Liu, J., Weng, S., & He, J. (2018). Comparative analysis of the bacterial community compositions of the shrimp intestine, surrounding water and sediment. J Appl Microbiol., 125(3), 792–799.

    Article  PubMed  CAS  Google Scholar 

  • Huang, G., Chen, S., Dai, C., Sun, L., Sun, W., Tang, Y., Xiong, F., He, R., & Ma, H. (2017). Effects of ultrasound on microbial growth and enzyme activity. Ultrasonics Sonochemistry., 37, 144–149.

    Article  PubMed  CAS  Google Scholar 

  • Jambrak, A. R., Vukušić, T., Stulić, V., Mrvčić, J., Milošević, S., Šimunek, M., & Herceg, Z. (2014). The effect of high power ultrasound and cold gas-phase plasma treatments on selected yeast in pure culture. Food and Bioprocess Technology., 8(4), 791–800.

    Article  Google Scholar 

  • Jayasooriya, S. D., Torley, P. J., D'Arcy, B. R., & Bhandari, B. R. (2007). Effect of high power ultrasound and ageing on the physical properties of bovine semitendinosus and longissimus muscles. Meat Sci., 75(4), 628–639.

    Article  PubMed  CAS  Google Scholar 

  • Jiang, W., Hu, Y., He, Y., You, J., Xiong, S., Liu, Y., & Yin, T. (2016). Effect of mild ozone oxidation on structural changes of silver carp (Hypophthalmichthys molitrix) myosin. Food and Bioprocess Technology., 10(2), 1–9.

    CAS  Google Scholar 

  • Kang, D. C., Gao, X. Q., Ge, Q. F., Zhou, G. H., & Zhang, W. G. (2017). Effects of ultrasound on the beef structure and water distribution during curing through protein degradation and modification. Ultrason Sonochem., 38, 317–325.

    Article  PubMed  CAS  Google Scholar 

  • Li, Q., Zhang, L., & Luo, Y. (2018). Changes in microbial communities and quality attributes of white muscle and dark muscle from common carp (Cyprinus carpio) during chilled and freeze-chilled storage. Food Microbiol., 73, 237–244.

    Article  PubMed  Google Scholar 

  • Luján-Facundo, M. J., Mendoza-Roca, J. A., Cuartas-Uribe, B., & Álvarez-Blanco, S. (2013). Ultrasonic cleaning of ultrafiltration membranes fouled with BSA solution. Separation and Purification Technology., 120, 275–281.

    Article  CAS  Google Scholar 

  • Magoc, T., & Salzberg, S. L. (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics., 27(21), 2957–2963.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mazue, G., Viennet, R., Hihn, J. Y., Carpentier, L., Devidal, P., & Albaina, I. (2011). Large-scale ultrasonic cleaning system: design of a multi-transducer device for boat cleaning (20kHz). Ultrason Sonochem., 18(4), 895–900.

    Article  PubMed  CAS  Google Scholar 

  • MOH. (2010). GB 4789.2-2010 Food microbiological examination: aerobic plate count. In. p^pp 1-5. SAC, Beijing, China.

  • Muthukumaran, S., Yang, K., Seuren, A., Kentish, S., Ashokkumar, M., Stevens, G. W., & Grieser, F. (2004). The use of ultrasonic cleaning for ultrafiltration membranes in the dairy industry. Separation and Purification Technology., 39(1-2), 99–107.

    Article  CAS  Google Scholar 

  • NHFPC (2016) GB/T 5009.228-2016 Determination of volatile basic nitrogen in food. In. p^pp 1-8. SAC, Beijing, China.

  • Nicolau-Lapeña, I., Lafarga, T., Viñas, I., Abadias, M., Bobo, G., & Aguiló-Aguayo, I. (2019). Ultrasound processing alone or in combination with other chemical or physical treatments as a safety and quality preservation strategy of fresh and processed fruits and vegetables: a review. Food and Bioprocess Technology., 12(9), 1452–1471.

    Article  CAS  Google Scholar 

  • Pastoriza, L., Bernárdez, M., Sampedro, G., Cabo, M. L., & Herrera, J. J. R. (2008). Use of sterile and ozonized water as a strategy to stabilize the quality of stored refrigerated fresh fish. Food Control., 19(8), 772–780.

    Article  CAS  Google Scholar 

  • Pedrós-Garrido, S., Condón-Abanto, S., Beltrán, J. A., Lyng, J. G., Brunton, N. P., Bolton, D., & Whyte, P. (2017). Assessment of high intensity ultrasound for surface decontamination of salmon (S. salar), mackerel (S. scombrus), cod (G. morhua) and hake (M. merluccius) fillets, and its impact on fish quality. Innovative Food Science & Emerging Technologies., 41, 64–70.

    Article  Google Scholar 

  • Petrier, C., Jeunet, A., Luche, J. L., & Reverdy, G. (1992). Unexpected frequency effects on the rate of oxidative processes induced by ultrasound. Journal of the American Chemical Society, 114(8), 3148–3150.

    Article  CAS  Google Scholar 

  • Rong, C., Qi, L., Ling, Z., & Huihui, M. (2016). Microbial flora analysis of oyster during refrigerated storage by high throughput sequencing technology. Transactions of the Chinese Society of Agricultural Engineering., 32(20), 275–280.

    Google Scholar 

  • Ronholm, J., Lau, F., & Banerjee, S. K. (2016). Emerging seafood preservation techniques to extend freshness and minimize Vibrio contamination. Front Microbiol., 7, 350.

    Article  PubMed  PubMed Central  Google Scholar 

  • Si, G., Yuan, J., Xu, X., Zhao, S., Peng, C., Wu, J., & Zhou, Z. (2018). Effects of an integrated rice-crayfish farming system on soil organic carbon, enzyme activity, and microbial diversity in waterlogged paddy soil. Acta Ecologica Sinica., 38(1), 29–35.

    Article  Google Scholar 

  • Siró, I., Vén, C., Balla, C., Jónás, G., Zeke, I., & Friedrich, L. (2009). Application of an ultrasonic assisted curing technique for improving the diffusion of sodium chloride in porcine meat. Journal of Food Engineering., 91(2), 353–362.

    Article  CAS  Google Scholar 

  • Society CF (2018) China crayfish industry development report. Ministry of Agriculture and Rural Affairs of the People’s Republic of China. Available at http://www.moa.gov.cn/xw/bmdt/201806/t20180612_6151805.htm.

  • VargasAlbores, F., PorchasCornejo, M. A., MartínezPorchas, M., VillalpandoCanchola, E., GollasGalván, T., & MartínezCórdova, L. R. (2017). Bacterial biota of shrimp intestine is significantly modified by the use of a probiotic mixture: a high throughput sequencing approach. Helgoland Marine Research., 71(1), 2–10.

    Article  Google Scholar 

  • Wallhäußer, E., Sayed, A., Nöbel, S., Hussein, M. A., Hinrichs, J., & Becker, T. (2013). Determination of cleaning end of dairy protein fouling using an online system combining ultrasonic and classification methods. Food and Bioprocess Technology., 7(2), 506–515.

    Article  CAS  Google Scholar 

  • Wang, X. (2014). Study on the preservation effect of acidic electolyzed water for Solenocera carssicornis College of Food Science and Biotechnology. Zhejiang Gongshang University.

  • Wang, J. Y., Yang, Y. L., Tang, X. Z., Ni, W. X., & Zhou, L. (2017). Effects of pulsed ultrasound on rheological and structural properties of chicken myofibrillar protein. Ultrason Sonochem., 38, 225–233.

    Article  PubMed  CAS  Google Scholar 

  • Wu, J., & Doan, H. (2005). Disinfection of recycled red-meat-processing wastewater by ozone. Journal of Chemical Technology & Biotechnology., 80(7), 828–833.

    Article  CAS  Google Scholar 

  • Xiaolin, M., Wenjun, L., & Guoxing, N. (2019). Effect of different factors on the fish intestinal microbiota. JOURNAL OF FISHERIES OF CHINA., 43(143-155).

  • Xiong, Z., Sun, D. W., Pu, H., Xie, A., Han, Z., & Luo, M. (2015). Non-destructive prediction of thiobarbituricacid reactive substances (TBARS) value for freshness evaluation of chicken meat using hyperspectral imaging. Food Chem., 179, 175–181.

    Article  PubMed  CAS  Google Scholar 

  • Yang, Z., Zhou, H., Gao, L., Rao, S., Yin, Y., & Fang, W. (2015). Effect of synergistic purification with ultrasonic and running water on bacterial load and microflora in crawfish (Procambarus clarkii). Food Science.

  • Ye, Z., Xie, W., Ruan, O., Ruan, J., Gong, X., & Zhao, C. (2018). Observation on the effect of medical ozone gas bath on the culture of normal humanepidermal cells in vitro. Chin Jinjuryrepairand Wound Heaiing., 13(4), 283–288.

    Google Scholar 

  • Zhang, M., Haili, N., Chen, Q., Xia, X., & Kong, B. (2018). Influence of ultrasound-assisted immersion freezing on the freezing rate and quality of porcine longissimus muscles. Meat Sci., 136, 1–8.

    Article  PubMed  CAS  Google Scholar 

  • Zotta, T., Parente, E., Ianniello, R. G., De Filippis, F., & Ricciardi, A. (2019). Dynamics of bacterial communities and interaction networks in thawed fish fillets during chilled storage in air. International Journal of Food Microbiology., 293, 102–113.

    Article  PubMed  CAS  Google Scholar 

Download references

Funding

The research was funded by the National Key R&D Program of China (2018YFD0901001), Major Program of Technical Innovation of Hubei Province (2019ABA087), and Ningbo Public Welfare Major Program (2015C110002). The high-throughput sequencing was supported by Beijing igeneCode Biotech Co., Ltd.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guangquan Xiong.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Appendix

Appendix

Fig. 5
figure 5

The appearance of raw (a) and cooked (b) crayfish subjected to different cleaning

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, L., Shi, L., Jiao, C. et al. Effect of Ultrasound Combined with Ozone Water Pretreatment on the Bacterial Communities and the Physicochemical Properties of Red Swamp Crayfish Meat (Procambarus clarkii). Food Bioprocess Technol 13, 1778–1790 (2020). https://doi.org/10.1007/s11947-020-02518-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11947-020-02518-6

Keywords

Navigation