Insights into the antibacterial effectiveness of linalool against Shigella flexneri on pork surface: Changes in bacterial growth and pork quality

Pork is internationally recognized as one of the most popular meats worldwide, owing to its high nutritional value, including high-quality proteins, essential amino acids, and vitamins. However, the nutrients and inherent characteristics of pork, such as water activity (higher than 0.82) and pH value (5.6–5.7) provide favorable conditions for the growth of various foodborne pathogens throughout pork processing, transportation, storage, sales, and consumption (Zhou et al., 2010). Thus, pork is highly susceptible to microbial contamination. Following microbial contamination, the composition of the pork microbiota changes, leading to the dominance of one or more microorganisms that cause meat spoilage (Aba et al., 2021; Xu et al., 2022). The growth of microorganisms will result in the depletion of low molecular components in pork, thereby altering the physicochemical and sensory characteristics of the meat (Demaitre et al., 2023). A case in point is that microorganisms form bacterial biofilms on the surface of meat, resulting in the development of a sticky coating. Pathogenic bacteria-contaminated pork not only results in significant economic losses but also poses threats to human health (Zeng et al., 2019). Nevertheless, most studies tend to concentrate on spoilage bacteria rather than investigating pathogenic bacteria that contaminate pork.

Shigella, a major pathogen, has been found throughout all aspects of pork processing (Hao et al., 2022; Haque et al., 2022). Furthermore, it can spread through contaminated food and water, particularly affecting meat and aquatic products (Rahimi et al., 2017). Human are suitable hosts for S. flexneri, which can directly damage the intestinal mucosa (Ahmed and Shimamoto, 2015; Jennison and Verma, 2004). It was estimated that 164.7 million annually were infected with shigellosis caused by Shigella spp. worldwide, of which 163.2 million were in developing countries (Cui et al., 2015). Given the food spoilage and food poisoning caused by S. flexneri, it is imperative to find effective measures for its control. Researchers have invested considerable effort in finding methods to reduce or eliminate pathogens in contaminated foods (Li et al., 2022; Zhang et al., 2016; Zhou et al., 2010). Currently, the decontamination technologies employed in the food industry primarily focus on reducing microbial contamination (Zhou et al., 2010).

Combatting S. flexneri is challenging due to its high acid/salt tolerance, resistance to chemical antimicrobial agents, and capacity to form biofilms (Koo et al., 2017). In recent years, natural compounds have gained significant attention due to their safe origin and their ability to exhibit multi-target antibacterial properties (Hao et al., 2023; Zhou et al., 2010). Linalool (C10H18O, 3,7-dimethyl-1,6-octadiene-3-ol), a perfume permitted in food additive standards, has been detected in more than 200 plant essential oils (Raguso, 2016). Studies have demonstrated that linalool, identified as the primary antioxidant component in coriander essential oil, exhibits potent effects in scavenging free radicals and preventing lipid peroxidation (Duarte et al., 2016). Furthermore, linalool exhibits numerous biological activities such as anti-inflammatory, anti-cancer, anti-proliferation effects (An et al., 2021). Notably, linalool is considered a potential antibacterial additive due to its significant antibacterial activities against Pseudomonas aeruginosa, Escherichia coli, Staphylococcus aureus, and other microorganisms (An et al., 2021). Cury Souza et al. (2016) reported its efficacy in treating Candida albicans strains resistant to conventional antifungal drugs (Cury Souza et al., 2016).

While linalool exerts significant antibacterial activity, there is limited study on its antibacterial mechanism against S. flexneri and its application on contaminated pork. In this study, we investigated the antibacterial mechanisms of linalool using growth curve analysis, along with examining its impact on the cell membrane and DNA of S. flexneri. Also, we demonstrated linalool's ability to inhibit the formation of S. flexneri biofilm and eliminate mature biofilms. Then, linalool was applied to contaminated pork to investigate the antibacterial efficacy by analyzing various physicochemical properties such as weight loss percentage, pH value, color index, TVB-N value. Proteomics analysis was employed to explore the impact of linalool on the quality of contaminated pork and to provide evidence of its antibacterial effectiveness. This study aims to provide novel insights into preventing and controlling food contamination of S. flexneri.

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