Grapefruit essential oil combined with UV-C treatment: A technology to improve the microbial safety of fresh produce

Fresh fruits and vegetables are essential food groups in many regions of the world. The importance of including fresh produce in a healthy diet stem from its abundant reserves of vitamins, minerals, fiber, and antioxidants. However, the food industry faces unique challenges when handling these fruits and vegetables, as variations in morphology and maturity within the diverse range of soft fruits and leafy greens can affect the effectiveness of sanitization methods. As a consequence, the rise in fresh fruit and vegetable intake has caused a greater incidence of foodborne disease, particularly due to the uncooked state of these items (Thomas, Gil, Müller, Rogers, & Berger, 2023). Contamination of fresh produce can occur through contact with human feces in agricultural fields or through unhygienic handling by infected food handlers. In particular, Escherichia coli O157:H7 (E. coli O157:H7) and human norovirus (HuNoV) have emerged as the primary culprits, accounting for approximately 50% of reported outbreaks associated with fresh produce such as berries, lettuce, other leafy greens, and tomatoes (Hernández et al., 2022). E. coli O157:H7, a common bacterial pathogen responsible for hemorrhagic enteritis and hemolytic uremic syndrome, has gained significant attention as a global public health threat due to its association with outbreaks. In April 2018, a widespread foodborne illness outbreak linked to romaine lettuce occurred in the United States, resulting in 240 infections, 104 hospitalizations, and five deaths across 37 states (Bottichio et al., 2020). HuNoV, which accounts for over 90% of non-bacterial epidemic gastroenteritis cases, presents a considerable danger to human health because it can flourish at low infectious doses and its remarkable environmental stability, which facilitates its high transmissibility. In the European Region, the World Health Organization (WHO) estimates that Norovirus is the primary cause of most cases of food poisoning, with approximately 15 million cases reported in 2019 (Guix, Pintó, & Bosch, 2019). However, our understanding of the mechanisms underlying human norovirus disease remains limited due to the lack of robust in vivo models capable of simulating symptomatic infections. A recent study has made progress in this area by developing an in vitro infection model using human B cells to study human noroviruses (Jones et al., 2015). However, due to the complex in vitro cell culture system required for HuNoV, dependence on viral surrogates remains necessary. Two promising candidates for HuNoV surrogates are murine norovirus (MNV) and Tulane virus (TV) due to their ability to grow in cell culture, genetic relatedness, and similar physicochemical properties (Li & Chen, 2015).

Most of the available literature on the decontamination of fresh produce concludes that sanitizing wash processes result in a reduction of approximately 2 to 3 log CFU/g of microbial populations on the produce surface (Mendoza et al., 2022). In addition, regardless of the initial bacterial load, total counts after storage remain similar whether produce is washed with tap water or a sanitizing solution. Consequently, while sanitizers are effective in maintaining water quality and preventing cross-contamination during washing, their effectiveness in preventing microbial growth during product storage is limited or nonexistent due to the lack of residual activity (EFSA Panel on Biological Hazards (BIOHAZ) et al., 2023). This observation has sparked interest in exploring the potential use of essential oils (EOs) and ultraviolet C (UV-C) treatments for processed fruits and vegetables during storage. EOs are often recommended as potential preservatives for food due to their potent and extensive antimicrobial activity against microorganisms (Coimbra, Carvalho, Duarte, & Ferreira, 2022; Kang & Song, 2018). Nevertheless, it should be noted that the levels of EOs necessary to achieve noteworthy antimicrobial effects often surpass the limit that customers deem tolerable (Tsitlakidou, Tasopoulos, Chatzopoulou, & Mourtzinos, 2023). For example, thyme EO at a concentration of 0.9% showed efficacy in reducing Salmonella spp. in ground pork; however, sensory evaluation scores were below the acceptable limit, indicating lower product acceptability (scores <5) (Boskovic et al., 2017). In the case of fresh fish, EOs sourced from grapefruit peel, lime, thyme, garlic, lemon, onion, oregano, rosemary, and lemongrass have proven effective as antimicrobial agents against Listeria spp. (Pedrós-Garrido et al., 2020). Nevertheless, these products encounter sensory acceptance difficulties due to the robust tastes and odors linked with the oils that negatively impact the freshness perception (Rout et al., 2022). On the other hand, UV-C technology offers the possibility to inactivate microorganisms while minimally impacting the sensory and nutritional features of the products, provided that the processing parameters are suitable (Bigi et al., 2023). UV-C refers to short-wave ultraviolet radiation in the range of 200–280 nm. This non-thermal technique can be implemented at room temperature and achieves microbial inactivation by causing cellular harm. As a safe, effective and non-residual sterilization method, UV-C has potential for post-harvest preservation and handling of fruits and vegetables (Cankal, Unluturk, & Unluturk, 2023; Diesler et al., 2019). However, its efficacy against specific microorganisms is restricted and contingent on accurate processing parameters. In certain cases, achieving a satisfactory level of decontamination by UV-C treatment without compromising product quality remains a challenge (Bhatnagar et al., 2022; Xu et al., 2023).

The combination of EOs and UV-C presents a promising alternative approach that may curtail the necessary doses of EOs and lessen the UV-C intensity, leading to an escalated microbial inactivation rate (Iturralde-García et al., 2022). This approach also reduces any undesired impact on food quality. Therefore, the integration of EOs with UV-C treatment shows a potential to expand fresh product shelf life. The use of such combinations to enhance food safety and quality aligns with sustainable development goals aimed at promoting sustainable food consumption. Thus, this study aimed to assess the antimicrobial efficacy of grapefruit essential oils (GEO) and UV-C treatment combined against specific pathogens, specifically E. coli O157:H7 and HuNoV surrogates (MNV-1 and TV) on cherry tomatoes, lettuce, and blueberries. In addition, the variations in pathogen counts on fresh produce during storage, as well as the sensory attributes and overall quality of the produce were evaluated. Furthermore, this study investigated the key components of GEO and their potential antimicrobial mechanisms in combination with UV-C treatment.

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