Effect of acid adaptation on the resistance of Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium to X-ray irradiation in apple juice

Highlights

• We investigated the effect of acid adaptation on the resistance of foodborne pathogens to X-ray irradiation.

• The acid-adapted Escherichia coli O157:H7 cells acquired cross-protection against X-ray irradiation in apple juice.

• Acid adaptation did not affect the resistance of Salmonella Typhimurium cells to X-ray irradiation in apple juice.

• Irradiation with 1 kGy X-ray did not adversely affect the quality attributes of apple juice.

Abstract

This study aimed to investigate the effect of acid adaptation on the resistance of Escherichia coli O157:H7 and Salmonella Typhimurium to X-ray irradiation. The non-acid-adapted and acid-adapted E. coli O157:H7 cell counts decreased 8.02 and 5.48 log CFU/mL in apple juice, respectively, whereas the S. Typhimurium cell counts reduced by 3.87 and 3.98 log CFU/mL, respectively, after treatment with 1.0 kGy X-ray. In apple juice, the D_5d (dose required for 5-log reduction in cell count) values for non-acid-adapted and acid-adapted E. coli O157:H7 cells were 0.66 and 0.92 kGy, respectively, whereas those for non-acid-adapted and acid-adapted S. Typhimurium cells were 1.40 and 1.30 kGy, respectively. The acid-adapted E. coli O157:H7 cells exhibited higher X-ray resistance than the non-acid-adapted cells in apple juice. However, the acid-adapted and non-acid-adapted S. Typhimurium cells exhibited similar resistance to X-ray irradiation in apple juice. Additionally, the effect of X-ray irradiation on apple juice quality attributes was evaluated. The color, pH, and total phenolic contents of apple juice were not significantly affected (P > 0.05) at all treatment doses of X-ray. The results of this study suggest that the inactivation of acid-adapted cells of E. coli O157:H7, which is the predominant pathogen implicated in apple juice-related disease outbreaks, must be considered for the application of X-ray irradiation in apple juice sterilization process.

Introduction

Globally, apple juice is a popular beverage that is considered as wholesome and nutritious food as it contains health-promoting compounds (Jeon & Ha, 2020). However, the consumption of apple juice is reported to be associated with several foodborne disease outbreaks, which are caused by pathogenic microorganisms, such as Escherichia coli O157:H7 and Salmonella spp. (Danyluk, Goodrich-Schneider, Schneider, Harris, & Worobo, 2012). In the United States of America (USA), ten outbreaks associated with apple juice were reported by the Centers for Disease Control and Prevention (CDC) between 1995 and 2005 (Vojdani, Beuchat, & Tauxe, 2008). In fall 1996, multiple outbreaks of E. coli O157:H7 infection associated with contaminated apple cider result in 70 confirmed cases of serious illnesses, 14 cases of hemolytic uremic syndrome (HUS), and 1 died (Cody et al., 1999). Improper manufacturing practices, such as using soiled or animal manure-contaminated apple and improper washing of apples before processing contribute to the contamination of apple juice by foodborne pathogens (Friedman, Henika, & Mandrell, 2004). The US Food and Drug Administration (USFDA) established juice hazard analysis and critical control point (HACCP) regulations (21 CFR 120) to tackle the increasing apple juice-associated disease outbreaks. According to these regulations, the apple juice must be processed to obtain a 5-log reduction in the cell counts of pertinent pathogens (USFDA, 2001).

Conventionally, the shelf life of juice products is improved by thermal sterilization, which inactivates pathogenic microorganisms (Park & Ha, 2019a). However, thermal sterilization can affect the nutrient content and quality parameters of juice products, such as color and taste, which affects the consumer acceptance (Buchner, Krumbein, Rohn, & Kroh, 2006; Rattanathanalerk, Chiewchan, & Srichumpoung, 2005). Therefore, there is a need to develop an alternative pasteurization technology that can efficiently inactivate foodborne pathogens, including E. coli O157:H7 and Salmonella spp., in the fruit juices without negatively affecting the nutrient content and sensory properties. Non-thermal technologies, such as ultraviolet (UV) light and high hydrostatic pressure processing (HPP) have been used as pasteurization processing technologies for fruit juice to reduce the cell counts of foodborne pathogens. However, UV light, which has low transmittance, is mainly used by small number of producers (Ugarte-Romero, Feng, Martin, Cadwallader, & Robinson, 2006). HPP can inactivate microorganisms without altering quality attributes of fruit juices (Błaszczak, Amarowicz, & Górecki, 2017). However, HPP technology is not cost-effective for industrial applications. Additionally, HPP is ineffective to treat large volumes as it is applied as a batch treatment (Tahiri, Makhlouf, Paquin, & Fliss, 2006).

Ionizing irradiation is one of the effective non-thermal pasteurization technologies. A Joint Expert Committee on Food Irradiation (JECFI) established by the Food and Agriculture Organization, International Atomic Energy Agency, and the World Health Organization (FAO/IAEA/WHO) reported that ionizing radiation at doses up to 10 kGy improves the microbial safety of food without increasing the toxicity or decreasing the nutritional content of food (Fan & Sokorai, 2008). X-ray is a form of electromagnetic radiation that is generated when the high-velocity electrons collide with a metallic target. X-ray is reported to be a promising alternative to electron-beams (E-beams) or gamma-ray (Park & Ha, 2019b).

The X-ray irradiation have the specific advantages of absence of deleterious radioactive sources, such as Cobalt-60 and Cesium-137 associated with gamma-ray irradiation and higher penetration power than E-beam irradiation (Park & Ha, 2019a; Song et al., 2016). Hence, several studies have demonstrated that X-ray irradiation inactivates foodborne pathogens with high efficiency in various food products (Cho & Ha, 2019; Jung et al., 2015; Park & Ha, 2019b; Song et al., 2016; Zhang, Ha, Seck, & Zhou, 2020).

Bacteria are exposed to various stresses at all levels of food processing. A major stress for the microorganisms during fruit juice manufacturing is low pH, which may induce acid resistance and increase the survival of pathogens that may subsequently contaminate fruit juices (Patil, Bourke, Kelly, Frias, & Cullen, 2009). Several studies have reported that E. coli O157:H7 and S. Typhimurium, which are adapted to acidic conditions, exhibit prolonged survival in acidic foods (Foster, 1991; Miller & Kaspar, 1994; Oyarzabal, Nogueira, & Gombas, 2003). Furthermore, several studies have reported that the acid adaptation response increases the resistance of pathogenic microorganisms in fruit juices to other food sterilization processes, such as heat, ultrasound, or far-UVC treatments (Kang & Kang, 2019; Mazzotta, 2001; Patil et al., 2009). Therefore, the sterilization technology for juice products should focus on the inactivation of acid-adapted pathogenic bacteria, which exhibit high resistance to the acidic environment of juices. To the best of our knowledge, there are no published studies that have evaluated the inactivation of acid-adapted pathogenic bacteria in apple juice by X-ray irradiation.

This study aimed to investigate the inactivation effectiveness of X-ray radiation against non-acid-adapted and acid-adapted foodborne pathogens, including E. coli O157:H7 and S. Typhimurium, in apple juice and to evaluate the effect of X-ray irradiation on the quality parameters of apple juice. Additionally, predictive model equations were derived to identify the resistance of each pathogen to X-ray irradiation in the apple juice.