Inactivation of Emerging Opportunistic Foodborne Pathogens Cronobacter spp. and Arcobacter spp. on Fresh Fruit and Vegetable Products: Effects of Emerging Chemical and Physical Methods in Model and Real Food Systems—A Review
Abstract
1. Introduction
2. Incidence of Arcobacter spp. and Cronobacter spp. in Fruit and Vegetable Products
3. Emerging Strategies Tested for Decontamination of Arcobacter spp. and Cronobacter spp. in Fruit and Vegetable Products
3.1. Emerging Chemical Methods
3.1.1. Organic Acid and Chlorine
3.1.2. Extracts
Microorganism | Extract and Essential Oil | Matrix | Condition | Microbial Reduction | Potential Research Limitation | Reference |
---|---|---|---|---|---|---|
Arcobacter spp. | Extract virgin olive oils | In vitro test | Non-buffered (WEOO) and buffered (BEOO) extract virgin olive oils. | Reduction of 5 Log CFU/mL. | The effect of extract virgin olive oils on biofilm eradication has not been evaluated. | [26] |
Arcobacter spp. | Orange oil fractions | In vitro test | Seven commercial orange oil fractions. | No inhibition of Arcobacter spp. was detected by 6 out of 7 orange fractions except CP terpeneless Valencia orange oil, which produced inhibition zones varying from 9.5 ± 0.7 to 29 ± 1.4 mm. | Composition of the tested orange-based fractions was not determined. | [28] |
Cronobacter sakazakii | Blueberry proanthocyanidin (PAC) and commercial blueberry juice (BJ) | In vitro test | Blueberry PAC at 5 mg/mL, BJ (pH 2.8), neutralised BJ (pH 7), malic acid (pH 3.0), or PBS and incubated at 37 °C for 30 min, 1 h, 3 h, or 6 h. | Reductions of ~1 and 1.50 Log CFU/mL with BJ or blueberry PAC. Reduction of 8.25 ± 0.12 Log CFU/mL and 8.48 ± 0.03 Log CFU/mL, respectively, with BJ (pH 2.8) or blueberry PAC after 1 h, while malic acid (pH 3.0) showed 1.3 Log CFU/mL reduction for both strains. | Composition of blueberry polyphenolic fractions in commercial blueberry juice and blueberry proanthocyanidin (PAC) fraction has not been characterised. | [33] |
Cronobacter sakazakii | Chrysanthemum bud crude extract (CBCE) | In vitro test | Different concentrations of CBCE (0, 0.3125, 0.625, 1.25, 2.5, 5, 10, and 20 mg/mL). | Diameter of inhibition zone (DIZ), minimum inhibitory concentration (MIC), and minimum bactericide concentration (MBC) of CBCE against C. sakazakii were 14.55 ± 0.44–14.84 ± 0.38 mm, 10 mg/mL, and 20 mg/mL, respectively. | The composition (principal bioactive compounds) of the chrysanthemum bud crude extract (CBCE) has not been determined. | [39] |
Cronobacter spp. | Bacterial cellulose (BC) impregnated with plant extract and essential oil | In vitro test | Bacterial cellulose combined with extracts (Tulsi, Brahmi, lemon, blackberry, nettle root, and nettle leaf) and essential oils (cinnamon, sage, clove, mint, thyme, lemongrass, rosemary, lemon, anise, tea tree, lime, grapefruit, and tangerine) in agar diffusion methods. | The cellulose matrix with a 50% extract from Brahmi was found to effectively inhibit the growth of the selected Cronobacter strains. | Composition of the extract and essential oil fraction was not determined. | [63] |
Cronobacter spp. | Biocellulose impregnated with oregano essential oil | In vitro test | Biocellulose impregned with oregano essential oil (100%) in agar diffusion methods. | Bacterial cellulose impregnated with oregano essential oil had strong and moderate antimicrobial activity against all presented strains of the genus Cronobacter. | Composition of the extract and essential oil fraction was not determined. | [64] |
Cronobacter spp. | Thyme, cinnamon, clove, peppermint, marjoram, cumin, rosemary, fennel, basil, lime, bergamot orange, orange, lemon, grapefruit, mandarin, cardamom, anise, and ginger | In vitro test | Disc-diffusion method was used to screen the EOs. | Most effective EOs: thyme > cinnamon > marjoram. The clove, cumin, and fennel oils had moderately inhibiting effects on only some of the tested strains. | The effect of the essential oils on biofilm eradication was not evaluated. | [65] |
3.1.3. Essential Oils
3.2. Emerging Physical Methods
3.2.1. Combination of UV-C with Electrolysed Water
3.2.2. Ultrasound
3.2.3. Methods Not Explored: Cold Plasma as an Emerging Technology for Decontamination of Fruit and Vegetable Products
4. Conclusions and Future Perspective
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Food Matrix | Genus | Occurrence | Reference |
---|---|---|---|
Lettuce | Arcobacter spp. | - | [4] |
Alfalfa broccoli | Cronobacter sakazakii | 21/60 | [38] |
Small radish | Cronobacter muytjensii | ||
Lentil | Cronobacter turicensis | ||
Sunflower | Cronobacter malonaticus | ||
Leek and sprout mix | Cronobacter condiment | ||
Rucola | Cronobacter sakazakii | ||
Lamb’s lettuce | Cronobacter muytjensii | ||
Endive escarole | Cronobacter turicensis | ||
Leaf vegetables mix | Cronobacter malonaticus | ||
Lettuce | Arcobacter butzleri | 16/110 | [41] |
Rocket | Arcobacter butzleri | ||
Arcobacter cryaerophilus | |||
Carrot | Arcobacter skirrowii | ||
Arcobacter butzleri | |||
Beet root | Arcobacter skirrowii | 28/204 | [42] |
Arcobacter butzleri | |||
Cabbage | Arcobacter butzleri | ||
Lettuce | Arcobacter spp. | 21/90 | [44] |
Spinach | |||
Arugula | |||
Lettuce | Arcobacter butzleri | 44/160 | [46] |
Spinach | Arcobacter cryaerophilus | ||
Rocket | Arcobacter butzleri | ||
Valerian | Arcobacter butzleri | ||
Apple | Arcobacter spp. | 10/50 | [47] |
Lettuce | Cronobacter spp. | 122/403 | [49] |
Coriander | |||
Tomato | |||
Cucumber | |||
Vegetables | Cronobacter turicensis, | 71/602 | [51] |
Cronobacter muytjensii | |||
Vegetable | Cronobacter sakazaki | - | [52] |
Spinach | Arcobacter butzleri | 119/175 | [54] |
Lettuce | Arcobacter cryaerophilus | ||
Rocket | Arcobacter butzleri | ||
Valerian | Arcobacter butzleri |
Microorganism | Organic Acid and Chlorine | Matrix | Condition | Microbial Reduction | Potential Research Limitation | Reference |
---|---|---|---|---|---|---|
C. sakazakii | Chlorine, chlorine dioxide, and a peroxyacetic acid-based sanitiser | Surface of apples, cantaloupes, strawberries, lettuce, and tomatoes | Chlorine dioxide, and a peroxyacetic acid-based sanitiser (Tsunami 200) treatments (1 and 5 min). | Chlorine and chlorine dioxide 3.38 and 3.77 Log10 CFU/apple. Tsunami 200: 4 Log10 CFU/apple. Reductions of > or = 3.70 Log CFU/tomato with 10 ugml chlorine or chlorine dioxide or 40 microg/mL Tsunami 200 for 5 min. Treatment of lettuce with Tsunami 200 (40 and 80 microg/mL) reduction of 5.31 Log10 CFU/sample. | Only two treatment times (1 and 5 min) were evaluated. | [25] |
Arcobacter butzleri and Arcobacter cryaerophilus | Propionic acid, lactic acid, malic acid, ascorbic acid, formic acid, and tartaric acid. | In vitro test | Propionic, lactic, malic, and ascorbic acids (pH 5.5–5.0), formic, citric, and tartaric acids in the pH range of 6.0–5.5 | Arcobacter butzleri grows at pH 5.5. No viable cells were detected in BHI broth acidified to pH 5.0. with ascorbic, malic, lactic, or propionic acid; no growth observed at pH < 5.5. Arcobacter cryaerophilus: more susceptible to the decrease in pH values, regardless of the acidulant used. | The effect of the pH of brain heart infusion (BHI) broth as a positive control. | [26] |
C. sakazakii | Para-hydroxybenzoate (BPB) Malic acid | Apple Juice | pH values of 3.2 to 9.0, supplemented with selected concentrations of BPB ≤ 125 ppm and thermally treated (58 °C). | 6-Log10 reduction at 600 s, 125 ppm of BPB resulted in a 6-Log10 reduction in 30 s. | The effect on food quality has not been evaluated. | [31] |
C. sakazakii | Acetic acid Propionic acid Malic acid | In vitro test | Acidic acetic acid, propionic acid, malic acid, and heat stress (55 °C). | The order of resistance of the acid-shocked C. sakazakii to the organic acids was acetic acid > propionic acid > malic acid. | The effect of pH has not been evaluated. | [32] |
Microorganism | Emerging Physical | Matrix | Condition | Microbial Reduction | Potential Research Limitation | Reference |
---|---|---|---|---|---|---|
Cronobacter sakazakii | Combined ultrasound with organic acids | In situ test | Single treatment of ultrasound (frequency of 37 kHz and a power up to 380 W) treated with ultrasound alone for 5, 20, 40, 60, 80, and 100 min) or NaOCl 12% diluted with tap water to a final volume 80 mL and final concentrations of 50, 100, 150, and 200 ppm for 5 min. Combined ultrasound and NaOCl treatment, 24 combination treatments were compared with ultrasound (5, 20, 40,60, 80, and 100 min) and NaOCl (50, 100, 150, and 200 ppm for 5 min). | Despite the significant reduction in C. sakazakii with NaOCl treatment (200 ppm), the combination of 100 min ultrasound and 200 ppm NaOCl resulted in an additional 1.67 log-reduction in C. sakazakii (4.44 Log10 reduction = 2.77 + 1.67 Log10). | The minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) were not determined. | [34] |
Cronobacter sakazakii | Ultraviolet-C (UV-C) radiation, acidic electrolysed (AEW), and neutral electrolysed (NEW) waters | In situ test | The fruits were contaminated by dip inoculation, contaminated mangoes were disinfected using UV-C (2.5, 5, 7.5, and 10 kJ/m2), AEW, NEW, and sodium hypochlorite (SH), and the microorganisms were monitored. | C. sakazakii grew after and UV-C was more effective in reducing C. sakazakii (2.6 Log CFU/g) when compared with AEW, NEW, and SH (1.8 Log CFU/g). | The combined effect of AEW, NEW, and UV-C was not evaluated. | [37] |
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Molina-Hernandez, J.B.; Cellini, B.; Shanbeh Zadeh, F.; Vannini, L.; Rocculi, P.; Tappi, S. Inactivation of Emerging Opportunistic Foodborne Pathogens Cronobacter spp. and Arcobacter spp. on Fresh Fruit and Vegetable Products: Effects of Emerging Chemical and Physical Methods in Model and Real Food Systems—A Review. Foods 2025, 14, 2463. https://doi.org/10.3390/foods14142463
Molina-Hernandez JB, Cellini B, Shanbeh Zadeh F, Vannini L, Rocculi P, Tappi S. Inactivation of Emerging Opportunistic Foodborne Pathogens Cronobacter spp. and Arcobacter spp. on Fresh Fruit and Vegetable Products: Effects of Emerging Chemical and Physical Methods in Model and Real Food Systems—A Review. Foods. 2025; 14(14):2463. https://doi.org/10.3390/foods14142463
Chicago/Turabian StyleMolina-Hernandez, Junior Bernardo, Beatrice Cellini, Fatemeh Shanbeh Zadeh, Lucia Vannini, Pietro Rocculi, and Silvia Tappi. 2025. "Inactivation of Emerging Opportunistic Foodborne Pathogens Cronobacter spp. and Arcobacter spp. on Fresh Fruit and Vegetable Products: Effects of Emerging Chemical and Physical Methods in Model and Real Food Systems—A Review" Foods 14, no. 14: 2463. https://doi.org/10.3390/foods14142463
APA StyleMolina-Hernandez, J. B., Cellini, B., Shanbeh Zadeh, F., Vannini, L., Rocculi, P., & Tappi, S. (2025). Inactivation of Emerging Opportunistic Foodborne Pathogens Cronobacter spp. and Arcobacter spp. on Fresh Fruit and Vegetable Products: Effects of Emerging Chemical and Physical Methods in Model and Real Food Systems—A Review. Foods, 14(14), 2463. https://doi.org/10.3390/foods14142463