Recent Advances in the Application of Bacteriophages against Common Foodborne Pathogens
Abstract
:1. Introduction
1.1. Bacteriophages
1.2. Foodborne Pathogens
1.3. Salmonella
1.4. Escherichia coli
1.5. Listeria
1.6. Campylobacter
1.7. Yersinia
2. Perspectives
3. Conclusions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Bacteria | Symptoms | Transmission | Phages | Results | References |
---|---|---|---|---|---|
Campylobacter jejuni | Fever, muscle aches, headaches, arthralgia, abdominal pain and cramps, weakness, bloody diarrhea, gastric or intestinal pain, occurrence of Guillain-Barré syndrome | Poultry meat, milk, contaminated water, swimming in contaminated water bodies, contact with animal. | CJ01 | Mutton and chicken meat were stored at 4 °C and injected with 5 mL of C. jejuni with a concentration of 104 CFU/mL. The samples prepared in this way were incubated for 4 h. Then, they were sprayed with 5 mL of bacteriophage with PFU/mL, and the samples were again incubated for 48 h. The final result was 102 CFU/g. | [4] |
Φ7-izsam Φ16-izsam | The influence of bacteriophages on naturally or artificially contaminated poultry was investigated. Bacteriophages were given to the animals before slaughter and resulted in a reduction of 1 log10 CFU/g and 2 log10 CFU/g for both test groups. | [72] | |||
CP20 and CP30A | Poultry were infected and bacteriophages were administered 4 days later. Chickens were sacrificed every 24 h and the intestinal pathogen concentration was examined. The most prominent result was obtained on the second day of incubation and caused a decrease of bacteria by 2.4 log CFU/g in relation to the control. | [73] | |||
12673, P22, 29C; | The contaminated skin of chickens was examined. The level of the pathogen decreased by 2 log units when using the MOI of the phage 100:1 or 1000:1. | [100] | |||
Escherichia coli | Vomiting, headaches, stomach pain, low-grade fever or fever, diarrhea, weakness, bloody stools, hemolytic uremic syndrome, neonatal meningitis, pneumonia, sepsis | Pork, poultry, contaminated ruminants such as goats, deer, sheep, elk, water, milk and dairy products, direct contact with animals | FM10, DP16 and DP19 | The phage cocktail was tested on fresh intubated cucumber at two temperatures of 4 °C and 25 °C for 24 h. The number of bacteria was reduced by 1.97–2.01 log CFU/g and 1.16–2.01 log CFU/g at 25 °C and 4 °C. | [54] |
DW-EC | It was tested on many matrices, such as chicken meat, lettuce meat, fish meat, and tomato. The samples were contaminated with bacteria, then they were subjected to the phage section. A significant result was obtained at 6 days of incubation. The best effect was seen in the chicken feed samples where the pathogen value decreased by 80.93% after the first day and 87.29% after the 6th day. The weakest effect was observed on lettuce leaves. | [55] | |||
AZO145A | The effect of phage on the biofilm was investigated. Exposure to bacteriophage at a concentration of 1010 PFU/cm2 for 2 h resulted in a 4.0 log 10 PFU/mL reduction in biofilm on stainless steel. However, on the surface of beef, at 48 h incubation, the pathogen decreased by 3.1 log10 CFU/g. | [56] | |||
T4 | The aim of the study was to design an antimicrobial package by using the immobilization of T4 phage (105 CFU/mL) on the surface of the PCL foil. Contaminated beef was placed in this package. The bacterial concentration applied to the meat was 107 CFU/mL. After 48 h of incubation, the concentration of bacteria was reduced by 3 log CFU/mL. | [84] | |||
FAHEc1 | Contaminated raw beef as a test matrix; after using phage, the concentration of bacteria decreased by 2 or 4 log units at the appropriate storage temperatures, 24 °C and 37 °C. | [101] | |||
Listeria monocytogenes | Fever, chills, muscle aches, headaches, nausea and vomiting, confusion, local infections, inflammation of the lymph nodes, inflammation of the lungs, joints, bone marrow, pericarditis and myocarditis, inflammation of the eyeball, gastrointestinal infections. | Raw vegetables and fruit, unpasteurized dairy products (milk, cheese, ices cream), raw, cooked and frozen poultry meat, raw and smoked fish, delicatessen products, semi-finished products, fast-food products, soil, sewage, water, rotting plants, silage, wild and farm animals. | FWLLm1 | Bacterial levels dropped by 2 log units on the surface of the chicken that had become contaminated with Listeria. The samples were stored in a vacuum package at 4 °C and 30 °C. A positive result was observed only for the sample kept at 30 °C. | [7] |
A511 | Bacterial levels were tested in milk chocolate, mozzarella and brie cheese. The phage were given and incubated at 6 °C. Bacteria concentration dropped by 5 log units. | [102] | |||
Pseudomonas spp. | Pneumonia, fever, chills, severe shortness of breath, cough, confusion, chronic lower respiratory tract infection, Roth’s spots, i.e., petechiae on the retina, small painless erythematous changes on the hands and feet—Janeway symptom, painful reddish lumps on the fingers—Osler’s nodules, subungual petechiae | Water, soil, human and animal digestive tract. | UFJF_PfDIW6, UFJF_PfSW6 | The lyophilized phage cocktail was incubated with raw milk at 4 °C for 7 days. After the incubation period, the Pseudomonas bacterial population decreased by 3.2 log CFU/mL. | [103] |
V523, V524, JG003 | Three bacteriophages used separately and together as a cocktail were used to biocontrol bacteria in the water. The effect of the phages was tested against two bacteriophage strains: PAO1 and the environmental strain 17V1507. Of all the bacteriophages, V523 was most effective in reducing the PAO1 strain (>2.4 log10). The other strain was sensitive only to JG003, resulting in its reduction by 1.2 log10. The phage cocktail resulted in higher reductions in PAO1 (>3.4 log10) compared to using them alone. In contrast, the same reduction was observed in 17V1507 as with JG003 alone. | [104] | |||
Salmonella spp. | Abdominal pain, vomiting, diarrhea, fever, headache, chills, reduced urine output, dry mucous membranes, excessive sleepiness, apathy. | Chicken, turkey, pig, duck, goose meat, eggs, soil, water, cheese, milk, fruit, vegetables, contact with contaminated animals | LPSTLL, LPST94, LPST153 | The use of the bacteriophage cocktail decreased the concentration of bacteria by 3 log units. Chicken breasts were inoculated using an inoculum. The influence on the biofilm created by Salmonella was also examined, the administered cocktail effectively inhibited the growth after 72 h, the microplates decreased by 5.23 log units. | [46] |
LYPSET | The biocontrol was tested in milk and on lettuce leaves. In milk samples there was a decrease of bacteria by 2.19 log CFU/mL at 4 °C and 4.3 log CFU/mL at 25 °C. However, in the samples containing lettuce, there was a decrease of 2.2 log CFU/mL at 4 °C and 2.34 log CFU/mL at 25 °C at MOI = 10,000. | [45] | |||
SE07 | The effects of phage on eggs, beef and poultry meat were tested. The best effect for beef was obtained after 48 h of incubation; the bacterial value dropped from 4.23 log CFU/mL to 2.11 log CFU/mL, while for chicken the effect was even better as there was a decrease from 4.16 log CFU/mL to 2.14 log CFU/mL also at 48 h. | [47] | |||
SJ2 | The use of phage resulted in a significant reduction of bacteria in the soft pork and eggs. Incubation was carried out at 4 °C. | [105] | |||
BSPM4, BSP101, BSP22A | The phages were presented as a cocktail. The reduction of bacterial colonies was tested on lettuce leaves and fresh cucumber. There was a reduction of 4.7 log for lettuce and 5.8 log for cucumber. | [106] | |||
Shigella sp. | Vomiting, anorexia, abdominal cramps, bowel urgency, severe watery diarrhea, fever, diarrhea with an admixture of mucus and blood, rapid breathing, heart rate, low blood pressure, dry mouth and skin (dehydration), pain on palpation of the abdomen | Touching skin of contaminated person, oral cavity (fecal–oral route), contaminated water and food, sexual contact, swimming in contaminated water, by insects, such as housefly. | SSE1, SGF3, SGF2, | The influence of the SFE3 phage and its combination as a cocktail with other phages on the reduction of biofilm on polystyrene surfaces was investigated. It was found that the single SGF2 phage (isolated from wastewater) had the greatest impact on the development of biofilm; it caused growth inhibition by 26.6%. The lowest results were obtained for SGF3, while adding it to a phage cocktail increased its effectiveness by 25%. The phage is active against strains such as S. dysenteriae, S. baumannii, and S. flexneri. | [107] |
SD-11, SF-A2, SS-92 | The number of pathogens was decreased by 4 log in chicken meat, when they applied phage cocktail. It was stored at 4 °C. | [108] | |||
Staphylococcus sp. | Infections of the skin and subcutaneous tissue, which are characterized by the presence of purulent discharge, impetigo, folliculitis, boils, furunculosis (multiple boils), abscesses, inflammation of the sweat glands and inflammation of the mammary gland, high fever, drop in blood pressure, organ dysfunction | Transmission mainly by direct contact. Patients after surgery are most at risk | MDR, ME18, ME126 | Reducing biofilm in UHT milk at 25 °C using ME18 (MOI = 10) and MDR. They reduce biofilm in milk. However ME126 (MOI = 10) at 37 °C reduces CFU/mL by 87.2% compared to control sample. | [109] |
Vibrio parahaemolyticus | Watery diarrhea, abdominal cramps, nausea, vomiting, fever or chills, abscess formation, otitis media, otitis media and conjunctivitis | Contact with contaminated water, fruit, seafood | PVP1 and PVP2 | They treated sea cucumber contaminated with pathogen. MOI = 10 or MOI = 100. Test were performed at in 20 °C and it increased survival of sea cucumber to 80% compared with control sample without phage cocktail treatment, which was only 30%. | [110] |
Yersinia | Mild or high fever, cramping abdominal pain, loose stools often with mucus or blood, vomiting, right-hand stomach pain, tenderness when examining the abdominal cavity, fast heartbeat, joint pains, mainly in the knee, ankle and wrist, rapid breathing | Pork and pork offal, milk, water, raw vegetables and fruits. | fHe-Yen3-01 fHe-Yen9-01, fHe-Yen9-02 and fHe-Yen9-03 | Infected raw pork and cooking tools with the Rukola/71 strain. The kitchen tools were immersed in an inoculum at a concentration of 104 CFU/mL. The best effect was obtained for the phage fHe-Yen9-01, which reduced the number of bacteria by 1/3. | [86] |
PY100 | The given phage reduced the amount of bacteria in the meat MOI = 102 by 3 log10 units after 24 h incubation and at a MOI = 104 by 5 log10 units after 1.5 h incubation at 37 °C. However, when incubated at 4 °C, the bacteria count decreased by 2 log units after 24 h. | [111] |
Company | Product | Target | Reference | Regulatory & Certifications |
---|---|---|---|---|
Micreos Food Safety (The Netherlands) | PhageGuard Listex | Listeria sp. | [65,112,113] | Halal, OMRI, Kosher, Skal, FSSC 2200; FDA, GRN 198/21, EFSA; Swiss BAG; Israel Ministry of Health; Health Canada |
PhageGuard S | Salmonella enterica | [114] | Halal, FSSC 22000; FDA, GRN 468; USDA, FSIS Directive 7120.1, Swiss BAG | |
PhageGuard E | Escherichia coli O157:H7 | - | FSSC 22000 | |
Intralytix (USA) | ListShield | Listeria monocytogenes | [3,66,115,116,117] | Kosher; Halal; OMRI; FDA, 21 CFR 172.785; FDA, GRN 528; |
SalmoFresh | Salmonella enterica | [5,49,118,119,120] | Kosher; Halal; OMRI FDA, GRN 435; USDA, FSIS Directive 7120.1 | |
ShigaShield | Shigella sp. | [88,121,122] | FDA, GRN 672 | |
EcoShield PX | Escherichia coli | [9,123,124,125] | FDA, GRN 834; USDA, FSIS Directive 7120.1 | |
CampyloShield | Campylobacter spp. | [126] | GRAS | |
Proteon Pharmaceuticals SA (Poland) | Bafasal | Salmonella enterica | [96,127] | - |
Bafador | Pseudomonas sp., Aeromonas sp. | - | - | |
Passport Food Safety Solutions | Finalyse | E. coli O157:H7 | - | USDA, FSIS Directive 7120.1 |
Phagelux | SalmoPro | Salmonella spp. | - | FDA, GRN 603; USDA |
FINK TEC GmbH (Hamm, Germany) | Secure Shield E1 | E. coli | [93] | FDA,GRN 724 |
Arm and Hammer Animal & Food Production (USA) | Finalyse SAL | Salmonella | [128] | - |
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Hyla, K.; Dusza, I.; Skaradzińska, A. Recent Advances in the Application of Bacteriophages against Common Foodborne Pathogens. Antibiotics 2022, 11, 1536. https://doi.org/10.3390/antibiotics11111536
Hyla K, Dusza I, Skaradzińska A. Recent Advances in the Application of Bacteriophages against Common Foodborne Pathogens. Antibiotics. 2022; 11(11):1536. https://doi.org/10.3390/antibiotics11111536
Chicago/Turabian StyleHyla, Kinga, Izabela Dusza, and Aneta Skaradzińska. 2022. "Recent Advances in the Application of Bacteriophages against Common Foodborne Pathogens" Antibiotics 11, no. 11: 1536. https://doi.org/10.3390/antibiotics11111536
APA StyleHyla, K., Dusza, I., & Skaradzińska, A. (2022). Recent Advances in the Application of Bacteriophages against Common Foodborne Pathogens. Antibiotics, 11(11), 1536. https://doi.org/10.3390/antibiotics11111536