Review Article

Bacteriophages and Their Role in Food Safety

Table 3

Pre- and postharvest Salmonella phage applications.

YearAnimal/product Phage(s)StrategyMain outcomeRefs

Preharvest application

2001Poultry
(chicken)
Phage cocktailOral delivery
(direct and via feed)
Reduction of CFU in cecal counts between 0.3 and 1.3 log compared to controls birds[65]
2001Swine
(pig)
Felix01Oral delivery and i.m.Reduction of CFU in the tonsils and cecum[66]
2005Poultry
(broiler chickens)
CNPSA1, CNPSA3, CNPSA4Oral delivery
Reduction of CFU by 3.5 orders of magnitude after five days [67]
2005Poultry
(chickens)
Phage cocktail
(Sa2, S9, S11)
Oral delivery
phage/competitive exclusion
Reduction of CFU in cecum and ileum after phage cocktail and/or competitive exclusion treatment[68]
2007Poultry
(broiler chickens)
Φ151, Φ25, Φ10Oral delivery
(antacid suspension)
Reduction of 4.2 log and 2.19 log with phages Φ151 and Φ25 within 24 h compared with control[69]
2007Poultry
(broiler chickens)
Phage cocktail (CB4ϕ, WT45ϕ)Oral delivery Reduction of CFU in cecal tonsils after 24 h. No significant differences at 48 h compered to controls[70]
2008Poultry
(chickens)
Phage cocktailOral delivery
(coarse spray/drinking water)
Reduction of intestinal colonization of ten-day-old experimentally contaminated birds[71]
2010Swine
(pig)
Phage cocktailReduction of colonization by 99.0 to 99.9% in the tonsils, ileum, and cecum [72]
2011Swine
(weaned pigs)
Phage cocktailOral delivery
Significant reduction of CFU in the rectum[73]
2011Poultry
(chickens)
Oral delivery
(via feed)
Phage prevented horizontal transmission on six-week-old infected chickens[74]

Postharvest application

2001Processed food
(ripened cheese)
SJ2Added to milkNo survival during 89 days in pasteurized cheeses containing phages (MOI 104) [75]
2001Fresh produce
(fresh-cut melon and apple)
Phage cocktailAdded to foodsSignificant CFU reduction on melon but not on apple[76]
2003Meat
(chicken skin)
P22, 29CApplied on topMOI 1 caused less than 1 log reduction in CFU; MOI 100-1,000 caused 2 log reductions in CFU and eradicated resistant strains[13]
2003Meat
(chicken frankfurters)
Felix O1Approx. 2 log reduction with a MOI of 1.9 × 104[21]
2004Fresh produce
(sprouting seeds)
A, BApplied by immersion Phage-A reduced CFU by 1.37 logs on mustard seeds. Cocktail resulted in a 1.5-log reduction in CFU in the soaking water of broccoli seeds[77]
2005Meat
(broiler, turkey)
PHL 4SprayedPhage treatments reduced frequency of Salmonella recovery as compared with controls[78]
2008Meat
(raw/cooked beef)
P7Applied on topReduction in CFU of 2-3 log at 5°C and approx. 6 log at 24°C[16]
2009Fresh produce
(tomatoes)
Phage cocktailPhage + E. asburiae JX1 added to foodPrevalence reduction of internalized S. Javiana, although the major suppressing effect was via antagonistic activity of E. asburiae JX1[79]
2010Fresh produce (mung bean sprouts and alfalfa seeds)Phage cocktailPhage + E. asburiae JX1 added to foodsCombined biocontrol with E. asburiae and phage suppressed pathogen growth on mung beans and alfalfa seeds[80]
2011Meat
(pig skin)
Phage cocktail
(PC1)
Applied on topAbove 99% reduction in CFU for MOI of 10 or above at 4°C for 96 h[59]
2012Ready-to-eat foods and chocolate milkFO1-E2Added to foods and mixed in milkAt 8°C no viable cells. At 15°C reduction of CFU by 5 logs on turkey deli meats and in chocolate milk and by 3 logs on hot dogs