Advanced strategies to overcome the challenges of bacteriophage-based antimicrobial treatments in food and agricultural systems

Figures & data

Table 1. Commercial bacteriophage products for biocontrol applications

Product	Phage identity	Host	Applications	Company	References
AgriPhage	N/A^1	Xanthomonas campestris pv. Vesicatoria organism	Controlling plant disease in pre-harvesting	Omnilytics Inc.	(AgriPhage™, n.d.)
		Pseudomonas syringae pv.
AgriPhage-Fire Blight		Erwinia amylovora.
AgriPhage-CMM		Clavibacter michiganensis pv. michiganensis
AgriPhage-Citrus Canker		Xanthomonas citri pv. citri.
Biolyse®-PB	N/A^1	soft-rot Enterobacteriacea	Controlling fresh produce disease in packing house	APS Biocontrol Ltd.	(APS Biocontrol, n.d.)
BIOTECTOR	N/A^1	E. coli	Reducing foodborne pathogens in livestock	CheilJedang Corporation	(CheilJedang, n.d.)
		Clostridium
		Salmonella
ListShield™	Phage cocktail (List-1, List-2, List-3, List-4, List-36 and List-38)	Listeria monocytogenes	Foodborne pathogens control in food products	Intralytix Inc.	(Intralytix, n.d.)
SalmoFresh™	Phage cocktail (SPT-1, SBA-178, SBA-1781, SIT-128, SSE-121 and SDT-15)	Salmonella
ShigaShield™	Phage cocktail (SHSML-52-1, SHFML-11, SHSML-45, SHFML-26, and SHBML-50-1)	Shigella spp.
EcoShield PX™	Phage cocktail (ECML-117, ECML-359 and ECML363)	Shiga toxin-producing E. coli (STEC) in particular O157:H7 STEC
CampyShield™	Phage cocktail (J350, J375 and J386)	Campylobacter spp.
SalmoLyse®	Phage cocktail (SPT-1, SBA-178, SBA-1781, SIT-128, SSE-121 and SDT-15)	Salmonella spp.	Controlling foodborne pathogens in pet food products
ListPhage™	Phage cocktail (List-1, List-2, List-3, List-4, List-36 and List-38)	L. monocytogenes
Ecolicide®	ECML-117 and/or ECML-134	E. coli O157:H7
Ecolicide PX™	Phage cocktail (ECML-117, ECML-359 and ECML363)	E. coli O157:H7	Controlling foodborne pathogens in livestock	Intralytix Inc.	(Intralytix, n.d.)
PhageGuard Listex (Listex™ P100)	P100	L. monocytogenes	Controlling foodborne pathogens in food products	PhageGuard	(PhageGuard, n.d.)
PhageGuard S	Phage cocktail (Fo1a and S16)	Salmonella
PhageGuard E	Phage cocktail (EP75 and EP335)	E. coli O157:H7
Finalyse™SAL	Phage cocktail (BP-63 and LVR16A)	Salmonella	Controlling foodborne pathogens in poultry	ARM & HAMMER™	(ARM & HAMMER™, n.d.)
Pyo-Phage	N/A^1	Staphylococcus	Controlling foodborne pathogens	Brimrose Technology Corporation	(Brimrose, n.d.)
		Escherichia coli
		Streptococcus
		Pseudomonas aeruginosa
		Proteus
Intesti Phage	N/A^1	Shigella spp.
		Salmonella spp.
		Staphylococcus
		Proteus spp.
		E. coli
		P. aeruginosa
		Staphylococcus
SES Phage	N/A^1	Streptococcus
		E. coli
		Salmonellae spp.
EnkoPhagum	N/A^1	Shigellas spp.	Controlling foodborne pathogens	Brimrose Technology Corporation	(Brimrose, n.d.)
		Enteropathogenic E. coli
		Staphylococcus spp.
		Staphylococcus spp.
Fersisi Phage	N/A^1	Streptococcus spp.
		Staphylococcal
Mono-phage Preparations	N/A^1	E. coli
		Streptococcal
		P. aeruginosa
		Proteus

¹ N/A: Information is not available.

Figure 1. Challenges of using phages as antimicrobial agents in the food and agricultural systems.

Table 2. Effect of pH, temperature and UV irradiation on the stability of phages of foodborne pathogen

Challenge	Phage	Host	Optimal conditions	Lethal conditions	References
pH	Phage vB_SalS_1-23	Salmonella spp.	Stable at pH 8-10	Phage number (PFU/mL) reduce at pH < 7 or pH > 10 No phage detectable at pH < 2 or pH > 12	(Cong et al. 2021)
	Phage vB_SalS_3-29	Salmonella spp.	Stable at pH 4-10	Phage number (PFU/mL) reduce at pH < 4 or pH > 10 No phage detectable at pH < 2 or pH > 12
	Phage LSPTLL	Salmonella spp.	Stable at pH 3-12	Phage number (PFU/mL) reduce at pH < 3 or pH > 12 No phage detectable at pH < 2	(Guo et al. 2021)
	Phage TYM101	Salmonella Enteritidis	Stable at pH 5-10	After 1-h incubation at 37 °C: 2-log reduction of phage (PFU/mL) at pH 4 3-log reduction of phage (PFU/mL) at pH 3	(Abhisingha, Dumnil, and Pitaksutheepong 2020)
	Phage ENT101	Salmonella Typhimurium	Stable at pH 4-10	After 1-h incubation at 37 °C: 4-log reduction of phage (PFU/mL) at pH 3
	Phage LSE7621	Salmonella Enteritidis	Stable at pH 4-11	No phage detectable at pH < 4 or pH > 11	(Liu et al. 2020)
	Phage LPST10	Salmonella Typhimurium	Stable at pH 3-11	No phage detectable at pH < 3	(Huang et al. 2018)
	Phage SS3e	Salmonella enterica E. coli Shigella sonnei Enterobacter cloacae Serratia marcescens	Stable at pH 5-8	Phage number (PFU/mL) reduce at pH < 5 or pH > 8 Only 5% of initial phage survived at pH 3	(Kim et al. 2018)
	Phage vB_SenS_CSP01	Salmonella spp.	Stable at pH 5-9	After 1-h incubation at 37 °C: 2-log reduction of phage (PFU/mL) at pH 11 4-log reduction of phage (PFU/mL) at pH 3	(Chen et al. 2018)
	Phage vB_SenS_PHB06		Stable at pH 5-9	After 1-h incubation at 37 °C: 1-log reduction of phage (PFU/mL) at pH 11 4-log reduction of phage (PFU/mL) at pH 3
	Phage vB_SenS_PHB07		Stable at pH 5-11	After 1-h incubation at 37 °C: 2-log reduction of phage (PFU/mL) at pH 3
pH	Phage SE07	Salmonella Enteritidis	Stable at pH 5-11	Phage number (PFU/mL) reduces at pH < 5 No phage detectable at pH < 4	(Thung et al. 2017)
	Phage PA13076	Salmonella spp.	Stable at pH 6-11	Phage number (PFU/mL) reduces at pH < 6 or > 11 No phage detectable at pH < 3 or > 13	(Bao et al., 2015)
	Phage PC2184		Stable at pH 5-11	Phage number (PFU/mL) reduces at pH < 5 or >11 No phage detectable at pH < 4 or > 12
	Phage T7	E. coli BL21		No phage detectable at simulated gastric fluid (SGF) pH 1.2 after 30 min	(Huang and Nitin 2019)
	Phage cocktail (ΦJLA23, ΦKP26, ΦC119 and ΦE142)	E. coli O157:H7	Stable at pH 6-10	Phage number (PFU/mL) reduces at pH < 6 No phage detectable at pH < 2 No phage detectable at SGF with pH 2.4 after 30 min No phage detectable at SGF with pH 2 after 15 min	(Ramirez et al. 2018)
	Phage vB_SflM_004 vB_SdyM_006 vB_SsoS_008	Shigella	Stable at pH 7-9	No phage detectable at pH < 3 or > 12	(Shahin et al. 2021)
	Phage11895-B1	Vibrio spp.		At SGF with pH 1.2: 2-log reduction of phage (PFU/mL) after 30 min No phage detectable after 60 min	(Huang and Nitin 2019)
	Phage vB_VpaS_OMN	Vibrio parahaemolyticus.	Stable at pH 5-9	Phage number (PFU/mL) reduces at pH < 5 or > 9 No phage detectable at pH < 4	(Zhang et al. 2018)
	Phage CP220	Campylobacter jejuni HPC5	Stable at pH 5-11	Phage number (PFU/mL) reduces at pH < 5 No phage detectable at pH < 3	(El-Shibiny et al. 2009)
Temperature	Phage vB_SalS_1-23	Salmonella spp.	Stable at −20-60 °C for 80 min	No phage detectable at temperature > 70 °C after 40 min	(Cong et al. 2021)
	Phage vB_SalS_3-29		Stable at −20-50 °C for 80 min	Rapid decrease at temperature at 60 °C No phage detectable at temperature > 70 °C after 40 min
	Phage LSPTLL	Salmonella spp.	Stable at 30-60 °C for 60 min	Rapid decrease at temperature at 70 °C No phage detectable at temperature > 80 °C after 30 min	(Guo et al. 2021)
	Phage TYM101	Salmonella Enteritidis	Stable at 50-60 °C for 30 min	After 30-min incubation: 2-log reduction of phage (PFU/mL) at 70 °C 4-log reduction of phage (PFU/mL) at 80 °C No phage detectable at 90 °C	(Abhisingha, Dumnil, and Pitaksutheepong 2020)
	Phage ENT101	Salmonella Typhimurium	Stable at 50-60 °C for 30 min	After 30-min incubation: 1-log reduction of phage (PFU/mL) at 70 °C 4-log reduction of phage (PFU/mL) at 80 °C No phage detectable at 90 °C
	Phage LSE7621	Salmonella Enteritidis	Stable at 30-50 °C for 60 min	No phage detectable at 70 °C after 60 min	(Liu et al. 2020)
	Phage LPST10	Salmonella Typhimurium	Stable at 30-60 °C for 60 min	No phage detectable at 80 °C after 60 min	(Huang et al. 2018)
	Phage vB_SenS_CSP01	Salmonella spp.	Stable at 4-40 °C for 60 min	After 40-min incubation: 5-log reduction of phage (PFU/mL) at 60 °C No phage detectable at 70-80 °C	(Chen et al. 2018)
	Phage vB_SenS_PHB06		Stable at 4-50 °C for 60 min	No phage detectable at 60 °C after 60 min No phage detectable at 70-80 °C after 20 min
	Phage vB_SenS_PHB07		Stable at 4-50 °C for 60 min	No phage detectable at 70-80 °C after 40 min
Temperature	Phage SE07	Salmonella Enteritidis	Stable at 28-45 °C for 60 min	After 40-min incubation: 5-log reduction of phage (PFU/mL) at 65 °C	(Thung et al. 2017)
	Phage PA13076	Salmonella spp.	Stable at 30-50 °C for 60 min	No phage detectable at temperature > 70 °C after 30 min	(Bao et al. 2015)
	Phage PC2184		Stable at 30-60 °C for 60 min	After 30-min incubation: 2-log reduction of phage (PFU/mL) at 70 °C No phage detectable at 80 °C
	Phage P100	Listeria monocytogenes	Stable at 40-60 °C for 75 min	After 75-min incubation: 8-log reduction of phage (PFU/mL) at 70 °C No phage detectable at 80 °C	(Ahmadi et al. 2017)
	Phage A511		Stable at 40-60 °C for 75 min	After 75-min incubation: 6-log reduction of phage (PFU/mL) at 70 °C No phage detectable at temperature > 75 °C
	Phage φV05	V. parahaemolyticus (ATCC 17802)	Stable at 40-50 °C for 60 min	No phage detectable at temperature at 60 °C after 60 min	(Yin et al. 2019)
	Phage φV07
	Phage φV09
	Phage vB_VpaS_OMN	V. parahaemolyticus	Stable at 30-50 °C for 60 min	After 60-min incubation: 2-log reduction of phage (PFU/mL) at 60 °C No phage detectable at temperature > 70 °C	(Zhang et al. 2018)
	Phage vB_SflM_004 vB_SdyM_006	Shigella	Stable at −20-40 °C for 60 min	After 60-min incubation: Only 50% active phages at 60 °C No phage detectable at temperature > 80 °C	(Shahin et al. 2021)
	Phage cocktail (ΦJLA23, ΦKP26, ΦC119 and ΦE142)	E. coli O157:H7	Stable 25-50 °C for 90 min	Rapid decrease at temperature at 70 °C	(Ramirez et al. 2018)
UV irradiation	Phage T7	E. coli BL21	Exposing to UV-A irradiation: 2-log reduction of phage (PFU/mL) after 1 h No phage detectable after 3 h		(Huang and Nitin 2020)
	Phage cocktail (ΦJLA23, ΦKP26, ΦC119 and ΦE142)	E. coli O157:H7	Exposing to UV-C (λ = 254 nm) irradiation: No phage detectable after 15 min		(Ramirez et al. 2018)
	Phage SS3e	Salmonella enterica E. coli Shigella sonnei Enterobacter cloacae Serratia marcescens	Exposing to UV-C (λ = 254 nm) irradiation: No phage detectable after 15 min		(Kim et al. 2018)
	Phage T4	E. coli	Exposing to UV-C (λ = 254 nm) irradiation: The inactivation curve was log-linear at exposure times of 6 min or less		(John Hudson et al. 2010)

Figure 2. Current strategies for enhancing phages stability against environmental challenges.

Figure 3. Current strategies for enhanced delivery of phages in food and agricultural systems.

Table 3. Strategies of phage incorporation that improves stability of phages in harsh encironments

Strategy	Matrix	Challenge	Phage	Host	Treatment conditions	Phage viability	References
Encapsulation – Extrusion	Alginate-Ca^2+	Acid	UFV-AREG1	E. coli O157:H7	(In vitro) Simulated gastric fluid (SGF), pH 2.5, 37 °C, 120 min	2.39-log reduction (PFU/g)	(Silva Batalha et al. 2021)
			f3αSE	Salmonella Enterica	(In vitro) pH 2, pH 3 and pH 4, 25 °C, 60 min	Stable at pH 4 and pH 3	(Soto et al. 2018)
			T7	E. coli	(In vitro) SGF of pH 2.5, 37 °C, 40 min	5-log reduction (PFU/g)	(Moghtader, Eğri, and Piskin 2017)
			P008	Lactococcus lactis	(In vitro) SGF of pH 2, 37 °C, 30 min	Undetectable	(Samtlebe et al. 2016)
			Felix O1	Salmonella Enterica	(In vitro) pH 2 and pH 2.5, 41.4 °C, 30 min	8-log reduction (PFU/g) at pH 2 2-log reduction at pH 2.5	(Tang et al. 2013)
	Alginate-whey protein		UFV-AREG1	E. coli O157:H7	(In vitro) SGF of pH 2.5, 37 °C, 120 min	0.04-log reduction (PFU/g)	(Silva Batalha et al. 2021)
			P008	Lactococcus lactis	(In vitro) SGF of pH 2, 37 °C, 120 min	No significant reduction	(Samtlebe et al. 2016)
			Felix O1	Salmonella Enterica	(In vitro) pH 2 and pH 2.5, 41.4 °C, 120 min	0.5-log ∼ 2-log reduction (PFU/g) at pH 2 No significant reduction at pH 2.5	(Tang et al. 2013)
Encapsulation – Extrusion	Alginate-chitosan	Acid	UFV-AREG1	E. coli O157:H7	(In vitro) SGF of pH 2.5, 37 °C, 60 min	Undetectable	(Silva Batalha et al. 2021)
			ZSEC5	E. coli O157:H7	(In vitro) SGF of pH 2, 37 °C, 60 min	2-log reduction (PFU/mL)	(Abdelsattar et al. 2019)
	Chitosan-coated alginate		T4	E. coli	(In vitro) SGF of pH 2.5, 37 °C, 120 min	5-log reduction (PFU/g)	(Moghtader, Eğri, and Piskin 2017)
			Phage K	Staphylococcus aureus	(In vitro) SGF of pH 2.5, 37 °C, 60 min	2.4-log reduction (PFU/g)	(Ma et al. 2012)
			Felix O1	Salmonella Enterica	(In vitro) SGF of pH 2.4, 37 °C, 90 min	3-log reduction (PFU/g)	(Ma et al. 2008)
	Chitosan-coated alginate/honey/gelatin		ZSEC5	E. coli O157:H7	(In vitro) SGF of pH 2, 37 °C, 60 min	1-log reduction (PFU/g)	(Abdelsattar et al. 2019)
	Polyethylene-coated alginate		T4	E. coli	(In vitro) SGF of pH 2.5, 37 °C, 120 min	4-log reduction (PFU/g)	(Moghtader, Eğri, and Piskin 2017)
	Alginate-CaCO3		UVB_Phi20	Salmonella Typhimurium	(In vitro) SGF of pH 2.8, 37 °C, 60 min	No significant reduction	(Colom et al. 2017)
			UVB_Phi78			2.9-log reduction (PFU/mL)
			UVB_Phi87			3.5-log reduction (PFU/mL)
			Phage K	Staphylococcus aureus	(In vitro) SGF of pH 2.5, 37 °C, 120 min	0.17-log reduction (PFU/g)	(Ma et al. 2012)
Encapsulation – Extrusion	Alginate-caseinate	Acid	Felix O1	Salmonella Enterica	(In vitro) SGF of pH 2, 37 °C, 120 min	1.25-log reduction (PFU/g)	(Ergin et al. 2021)
	Alginate-carrageenan		UFV-AREG1	E. coli O157:H7	(In vitro) SGF of pH 2.5, 37 °C, 120 min	4.7-log reduction (PFU/g)	(Silva Batalha et al. 2021)
	Alginate-Ca^2+	Heat	f3αSE	Salmonella Enterica	60 °C	50% of phages survived after 1h	(Soto et al. 2018)
	Alginate-chitosan		ZSEC5	E. coli O157:H7	80 °C, 3 min	2.3-log reduction (PFU/mL)	(Abdelsattar et al. 2019)
	Chitosan-coated alginate/honey/gelatin					< 1-log reduction (PFU/mL)
	Alginate-chitosan-tarbush leaves extraction	UV irradiation	WA1 and WA3	E. coli DH5α	Irradiating 1 mL suspension by UV light (λmax = 365nm, 6w) for 20 min	4 log (PFU/mL) of phage survived	(Pacios-Michelena et al. 2023)
	Alginate-PVA-tarbush leaves extraction					4 log (PFU/mL) of phage survived
Encapsulation – Emulsification	Alginate-Eudragit®S100	Acid	T3	E. coli	(In vitro) SGF of pH 1, pH 1.5, pH 2 and pH 2.5, 37 °C, 120 min	No significant reduction	(Richards and Malik 2021a)
	Milk protein		P008	Lactococcus lactis	(In vitro) SGF of pH 2, 37 °C, 120 min	2.2-log reduction (PFU/mL)	(Samtlebe et al. 2016)
	Alginate-Eudragit®S100	Heat	T3	E. coli	75, 85 and 95 °C, 2 min	< 2.5-log reduction (PFU/g) at all temperatures	(Richards and Malik 2021a)
Encapsulation – Liposome	Unilamellar liposome	Acid	UVB_Phi20	Salmonella Typhimurium	(In vitro) SGF of pH 2.8, 42 °C, 30 min	3.2-log reduction (PFU/mL)	(Colom et al. 2015)
			UVB_Phi78			4-log reduction (PFU/mL)
			UVB_Phi87			3.3-log reduction (PFU/mL)
	Pronanosome Nio-N™	Heat	phiIPLA-RODI	Staphylococcus aureus	60 °C, 90 min	2.24-log reduction (PFU/mL)	(González-Menéndez et al. 2018)
Encapsulation – MPN	Tannic acid and ferric network	UV irradiation	T4 phage	E. coli P301	Irradiation using UV lamp for 20 min	> 3-log reduction (PFU/mL)	(Sun et al. 2022)
Immobilization – Dip coating (physisorption)	Whey protein isolate (WPI)-glycerol	Acid	T7	E. coli	(In vitro) SGF of pH 1.2, 37 °C, 60 min	1.6-log reduction (PFU/pellet)	(Huang and Nitin 2019)
			Phage 11985-B1	Vibrio spp.		< 1.5-log reduction (PFU/pellet)
Immobilization – Spray coating (physisorption)			T7	E. coli		1.6-log reduction (PFU/pellet)
			Phage 11985-B1	Vibrio spp.		< 1.5-log reduction (PFU/pellet)

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