A review of phage mediated antibacterial applications

Figures & data

Figure 1. Selection process of research articles for inclusion in this review

Table 1. In vivo human phage therapy trials

Phage therapy in humans	Phage type	Source of phages	Pathogens targeted	Serovar/pathotype	efficacy	Ref
Treatment of diabetic toe ulcers	Staphylococcal phage Sb-1	Eliava Institute	S. aureus (MRSA and MSSA)	-	100%	[93]
Treatment of GIT MRSA infection	polyvalent S. aureus bacteriophages	L. Hirszfeld Institute collection	S. aureus (MRSA)	-	100%	[94]
Treatment of burn infections	-	J. Soothill	P. aeruginosa	-	100%	[95]
Treatment of infected venous stasis ulcers and other poorly healing wounds	Pyophage in PhagoBioDerm films	Eliava Institute	P. aeruginosa, E. coli, S. aureus, Proteus, and Streptococcus	-	76%	[49]
Treatment of corneal abscess and interstitial keratitis	S. aureus bacteriophage SATA-8505	ATCC	VRSA	-	100%	[96]
Treatment of burn wound infection	Cocktail of P. aeruginosa phages 14/1 (Myoviridae) and PNM (Podoviridae) and S. aureus phage ISP (Myoviridae)	Merabishvili et al 2009	S. aureus and P. aeruginosa	-	0%	[69]
Treatment of chronic otitis antibiotic-resistant P. aeruginosa Infection	Biophage-PA	NCIMB	MDR P. aeruginosa	-	80%	[97]
Treatment of P. aeruginosa UTI	PA Phage cocktail (Pyophage #051007)	Eliava Institute	MDR P. aeruginosa	-	100%	[98]
Treatment of acute bacterial diarrhea	T4-like coliphages cocktail	Microgen-Russia	E. coli	-	0%	[70]
Treatment chronic bacterial prostatitis	IIET bacteriophage collection	IIET bacteriophage collection sewage, environmental, or drinking water	Enterococcus faecalis	-	100%	[99]
Phage safety analysis	Phage cocktail Coli Proteus	Microgen Russia	E. coli and proteus	-	-	[30]

Table 2. Phage-mediated biocontrol of bacterial growth in ethanol fermentation, foods, and beverages

Field of application	Phage/phage part used	Source of phages/part	Level of application	Bacteria type controlled	Bacteria serotype/Strain	Efficacy	Ref.
Ethanol fermentation	Streptococcal phage LambdaSa2 (λSa2) endolysin	EMD Biosciences, San Diego,CA)	Laboratory experiment	Lactobacillus, staphylococci, and streptococci		77.3%	[100]
	LysA, LysA2, LysgaY and λSa2 endolysin proteins	Subcloned into the pET21a E. coli expression vector
Ethanol fermentation	Lytic enzymes LysA and LysA2	endolysins genes expressed in Saccharomyces cerevisiae	Laboratory experiment	Lactobacillus fermentum, Lactobacillus brevis, and Lactobacillus mucosae.		~ 90%	[101]
Ethanol fermentation	EcoSau and EcoInf	Wastewater influent	Laboratory experiment	L. fermentum		100%	[37]
Ethanol fermentation	ATCC® 8014-B1™ (phage B1) and ATCC® 8014-B2™ (phage B2)	ATCC	Laboratory experiment	Lactobacillus plantarum ATCC® 8014™	ATCC® 8014™	99%	[92]
Dairy (Cheese)	Phage P100	Dairy plant sewage effluent	Laboratory experiment	L. monocytogenes	WSLC 1001	100%	[39]
Dairy (Milk)	vB_SauS-phiIPLA35	Dairy environment	Laboratory experiment	Staphylococcus aureus		100% for cocktail	[102]
Dairy (Milk) and control of E. coli biofilms	BECP2 and BECP6 phages	Sewage	Laboratory experiment	E. coli	O157:H7	90%	[103]
Dairy (Milk fermentation)	Coliphages DT1 and DT6	Feces	Laboratory experiment	E. coli	O157:H7 STEC	100%	[104]
Dairy (Cheese)	phage A511	-	Laboratory experiment	Listeria monocytogenes,		90%	[105]
Fruits (Cucumber, Apple, and Tomatoes)	T7 bacteriophages		Laboratory experiment	Escherichia coli	BL21	99.9%	[106]
Fresh-cut fruits and vegetables	LM-103 and LMP-102,	Intralytix, Inc. (Baltimore, Md.).	Laboratory experiment	Listeria monocytogenes,		99.9%	[107]
Dairy, poultry, beef products, sea food, and vegetables	A511 and P100	-	Laboratory experiment	Listeria monocytogenes	WSLC 1001 (serovar 1/2 c) and Scott A (serovar 4b)	100%	[108]
Beer industry	Myophage SA-C12	Fresh silage	Laboratory experiment	Lactobacillus brevis	8840 (NCIMB culture collection),	100%	[109]
Chicken cuts	FSP-1 and FSP-3/PSZ1 and/PSZ2		Laboratory Experiment	Salmonella enterica	Strain S49	92%	[110]
Spinach	-	Feedlot cattle feces	Laboratory Experiment	Escherichia coli	O157:H7	100%	[111]
Oysters	Siphoviridae phage pVp-1,	-	Laboratory experiment/trial on oysters	Vibrio parahaemolyticus	CRS 09–17	~99.999%	[112]
Fermented Soy bean paste	BCP1-1 and BCP8-2	Fermented food products	Laboratory experiment	Bacillus cereus	ATCC27348, ATCC21768, ATCC13061	100%	[113]
Bioactive packaging materials (meat and alfalfa seeds and sprouts)	LinM-AG8, LmoM-AG13, and LmoM-AG20, while the E. coli O104:H4 EcoM-HG2, EcoM-HG7 and EcoM-HG8 (Myoviridae)	Canadian Research Institute for Food Safety	Laboratory experiments	Listeria monocytogenes and Escherichia coli	E. coli O104:H4, LJH391 serotype 1/2b,	100%	[114]
Infant formula milk	ESP 1–3 and ESP 732–1	Sewage	Laboratory experiment	Enterobacter sakazakii	ATCC 29,544, 236/04, 732/03	100%	[115]
Infant formula milk	leB, leE and leN	Slurry	Laboratory experiment	Cronobacter sakazakii	C. sakazakii ATCC BAA 894, C. sakazakii ATCC BAA 894 LUX	100%	[40]
Pork, milk, and kitchenware	fHe-Yen3-01 (Podoviridae) fHe-Yen9-01, fHe-Yen9-02, fHe-Yen9-03 (Myoviridae)	Sewage	Laboratory experiment	Yersinia enterocolitica	O:3 strain 6471/76 and O:9 strain Ruokola/71	100%	[41]
Milk, sausage, and lettuce	LPST10, LPST18, and LPST23(Siphoviridae family)	Waste water, sewage, farm ditch, poultry house	Laboratory experiment	Salmonella strains Typhimurium and Salmonella Enteritidis	Salmonella Typhimurium ATCC 14,028	64.1%	[116]
Active food packaging system (cellulose acetate films)	BFSE16, BFSE18, PaDTA1, PaDTA9,PaDTA10 and PaDTA11	Chickenfeces, poultry exudates, and swine feces	Laboratory experiment	Salmonella enterica subsp.	Enterica serovar Typhimurium ATCC 14,028	100%	[117]
Bioctive food packaging system	BFSE16, BFSE18, PaDTA1, PaDTA9, PaDTA10 and PaDTA11	Poultry exudates and swine feces	Laboratory experiment	Salmonella enterica subsp.	Enterica serovar Typhimurium ATCC 14,028.	~ 99.99%	[118]
Sea food (Cockles)	phT4A, ECA2	Sewage	Laboratory experiment	Escherichia coli	ATCC 13,706),	90%	[119]

Table 3. In vitro phage therapy against clinical isolates assays

Field of application	Phage/phage part used	Source of phages/part	Level of application	Bacterial targeted	Strain/serovar/pathotype	Level of efficacy	Ref.
Phage activity against STEC and EHEC clinical isolates	CA911, CA933P, MFA933P and MFA45D	Minced meat, pork sauasage & bovine feces.	Laboratory experiment	Escherichia coli	STEC and EHEC	100%	[44]
Phage-Antibiotics synergism against E. coli biofilm	T4 bacteriophage ATTC 11,303-B4	LGC Standards, Middlesex, UK)	Laboratory experiment	E. coli biofilms	E. coli 11,303	100%	[120]
Phage activity against Bacillus pumilus	Phage FBa1, FBa2, and FBa3	River water	Laboratory experiment	Bacillus pumilus		100%	[121]
Phage activity against Salmonella Typhimurium	phSE-1, phSE-2, and phSE-5 (family Siphoviridae)	Sewage	Laboratory experiment	Salmonella Typhimurium	Enterica serovar Typhimurium	99%	[42]
Phage activity against S. aureus clinical isolates	Sb-1	-	Laboratory experiment	Staphylococcus aureus	-	100%	[122]
Phage activity against Pseudomonas fluorescens biofilms	Phage ϕIBB-PF7A	sewage treatment plant	Laboratory experiment	P. fluorescens biofilms		91%	[123]
Phage activity against SalmonellaTyphimurium	P22-B1, P22, PBST10, PBST13, PBST32, and PBST 35)	ATCC and Hankuk University of Foreign Studies	Laboratory experiment	SalmonellaTyphimurium	KCCM 40,253, ATCC 19,585, ATCC 19,585, and CCARM 8009.	54%	[124]
Phage activity against Staphylococcus aureus biofilm	Phage DRA88 and SAB4328-A	Sewage	Laboratory experiment and ex vivo-burn models	Staphylococcus aureus biofilm	RN6390B, RN6911, B4328, MSSA 3, MSSA 10, MRSA 82	Reduced biofilm formation	[125]
Phage activity against Pseudomonas aeruginosa biofilm	DL 52, DL 54, DL 60, DL 62, DL 64, and DL 68	Crude sewage	Laboratory experiment	P. aeruginosa biofilm	PAO1, PA45311, PA45291, PA45235	95%	[35]
Phage activity against Staphylococcus aureus biofilm	DRA88 and phage K	Crude sewage	Laboratory experiment	Staphylococcus aureus biofilm	1598, MRSA 252, & H325	100%	[36]
Phage therapy against Staphylococcus aureus	phage K and phage 92	ATCC	Laboratory experiment	MRSA/MSSA	MRSA (N315, COL, Mu50) ATCC 6538	100%	[126]
Ex vivo Phage activity against catheter MRSA biofilm	phage K	ATCC	Laboratory experiment (Catheter)	MRSA biofilms	Staphylococcus aureus 46,106	99%	[127]
Ex vivo Phage activity against catheter Proteus mirabilis and Escherichia coli biofilms	Escherichia coli T4 phage ATCC 11,303-B4	Bacteriofag coli-proteic, Microgen Pharma, Russia	Laboratory experiment (Catheter)	Proteus mirabilis and E. coli biofilms	E. coli ATCC 11,303 and P. mirabilis 13 HER1094	99.99%	[128]
Phage activity against Pseudomonas aeruginosa biofilm	-	Hospital environmental dirt, sewage disposal, and cattle waste effluents	Laboratory experiment	P. aeruginosa biofilms	-	50%	[129]
Phage therapy against Staphylococcus aureus	P128 proteins	Inducible T7 expression system in E. coli ER2566 strain	Laboratory experiment	Staphylococcus aureus	BK#13,725, BK#9894, BK#13,993	99.99%	[130]
Phage activity against K. pneumoniae biofilms	KPO1K2 and NDP, depolymerase, and nondepolymerase producing phages	-	Laboratory experiment	K. pneumoniae biofilms	B5055 (O1:K2)	Significant eradication	[131]
phage activity against MRSA & MSSA	.	Hospital environmental dirt, sewage disposal, and cattle waste	Laboratory experiment	MRSA and MSSA		100% for MSSA and 78% MRSA	[132]
Phage activity against MDR Acinetobacter baumanni	Phage ϕAB2	Sewage	Laboratory experiment	MDR Acinetobacter baumanni	A. baumannii M3237	99.90%	[56]
Phage activity against MDR P. aeruginosa		Sewage	Laboratory Experiment	MDR P. Aeruginosa	-	100%	[133]
Phage therapy assay against Pseudomonas aeruginosa and Staphylococcus spp clinical isolates	Intesti and Pyobacteriophag	Eliava BioPreparations, Tbilisi, Georgia	Laboratory experiment	P. aeruginosa and Staphylococcus spp.	-	100%	[134]
Phage bacterial lytic activity against resistant S. aureus	SA11 (Siphoviridae family	Hankuk University of Foreign studies	Laboratory experiment	Resistant S. aureus	ATCC 13,301 and CCARM 3080	99.99&	[135]
Phage bacterial lytic activity against S. aureus biofilms isolated from orthopedic Implant	StaPhage (Myoviridae)	AusPhage Pty Ltd and sewage water	Laboratory experiment	Staphylococcus aureus biofilms	ORI16C02N and ORI16025	98%	[136]
Phage activity against P. aeruginosa biofilms	P. aeruginosa phage M4	Health Protection Agency, Colindale, United Kingdom	Laboratory experiment (In vitro model system)	Pseudomonas aeruginosa biofilms	M4	99.9%	[137]

Table 4. In vivo and ex vivo phage therapy experiments in animal models/tissues, fish, plants, poultry, piggery, and bees

Field of application	Phages	Source of phages	Level of application	Target bacteria	Target bacteria strain/pathotype	Level of efficacy	Ref.
Phage therapy in model organisms
Treatment of P. aeruginosa infection in insect	PA5oct and KT28	Natural wastewater treatment plant	In vivo-insect model	P. aeruginosa	PA PAO1 and 0038	93.60%	[138]
Treatment of Burkholderia pseudomallei in mice	Phage C34	Sea water	In vivo-mouse model	Burkholderia pseudomallei	-	33.30%	[139]
Treatment of S. aureus infection in BALB/C mice	MR-10	-	In vivo-mouse model	S. aureus	ATCC 43,300 (MRSA) and ATCC 29,213(MSSA)	100%	[140]
Treatment of S. aureus osteomyelitis in Rabbits	SA-BHU1, SA-BHU2, SA-BHU8, SA-BHU15 and SA-BHU21, SA-BHU37, SA-BHU47)	River, pond, and sewage	In vivo-Rabbit model	MRSA	-	100%	[58]
Treatment of GIT pathogenic E. coli infection in white rats	EHEC-specific coliphage	http://www.sumobrain.com/patents/wipo/Methodsbacteriophage-design/WO201 0064044A1.pdf.	In vivo-mouse model	E. coli.	EHEC and non-EHEC E. coli	99.9%	[141]
Treatment of A. baumannii infection in Mouse Model	BɸC62 of Myoviridae family	Sewage water	In vivo-mouse model	Carbapenem resistant A. baumannii		100%	[34]
Treatment of A. baumannii pneumonia in BALB/c mice	vB_AbaM-IME-AB2 (IME-AB2),	Sewage	In vivo-mouse model	A. baumannii clinical isolates (MDR and sensitive)	-	100%	[59]
Treatment of P. aeruginosa keratitis in mice	фR18 and ФS12-1	Sewage	In vivo-mouse model	P. aeruginosa	-	99.78%	[142]
Prevention of V. cholerae infections in mouse and rabbits	Vibrio phages ICP1, ICP2, and ICP3	Human feces	In vivo-mouse and rabbit models	V. cholerae	AC 53, AC2846, and AC4653	100%	[143]
Treatment of S. Enteritidis infection in Caenorhabditis elegans worms	ΦSP-1 and ΦSP-3	Chicken feces	In vivo-worm model	Salmonella enteritidis	S49	94.8%	[144]
Treatment of PDR A. baumannii infections in Mice and human cells	Abp1	Sewage	In vivo-mice model and Ex vivo-human HeLa cells	PDR A. baumanni	-	100%	[60]
Treatment of Pseudomonas aeruginosa skin infections	Phage PA709 characterized	Sewage water	Ex vivo-human skin	MDR P. aeruginosa	MDR P. aeruginosa 709	99.99%	[145]
Treatment of K. pneumoniae wound infections in BALB/c mice	phage Kpn5	Sewage	In vivo experiment	Klebsiella pneumoniae	B5055	100%	[146]
Crop protection
Biocontrol of potato bacterial wilt	P-PSG-3, P-PSG-4, P-PSG-1, P-PSG-8 to P-PSG-12	water	Field trial	Ralstonia solanacearum	PS-X4-1, PS-X10-2, and PS-X13-1	80% in vivo and 98% in vitro	[147]
Biocontrol of alfalfa seeds spoilage Salmonella enterica	Phages SSP5 and SSP6	sewage	In vitro and in vivo laboratory experiments	Salmonella enterica	S. oranienburg	0%	[148]
Biocontrol of tomato bacterial wilt	RsPod1EGY	Soil	In vitro and in vivo laboratory experiments	Ralstonia solanacearum	K3, K9, K10, K11, K12, K16, K17, and K19	100%	[149]
Phage biocontrol of antibiotics resistant Dickeya dadantii which causes potato tuber rot	Myoviridae family	Caspian Sea water	Laboratory experiment/field Trial	Dickeya dadantii		100% in vitro 88.9% for trial	[150]
Acquaculture
Aquaculture	H20-Siphovirus and KVP40-Myovirus	Sea water	Laboratory experiment	Vibrio anguillarum	(BA35 and PF430-3)	Reduced biofilms	[151]
Aquaculture (treatment of ulcerative lesions in catfish)	PA phages	Waste water	Field trial	Pseudomonas aeruginosa (MDR)	-	100%	[152]
aquaculture	VP-2 and VA-1 phage	Sewage water	Laboratory experiment and trial	Vibrio. anguillarum		100%	[13]
Aquaculture	FpV-4, FpV-9, and FpV-21	pond water	Laboratory Experiment	Flavobacterium psychrophilum		Reduced bacterial growth	[153]
Treatment of Vibrio parahaemolyticus shrimp infections	V. parahaemolyticus phages (Myoviridae family)	Shrimp pond water suspended sediment	Laboratory experiment/trial	Vibrio parahaemolyticus	N1A and N7A	90%	[154]
Phage therapy in poultry
In vivo phage therapy against Campylobacter spp. infections in broiler chicken	typeIII phages NCTC12672, 12,673, 12,674, and 12,678 of the British phage typing scheme	Lohmann Animal Health, GmbH.	Field trial	Campylobacter spp.		∼99%	[155]
In vitro phage therapy against APEC	Phage ØEC1	Chicken feces	Laboratory experiment	E. coli	APEC O78:K80	∼99.99%	[156]
Phage therapy in piggery
In vivo phage therapy of Staphylococcus aureus nasal infection in pigs	phage K*710 and P68	Novolytics Ltd	Trial using animal model	Staphylococcus aureus (MRSA)	ST398, spa type t011, SCCmec type V	0%	[71]
Phage therapy in apiculture
In vivo phage therapy of American foulbrood caused by Paenibacillus larvae	Siphoviridae (HB10c2)	Glue-like liquid of a beehive	Laboratory experiment and field Trial	Paenibacillus larvae	ERIC I DSM 7030 and ERIC II DSM 25,430	2%	[43]

Table 5. Phage application in biosanitization

Field of application	Phage	Phage source	Level of application	Target bacteria	Bacteria strain/pathotype	Level of efficacy	Ref
Water and sewage treatment
Water purification	vB_AspP-UFV1 (Podoviridae)	Sludge of wastewater	Laboratory experiment	A. soli, Pseudomonas sp., and Brevundimonas sp.	AO1-02, AO2-07, AO1-30, and AO1-33	Significant biofilm control	[157]
Coliform phage biocontrol in sewage	Coliphage (Myovirus and Podovirus)	River water	Laboratory experiment	E. coli	E. coli SBSWF27	95.40%	[158,159]
Biosanitization
Hospital anitizer	Staphylococcal phage and Pyophage; GA,	Eliava Institute	Laboratory experiment	S. aureus, E. coli, and P. aeruginosa	S. aureus (SA2-R73), E. coli (EC-R60), and P. aeruginosa (PAV6).	90%	[86]
Hospital sanitizer	ϕAB1, AB2, AB6, AB7 phages	Sewage or river water	Laboratory experiment and trial	CR A. baumannii	-	47.50%	[87]
Hospital sanitizer	Pyobacteriophag polyvalent	Research and Production Association “Microgen” (Russia))	Trial	staphylococci, streptococci, enterococci, proteus, klebsiella (pneumoniae, and oxytoca), P. aeruginosa and E. coli	-	100%	[88]
Phage cream and sanitizers	Polyvalent Anti-Staphylococcus Phage K	ATCC 19,685-B1	Laboratory experiment and trial	MDR Staphylococcus aureus (MRSA and VRSA)	-	100%	[89]
Use of phages in semi solid creams for control of Propionibacterium acnes growth	PAC1 to PAC10	P. acnes strains isolated from facial skin swabs	Laboratory experiment	Propionibacterium acnes	A1, A2, or E8	100%	[90]

Figure 2. Comparison of mean MOIs between in vivo, in vitro, and ex vivo phage therapy. Tukey’s multiple-comparison test was used to compute and compare MOIs P value of 0.0002 < 0.05 generated indicating significant variation between ex vivo/in vivo PT and in vitro PT

Figure 3. Comparison of phage therapy (PT), phage-mediated biocontrol/diagnosis mean efficacy percentages. Tukey’s multiple-comparison test was used to calculate and compare the mean percentage efficacies generating a P value of 0.148 > 0.05 after exclusion of fields with less than three studies (water, piggery poultry, and apiculture)

Leszczyński P, et al. Successful eradication of methicillin-resistant Staphylococcus aureus (MRSA) intestinal carrier status in a healthcare worker–case report. Folia Microbiol (Praha). 2006;51(3):236–238. .

 PubMed Web of Science ®Google Scholar

Marza JAS, et al. Multiplication of therapeutically administered bacteriophages in Pseudomonas aeruginosa infected patients. Burns. 2006;32(5):644–646. .

 PubMed Web of Science ®Google Scholar

Fadlallah A, Chelala E, Legeais J-MJTOOJ. Corneal infection therapy with topical bacteriophage administration. 2015;9:167.

 Google Scholar

Markoishvili K, et al. A novel sustained‐release matrix based on biodegradable poly (ester amide) s and impregnated with bacteriophages and an antibiotic shows promise in management of infected venous stasis ulcers and other poorly healing wounds. 2002;41(7):453–458.

 Google Scholar

Wright A, et al. A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic‐resistant Pseudomonas aeruginosa; a preliminary report of efficacy. 2009;34(4):349–357.

 Google Scholar

Sarker S, et al. Oral phage therapy of acute bacterial diarrhea with two coliphage preparations: a randomized trial in children from Bangladesh. 2016;4:124–137.

 Google Scholar

Khawaldeh A, et al. Bacteriophage therapy for refractory Pseudomonas aeruginosa urinary tract infection. J Med Microbiol. 2011;60(Pt 11):1697–1700. .

 Web of Science ®Google Scholar

Letkiewicz S, et al. Eradication of Enterococcus faecalis by phage therapy in chronic bacterial prostatitis—case report. 2009;54(5):457.

 Google Scholar

Verstappen KM, et al. The effectiveness of bacteriophages against methicillin-resistant Staphylococcus aureus ST398 nasal colonization in pigs. PLoS One. 2016;11(8):e0160242.

 Web of Science ®Google Scholar

Roach DR, et al. Bacteriophage-encoded lytic enzymes control growth of contaminating Lactobacillus found in fuel ethanol fermentations. 2013;6(1):20.

 Google Scholar

McCallin S, et al. Safety analysis of a Russian phage cocktail: from metagenomic analysis to oral application in healthy human subjects. 2013;443(2):187–196.

 Google Scholar

Khatibi PA, et al. Saccharomyces cerevisiae expressing bacteriophage endolysins reduce Lactobacillus contamination during fermentation. 2014;7(1):104.

 Google Scholar

Obeso JM, et al. Use of logistic regression for prediction of the fate of Staphylococcus aureus in pasteurized milk in the presence of two lytic phages. Appl Environ Microbiol. 2010;76(18):6038–6046. .

 PubMed Web of Science ®Google Scholar

Liu M, et al. Bacteriophage application restores ethanol fermentation characteristics disrupted by Lactobacillusfermentum. 2015;8(1):132.

 Google Scholar

Fish R, et al. Bacteriophage treatment of intransigent diabetic toe ulcers: a case series. 2016;25(Sup7):S27–S33.

 Google Scholar

Carlton RM, Noordman WH, Biswas B, et al. Bacteriophage P100 for control of Listeria monocytogenes in foods: genome sequence, bioinformatic analyses, oral toxicity study, and application. Regul Toxicol Pharmacol. 2005;43(3):301–312. .

 PubMed Web of Science ®Google Scholar

Lee Y-D, Park J-H. Characterization and application of phages isolated from sewage for reduction of Escherichia coli O157:H7 in biofilm. Lebensmittel-Wissenschaft + [i.e. und] Tech. 2015;60(no. 1):571–577–2015.

 Google Scholar

Tomat D, Mercanti D, Balagué C, et al. Phage biocontrol of enteropathogenic and Shiga toxin-producing Escherichia coli during milk fermentation. Lett Appl Microbiol. 2013;57(1):3–10. .

 PubMed Web of Science ®Google Scholar

Guenther S, Loessner MJ. Bacteriophage biocontrol of Listeria monocytogenes on soft ripened white mold and red-smear cheeses. J App Bacteri. 2011;1(2):94–100.

 Google Scholar

Vonasek EL, et al. Incorporating phage therapy into WPI dip coatings for applications on fresh whole and cut fruit and vegetable surfaces. 2018;83(7):1871–1879.

 Google Scholar

Leverentz B, et al. Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. 2003;69(8):4519–4526.

 Google Scholar

Guenther S, et al. Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods. J App environ microbio. 2009;75(1):93–100.

 Google Scholar

Deasy T, et al. Isolation of a virulent Lactobacillus brevis phage and its application in the control of beer spoilage. 2011;74(12):2157–2161.

 Google Scholar

Augustine J, Bhat SG. Biocontrol of Salmonella Enteritidis in spiked chicken cuts by lytic bacteriophages ΦSP‐1 and ΦSP‐3. J basic microbio. 2015;55(4):500–503.

 Google Scholar

Patel J, et al. Inactivation of Escherichia coli O157: H7 attached to spinach harvester blade using bacteriophage. 2011;8(4):541–546.

 Google Scholar

Jun JW, et al. Eating oysters without risk of vibriosis: application of a bacteriophage against Vibrio parahaemolyticus in oysters. 2014;188:31–35.

 Google Scholar

Bandara N, et al. Bacteriophages BCP1-1 and BCP8-2 require divalent cations for efficient control of Bacillus cereus in fermented foods. 2012;31(1):9–16.

 Google Scholar

Lone A, et al. Development of prototypes of bioactive packaging materials based on immobilized bacteriophages for control of growth of bacterial pathogens in foods. 2016;217:49–58.

 Google Scholar

Kim KP, Klumpp J, Loessner MJ. Enterobacter sakazakii bacteriophages can prevent bacterial growth in reconstituted infant formula. Int J Food Microbiol. 2007;115(2):195–203.

 PubMed Web of Science ®Google Scholar

Huang C, et al. Isolation, characterization, and application of a novel specific Salmonella bacteriophage in different food matrices. Food Res Int. 2018;111:631–641.

 PubMed Web of Science ®Google Scholar

Endersen L, Buttimer C, Nevin E, et al. Investigating the biocontrol and anti-biofilm potential of a three phage cocktail against Cronobacter sakazakii in different brands of infant formula. Int J Food Microbiol. 2017;253:1–11.

 PubMed Web of Science ®Google Scholar

Jun JW, et al. Bacteriophages reduce Yersinia enterocolitica contamination of food and kitchenware. 2018;271:33–47.

 Google Scholar

Gouvêa DM, et al. Acetate cellulose film with bacteriophages for potential antimicrobial use in food packaging. 2015;63(1):85–91.

 Google Scholar

Gouvêa DM, et al. Absorbent food pads containing bacteriophages for potential antimicrobial use in refrigerated food products. 2016;67:159–166.

 Google Scholar

Pereira C, et al. Application of phage therapy during bivalve depuration improves Escherichia coli decontamination. 2017;61:102–112.

 Google Scholar

Ryan EM, et al. Synergistic phage-antibiotic combinations for the control of Escherichia coli biofilms in vitro. 2012;65(2):395–398.

 Google Scholar

Dini C, De Urraza PJ. Isolation and selection of coliphages as potential biocontrol agents of enterohemorrhagic and Shiga toxin-producing E. coli (EHEC and STEC) in cattle. J Appl Microbiol. 2010;109(3):873–887.

 Web of Science ®Google Scholar

Kusmiatun A, Rusmana I, Budiarti S. Characterization of bacteriophage specific to bacillus pumilus from Ciapus River in Bogor, West Java, Indonesia. HAYATI J Biosci. 2015;22(1):27–33.

 Google Scholar

Kvachadze L, et al. Evaluation of lytic activity of staphylococcal bacteriophage Sb‐1 against freshly isolated clinical pathogens. 2011;4(5):643–650.

 Google Scholar

Pereira C, et al. Bacteriophages with potential to inactivate Salmonella Typhimurium: use of single phage suspensions and phage cocktails. 2016;220:179–192.

 Google Scholar

Sillankorva S, Neubauer P, Azeredo JJBB. Pseudomonas fluorescens biofilms subjected to phage phiIBB-PF7A. 2008;8(1):79.

 Google Scholar

Jung L-S, et al. Evaluation of lytic bacteriophages for control of multidrug-resistant Salmonella Typhimurium. 2017;16(1):1–9.

 Google Scholar

Alves DR, et al. Development of a high-throughput ex-vivo burn wound model using porcine skin, and its application to evaluate new approaches to control wound infection. J Frontiers cellular infec microbio. 2018;8:196.

 Google Scholar

Ghosh A, et al. Combined application of essential oil compounds and bacteriophage to inhibit growth of Staphylococcus aureus in vitro. 2016;72(4):426–435.

 Google Scholar

Alves DR, et al. A novel bacteriophage cocktail reduces and disperses P seudomonas aeruginosa biofilms under static and flow conditions. J Microbial biotech. 2016;9(1):61–74.

 Google Scholar

Alves D, et al. Combined use of bacteriophage K and a novel bacteriophage to reduce Staphylococcus aureus biofilm formation. J App Environ Microbio. 2014;80(21):6694–6703.

 Google Scholar

Lungren MP, et al. Bacteriophage K for reduction of Staphylococcus aureus biofilm on central venous catheter material. 2013;3(4):e26825.

 Google Scholar

Carson L, Gorman S, Gilmore B. The use of lytic bacteriophages in the prevention and eradication of biofilms of Proteus mirabilis  and Escherichia coli. 2010;59(3):447–455.

 Google Scholar

Nouraldin AAM, et al. Bacteriophage-antibiotic synergism to control planktonic and biofilm producing clinical isolates of Pseudomonas aeruginosa. 2016;52(2):99–105.

 Google Scholar

Vipra AA, et al. Antistaphylococcal activity of bacteriophage derived chimeric protein P128. 2012;12(1):41.

 Google Scholar

Chhibber S, Nag D, Bansal SJBM. Inhibiting biofilm formation by Klebsiella pneumoniae B5055 using an iron antagonizing molecule and a bacteriophage. 2013;13(1):1–8.

 Google Scholar

Abdulamir AS, et al. The potential of bacteriophage cocktail in eliminating Methicillin-resistant Staphylococcus aureus biofilms in terms of different extracellular matrices expressed by PIA, ciaA-D and FnBPA genes. 2015;14(1):49.

 Google Scholar

Didamony GE, Askora A, Shehata AA. Isolation and characterization of T7-Like Lytic Bacteriophages Infecting multidrug resistant pseudomonas aeruginosa isolated from Egypt. Curr Microbiol. 2015;70(6):786–791.

 Web of Science ®Google Scholar

Chen L-K, et al. Potential of bacteriophage ΦAB2 as an environmental biocontrol agent for the control of multidrug-resistant Acinetobacter baumannii. 2013;13(1):1–10.

 Google Scholar

Niculae C-M, et al. The 12th Edition of the Scientific Days of the National Institute for Infectious Diseases “Prof. Dr. Matei Bals” and the 12th National Infectious Diseases Conference. 99. Neguț AC, Săndulescu O, Streinu-Cercel A, et al. Influence of bacteriophages on sessile Gram-positive and Gramnegative bacteria. . in BMC Infectious diseases. 2016. BioMed Central.

 Google Scholar

Woo J, Ahn JJAOM. Assessment of synergistic combination potential of probiotic and bacteriophage against antibiotic-resistant Staphylococcus aureus exposed to simulated intestinal conditions. 2014;196(10):719–727.

 Google Scholar

Morris J, et al. Evaluation of bacteriophage anti-biofilm activity for potential control of orthopedic implant-related infections caused by Staphylococcus aureus. 2019;20(1):16–24.

 Google Scholar

Fu W, et al. Bacteriophage cocktail for the prevention of biofilm formation by Pseudomonas aeruginosa on catheters in an in vitro model system. 2010;54(1):397–404.

 Google Scholar

Olszak T, et al. In vitro and in vivo antibacterial activity of environmental bacteriophages against Pseudomonas aeruginosa strains from cystic fibrosis patients. 2015;99(14):6021–6033.

 Google Scholar

Guang-Han O, et al. Experimental phage therapy for Burkholderia pseudomallei infection. 2016;11(7):e0158213.

 Google Scholar

Chhibber S, Gupta P, Kaur SJBM. Bacteriophage as effective decolonising agent for elimination of MRSA from anterior nares of BALB/c mice. 2014;14(1):212.

 Google Scholar

Abdulamir AS, et al. Novel approach of using a cocktail of designed bacteriophages against gut pathogenic E. colifor bacterial load biocontrol. 2014;13(1):39.

 Google Scholar

Kishor C, et al. Phage therapy of staphylococcal chronic osteomyelitis in experimental animal model. Indian J Med Res. 2016;143(1):87–94. .

 PubMedGoogle Scholar

Furusawa T, et al. Phage therapy is effective in a mouse model of bacterial equine keratitis. 2016;82(17):5332–5339.

 Google Scholar

Jeon J, et al. In vivo application of bacteriophage as a potential therapeutic agent to control OXA-66-like carbapenemase-producing Acinetobacter baumannii strains belonging to sequence type 357. 2016;82(14):4200–4208.

 Google Scholar

Wang Y, et al. Intranasal treatment with bacteriophage rescues mice from Acinetobacter baumannii-mediated pneumonia. 2016;11(5):631–641.

 Google Scholar

Yen M, Cairns LS, Camilli AJNC. A cocktail of three virulent bacteriophages prevents Vibrio cholerae infection in animal models. 2017;8(1):1–7.

 Google Scholar

Augustine J, Gopalakrishnan MV, Bhat SG. Application of ΦSP-1 and ΦSP-3 as a therapeutic strategy against Salmonella Enteritidis infection using Caenorhabditis elegans as model organism. J FEMS Microbio Letters. 2014;356(1):113–117.

 Google Scholar

Vieira A, et al. Phage therapy to control multidrug-resistant Pseudomonas aeruginosa skin infections: in vitro and ex vivo experiments. 2012;31(11):3241–3249.

 Google Scholar

Yin S, Huang G, Zhang Y, et al. Phage Abp1 rescues human cells and mice from infection by pan-drug resistant Acinetobacter Baumannii. Cell Physiol Biochem. 2017;44(6):2337–2345. .

 PubMedGoogle Scholar

Kumari S, Harjai K, Chhibber Sjtjoiidc. Topical treatment of Klebsiella pneumoniae B5055 induced burn wound infection in mice using natural products. 2010;4(6):367–377.

 Google Scholar

Wei C, et al. Developing a bacteriophage cocktail for biocontrol of potato bacterial wilt. Virol Sin. 2017;32(6):476–484. .

 Web of Science ®Google Scholar

Kocharunchitt C, Ross T, McNeil DL. Use of bacteriophages as biocontrol agents to control Salmonella associated with seed sprouts. Int J Food Microbiol. 2009;128(3):453–459.

 Web of Science ®Google Scholar

Elhalag K, et al. Potential use of soilborne lytic Podoviridae phage as a biocontrol agent against Ralstonia solanacearum. J Basic Microbiol. 2018;58(8):658–669. .

 Web of Science ®Google Scholar

Soleimani-Delfan A, et al. Isolation of Dickeya dadantii strains from potato disease and biocontrol by their bacteriophages. 2015;46(3):791–797.

 Google Scholar

Tan D, et al. Vibriophages differentially influence biofilm formation by Vibrio anguillarum strains. Appl Environ Microbiol. 2015;81(13):4489–4497.

 Google Scholar

Khairnar K, et al. Novel bacteriophage therapy for controlling metallo-beta-lactamase producing Pseudomonas aeruginosainfection in Catfish. BMC Vet Res. 2013;9(1):264. .

 Google Scholar

Christiansen RH, et al. Effect of bacteriophages on the growth of flavobacterium psychrophilum and development of phage-resistant strains. Microb Ecol. 2016;71(4):845–859.

 Web of Science ®Google Scholar

Silva YJ, et al. Phage therapy as an approach to prevent Vibrio anguillarum infections in fish larvae production. 2014;9(12):e114197.

 Google Scholar

Stalin N, Srinivasan P. Characterization of Vibrio parahaemolyticus and its specific phage from shrimp pond in Palk Strait, South East coast of India. Biologicals. 2016;44(6):526–533.

 PubMed Web of Science ®Google Scholar

Kittler S, et al. Effect of bacteriophage application on Campylobacter jejuni loads in commercial broiler flocks. 2013;79(23):7525–7533.

 Google Scholar

Lau GL, Sieo CC, Tan WS, et al. Characteristics of a phage effective for colibacillosis control in poultry. J Sci Food Agric. 2012;92(13):2657–2663. .

 Web of Science ®Google Scholar

Belgini DRB, et al. Culturable bacterial diversity from a feed water of a reverse osmosis system, evaluation of biofilm formation and biocontrol using phages. World J Microbiol Biotechnol. 2014;30(10):2689–2700. .

 Web of Science ®Google Scholar

Rodríguez-Rubio L, et al. Bacteriophage virion-associated peptidoglycan hydrolases: potential new enzybiotics. Crit Rev Microbiol. 2013;39(4):427–434. .

 PubMed Web of Science ®Google Scholar

Beims H, et al. Paenibacillus larvae-directed bacteriophage HB10c2 and its application in American foulbrood-affected honey bee larvae. 2015;81(16):5411–5419.

 Google Scholar

Maal KB, et al. Isolation and identification of two novel Escherichia Coli bacteriophages and their application in wastewater treatment and coliform’s phage therapy. 2015;8:3. J Jundishapur j microbio.

 Google Scholar

Bull JJ, Levin BR, DeRouin T, et al. Dynamics of success and failure in phage and antibiotic therapy in experimental infections. BMC Microbiol. 2002;2(1):35.

 Google Scholar

Ho YH, et al. Application of bacteriophage-containing aerosol against nosocomial transmission of carbapenem-resistant acinetobacter baumannii in an intensive care unit. PLoS One. 2016;11(12):e0168380. .

 PubMed Web of Science ®Google Scholar

Akimkin V, Shestopalov N, Shumilov V, et al. ICPIC, meeting abstracts from international conference on prevention & infection control (ICPIC 2017), biological disinfection with bacteriophages. Antimicrob Resist Infect Control. 2017;6(3):52.

 Google Scholar

O’flaherty S, et al. Potential of the polyvalent anti-Staphylococcus bacteriophage K for control of antibiotic-resistant staphylococci from hospitals. 2005;71(4):1836–1842.

 Google Scholar

Brown TL, et al. The formulation of bacteriophage in a semi solid preparation for control of propionibacterium acnes growth. PLoS One. 2016;11(3):e0151184. .

 PubMed Web of Science ®Google Scholar

Beckner M, Ivey ML, Phister TG. Microbial contamination of fuel ethanol fermentations. 2011;53(4):387–394.

 Google Scholar