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Bacteriophages for prophylaxis and therapy in cattle, poultry and pigs

Published online by Cambridge University Press:  22 December 2008

R. P. Johnson ,
C. L. Gyles ,
W. E. Huff ,
S. Ojha ,
G. R. Huff ,
N. C. Rath  and
A. M. Donoghue
R. P. Johnson*
Affiliation:
Public Health Agency of Canada, Laboratory for Foodborne Zoonoses, Guelph, Ontario, N1G 3W4, Canada
C. L. Gyles
Affiliation:
Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, Ontario, N1G 2W1, Canada
W. E. Huff
Affiliation:
USDA, ARS, Poultry Production and Product Safety Research Unit, Poultry Science Center, University of Arkansas, Fayetteville, AR7270, USA
S. Ojha
Affiliation:
Public Health Agency of Canada, Laboratory for Foodborne Zoonoses, Guelph, Ontario, N1G 3W4, Canada
G. R. Huff
Affiliation:
USDA, ARS, Poultry Production and Product Safety Research Unit, Poultry Science Center, University of Arkansas, Fayetteville, AR7270, USA
N. C. Rath
Affiliation:
USDA, ARS, Poultry Production and Product Safety Research Unit, Poultry Science Center, University of Arkansas, Fayetteville, AR7270, USA
A. M. Donoghue
Affiliation:
USDA, ARS, Poultry Production and Product Safety Research Unit, Poultry Science Center, University of Arkansas, Fayetteville, AR7270, USA
*
*Corresponding author. E-mail: roger_johnson@phac-aspc.gc.ca
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Abstract

The successful use of virulent (lytic) bacteriophages (phages) in preventing and treating neonatal enterotoxigenic Escherichia coli infections in calves, lambs and pigs has prompted investigation of other applications of phage therapy in food animals. While results have been very variable, some indicate that phage therapy is potentially useful in virulent Salmonella and E. coli infections in chickens, calves and pigs, and in control of the food-borne pathogens Salmonella and Campylobacter jejuni in chickens and E. coli O157:H7 in cattle. However, more rigorous and comprehensive research is required to determine the true potential of phage therapy. Particular challenges include the selection and characterization of phages, practical modes of administration, and development of formulations that maintain the viability of phages for administration. Also, meaningful evaluation of phage therapy will require animal studies that closely represent the intended use, and will include thorough investigation of the emergence and characteristics of phage resistant bacteria. As well, effective use will require understanding the ecology and dynamics of the endemic and therapeutic phages and their interactions with target bacteria in the farm environment. In the event that the potential of phage therapy is realized, adoption will depend on its efficacy and complementarity relative to other interventions. Another potential challenge will be regulatory approval.

Keywords

Escherichia coliSalmonellaCampylobacterStaphylococcusO157:H7bacteriophagebacteriophage therapy
Type
Review Article
Information
Animal Health Research Reviews , Volume 9 , Issue 2: Symposium on Antimicrobial Resistance in Bacteria from Animals , December 2008 , pp. 201 - 215
Copyright
Copyright © Cambridge University Press 2008

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References

Andreatti Filho, RL, Higgins, JP, Higgins, SE, Gaona, G, Wolfenden, AD, Tellez, G and Hargis, BM (2007). Ability of bacteriophages isolated from different sources to reduce Salmonella enterica serovar enteritidis in vitro and in vivo. Poultry Science 86: 1904–1909.CrossRefGoogle ScholarPubMed
Atterbury, RJ, Dillon, E, Swift, C, Connerton, PL, Frost, JA, Dodd, CE, Rees, CE and Connerton, IF (2005). Correlation of Campylobacter bacteriophage with reduced presence of hosts in broiler chicken ceca. Applied and Environmental Microbiology 71: 4885–4887.CrossRefGoogle ScholarPubMed
Atterbury, RJ, Van Bergen, MA, Ortiz, F, Lovell, MA, Harris, JA, De Boer, A, Wagenaar, JA, Allen, VM and Barrow, PA (2007). Bacteriophage therapy to reduce Salmonella colonization of broiler chickens. Applied and Environmental Microbiology 73: 4543–4549.CrossRefGoogle ScholarPubMed
Bach, SJ, McAllister, TA, Veira, DM, Gannon, VPJ and Holly, RA (2008). Effect of bacteriophage DC22 on Escherichia coli O157:H7 in an artificial rumen system (Rusitec) and inoculated sheep. Annual Review of Microbiology 52: 89–101.Google Scholar
Barnes, JH, Vaillancourt, JP and Gross, WB (2003). Colibacillosis. In: Saif, YM (ed.) Diseases of Poultry. Ames, IA: Iowa State University Press, pp. 631–656.Google Scholar
Barrow, P, Lovell, M and Berchieri, A (1998). Use of lytic bacteriophage for control of experimental Escherichia coli septicemia and meningitis in chickens and calves. Clinical and Diagnostic Laboratory Immunology 5: 294–298.CrossRefGoogle ScholarPubMed
Barrow, PA (2001). The use of bacteriophages for treatment and prevention of bacterial disease in animals and animal models of human infection. Journal of Chemical Technology and Biotechnology 76: 677–682.CrossRefGoogle Scholar
Berchieri, A Jr, Lovell, MA and Barrow, PA (1991). The activity in the chicken alimentary tract of bacteriophages lytic for Salmonella typhimurium. Research in Microbiology 142: 541–549.CrossRefGoogle ScholarPubMed
Besser, TE, Hancock, DD, Pritchett, LC, McRae, EM, Rice, DH and Tarr, PI (1997). Duration of detection of fecal excretion of Escherichia coli O157:H7 in cattle. Journal of Infectious Diseases 175: 726–729.CrossRefGoogle ScholarPubMed
Biswas, B, Adhya, S, Washart, P, Paul, B, Trostel, AN, Powell, B, Carlton, R and Merril, CR (2002). Bacteriophage therapy rescues mice bacteremic from a clinical isolate of vancomycin-resistant Enterococcus faecium [erratum appears in Infection and Immunity 2002;70(3):1664]. Infection and Immunity 70: 204–210.CrossRefGoogle Scholar
Boerlin, P, Travis, R, Gyles, CL, Reid-Smith, R, Janecko, N, Lim, H, Nicholson, V, McEwen, SA, Friendship, R and Archambault, M (2005). Antimicrobial resistance and virulence genes of Escherichia coli isolates from swine in Ontario. Applied and Environmental Microbiology 71: 6753–6761.CrossRefGoogle ScholarPubMed
Brüssow, H and Kutter, E (2005) Phage Ecology. In: Kutter, E and Sulakvelidze, A (eds) Bacteriophages Biology and Applications. Boca Raton, FL: CRC Press, pp. 129–163.Google Scholar
Callaway, TR, Edrington, TS, Brabban, AD, Anderson, RC, Rossman, ML, Engler, MJ, Carr, MA, Genovese, KJ, Keen, JE, Looper, ML, Kutter, EM and Nisbet, DJ (2008). Bacteriophage isolated from feedlot cattle can reduce Escherichia coli O157:H7 populations in ruminant gastrointestinal tracts. Foodborne Pathogens and Disease 5: 183–191.CrossRefGoogle ScholarPubMed
Carlton, RM, Noordman, WH, Biswas, B, de Meester, ED and Loessner, MJ (2005). Bacteriophage P100 for control of Listeria monocytogenes in foods: genome sequence, bioinformatic analyses, oral toxicity study, and application. Regulatory Toxicology and Pharmacology 43: 301–312.CrossRefGoogle ScholarPubMed
Chibani-Chennoufi, S, Bruttin, A, Dillmann, ML and Brussow, H (2004). Phage–host interaction: an ecological perspective. Journal of Bacteriology 186: 3677–3686.CrossRefGoogle ScholarPubMed
Connerton, IF, Connerton, PL, Barrow, P, Seal, BS and Atterbury, RJ (2008). Bacteriophage therapy and Campylobacter. In: Nachamkin, I, Szymanski, CM and Blaser, MJ (eds) Campylobacter. Washington, DC: ASM Press, pp. 679–693.Google Scholar
Connerton, PL, Loc Carrillo, CM, Swift, C, Dillon, E, Scott, A, Rees, CE, Dodd, CE, Frost, J and Connerton, IF (2004). Longitudinal study of Campylobacter jejuni bacteriophages and their hosts from broiler chickens. Applied and Environmental Microbiology 70: 3877–3883.CrossRefGoogle ScholarPubMed
d'Herelle, F (1917). Sur un microbe invisible antagoniste des bacilles dysentériques. Comptes rendus Académie Sciences 165: 373–375.Google Scholar
Fiorentin, L, Vieira, ND and Barioni, W Jr (2005). Oral treatment with bacteriophages reduces the concentration of Salmonella enteritidis PT4 in caecal contents of broilers. Avian Pathology 34: 258–263.CrossRefGoogle ScholarPubMed
Fischetti, VA (2005). Bacteriophage lytic enzymes: novel anti-infectives. Trends in Microbiology 13: 491–496.CrossRefGoogle ScholarPubMed
Gannon, VP, Graham, TA, King, R, Michel, P, Read, S, Ziebell, K and Johnson, RP (2002). Escherichia coli O157:H7 infection in cows and calves in a beef cattle herd in Alberta, Canada. Epidemiology and Infection 129: 163–172.CrossRefGoogle Scholar
Gill, JJ, Pacan, JC, Carson, ME, Leslie, KE, Griffiths, MW and Sabour, PM (2006a). Efficacy and pharmacokinetics of bacteriophage therapy in treatment of subclinical Staphylococcus aureus mastitis in lactating dairy cattle. Antimicrobial Agents and Chemotherapeutics 50: 2912–2918.CrossRefGoogle ScholarPubMed
Gill, JJ, Sabour, PM, Leslie, KE and Griffiths, MW (2006b). Bovine whey proteins inhibit the interaction of Staphylococcus aureus and bacteriophage K. Journal of Applied Microbiology 101: 377–386.CrossRefGoogle ScholarPubMed
Greer, GG (2005). Bacteriophage control of foodborne bacteria. Journal of Food Protection 68: 1102–1111.CrossRefGoogle Scholar
Guttman, B, Raya, R and Kutter, E (2005). Basic phage biology. In: Kutter, E and Sulakvelidze, A (eds) Bacteriophages Biology and Applications. Boca Raton, FL: CRC Press, pp. 29–66.Google Scholar
Hagens, S and Loessner, MJ (2007). Application of bacteriophages for detection and control of foodborne pathogens. Applied Microbiology and Biotechnology 76: 513–519.CrossRefGoogle ScholarPubMed
Hansen, VM, Rosenquist, H, Baggesen, DL, Brown, S and Christensen, BB (2007). Characterization of Campylobacter phages including analysis of host range by selected Campylobacter Penner serotypes. BMC Microbiology 7: 90.CrossRefGoogle ScholarPubMed
Harris, DL and Lee, N (2003). Compositions and methods for reducing the amount of Salmonella in livestock. US Patent No. 6,656,463.Google Scholar
Higgins, JP, Higgins, SE, Guenther, KL, Huff, W, Donoghue, AM, Donoghue, DJ and Hargis, BM (2005). Use of a specific bacteriophage treatment to reduce Salmonella in poultry products. Poultry Science 84: 1141–1145.CrossRefGoogle ScholarPubMed
Hudson, JA, Billington, C, Carey-Smith, G and Greening, G (2005). Bacteriophages as biocontrol agents in food. Journal of Food Protection 68: 426–437.CrossRefGoogle ScholarPubMed
Huff, WE, Huff, GR, Rath, NC, Balog, JM, Xie, H, Moore, PA Jr and Donoghue, AM (2002a). Prevention of Escherichia coli respiratory infection in broiler chickens with bacteriophage (SPR02). Poultry Science 81: 437–441.CrossRefGoogle ScholarPubMed
Huff, WE, Huff, GR, Rath, NC, Balog, JM and Donoghue, AM (2002b). Prevention of Escherichia coli infection in broiler chickens with a bacteriophage aerosol spray. Poultry Science 81: 1486–1491.CrossRefGoogle ScholarPubMed
Huff, WE, Huff, GR, Rath, NC, Balog, JM and Donoghue, AM (2003a). Evaluation of aerosol spray and intramuscular injection of bacteriophage to treat an Escherichia coli respiratory infection. Poultry Science 82: 1108–1112.CrossRefGoogle ScholarPubMed
Huff, WE, Huff, GR, Rath, NC, Balog, JM and Donoghue, AM (2003b). Bacteriophage treatment of a severe Escherichia coli respiratory infection in broiler chickens. Avian Diseases 47: 1399–1405.CrossRefGoogle ScholarPubMed
Huff, WE, Huff, GR, Rath, NC, Balog, JM and Donoghue, AM (2004). Therapeutic efficacy of bacteriophage and Baytril (enrofloxacin) individually and in combination to treat colibacillosis in broilers. Poultry Science 83: 1944–1947.CrossRefGoogle ScholarPubMed
Jamalludeen, N, Johnson, RP, Friendship, R, Kropinski, AM, Lingohr, EJ and Gyles, CL (2007). Isolation and characterization of nine bacteriophages that lyse O149 enterotoxigenic Escherichia coli. Veterinary Microbiology 124: 47–57.CrossRefGoogle ScholarPubMed
Jamalludeen, N, Kropinski, AM, Johnson, RP, Lingohr, E, Harel, J and Gyles, CL (2008). Complete genomic sequence of bacteriophage phiEcoM-GJ1, a novel phage that has myovirus morphology and a podovirus-like RNA polymerase. Applied and Environmental Microbiology 74: 516–525.CrossRefGoogle Scholar
Jorgensen, F, Bailey, R, Williams, S, Henderson, P, Wareing, DR, Bolton, FJ, Frost, JA, Ward, L and Humphrey, TJ (2002). Prevalence and numbers of Salmonella and Campylobacter spp. on raw, whole chickens in relation to sampling methods. International Journal of Food Microbiology 76: 151–164.CrossRefGoogle ScholarPubMed
Kallings, LO (1967). Sensitivity of various Salmonella strains to felix 0–1 phage. Acta Pathologica et Microbiologica Scandinavica 70: 446–454.CrossRefGoogle ScholarPubMed
Kropinski, AM (2006). Phage therapy – everything old is new again. Canadian Journal of Infectious Diseases and Medical Microbiology 17: 297–306.CrossRefGoogle Scholar
Kudva, IT, Jelacic, S, Tarr, PI, Yourderian, P and Hovde, CJ (1999). Biocontrol of Escherichia coli O157 with O157-specific bacteriophages. Applied and Environmental Microbiology 65: 3767–3773.CrossRefGoogle ScholarPubMed
Laegreid, WW, Elder, RO and Keen, JE (1999). Prevalence of Escherichia coli O157:H7 in range beef calves at weaning. Epidemiology and Infection 123: 291–298.CrossRefGoogle ScholarPubMed
Lee, JH (2003). Methicillin (oxacillin)-resistant Staphylococcus aureus strains isolated from major food animals and their potential transmission to humans. Applied and Environmental Microbiology 69: 6489–6494.CrossRefGoogle ScholarPubMed
Lee, N and Harris, DL (2001). The Effect of Bacteriophage Treatment as a Preharvest Intervention Strategy to Reduce the Rapid Dissemination of Salmonella typhimurium in Pigs. American Association of Swine Veterinarians (AASV), Perry, IA: AASV, p. 555.Google Scholar
Loc Carillo, C, Atterbury, RJ, el Shibiny, A, Connerton, PL, Dillon, E, Scott, A and Connerton, IF (2005). Bacteriophage therapy to reduce Campylobacter jejuni colonization of broiler chickens. Applied and Environmental Microbiology 71: 6554–6563.CrossRefGoogle Scholar
Luby, CD and Middleton, JR (2005). Efficacy of vaccination and antibiotic therapy against Staphylococcus aureus mastitis in dairy cattle. Veterinary Record 157: 89–90.CrossRefGoogle ScholarPubMed
Ma, Y, Pacan, JC, Wang, Q, Xu, Y, Huang, X, Korenevsky, A and Sabour, PM (2008). Microencapsulation of bacteriophage felix O1 into chitosan-alginate microspheres for oral delivery. Applied and Environmental Microbiology 74: 4799–4805.CrossRefGoogle ScholarPubMed
Makovec, JA and Ruegg, PL (2003). Antimicrobial resistance of bacteria isolated from dairy cow milk samples submitted for bacterial culture: 8,905 samples (1994–2001). Journal of the American Veterinary Medical Association 222: 1582–1589.CrossRefGoogle Scholar
Matsuda, T, Freeman, TA, Hilbert, DW, Duff, M, Fuortes, M, Stapleton, PP and Daly, JM (2005). Lysis-deficient bacteriophage therapy decreases endotoxin and inflammatory mediator release and improves survival in a murine peritonitis model. Surgery 137: 639–646.CrossRefGoogle Scholar
Matsuzaki, S, Yasuda, M, Nishikawa, H, Kuroda, M, Ujihara, T, Shuin, T, Shen, Y, Jin, Z, Fujimoto, S, Nasimuzzaman, MD, Wakiguchi, H, Sugihara, S, Sugiura, T, Koda, S, Muraoka, A and Imai, S (2003). Experimental protection of mice against lethal Staphylococcus aureus infection by novel bacteriophage phi MR11. Journal of Infectious Diseases 187: 613–624.CrossRefGoogle ScholarPubMed
Matthews, L, McKendrick, IJ, Ternent, H, Gunn, GJ, Synge, B and Woolhouse, ME (2006). Super-shedding cattle and the transmission dynamics of Escherichia coli O157. Epidemiology and Infection 134: 131–142.CrossRefGoogle ScholarPubMed
Maynard, C, Fairbrother, JM, Bekal, S, Sanschagrin, F, Levesque, RC, Brousseau, R, Masson, L, Lariviere, S and Harel, J (2003). Antimicrobial resistance genes in enterotoxigenic Escherichia coli O149:K91 isolates obtained over a 23-year period from pigs. Antimicrobial Agents and Chemotherapeutics 47: 3214–3221.CrossRefGoogle Scholar
Mizoguchi, K, Morita, M, Fischer, CR, Yoichi, M, Tanji, Y and Unno, H (2003). Coevolution of bacteriophage PP01 and Escherichia coli O157:H7 in continuous culture. Applied and Environmental Microbiology 69: 170–176.CrossRefGoogle ScholarPubMed
Naylor, SW, Low, JC, Besser, TE, Mahajan, A, Gunn, GJ, Pearce, MC, McKendrick, IJ, Smith, DG and Gally, DL (2003). Lymphoid follicle-dense mucosa at the terminal rectum is the principal site of colonization of enterohemorrhagic Escherichia coli O157:H7 in the bovine host. Infection and Immunity 71: 1505–1512.CrossRefGoogle ScholarPubMed
Niu, YD, Xu, Y, McAllister, TA, Rozema, EA, Stephens, TP, Bach, SJ, Johnson, RP and Stanford, K (2008). Comparison of fecal versus rectoanal mucosal swab sampling for detecting Escherichia coli O157:H7 in experimentally inoculated cattle used in assessing bacteriophage as a mitigation strategy. Journal of Food Protection 71: 691–698.CrossRefGoogle ScholarPubMed
Oot, RA, Raya, RR, Callaway, TR, Edrington, TS, Kutter, EM and Brabban, AD (2007). Prevalence of Escherichia coli O157 and O157:H7-infecting bacteriophages in feedlot cattle feces. Letters in Applied Microbiology 45: 445–453.CrossRefGoogle ScholarPubMed
Parisien, A, Allain, B, Zhang, J, Mandeville, R and Lan, CQ (2008). Novel alternatives to antibiotics: bacteriophages, bacterial cell wall hydrolases, and antimicrobial peptides. Journal of Applied Microbiology 104: 1–13.Google ScholarPubMed
Payne, RJ and Jansen, VA (2003). Pharmacokinetic principles of bacteriophage therapy. Clinical Pharmacokinetics 42: 315–325.CrossRefGoogle ScholarPubMed
Piercy, DW and West, B (1976). Experimental Escherichia coli infection in broiler chickens: course of the disease induced by inoculation via the air sac route. Journal of Comparative Pathology 86: 203–210.CrossRefGoogle ScholarPubMed
Rangel, JM, Sparling, PH, Crowe, C, Griffin, PM and Swerdlow, DL (2005). Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982–2002. Emerging Infectious Diseases 11: 603–609.CrossRefGoogle ScholarPubMed
Raya, RR, Varey, P, Oot, RA, Dyen, MR, Callaway, TR, Edrington, TS, Kutter, EM and Brabban, AD (2006). Isolation and characterization of a new T-even bacteriophage, CEV1, and determination of its potential to reduce Escherichia coli O157:H7 levels in sheep. Applied and Environmental Microbiology 72: 6405–6410.CrossRefGoogle ScholarPubMed
Rosenquist, H, Nielsen, NL, Sommer, HM, Norrung, B and Christensen, BB (2003). Quantitative risk assessment of human Campylobacteriosis associated with thermophilic Campylobacter species in chickens. International Journal of Food Microbiology 83: 87–103.CrossRefGoogle ScholarPubMed
Sheng, H, Knecht, HJ, Kudva, IT and Hovde, CJ (2006). Application of bacteriophages to control intestinal Escherichia coli O157:H7 levels in ruminants. Applied and Environmental Microbiology 72: 5359–5366.CrossRefGoogle ScholarPubMed
Sklar, IB and Joerger, RD (2001). Attempts to utilize bacteriophage to combat Salmonella enterica serovar Enteritidis infection in chickens. Journal of Food Safety 21: 15–29.CrossRefGoogle Scholar
Smith, HW and Huggins, MB (1982). Successful treatment of experimental Escherichia coli infections in mice using phage: its general superiority over antibiotics. Journal of General Microbiology 128: 2–18.Google ScholarPubMed
Smith, HW and Huggins, MB (1983). Effectiveness of phages in treating experimental Escherichia coli diarrhoea in calves, piglets and lambs. Journal of General Microbiology 129: 2659–2675.Google ScholarPubMed
Smith, HW, Huggins, MB and Shaw, KM (1987a). The control of experimental Escherichia coli diarrhoea in calves by means of bacteriophages. Journal of General Microbiology 133: 1111–1126.Google ScholarPubMed
Smith, HW, Huggins, MB and Shaw, KM (1987b). Factors influencing the survival and multiplication of bacteriophages in calves and in their environment. Journal of General Microbiology 133: 1127–1135.Google ScholarPubMed
Sulakvelidze, A and Barrow, P (2005). Phage therapy in animals and agribusiness. In: Kutter, E and Sulakvelidze, A (eds) Bacteriophages Biology and Application. Boca Raton, FL: CRC Press, pp. 335–380.Google Scholar
Sulakvelidze, A, Alavidze, Z and Morris, JG Jr (2001). Bacteriophage therapy. Antimicrobial Agents and Chemotherapy 45: 649–659.CrossRefGoogle ScholarPubMed
Summers, W (2005). Bacteriophage research: early history. In: Kutter, E and Sulakvelidze, A (eds) Bacteriophages Biology and Applications. Boca Raton, FL: CRC Press, pp. 5–27.Google Scholar
Taylor, WI and Silliker, JH (1958). Hatching of eggs. U.S. Patent No. 2,851,006.Google Scholar
Toro, H, Price, SB, McKee, AS, Hoerr, FJ, Krehling, J, Perdue, M and Bauermeister, L (2005). Use of bacteriophages in combination with competitive exclusion to reduce Salmonella from infected chickens. Avian Diseases 49: 118–124.CrossRefGoogle ScholarPubMed
Twort, FW (1915). An investigation on the nature of the ultramicroscopic viruses. Lancet 189: 1241–1243.CrossRefGoogle Scholar
Van den Bogaard, AE and Stobberingh, EE (2000). Epidemiology of resistance to antibiotics links between animals and humans. International Journal of Antimicrobial Agents 14: 327–335.CrossRefGoogle Scholar
Viscardi, M, Perugini, AG, Auriemma, C, Capuano, F, Morabito, S, Kim, KP, Loessner, MJ and Iovane, G (2008). Isolation and characterisation of two novel coliphages with high potential to control antibiotic-resistant pathogenic Escherichia coli (EHEC and EPEC). International Journal of Antimicrobial Agents 31: 152–157.CrossRefGoogle ScholarPubMed
Waddell, T, Mazzocco, A, Johnson, RP, Pacan, J, Campbell, S, Perets, A, MacKinnon, J, Holtslander, B and Poppe, C (2000). Control of Escherichia coli O157:H7 infection of calves by bacteriophages. In: Proceedings of the 4th International Symposium and Workshop on Shiga toxin (verocytotoxin)-producing Escherichia coli (VTEC 2000) Kyoto, Japan. 29 October–2 November 2000 [abstract].Google Scholar
Waddell, TE, Johnson, RP and Mazzocco, A (2004). Methods and compositions for controlled release of bioactive compounds. U.S. Patent Application No. 60/463,319.Google Scholar
Wagenaar, JA, Van Bergen, MA, Mueller, MA, Wassenaar, TM, Carlton, RM (2005). Phage therapy reduces Campylobacter jejuni colonization in broilers. Veterinary Microbiology 109: 275–283.CrossRefGoogle ScholarPubMed
Weber-Dabrowska, B, Mulczyk, M and Gorski, A (2000). Bacteriophage therapy of bacterial infections: an update of our institute's experience. Archivum Immunologiae et Therapiae Experimentalis 48: 547–551.Google ScholarPubMed
Yoichi, M, Morita, M, Mizoguchi, K, Fischer, CR and Tanji, Y (2004). The criterion for selecting effective phage for Escherichia coli control. Biochemical Engineering Journal 19: 221–227.CrossRefGoogle Scholar