Korean Journal of Veterinary Research (대한수의학회지)

The Korean Society of Veterinary Science (대한수의학회)
권호 표지

Evaluation of in vitro and in vivo bacteriophage efficacy against Salmonella enterica serovar Enteritidis infection

Bacteriophage의 Salmonella enterica serovar Enteritidis에 대한 in vitro 및 in vivo 효능 평가

  • Cha, Seung-Bin (College of Veterinary Medicine, BK 21 for Veterinary Science and KRF Zoonotic Priority Research Institute, Seoul National University) ;
  • Rayamajhi, Nabin (College of Veterinary Medicine, BK 21 for Veterinary Science and KRF Zoonotic Priority Research Institute, Seoul National University) ;
  • Lee, Won-Jung (College of Veterinary Medicine, BK 21 for Veterinary Science and KRF Zoonotic Priority Research Institute, Seoul National University) ;
  • Shin, Min-Kyoung (College of Veterinary Medicine, BK 21 for Veterinary Science and KRF Zoonotic Priority Research Institute, Seoul National University) ;
  • Roh, Yu-Mi (College of Veterinary Medicine, BK 21 for Veterinary Science and KRF Zoonotic Priority Research Institute, Seoul National University) ;
  • Jung, Myung-Hwan (College of Veterinary Medicine, BK 21 for Veterinary Science and KRF Zoonotic Priority Research Institute, Seoul National University) ;
  • Myoung, Kil-Sun (R&D center, Korea Yakult) ;
  • Ahn, Young-Tae (R&D center, Korea Yakult) ;
  • Huh, Chul-Sung (R&D center, Korea Yakult) ;
  • Yoo, Han Sang (College of Veterinary Medicine, BK 21 for Veterinary Science and KRF Zoonotic Priority Research Institute, Seoul National University)
  • 차승빈 (서울대학교 수의과대학, BK21 수의과학인력양성 사업단, 중점연구소) ;
  • ;
  • 이원정 (서울대학교 수의과대학, BK21 수의과학인력양성 사업단, 중점연구소) ;
  • 신민경 (서울대학교 수의과대학, BK21 수의과학인력양성 사업단, 중점연구소) ;
  • 노유미 (서울대학교 수의과대학, BK21 수의과학인력양성 사업단, 중점연구소) ;
  • 정명환 (서울대학교 수의과대학, BK21 수의과학인력양성 사업단, 중점연구소) ;
  • 명길선 (한국 야쿠르트 R&D Center) ;
  • 안영태 (한국 야쿠르트 R&D Center) ;
  • 허철성 (한국 야쿠르트 R&D Center) ;
  • 유한상 (서울대학교 수의과대학, BK21 수의과학인력양성 사업단, 중점연구소)
  • Accepted : 2010.06.29
  • Published : 2010.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Salmonella (S.) Enterica infection ranks among the most common food borne bacterial infections worldwide. Although there are six subspecies of S. Enterica, the vast majority of human and animal infections are caused by strains belonging to subspecies 1 serovar Typhimurium and Enteritidis. Recent reports on antibiotic resistance of Salmonella spp. are rising steadily. The increasing problem of antibiotic resistance has rekindled interest in bacteriophage to therapy. Therefore, we investigated the efficacy of bacteriophage in S. enterica serovar Enteritidis infected mice and pigs by measuring of body condition, body weight, bacterial colonization and weight of organs based on the in vitro analysis. In vitro experiment, phage cultured with S. Enteritidis showed clear lysis pattern, the plaque forming unit (PFU) of our phage culture was $1.5{\times}10^{11}PFU/mL$, and phage showed its maximum activity at 4 h post inoculation. In mouse experiment, there was no significant difference among experimental groups in the general body conditions and body weight of mice. However, there was difference in weight of liver and spleen depending on the experimental group (p < 0.05). The weight of liver and spleen were reduced by the phage treatment. Also bacterial colonization in spleen and liver were significantly reduced by the phage treatment. In pig experiment, the general body conditions and body temperature exhibited not much difference among the pigs except few pigs in group 3 which showed poor body conditions. From the feces in each group, we could isolate the S. Enteritidis only from group 3. Bacterial enrichment culture was necessary for isolating the bacteria from 5 dpi and 10 dpi, however direct isolation was possible from 15 dpi feces. In phage treated group, postmortem lesion was better than non-phage treated group. Recently, antibiotic resistance concerns on the food-borne bacterial pathogens have been increasing because of the wide spread of the antibiotics resistance genes. This concern is widely transmitted to the human related public health. As one of the alternative treatments on the bacterial pathogens, attempt using phages have been made to control the bacterial diseases. The positive possibility of the trail using phage was observed to control the S. enterica serovar Enteritidis in this study even though the further analysis has been remained.

Keywords

References

  1. Atterbury RJ, Van Bergen MA, Ortiz F, Lovell MA, Harris JA, De Boer A, Wagenaar JA, Allen VM, Barrow PA. Bacteriophage therapy to reduce Salmonella colonization of broiler chickens. Appl Environ Microbiol 2007, 73, 4543-4549. https://doi.org/10.1128/AEM.00049-07
  2. Bertani G. Lysogenic versus lytic cycle of phage multiplication. Cold Spring Harb Symp Quant Biol 1953, 18, 65-70. https://doi.org/10.1101/SQB.1953.018.01.014
  3. Biswas B, Adhya S, Washart P, Paul B, Trostel AN, Powell B, Carlton R, Merril CR. Bacteriophage therapy rescues mice bacteremic from a clinical isolate of vancomycin-resistant Enterococcus faecium. Infect Immun 2002, 70, 204-210. https://doi.org/10.1128/IAI.70.1.204-210.2002
  4. Brussow H, Kutter E. Phage ecology. In: Kutter E, Sulakvelidze A (eds.). Bacteriophages: Biology and Applications. pp. 129-163, CRC Press, Boca Raton, 2005.
  5. Chernomordik AB. Bacteriophages and their therapeuticprophylactic use. Med Sestra 1989, 48, 44-47.
  6. Delpech V, McAnulty J, Morgan K. A salmonellosis outbreak linked to internally contaminated pork meat. Aust N Z J Public Health 1998, 22, 243-246. https://doi.org/10.1111/j.1467-842X.1998.tb01181.x
  7. d'Herelle F. Bacteriophage as a treatment in acute medical and surgical infections. Bull N Y Acad Med 1931, 7, 329-348.
  8. Fiorentin L, Vieira ND, Barioni W Jr. Oral treatment with bacteriophages reduces the concentration of Salmonella Enteritidis PT4 in caecal contents of broilers. Avian Pathol 2005, 34, 258-263. https://doi.org/10.1080/01445340500112157
  9. Foley SL, Lynne AM. Food animal-associated Salmonella challenges: pathogenicity and antimicrobial resistance. J Anim Sci 2008, 86 (Suppl), E173-187. https://doi.org/10.2527/jas.2007-0447
  10. Greer GG. Bacteriophage control of foodborne bacteria. J Food Prot 2005, 68, 1102-1111. https://doi.org/10.4315/0362-028X-68.5.1102
  11. Guttman B, Raya R, Kutter E. Basic phage biology. In: Kutter E, Sulakvelidze A (eds.). Bacteriophages: Biology and Applications. pp. 29-66, CRC Press, Boca Raton, 2005.
  12. Higgins JP, Higgins SE, Guenther KL, Huff W, Donoghue AM, Donoghue DJ, Hargis BM. Use of a specific bacteriophage treatment to reduce Salmonella in poultry products. Poult Sci 2005, 84, 1141-1145. https://doi.org/10.1093/ps/84.7.1141
  13. Hudson JA, Billington C, Carey-Smith G, Greening G. Bacteriophages as biocontrol agents in food. J Food Prot 2005, 68, 426-437. https://doi.org/10.4315/0362-028X-68.2.426
  14. Jansen A, Frank C, Stark K. Pork and pork products as a source for human salmonellosis in Germany. Berl Munch Tierarztl Wochenschr 2007, 120, 340-346.
  15. Johnson RP, Gyles CL, Huff WE, Ojha S, Huff GR, Rath NC, Donoghue AM. Bacteriophages for prophylaxis and therapy in cattle, poultry and pigs. Anim Health Res Rev 2008, 9, 201-215. https://doi.org/10.1017/S1466252308001576
  16. Jung BG, Toan NT, Cho SJ, Ko JH, Jung YK, Lee BJ. Dietary aluminosilicate supplement enhances immune activity in mice and reinforces clearance of porcine circovirus type 2 in experimentally infected pigs. Vet Microbiol 2010, 143, 117-125. https://doi.org/10.1016/j.vetmic.2009.11.009
  17. Kodama M, Oyama A, Takagi H. Control of interstitial pneumonia by drip infusion of megadose vitamin C, dehydroepiandrosterone and cortisol. A short review of our experience. In Vivo 2008, 22, 263-267.
  18. Kropinski AM. Phage therapy - Everything old is new again. Can J Infect Dis Med Microbiol 2006, 17, 297-306.
  19. Kudva IT, Jelacic S, Tarr PI, Youderian P, Hovde CJ. Biocontrol of Escherichia coli O157 with O157- specific bacteriophages. Appl Environ Microbiol 1999, 65, 3767-3773.
  20. Kwon HJ, Cho SH, Kim TE, Won YJ, Jeong J, Park SC, Kim JH, Yoo HS, Park YH, Kim SJ. Characterization of a T7-like lytic bacteriophage (phiSG-JL2) of Salmonella enterica serovar gallinarum biovar gallinarum. Appl Environ Microbiol 2008, 74, 6970-6979. https://doi.org/10.1128/AEM.01088-08
  21. Matsuzaki S, Rashel M, Uchiyama J, Sakurai S, Ujihara T, Kuroda M, Ikeuchi M, Tani T, Fujieda M, Wakiguchi H, Imai S. Bacteriophage therapy: a revitalized therapy against bacterial infectious diseases. J Infect Chemother 2005, 11, 211-219. https://doi.org/10.1007/s10156-005-0408-9
  22. 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, Imai S. Experimental protection of mice against lethal Staphylococcus aureus infection by novel bacteriophage phi MR11. J Infect Dis 2003, 187, 613-624. https://doi.org/10.1086/374001
  23. O'Flynn G, Coffey A, Fitzgerald GF, Ross RP. The newly isolated lytic bacteriophages st104a and st104b are highly virulent against Salmonella enterica. J Appl Microbiol 2006, 101, 251-259. https://doi.org/10.1111/j.1365-2672.2005.02792.x
  24. Parisien A, Allain B, Zhang J, Mandeville R, Lan CQ. Novel alternatives to antibiotics: bacteriophages, bacterial cell wall hydrolases, and antimicrobial peptides. J Appl Microbiol 2008, 104, 1-13.
  25. Payne RJ, Jansen VA. Pharmacokinetic principles of bacteriophage therapy. Clin Pharmacokinet 2003, 42, 315-325. https://doi.org/10.2165/00003088-200342040-00002
  26. Sheng H, Knecht HJ, Kudva IT, Hovde CJ. Application of bacteriophages to control intestinal Escherichia coli O157:H7 levels in ruminants. Appl Environ Microbiol 2006, 72, 5359-5366. https://doi.org/10.1128/AEM.00099-06
  27. Sillankorva S, Pleteneva E, Shaburova O, Santos S, Carvalho C, Azeredo J, Krylov V. Salmonella Enteritidis bacteriophage candidates for phage therapy of poultry. J Appl Microbiol 2010, 108, 1175-1186. https://doi.org/10.1111/j.1365-2672.2009.04549.x
  28. Smith HW, Huggins MB. Successful treatment of experimental Escherichia coli infections in mice using phage: its general superiority over antibiotics. J Gen Microbiol 1982, 128, 307-318.
  29. Sulakvelidze A, Alavidze Z, Morris JG Jr. Bacteriophage therapy. Antimicrob Agents Chemother 2001, 45, 649-659. https://doi.org/10.1128/AAC.45.3.649-659.2001
  30. Sulakvelidze A, Barrow P. Phage therapy in animals and agribusiness. In: Kutter E, Sulakvelidze A (eds.). Bacteriophages: Biology and Applications. pp. 335- 380, CRC Press, Boca Raton, 2005.
  31. Summers W. Bacteriophage research: early history. In: Kutter E, Sulakvelidze A (eds.). Bacteriophages: Biology and Applications. pp. 5-27, CRC Press, Boca Raton, 2005.
  32. Weber-Dabrowska B, Mulczyk M, Grski A. Bacteriophage therapy of bacterial infections: an update of our institute's experience. Arch Immunol Ther Exp (Warsz) 2000, 48, 547-551.