Browse > Article
http://dx.doi.org/10.7853/kjvs.2011.34.4.341

Evaluation of bacteriophages for prevention and treatment of diarrhea due to experimental enterotoxigenic Escherichia coli K88 infection of weaned piglets  

Kim, Sung-Jae (College of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University)
Kim, Jin-Dong (Bio Business Unit, CJ ChilJedang Corp.)
Yang, Si-Yong (Bio Business Unit, CJ ChilJedang Corp.)
Kim, Nam-Hee (College of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University)
Lee, Chang-Hee (College of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University)
Yang, Don-Sik (College of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University)
Han, Jeong-Hee (College of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University)
Publication Information
Korean Journal of Veterinary Service / v.34, no.4, 2011 , pp. 341-352 More about this Journal
Abstract
Colibacillosis in pigs remain a major swine industry bruden worldwide. Although some progress has been made in treating collibacillosis in pigs by using biosecurity and antimicrobials, it still remain a considerable problem. The use of host-specific bateriophages as a biocontrol is one possible alternative. The purpose of this study was to evaluate the effect of bacteriophage against enterotoxigenic Escherichia coli (ETEC) K88 infection in piglets. Twenty-eight piglets were randomly divided into four groups and each group was allocated with 7 pigs. Group B, C and D were inoculated with 5 ml of ETEC K88 ($1{\times}10^8$ CFU/ml) per head of piglet via oral. Group C and D were fed with bacteriophages (Group C, $1.0{\times}10^6$ PFU/g; Group D, $1.0{\times}10^8$ PFU/g; CJ CheilJedang Corp., Korea) orally as treatment. In piglets administrated bacteriophages and challenged with ETEC K88 (Group C and D), Clinical signs and the growth performance were improved and antibody titers were maintained low level compared with piglets challenged with ETEC K88 (Group B, P<0.05). Group B were shown high pH in the alimentary tracts compared with other piglets (P<0.05). In quantitative analysis by real-time PCR, the results of Group C and D were lower than those Group B in faecal and intestinal samples (P<0.05). Severe villus atrophy and crypt hyperplasia were observed in Group B consequently V/C ratio increased, compared with other piglets. These results indicate that feeding with bacteriophage has effect to prevent ETEC K88 infection in piglets and suggest that use of bacteriophage can be considered a valid antibiotic alternative.
Keywords
Bacteriophage; Enterotoxigenic Escherichia coli (ETEC); Quantitative real-time PCR; Gastrointestinal pH; V/C ratio;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Mainil JG, Bex F, Jacquemin E, Pohl P, Couturier M, Kaeckenbeeck A. 1990. Prevalence of four enterotoxin (STaP, STaH, STb, and LT) and four adhesin subunit (K99, K88, 987P, and F41) genes among Escherichia coli isolates from cattle. Am J Vet Res 51: 187-190.
2 Matsuda T, Freeman TA, Hilbert DW, Duff M, Fuortes M, Stapleton PP, 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.   DOI   ScienceOn
3 Matsuzaki S, Rashel M, Uchiyama J, Sakurai S, Ujihara T, Kuroda M, Ikeuchi M, Tani T, Fujieda M, Wakiguchi H, Imai S. 2005. Bacteriophage therapy: a revitalized therapy against bacterial infectious diseases. J Infect Chemother 11: 211-219.   DOI   ScienceOn
4 Merril CR, Biswas B, Carlton R, Jensen NC, Creed GJ, Zullo S, Adhya S. 1996. Long-circulating bacteriophage as antibacterial agents. Proc Natl Acad Sci USA 93: 3188-3192.   DOI   ScienceOn
5 McEwan GT, Daniel H, Fett C, Burgess MN, Lucas ML. The effect of Escherichia coli STa enterotoxin and other secretagogues on mucosal surface pH of rat small intestine. Proc R Soc Lond B Biol Sci 234: 219-237.   DOI
6 Moon HW, Bunn TO. 1993. Vaccines for preventing enterotoxigenic Escherichia coli infections in farm animals. Vaccine 11: 213-220.   DOI   ScienceOn
7 Moon HW, Kohler EM, Schneider RA, Whipp SC. 1980. Prevalence of pilus antigens, enterotoxin types, and enteropathogenicity among K88-negative enterotoxigenic Escherichia coli from neonatal pigs. Infect Immun 27: 222-230.
8 Higgins JP, Higgins SE, Guenther KL, Huff W, Donoghue AM, Donoghue DJ, Hargis BM. 2005. Use of a specific bacteriophage treatment to reduce Salmonella in poultry products. Poult Sci 84: 1141-1145.   DOI
9 Ho DW, Field PR, Sjogren-Jansson E, Jeansson S, Cunningham AL. 1992. Indirect ELISA for the detection of HSV-2 specific IgG and IgM antibodies with glycoprotein G (gG-2). J Virol Methods 36: 249-264.   DOI   ScienceOn
10 Johnson RP, Gyles CL, Huff WE, Ojha S, Huff GR, Rath NC, Donoghue AM. 2008. Bacteriophages for prophylaxis and therapy in cattle, poultry and pigs. Anim Health Res Rev 9: 201-215.   DOI   ScienceOn
11 Kwon D, Kim O, Chae C. 1999. Prevalence of genotypes for fimbriae and enterotoxins and of O serogroups in Escherichia coli isolated from diarrheic piglets in Korea. J Vet Diagn Invest 11: 146-151.   DOI   ScienceOn
12 Lalles JP. 1993. Nutritional and antinutritional aspects of soybean and field pea proteins used in veal calf production: a review. Livest Prod Sci 34: 181-202.   DOI   ScienceOn
13 Lee CH, Adler-Nissen J, Barwald G. 1994. Improtance of lactic acid bacteria in non-diary food fermentation. pp. 8-25. In: Lee CH, Adler-Nissen J, Barwald G(ed.). Lactic acid fermentation of non-dairy food and beverages. Harn Lim Won, Seoul.
14 Lee SI, Kang SG, Kang ML, Yoo HS. 2008. Development of multiplex polymerase chain reaction assays for detecting enterotoxigenic Escherichia coli and their application to field isolates from piglets with diarrhea. J Vet Diagn Invest 20: 492-496.   DOI   ScienceOn
15 Loc Carrillo C, Atterbury RJ, el-Shibiny A, Connerton PL, Dillon E, Scott A, Connerton IF. 2005. Bacteriophage therapy to reduce Campylobacter jejuni colonization of broiler chickens. Appl Environ Microbiol 71: 6554-6563.   DOI   ScienceOn
16 Levine MM. 1987. Escherichia coli that cause diarrhea: Enterotoxigenic, enteropathogenic, enteroinvasive, enterohemorrhagic, and enteroadherent. J Infect Dis 155: 377-389.   DOI   ScienceOn
17 Li DF, Nelssen JL, Reddy PG, Blecha F, Hancock JD, Allee GL, Goodband RD, Klemm RD. 1990. Transient hypersensitivity to soybean meal in the early-weaned pig. J Anim Sci 68: 1790-1799.
18 Li X, Yin J, Li D, Chen X, Zang J, Zhou X. 2006. Dietary supplementation with zinc oxide increases IGF-I and IGF-I receptor gene expression in the small intestine of weanling piglets. J Nutr 136: 1786-1791.
19 Bertani G. 1953. Lysogenic versus lytic cycle of phage multiplication. Cold Spring Harb Symp Quant Biol 18: 65-70.   DOI   ScienceOn
20 Bertschinger HU, Bachmann M, Mettler C, Pospischil A, Schraner EM, Stamm M, Sydler T, Wild P. 1990. Adhesive fimbriae produced in vivo by Escherichia coli O139: K12 (B): H1 associated with enterotoxaemia in pigs. Vet Microbiol 25: 267-281.   DOI   ScienceOn
21 Biswas B, Adhya S, Washart P, Paul B, Trostel AN, Powell B, Carlton R, Merril CR. 2002. Bacteriophage therapy rescues mice bacteremic from a clinical isolate of vancomycin- resistant Enterococcus faecium. Infect Immun 70: 204-210.   DOI   ScienceOn
22 Bosi P, Casini L, Finamore A, Cremokolini C, Merialdi G, Trevisi P, Nobili F, Mengheri E. 2004. Spray-dried plasma improves growth performance and reduces inflammatory status of weaned pigs challenged with enterotoxigenic Escherichia coli K88. J Anim Sci 82: 1764-1772.
23 Brandtzaeg P. 2003. Role of secretory antibodies in the defence against infections. Int J Med Microbiol 293: 3-15.   DOI   ScienceOn
24 Demicheli V, Jefferson T. 1996. Economic aspects of vaccination. Vaccine 14: 941-943.   DOI   ScienceOn
25 Goode D, Allen VM, Barrow PA. 2003. Reduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophages. Appl Environ Microbiol 69: 5032-5036.   DOI   ScienceOn
26 Fairbrother JM, Nadeau E, Gyles CL. 2005. Escherichia coli in postweaning diarrhea in pigs: an update on bacterial types, pathogenesis, and prevention strategies. Anim Health Res Rev 6: 17-39.   DOI   ScienceOn
27 Fiorentin L, Vieira ND, Barioni W Jr. 2005. Oral treatment with bacteriophages reduces the concentration of Salmonella enteritidis PT4 in caecal contents of broilers. Avian Pathol 34: 258-263.   DOI   ScienceOn
28 Gill JJ, Pacan JC, Carson ME, Leslie KE, Griffiths MW, Sabour PM. 2006. Efficacy and pharmacokinetics of bacteriophage therapy in treatment of subclinical Staphylococcus aureus mastitis in lactating dairy cattle. Antimicrob Agents Chemother 50: 2912-2918.   DOI   ScienceOn
29 Guttman B, Raya R, Kutter E. 2005. Basic phage biology. pp. 29-66. In: Kutter E, Sulakvelidze A(ed.). Bacteriophages: biology and applications. CRC press, Boca Raton.
30 조미선, 한성경, 유지숙, 최지현, 구본철, 신명숙, 안종석, 이완규. 2008. 양돈사료 첨가용 김치 유산균의 효능. 한국임상수의학회지 25: 67-72.
31 Arqenzio RA, Southworth M. 1975. Sites of organic acid production and absorption in gastrointestinal tract of the pig. Am J Phys 228: 454-460.
32 Barrow P, Lovell M, Berchieri A Jr. 1998. Use of lytic bacteriophage for control of experimental Escherichia coli septicemia and meningitis in chickens and calves. Clin Vaccine Immunol 5: 294-298.
33 Barrow PA, Soothill JS. 1997. Bacteriophage therapy and prophylaxis: rediscovery and renewed assessment of potential. Trends Microbiol 5: 268-271.   DOI   ScienceOn
34 Berchieri A Jr, Lovell MA, Barrow PA. 1991. The activity in the chicken alimentary tract of bacteriophages lytic for Salmonella typhimurium. Res Microbiol 142: 541-549.   DOI   ScienceOn
35 Van den Broeck W, Cox E, Goddeeris B. 1999. Induction of immune responses in pigs following oral administration of purified F4 fimbriae. Vaccine 17: 2020-2029.   DOI   ScienceOn
36 Steffen E, Berg R. 1983. Relationship between cecal population levels of indigenous bacteria and translocation to the mesenteric lymph nodes. Infect Immun 39: 1252-1259.
37 Sulakvelidze A, Alavidze Z, Morris JG Jr. 2001. Bacteriophage therapy. Antimicrob Agents Chemother 45: 649-659.   DOI   ScienceOn
38 Toro H, Price S, McKee S, Hoerr F, Krehling J, Perdue M, Bauermeister L. 2005. Use of bacteriophages in combination with competitive exclusion to reduce Salmonella from infected chickens. Avian Dis 49: 118-124.   DOI   ScienceOn
39 Xie H, Zhuang X, Kong J, Ma G, Zhang H. 2005. Bacteriophage Esc-A is an efficient therapy for Escherichia coli 3-1 caused diarrhea in chickens. J Gen App Microbiol 51: 159-163.   DOI   ScienceOn
40 Yi GF, Carroll JA, Allee GL, Gaines AM, Kendall DC, Usry JL, Toride Y, Izuru S. 2005. Effect of glutamine and spray-dried plasma on growth performance, small intestinal morphology, and immune responses of Escherichia coli $K88^+$-challenged weaned pigs. J Anim Sci 83: 634-643.
41 Yin J, Li X, Li D, Yue T, Fang Q, Ni J, Zhou X, Wu G. 2009. Dietary supplementation with zinc oxide stimulates ghrelin secretion from the stomach of young pigs. J Nutr Biochem 20: 783-790.   DOI   ScienceOn
42 Nataro JP, Kaper JB. 1998. Diarrheagenic Escherichia coli. Clin Microbiol Rev 11: 142-201.
43 O'Flynn G, Coffey A, Fitzgerald G, Ross R. 2006. The newly isolated lytic bacteriophages st104a and st104b are highly virulent against Salmonella enterica. J Appl Microbiol 101: 251-259.   DOI   ScienceOn
44 Ramesh V, Fralick JA, Rolfe RD. 1999. Prevention of Clostridium difficile-induced ileocecitis with bacteriophage. Anaerobe 5: 69-78.   DOI   ScienceOn
45 Rao MC. 1985. Toxins which activate guanylate cyclase: heat-stable enterotoxins. Ciba Found Symp 112: 74-93.
46 Sherman DM, Acres SD, Sadowski PL, Springer JA, Bray B, Raybould TJ, Muscoplat CC. 1983. Protection of calves against fatal enteric colibacillosis by orally administered Escherichia coli K99-specific monoclonal antibody. Infect Immun 42: 653-658.
47 Rose R, Whipp SC, Moon HW. 1987. Effects of E. coli heat stable enterotoxin b on small intestinal villi in pigs, rabbits and lambs. Vet Pathol 24: 71-79.
48 Sarmiento JI, Casey TA, Moon HW. 1988. Postweaning diarrhea in swine: Experimental model of enterotoxigenic Escherichia coli infection. Am J Vet Res 49: 1154-1159.
49 Sasaki T, Fukami S, Namioka S. 1994. Enhancement of cytotoxic activity of lymphocytes in mice by oral administration of peptidoglycan (PG) derived from bifidobacterium thermophilum. J Vet Med Sci 56: 1129-1133.   DOI   ScienceOn
50 Smith HW. 1971. The bacteriology of the alimentary tract of domestic animals suffering from Escherichia coli infection. Ann N Y Acad Sci 176: 110-125.   DOI   ScienceOn
51 Smith HW. Huggins MB. 1982. Successful treatment of experimental Escherichia coli infections in mice using phage: Its general superiority over antibiotics. J Gen Microbiol 129: 307-318.