Ionophores: Their use as ruminant growth promotants and impact on food safety

Current Issues in Intestinal Microbiology

Volumn 4, Issue 2, 2003, Pages 43-51

  Callaway, T R ^a   Edrington, T S ^a   Rychlik, J L ^b   Genovese, K J ^a   Poole, T L ^a   Jung, Y S ^a   Bischoff, K M ^a   Anderson, R C ^a   Nisbet, David J ^a  

^a SOUTHERN PLAINS AGRICULTURAL RESEARCH CENTER   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; AVOPARCIN; BAMBERMYCIN; CARBON; GROWTH PROMOTOR; IONOPHORE; LAIDLOMYCIN; LASALOCID; MONENSIN; NARASIN; NITROGEN; SALINOMYCIN; VANCOMYCIN DERIVATIVE;

ANIMAL FOOD; ANIMAL HEALTH; ANTIBIOTIC PROPHYLAXIS; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; CATTLE FARMING; CELL MEMBRANE; COST BENEFIT ANALYSIS; DRUG COST; DRUG MECHANISM; ECOLOGY; ENERGY EXPENDITURE; ESCHERICHIA COLI; FOOD SAFETY; INTESTINE FLORA; ION TRANSPORT; NONHUMAN; SALMONELLA;

ANIMALS; ANIMALS, DOMESTIC; CATTLE; DRUG RESISTANCE; DRUG RESISTANCE, BACTERIAL; FOOD; FOOD ADDITIVES; GROWTH SUBSTANCES; IONOPHORES; RUMINANTS; SAFETY;

ANIMALIA; BACTERIA (MICROORGANISMS); BOS TAURUS; ESCHERICHIA COLI; SALMONELLA;

EID: 0141858773     PISSN: 1466531X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (88)

1. Aarestrup, F.M., Bager, F., Jensen, N.E., Madsen, M., Meyling, A., and Wegener, H.C. 1998. Surveillance of antimicrobial resistance in bacteria isolated from food animals to antimicrobial growth promoters and related therapeutic agents in Denmark. APMIS. 106: 606-622.
2. Aarestrup, F.M., Kruse, H., Tast, E., Hammerum, A.M., and Jensen, L.B. 2000. Associations between the use of antimicrobial agents for growth promotion and the occurence of resistance among Enterococcus faecium from broilers and pigs in Denmark, Finland, and Norway. Microb. Drug. Resis. 6: 63-70.
3. Ahmed, S., and Booth, I.R. 1981. Quantitative measurements of the proton-motive force and its relation to steady state lactose accumulation in Escherichia coli. Biochem. J. 200: 573-581.
4. APUA. 1999. Facts about antibiotics in animals and their impact on resistance. Alliance for the Prudent Use of Antibiotics. 23 October 2002. Available at: http://www.tufts.edu/med/apua/Ecology/faair.html.
5. Bartley, E.E., Nagaraja, T.G., Pressman, E.S., Dayton, A.D., Katz, M.P., and Fina, L.R. 1985. Effects of lasalocid or monensin on legume or grain (feedlot) bloat. J. Anim. Sci. 56: 1400-1406.
6. Bergen, W.G., and Bates, D.B. 1984. Ionophores: Their effect on production efficiency and mode of action. J. Anim. Sci. 58: 1465-1483.
7. Blaxter, K. 1962. The energy metabolism of ruminants. In: The energy metabolism of ruminants. K. Blaxter, ed. Charles C. Thomas, Springfield, IL. p. 197-200.
8. Bolhuis, H., Molenaar, D., Poelarends, G., van Veen, H.W., Poolman, B., Driessen, A.J., and Konings, W.N. 1994. Proton motive force-driven and ATP-dependent drug extrusion systems in multidrug-resistant Lactococcus lactis. J. Bacteriol. 176: 6957-6964.
9. Booth, I.R. 1985. Regulation of cytoplasmic pH in bacteria. Microbiol. Rev. 49: 359-378.
10. Borgen, K., Sorum, M., Wasteson, Y., and Kruse, H. 2001. VanA-type vancomycin-resistant Enterococci (VRE) remain prevalent in poultry carcasses 3 years after avoparcin was banned. Int. J. Food Microbiol. 64: 89-94.
11. Buchko, S.J., Holley, R.A., McAllister, T.A., McMahon, L.R., and Veira, D.M. 2000. Effect of monensin on E coli O157: H7 and E. coli ATCC 25922. Can. J. Anim. Sci. 80: 777.
12. Burrin, D.G., and Britton, R.A. 1986. Response to monensin in cattle during subacute acidosis in cattle. J. Anim. Sci. 63: 888-893.
13. Callaway, T.R., Adams, K.A., and Russell, J.B. 1999. The abilityof "low G+Cgram-positive" ruminal bacteria to resist monensin and counteract potassium depletion. Curr. Microbiol. 39: 226-230.
14. Callaway, T.R., Carneiro De Melo, A.M.S., and Russell, J.B. 1997. The effect of nisin and monensin on ruminal fermentation in vitro. Curr. Microbiol. 35: 90-96.
15. Callaway, T.R., and Russell, J.B. 1999. Selection of a highly monensin-resistant Prevotella bryantii subpopulation with altered outer membrane characteristics. Appl. and Environ. Microbiol. 65: 4753-4759.
16. Callaway, T.R., and Russell, J.B. 2000. Variations in the ability of ruminal gram-negative Prevotella species to resist monensin. Curr. Microbiol. 40: 185-189.
17. Chalupa, W. 1976. Degradation of amino acids by the mixed rumen microbial population. J. Anim. Sci. 43: 828-834.
18. Chen, G., and Russell, J.B. 1989. More monensin-sensitive, ammonia-producing bacteria from the rumen. Appl. Environ. Microbiol. 55: 1052-1057.
19. Chen, M., and Wolin, M.J. 1979. Effect of monensin and lasalocid-sodium on the growth of methanogenic and rumen saccharolytic bacteria. Appl. Enviro. Microbiol. 38: 72-77.
20. Chow, J.M., and Russell, J.B. 1990. Effect of ionophores and pH on growth of Streptococcus bovis in batch and continuous culture. Appl. Environ. Microbiol. 56: 1588-1593.
21. Chow, J.M., and Russell, J.B. 1992. Effect of pH and monensin on glucose transport by Fibrobacter succinogenes, a cellulolytic ruminal bacterium. Appl. Environ. Microbiol. 58: 1115-1120.
22. Chow, J.M., Van Kessel, J.A.S., and Russell, J.B. 1994. Binding of radiolabeled monensin and lasalocid to ruminal microorganisms and feed. J. Anim. Sci. 72: 1630-1635.
23. Czerkawski, J.W., Harfoot, C.G., and Breckenridge, G. 1972. The relationship between methane production and concentrations of hydrogen in the aqueous and gaseous phases during rumen fermentation in vitro. J. Appl. Bacteriol. 35: 537-551.
24. Dargatz, D.A., Wells, S.J., Thomas, L.A., Hancock, D.D., and Garber, L.P. 1997. Factors associated with the presence of Escherichia coli O157 in feces of feedlot cattle. J. Food Prot. 60: 466-470.
25. Dawson, K.A., and Boling, J.A. 1987. Effects of potassium ion concentrations on the antimicrobial activities of ionophores against ruminal anaerobes. Appl. Environ. Microbiol. 53: 2363-2367.
26. Dealy, J., and Moeller, M.W. 1976. Influence of bambermycins on Salmonella infection and antibiotic resistance in swine. J. Anim. Sci. 42: 1331-1336.
27. Dealy, J., and Moeller, M.W. 1977. Influence of bambermycins on Salmonella infection and antibiotic resistance in calves. J. Anim. Sci. 44: 734-738.
28. Dellinger, C.A., and Ferry, J.G. 1984. Effect of monensin on growth and methanogenesis of Methanobacterium formicicum. Appl. Environ. Microbiol. 48: 680-682.
29. Dennis, S.M., Nagaraja, T.G., and Bartley, E.E. 1981. Effects of lasalocid or monensin on lactate-producing or using rumen bacteria. J. Anim. Sci. 52: 418-426.
30. Dinius, D.A., Simpson, M.E., and Marsh, P.B. 1976. Effect of monensin fed with forage on digestion and the ruminal ecosystem of steers. J. Anim. Sci. 42: 229-234.
31. Edrington, T.S., Callaway, T.R., Bischoff, K.M., Genovese, K.J., Elder, R.O., Anderson, R.C., and Nisbet, D.J. 2003a. Effect of feeding the ionophores monensin and laidlomycin propionate and the antimicrobial bambermycin to sheep experimentally infected with E. coli O157: H7 and Salmonella Typhimurium. J. Anim. Sci. 81: 553-560.
32. Edrington, T.S., Callaway, T.R., Varey, P.D., Jung, Y.S., Bischoff, K.M., Elder, R.O., Anderson, R.C., Kutter, E., Brabban, A.D., and Nisbet, D.J. 2003b. Effects of the antibiotic ionophores monensin, lasalocid, laidlomycin propionate and bambermycin on Salmonella and E. coli 0157: H7 in vitro. J. Appl. Microbiol. 94: 207-213.
33. Federic, F., and Sokol, A. 1973. Effect of peroral application of a colicinogenic strain of Escherichia coli on the incidence of different categories of plasmids in Escherichia coli isolated from weaned piglets fed on flavomycin. Folia Microbiol. 18: 65.
34. Fridkin, S.K., Lawton, R., Edwards, J.R., Tenover, F.C., McGowan, J.E., and Gaynes, R.P. 2002. Monitoring antimicrobial use and resistance: comparison with a national benchmark on reducing vancomycin use and vancomycin-resistant Enterococci. Emerg. Infect. Dis. 8: 702-707.
35. Galyean, M.L., and Owens, F.N. 1988. Effects of monensin on growth, reproduction, and lactation in ruminants. In: ISI Atlas of Science: Anim. Plant Sci. ed. ISI Press, Philadelphia, PA. p. 71-75
36. Garber, L.P., Wells, S.J., Hancock, D.D., Doyle, M.P., Tuttle, J., Shere, J.A., and Zhao, T. 1995. Risk factors for fecal shedding of Escherichia coli O157: H7 in dairy calves. J. Amer. Vet. Med. Assoc. 207: 46-49.
37. Goodrich, R.D., Garrett, J.E., Gast, D.R., Kirick, M.A., Larson, D.A., and Meiske, J.C. 1984. Influence of monensin on the performance of cattle. J. Anim. Sci. 58: 1484-1498.
38. Griffin, P.M., and Tauxe, R.V. 1991. The epidemiology of infection caused by Escherichia coli O157: H7, other enterohemorrhagic E. coli, and the associated hemolytic uremic syndrome. Epidemiol. Rev. 13: 60-97.
39. Hegarty, R.S. 1999. Mechanisms for competitively reducing ruminal methanogenesis. Aust. J. Agric. Rev. 50: 1299-1305.
40. Herriott, D.E., Hancock, D.D., Ebel, E.D., Carpenter, L.V., Rice, D.H., and Besser, T.E. 1998. Association of herd management factors with colonization of dairy cattle by shiga toxin-positive Escherichia coli O157. J. Food Prot. 61: 802-807.
41. Honeyfield, D.C., Carlson, J.R., Nocerini, M.R., and Breeze, R.G. 1985. Duration and inhibition of 3-methylindole production by monensin. J. Anim. Sci. 60: 226-231.
42. Hooper, D.C. 2002. Fluoroquinolone resistance among Gram-positive cocci. Lancet. Infect. Dis. 2: 530-538.
43. Hungate, R.E. 1966. The rumen and its microbes. Academic Press, New York, NY.
44. Johnson, K.A., and Johnson, D.E. 1995. Methane emissions from cattle. J. Anim. Sci. 73: 2483-2494.
45. Kajikawa, H., and Russell, J.B. 1992. The effect of ionophores on proton flux in the ruminal bacterium, Streptococcus bovis. Curr. Microbiol. 25: 327-330.
46. Katz, M.P., Nagaraja, T.G., and Fina, L.R. 1986. Ruminal changes in monensin and lasalocid fed cattle grazing bloat provocative alfalfa pasture. J. Anim. Sci. 63: 1246-1257.
47. Krause, D.O., and Russell, J.B. 1996. An rRNA approach for assessing the role of obligate amino acid fermenting bacteria in ruminal amino acid degradation. Appl. Environ. Microbiol. 62: 815-821.
48. Lana, R.P., Fox, D.G., Russell, J.B., and Perry, T.C. 1997. Influence of monensis on holstein steers fed high-concentrate diets containing soybean meal or urea. J. Anim. Sci. 75: 2571-2579.
49. Lana, R.P., and Russell, J.B. 1996. Use of potassium depletion to assess adaption of ruminal bacteria to ionophores. Appl. Environ. Microbiol. 62: 4499-4503.
50. Lewis, K., Naroditskaya, V., Ferrante, A., and Fokina, I. 1994. Bacterial resistance to uncouplers. J. Bioenerg. Biomemb. 20: 639-646.
51. Losinger, W.C., Garber, L.P., Smith, M.A., Hurd, H.S., Biehl, L.G., Fedorka-Cray, P.J., Thomas, L.A., and Ferris, K. 1997. Management and nutritional factors associated with the detection of Salmonella sp. from cattle fecal specimens from feedlot operation in the United States. Prev. Vet. Med. 31: 231-244.
52. Mitchell, P. 1961. Coupling of phosphoprylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature. 191: 144-148.
53. Nagaraja, T.G., Avery, T.B., Bartley, E.E., Roof, S.K., and Dayton, A.D. 1982. Effect of lasalocid, monensin or thiopeptin on lactic acidosis in cattle. J. Anim. Sci. 54: 649-658.
54. Nagaraja, T.G., and Chengappa, M.M. 1998. Liver abscesses in feedlot cattle: A review. J. Anim. Sci. 76: 287-298.
55. Newbold, C.J., and Wallace, R.J. 1989. Changes in the rumen bacterium, Bacteroides ruminicola, grown in the presence of the ionophore, tetronasin. Asian Austral. J. Anim. Sci. 2: 452-453.
56. Newbold, C.J., Wallace, R.J., and Walker, N.D. 1993. The effect of tetronasin and monensin on fermentation, microbial numbers and the development of ionophore-resistant bacteria in the rumen. J. Appl. Bacteriol. 75: 129-134.
57. Owens, F.N. 1988. Protein metabolism of ruminant animals. In: The ruminant animal. D.C. Church, ed. Waveland Press, Prospect Heights, IL. p. 227-249
58. Paulsen, I.T., Brown, M.H., and Skurray, R.A. 1996. Proton-dependent multidrug efflux systems. Microbiol. Rev. 60: 575-608.
59. Perry, T.W., Shields, D.R., Dunn, W.J., and Mohler, M.T. 1983. Protein levels and monensin for growing and finishing steers. J. Anim. Sci. 57: 1067-1076.
60. Poos, M.I., Hanson, T.L., and Klopfenstein, T.J. 1979. Monensin effects on diet digestibility, ruminal protein bypass and microbial protein synthesis. J. Anim. Sci. 48: 1516-1524.
61. Potter, E.L., Cooley, C.O., Richardson, L.F., Raun, A.P., and Rathmacher, R.P. 1976a. Effect of monensin on performance of cattle fed forage. J. Anim. Sci. 43: 665-669.
62. Potter, E.L., Raun, A.P., Cooley, C.O., Rathmacher, R.P., and Richardson, L.F. 1976b. Effect of monensin on carcass characteristics, carcass composition and efficiency of converting feed to carcass. J. Anim. Sci. 43: 678-683.
63. Pressman 1976. Biological applications of ionophores. Ann. Rev. Biochem. 45: 501-530.
64. Rasmussen, M.A., Wickman, T.L., Cray, W.C., and Casey, T.A. 1999. Escherichia coli O157: H7 and the rumen environment. In: E. coli O157 in Farm Animals. C.S. Stewart and H.J. Flint, ed. CAB International, p. 39
65. Raun, A.P., Cooley, C.O., Potter, E.L., Rathmacher, R.P., and Richardson, L.F. 1976. Effect of monensin on feed efficiency of feedlot cattle. J. Anim. Sci. 43: 670-677.
66. Richardson, L.F., Raun, A.P., Potter, E.L., Cooley, C.O., and Rathmacher, R.P. 1976. Effect of monensin on rumen fermentation in vitro and in vivo. J. Anim. Sci. 43: 657-664.
67. Rogers, M., Jouany, J.P., Thivend, P., and Fontenot, J.P. 1997. The effects of short-term and long-term monensin supplementation, and its subsequent withdrawal on digestion in sheep. Anim. Feed Sci. Technol. 65: 113-127.
68. Rosen, B.P. 1986. Recent advances in bacterial ion transport. Ann. Rev. Microbiol. 40: 263-286.
69. Rumpler, W.V, Johnson, D.E., and Bates, D.B. 1986. The effect of high dietary cation concentration on methanogenesis by steers fed diets with and without ionophores. J. Anim. Sci. 62: 1737-1741.
70. Russell, J.B. 1987. A proposed mechanism of monensin action in inhibiting ruminal bacterial growth: effects on ion flux and protonmotive force. J. Anim. Sci. 64: 1519-1525.
71. Russell, J.B., and Rychlik, J.L. 2001. Factors that alter rumen microbial ecology. Science. 292: 1119-1122.
72. Russell, J.B., and Strobel, H.J. 1989. Effect of ionophores on ruminal fermentation. Appl. Environ. Microbiol. 55: 1-6.
73. Rychlik, J.L., and Russell, J.B. 2002. The adaptation and resistance of Clostridium aminophilum F to the butyrivibriocin-like substance of Butyrivibrio fibrisolvens JL5 and monensin. FEMS Microbiol. Left. 209: 93-98.
74. Saier, M.H., Paulsen, I.T., Sliwinski, M.K., Pao, S.S., Skurray, R.A., and Nikaido, H. 1998. Evolutionary origins of multidrug and drug-specific efflux pumps in bacteria. FASEB J. 12: 265-274.
75. Schnappinger, D., and Hillen, W. 1996. Tetracyclines: antibiotic action, uptake, and resistance mechanisms. Arch. Microbiol. 165: 359-369.
76. Shoemaker, N.B., Vlamakis, H., Hayes, K., and Salyers, A.A. 2001. Evidence for extensive resistance gene transfer among Bacteroides spp. and among Bacteroides and other genera in the human colon. Appl. and Environ. Microbiol. 67: 561-568.
77. Slyter, L.L. 1979. Monensin and dichloroacetamide influences on methane and volatile fatty acid production by rumen bacteria in vitro. Appl. Environ. Microbiol. 37: 283-288.
78. Sokol, A., Kremery, V., Federic, F., Fajtar, V., and Janouskova, J. 1973. The influence of flavomycin on the elimination of R-factors of Escherichia coli in vitro. Folia Microbiol. 18: 176.
79. Stahl, D.A., Flesher, B., Mansfield, H.R., and Montgomery, L. 1988. Use of phylogenetically based hybridization probes for studies of ruminal microbial ecology. Appl. Environ. Microbiol. 54: 1079-1084.
80. Steen, W., Gay, N., Boling, J.A., Bradley, N.W., McCormick, J.W., and Pendlum, L.C. 1978. Effect of monensin on performance and plasma metabolites in growing-finishing steers. J. Anim. Sci. 46: 350-355.
81. Stewart, C.S., and Bryant, M.P. 1988. The rumen microbial ecosystem. P.N. Hobson. Elsevier Science Publishers, Ltd, London, UK. p. 21.
82. Van Kessel, J.S., and Russell, J.B. 1992. Energetics of arginine and lysine transport by whole cells and membrane vesicles of strain SR, a monensin-sensitive ruminal bacterium. Appl. Environ. Microbiol. 58: 969-975.
83. Van Nevel, C.J., and Demeyer, D.I. 1977. Effect of monensin on rumen metabolism in vitro. Appl. Enviro. Microbiol. 34: 251-257.
84. Vogel, G. 1996. A review of large pen research trials. In: Scientific update on Rumensin/Tylan/Micotil for the professional feedlot consultant. ed. Elanco Animal Health, Indianapolis, IN. p. 16.
85. Wedegaertner, T.C., and Johnson, D.E. 1983. Monensin effects on digestibility, methanogenesis and heat uncrement of a cracked corn-silage diet fed to steers. J. Ani. Sci. 57: 168-177.
86. Woodford, N. 1998. Glycopeptide-resistant enterococci: a decade of experience. J. Med. Microbiol. 47: 849-862.
87. Yang, C.M.J., and Russell, J.B. 1993a. The effect of monensin supplementation on ruminal ammonia accumulation in vivo and the numbers of amino acid-fermenting bacteria. J. Anim. Sci. 71: 3470-3476.
88. Yang, M.J., and Russell, J.B. 1993b. Effect of monensin on the specific activity of ammonia production by ruminal bacteria and disappearance of amino nitrogen from the rumen. Appl. Envir. Microbiol. 59: 3250-3254.