Effects of thymol and diphenyliodonium chloride against Campylobacter spp. during pure and mixed culture in vitro

Journal of Applied Microbiology

Volumn 107, Issue 4, 2009, Pages 1258-1268

  Anderson, R C ^a   Krueger, N A ^a   Byrd, J A ^a   Harvey, R B ^a   Callaway, T R ^a   Edrington, T S ^a   Nisbet, D J ^a  

^a SOUTHERN PLAINS AGRICULTURAL RESEARCH CENTER   (United States)

Author keywords

Biocides; Campylobacter; Cell injury sub lethal injury; Mechanism of action; Metabolism

Indexed keywords

AMMONIA; BACTERIA; CHLORINE COMPOUNDS; PHENOLS;

AMMONIA PRODUCTION; CAMPYLOBACTER SPP; CAMPYLOBACTERS; CELL INJURY; CELL INJURY/SUB-LETHAL INJURY; CULTURE IN VITRO; MECHANISM OF ACTION; MIXED CULTURES; MONENSIN; PURE CULTURE;

ETHANOL;

ALCOHOL; AMMONIA; DIPHENYLIODONIUM SALT; MONENSIN; THYMOL;

AMMONIA; BACTERIUM; CHLORIDE; DISSOLVED INORGANIC CARBON; ENZYME ACTIVITY; ETHANOL; FECES; GROWTH RATE; INHIBITOR; INJURY; METABOLISM; PESTICIDE; PHENOL; PHYSIOLOGY; SURVIVAL;

AMMONIA FORMATION; ARTICLE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIUM CULTURE; CAMPYLOBACTER COLI; CAMPYLOBACTER JEJUNI; CELL LYSATE; COLONY FORMING UNIT; CONTROLLED STUDY; FECES MICROFLORA; GROWTH RATE; IN VITRO STUDY; INCUBATION TIME; MIXED CELL CULTURE; NONHUMAN;

CAMPYLOBACTER; CAMPYLOBACTER JEJUNI; SUS;

EID: 70349097981     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2009.04308.x     Document Type: Article

References (75)

1. Anderson, A.D., Nelson, J.M., Rossiter, S. Angulo, F.J. (2003) Public health consequences of use of antimicrobial agents in food animals in the United States. Microb Drug Resist 9, 373 379.
2. Apajalahti, J. (2005) Comparative gut microflora, metabolic challenges, and potential opportunities. J Appl Poult Res 14, 444 453.
3. Beach, J.C., Murano, E.A. Acuff, G.R. (2002) Prevalence of Salmonella and Campylobacter in beef cattle from transport to slaughter. J Food Prot 65, 1687 1693.
4. Besser, T.E., LeJune, J.T., Rice, D.H., Berg, J., Stilborn, R.P., Kaya, K., Bae, W. Hancock, D.D. (2005) Increasing prevalence of Campylobacter jejuni in feedlot cattle through feeding period. Appl Environ Microbiol 71, 5752 5758.
5. Broderick, G.A. Balthrop, J.E. (1979) Chemical inhibition of amino acid deamination by ruminal microbes in vitro. J Anim Sci 49, 1101 1111.
6. Burt, S. (2004) Essential oils: Their antibacterial properties and potential applications in foods - a review. Int J Food Microbiol 94, 223 253.
7. Byrd, J.A., Hargis, B.M., Caldwell, D.J., Herron, K.L., McReynolds, J.L., Brewer, R.L., Anderson, R.C., Bischoff, K.M. et al. (2001) Effect of lactic acid administration in the drinking water during preslaughter feed withdrawal on Salmonella and Campylobacter contamination of broilers. J Poultry Sci 80, 278 283.
8. Callaway, T.R., Edrington, T.S., Rychlik, J.L., Genovese, K.J., Poole, T.L., Jung, Y.S., Bischoff, K.M., Anderson, R.C. et al. (2003) Ionophores: their use as ruminant growth promotants and impact on food safety. Curr Issues Intest Microbiol 4, 43 51.
9. Callaway, T.R., Keen, J.E., Edrington, T.S., Baumgard, L.H., Spicer, L., Fonda, E.S., Griswold, K.E., Overton, T.R. et al. (2005) Fecal prevalence and diversity of Salmonella spp. in lactating dairy cattle in four states. J Dairy Sci 88, 3603 3608.
10. Chakraborty, S. Massey, V. (2002) Reaction of reduced flavins and flavoproteins with diphenyliodonium chloride. J Biol Chem 277, 41507 41516.
11. Chalupa, W., Patterson, J.A., Parish, R.C. Chow, A.W. (1983a) Effects of diaryliodonium chemicals on nitrogen utilization in growing steers. J Anim Sci 57, 195 200.
12. Chalupa, W., Patterson, J.A., Parish, R.C. Chow, A.W. (1983b) Effects of diaryliodonium chemicals on rumen fermentation in vitro and in vivo. J Anim Sci 57, 186 194.
13. Chaney, A.L. Marbach, E.P. (1962) Modified reagents for determination of urea and ammonia. Clin Chem 8, 130 132.
14. Cole, K., Farnell, M.B., Donoghue, A.M., Stern, N.J., Svetoch, E.A., Eruslanov, B.N., Volodina, L.I., Kovalev, Y.N. et al. (2006) Bacteriocins reduce Campylobacter colonization and alter gut microbiology in turkey poults. Poult Sci 85, 1570 1575.
15. Corry, J.E.L. Atabay, H.I. (2001) Poultry as a source of Campylobacter and related organisms. J Appl Microbiol 90, 96S 114S.
16. Cotta, M.A., Whitehead, T.R. Zeltwanger, R.L. (2003) Isolation, characterization and comparison of bacteria from swine faeces and manure storage pits. Environ Microbiol 5, 737 745.
17. Dargatz, D.S., Wells, S.J., Thomas, L.A., Hancock, D.D. Garber, L.P. (1997) Factors associated with the presence of Escherichia coli O157 in feces of feedlot cattle. J Food Prot 60, 466 470.
18. Edrington, T.S., Callaway, T.R., Bischoff, K.M., Genovese, K.J., Elder, R.O., Anderson, R.C. Nisbet, D.J. (2003a) Effect of feeding the ionophores monensin and laidlomycin propionate and the ionophore bambermycin to sheep experimentally infected with Escherichia coli O157:H7 and Salmonella typhimurium. J Anim Sci 81, 553 560.
19. Edrington, T.S., Callaway, T.R., Varey, P.D., Jung, Y.S., Bischoff, K.M., Elder, R.O., Anderson, R.C., Kutter, K. et al. (2003b) Effects of the antibiotic ionophores monensin, lasalocid, laidlomycin propionate and bambermycin on Salmonella and E. coli O157:H7 in vitro. J Appl Microbiol 94, 207 213.
20. Engberg, J., Aarestrup, F.M., Taylor, D.E., Gerner-Smidt, P. Nachamkin, I. (2001) Quinolone and macrolide resistance in Campylobacter jejuni and C. coli: resistance mechanisms and trends in human isolates. Emerg Infect Dis 7, 24 34.
21. Friedman, M., Henika, P.R. Mandrell, R.E. (2002) Bactericidal activities of plant essential oils and some of their isolated constituents against Campylobacter jejuni, Escherichia coli, Listeria monocytogenes, and Salmonella enterica. J Food Prot 65, 1545 1560.
22. Garber, L.P., Wells, S.J., Hancock, D.D., Doyle, M.P., Tuttle, J., Shere, J.A. Zhao, T. (1995) Risk factors for fecal shedding of Escherichia coli O157:H7 in dairy calves. J Am Vet Med Assoc 207, 46 49.
23. Harvey, R.B., Young, C.R., Ziprin, R.L., Hume, M.E., Genovese, K.J., Anderson, R.C., Droleskey, R.E., Stanker, L.H. et al. (1999) Prevalence of Campylobacter spp isolated from the intestinal tract of pigs raised in an integrated swine production system. J Am Vet Med Assoc 215, 1601 1604.
24. Harvey, R.B., Anderson, R.C., Young, C.R., Swindle, M.M., Genovese, K.J., Hume, M.E., Droleskey, R.E., Farrington, L.A. et al. (2001) Effects of feed withdrawal and transport on cecal environment and Campylobacter concentrations in a swine surgical model. J Food Prot 64, 730 733.
25. Helander, I.M., Alakomi, H.-L., Latva-Kala, K., Mattila-Sandholm, T., Pol, I., Smid, E.J., Gorris, L.G.M. von Wright, A. (1998) Characterization of the action of selected essential oil components on Gram-negative bacteria. J Agric Food Chem 46, 3590 3595.
26. Hernández, F., Madrid, J., García, V., Orengo, J. Megías, M.D. (2004) Influence of two plant extracts on broiler performance, digestibility, and digestive organ size. Poult Sci 83, 169 174.
27. Hoffman, P.S. Goodman, T.G. (1982) Respiratory physiology and energy conservation efficiency of Campylobacter jejuni. J Bacteriol 150, 319 326.
28. Hughes, R., Magee, E.A.M. Bingham, S. (2000) Protein degradation in the large intestine: relevance to colorectal cancer. Curr Issues Intest Microbiol 1, 51 58.
29. Jensen, A.N., Dalsgaard, A., Baggesen, D.L. Neilsen, E.M. (2006) The occurrence and characterization of Campylobacter jejuni and C. coli in organic pigs and their outdoor environment. Vet Microbiol 116, 96 105.
30. Laanbroek, H.J., Lambers, J.T., De Vos, V.M. Veldkamp, H. (1978a) L-asparate fermentation by a free-living Campylobacter species. Arch Microbiol 117, 109 114.
31. Laanbroek, H.J., Stal, L.J. Veldkamp, H. (1978b) Utilization of hydrogen and formate by Campylobacter spec. under aerobic and anaerobic conditions. Arch Microbiol 119, 99 102.
32. Lee, M.D. Newell, D.G. (2006) Campylobacter in poultry: filling an ecological niche. Avian Dis 50, 1 9.
33. Loc Carrillo, C., Atterbury, R.J., El-Shibiny, A., Connerton, P.L., Dillon, E., Scott, A. Connerton, I.F. (2005) Bacteriophage therapy to reduce Campylobacter jejuni colonization of broiler chickens. Appl Environ Microbiol 71, 6554 6563.
34. Mead, P.S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee, J.S., Shapiro, C., Griffinm, P.M. Tauxe, R.V. (1999) Food-related illness and death in the United States. Emerg Inf Dis 5, 607 625.
35. Mendz, G.L. Hazell, S.L. (1996) Utilization of amino acids by Campylobacter jejuni. In Campylobacters, Helicobacters, and Related Organisms ed Newell, N.R., Ketley, J.M. Feldman, R.A. pp. 67 73. NY : Plenum Press.
36. Michiels, J., Missotten, J., Fremaut, D., De Smet, S. Dierick, N. (2007) In vitro dose-response of carvacrol, thymol, eugenol and trans-cinnamaldehyde and interaction of combinations for the antimicrobial activity against the pig gut flora. Livestock Sci 109, 157 160.
37. Mohammed, K.A.S., Miles, R.J. Halablad, M.A. (2004) The pattern and kinetics of substrate metabolism of Campylobacter jejuni and Campylobacter coli. Lett Appl Microbiol 39, 261 266.
38. Moulton, P., Martin, H., Ainger, A., Cross, A., Hoare, C., Doel, J., Harrison, R., Eisenthal, R. et al. (2000) The inhibition of flavoproteins by phenoxaiodonium, a new iodonium analogue. Eur J Pharmacol 401, 115 120.
39. Muhl, A. Liebert, F. (2007a) Growth and parameters of microflora in intestinal and faecal samples of piglets due to application of a phytogenic feed additive. J Anim Physiol Anim Nutr 91, 411 418.
40. Muhl, A. Liebert, F. (2007b) No impact of a phytogenic feed additive on digestion and unspecific immune reaction in piglets. J Anim Physiol Anim Nutr 91, 426 431.
41. Nachamkin, I., Allos, B.M. Ho, T. (1998) Campylobacter species and Guillain-Barré syndrome. Clin Microbiol Rev 11, 555 567.
42. Newbold, C.J., McIntosh, F.M., Williams, P., Losa, R. Wallace, R.J. (2004) Effects of a specific blend of essential oil compounds on rumen fermentation. Anim Feed Sci Technol 114, 105 112.
43. Oussalah, M., Caillet, S. Lacroix, M. (2006) Mechanism of action of Spanish oregano, Chinese cinnamon, and savory essential oils against cell membranes and walls of Escherichia coli O157:H7 and Listeria monocytogenes. J Food Prot 69, 1046 1055.
44. Pattison, M. (2001) Practical intervention strategies for Campylobacter. J Appl Microbiol 90, 121S 125S.
45. Pearce, R.A., Wallace, F.M., Call, J.E., Dudley, R.L., Oser, A., Yoder, L., Sheridan, J.J. Luchansky, J.B. (2003) Prevalence of Campylobacter within a swine slaughter and processing facility. J Food Prot 66, 1550 1556.
46. Ramirez Piñeres, M.A., Ellis, W.C., Wu, G. Ricke, S.C. (1997) Effects of diphenyliodonium chloride on proteolysis and leucine metabolism by rumen microorganisms. Anim Feed Sci Technol 65, 139 149.
47. Sahin, O., Morishita, T.Y. Zhang, Q. (2002) Campylobacter colonization in poultry: sources of infection and modes of transmission. Anim Health Res Rev 3, 95 105.
48. 3. Infect Immun 64, 2945 2949.
49. Sellars, M.J., Hall, S.J. Kelly, D.J. (2002) Growth of Campylobacter jejuni supported by respiration of fumarate, nitrate, nitrite, trimethylamine-N-oxide, or dimethyl sulfoxide requires oxygen. J Bacteriol 184, 4187 4196.
50. Si, W., Gong, J., Zhou, T., Yu, H., Poppe, C., Johnson, R. Du, Z. (2006) Antimicrobial activity of essential oils and structurally related synthetic food additives towards selected pathogenic and beneficial gut bacteria. J Appl Microbiol 100, 296 305.
51. Smith, E.A. Macfarlane, G.T. (1997) Dissimilatory amino acid metabolism in human colonic bacteria. Anaerobe 3, 327 337.
52. Smith, M.A., Mendz, G.L., Jorgensen, M.A. Hazell, S.L. (1999) Fumarate metabolism and microaerophily of Campylobacter species. Int J Biochem Cell Biol 31, 961 975.
53. Solis de los Santos, F., Donoghue, A.M., Venkitanarayanan, K., Dirain, M.L., Reyes-Herrera, I., Blore, P.J. Donoghue, D.J. (2008) Caprylic acid supplemented in feed reduces enteric Campylobacter jejuni colonization in ten-day-old broiler chickens. Poult Sci 87, 800 804. (Pubitemid 351601008)
54. Stanley, K. Jones, K. (2003) Cattle and sheep farms as reservoirs of Campylobacter. J Appl Microbiol 94, 104S 113S.
55. Stern, N.J., Wojton, B. Kwiater, K. (1992) A differential selective medium, and dry-ice generated atmosphere for recovery of Campylobacter jejuni. J Food Prot 55, 514 517.
56. Stern, N.J., Clavero, M.R.S., Bailey, J.S., Cox, N.A. Robach, M.C. (1995) Campylobacter spp. in broilers on the farm and after transport. Poult Sci 74, 937 941.
57. Stern, N.J., Fedorka-Cray, P., Bailey, J.S., Cox, N.A., Craven, S.E., Hiett, K.L., Musgrove, M.T., Ladley, S. et al. (2001) Distribution of Campylobacter spp. in selected U.S. poultry production and processing operations. J Food Prot 64, 1705 1710.
58. Stern, N.J., Svetoch, E.A., Eruslanov, B.V., Kovalev, Y.N., Volodina, L.I., Perelygin, V.V., Mitsevich, E.V., Mitsevich, I.P. et al. (2005) Paenibacillus polymyxa purified bacteriocin to control Campylobacter jejuni in chickens. J Food Prot 68, 1450 1453.
59. Stern, N.J., Svetoch, E.A., Eruslanov, B.V., Perelygin, V.V., Mitsevich, E.V., Mitsevich, I.P., Pokhilenko, V.D., Levchuk, V.P. et al. (2006) Isolation of a Lactobacillus salivarius strain and purification of its bacteriocin, which is inhibitory to Campylobacter jejuni in the chicken gastrointestinal system. Antimicrob Agents Chemother 50, 3111 3116.
60. Tam, C.C., O'Brien, S.J., Adak, G.K., Meakins, S.M. Frost, J.A. (2003) Campylobacter coli - an important foodborne pathogen. J Infect 47, 28 32.
61. Thakur, S. Gebreyes, W.A. (2005) Campylobacter coli in swine production: antimicrobial resistance mechanisms and molecular epidemiology. Appl Environ Microbiol 71, 5705 5714. (Pubitemid 41612352)
62. Thakur, S., Morrow, W.E.M., Funk, J.A., Bahnson, P.B. Gebreyes, W.A. (2006) Molecular epidemiologic investigation of Campylobacter coli in swine production systems, using sequence typing. Appl Environ Microbiol 72, 5666 5669.
63. Van Baale, M.J., Sargeant, J.M., Gnad, D.P., DeBay, B.M., Lechtenberg, K.F. Nagaraja, T.G. (2004) Effect of forage or grain diets with or without monensin on ruminal persistance and fecal Escherichia coli O157:H7 in cattle. Appl Environ Microbiol 70, 5336 5342.
64. Varel, V.H. (2002) Carvacrol and thymol reduce swine waste odor and pathogens: Stability of oils. Curr Microbiol 44, 38 43.
65. Varel, V.H. Miller, D.N. (2000) Effect of antimicrobial agents on livestock waste emissions. Curr Microbiol 40, 392 397.
66. Varel, V.H. Miller, D.N. (2001) Plant-derived oils reduce pathogens and gaseous emissions from stored cattle waste. Appl Environ Microbiol 67, 1366 1370.
67. Varel, V.H. Miller, D.N. (2004) Eugenol stimulates lactate accumulation yet inhibits volatile fatty acid production and eliminates coliform bacteria in cattle and swine waste. J Appl Microbiol 97, 1001 1005.
68. Varel, V.H. Wells, J.E. (2007) Influence of thymol and a urease inhibitor on coliform bacteria, odor, urea, and methane from a swine production manure pit. J Environ Qual 36, 773 779.
69. Varel, V.H., Miller, D.N. Berry, E.D. (2006) Incorporation of thymol into corncob granules for reduction of odor and pathogens in feedlot cattle waste. J Anim Sci 84, 481 487.
70. Varel, V.H., Wells, J.E. Miller, D.N. (2007) Combination of a urease inhibitor and a plant essential oil to control coliform bacteria, odour production, and ammonia loss from cattle waste. J Appl Microbiol 102, 472 477.
71. Velayudhan, J. Kelly, D.J. (2002) Analysis of gluceoneogenic and anaplerotic enzymes in Campylobacter jejuni: an essential role for phosphoenolpyruvate carboxykinase. Microbiology 148, 685 694.
72. Velayudhan, J., Jones, M.A., Barrow, P.A. Kelly, D.J. (2004) L-serine catabolism via an oxygen-labile L-serine dehydratase is essential for colonization of the avian gut by Campylobacter jejuni. Infect Immun 72, 260 268.
73. Wagenaar, J.A., Van Bergen, M.A.P., Mueller, M.A., Wassenaar, T.M. Carlton, R.M. (2005) Phage therapy reduces Campylobacter jejuni colonization in broilers. Vet Microbiol 109, 275 283.
74. Wallace, R.J. (2004) Antimicrobial properties of plant secondary metabolites. Proc Nutr Soc 63, 621 629.
75. Westfall, H.N., Rollins, D.M. Weiss, E. (1986) Substrate utilization by Campylobacter jejuni and Campylobacter coli. Appl Environ Microbiol 52, 700 705.