Swine Dysentery (SD) is a severe mucohaemorhagic enteric disease of pigs caused by Brachyspira hyodysenteriae, which has a large impact on pig production and causes important losses due to mortality and sub-optimal performance. Although B. hyodysenteriae has been traditionally considered a pathogen mainly transmitted by direct contact, through the introduction of subclinically infected animals into a previously uninfected herd, recent findings position B. hyodysenteriae as a potential threat for indirect transmission between farms. This article summarizes the knowledge available on the etiological agent of SD and its virulence traits, and reviews the determinants of SD transmission. The between-herds and within-herd transmission routes are addressed. The factors affecting disease transmission are thoroughly discussed, i.e., environmental survival of the pathogen, husbandry factors (production system, production stage, farm management), role of vectors, diet influence and interaction of the microorganism with gut microbiota. Finally, prophylactic and therapeutic approaches to fight against the disease are briefly described.
References
[1]
Wills, R.W. Diarrhea in growing-finishing swine. Vet. Clin. North Am. Food Anim. Pract. 2000, 16, 135–161.
Taylor, D.J.; Alexander, T.J.L. The production of dysentery in swine by feeding cultures containing a spirochaete. Br. Vet. J. 1971, 127, 58–61.
[4]
Harris, D.L.; Glock, R.D.; Christensen, C.R.; Kinyon, J.M. Inoculation of pigs with Treponema hyodysenteriae (new species) and reproduction of the disease. Vet. Med. Small Anim. Clin. 1972, 67, 61–64.
[5]
Hampson, D.J.; Fellstrom, C.; Thomson, J.R. Swine dysentery. In Diseases of Swine; Straw, B.E., Zimmerman, J.J., D’Allaire, S., Eds.; Blackwell Publishing Professional: Ames, IA, USA, 2006; pp. 785–805.
[6]
Suh, D.K.; Song, J.C. Simultaneous detection of Lawsonia intracellularis, Brachyspira hyodysenteriae and Salmonella spp. in swine intestinal specimens by multiplex polymerase chain reaction. J. Vet. Sci. 2005, 6, 231–237.
[7]
Fellstrom, C.; Pettersson, B.; Johansson, K.E.; Lundeheim, N.; Gunnarsson, A. Prevalence of Serpulina species in relation to diarrhea and feed medication in pig-rearing herds in Sweden. Am. J. Vet. Res. 1996, 57, 807–811.
[8]
M?ller, K.; Jensen, T.K.; Jorsal, S.E.; Leser, T.D.; Carstensen, B. Detection of Lawsonia intracellularis, Serpulina hyodysenteriae, weakly beta-hemolytic intestinal spirochaetes, Salmonella enterica, and Escherichia coli from swine herds with and without diarrhoea among growing pigs. Vet. Microbiol. 1998, 62, 59–72, doi:10.1016/S0378-1135(98)00199-0.
Carvajal, A.; de Arriba, M.L.; Rodríguez, H.; Vidal, A.B.; Duhamel, G.E.; Rubio, P. Prevalence of Brachyspira species in pigs with diarrhoea in Spain. Vet. Rec. 2006, 158, 700–701, doi:10.1136/vr.158.20.700.
[11]
Johnston, W.T.; Dewey, C.E.; Friendship, R.M.; Smart, N.; McEwen, B.J.; Stalker, M.; de Lange, C.F.M. An investigation of the aetiology of a mild diarrhea observed in a group of grower/finisher pigs. Can. Vet. J. 2001, 42, 33–37.
[12]
Jacobson, M.; Gerth Lofstedt, M.; Holmgren, N.; Lundeheim, N.; Fellstrom, C. The prevalences of Brachyspira spp. and Lawsonia intracellularis in Swedish piglet producing herds and wild board population. J. Vet. Med. 2005, 52, 386–391, doi:10.1111/j.1439-0450.2005.00865.x.
[13]
Hampson, D.J. The Serpulina Story. In Proceedings of the 16th International Pig Veterinary Society Congress, Melbourne, Australia, 17–21 September 2000; pp. 1–5.
[14]
Fries, R. Conclusions and activities of previous expert groups: The scientific steering committee of the EU. J. Vet. Med. 2004, 51, 403–407, doi:10.1111/j.1439-0450.2004.00794.x.
[15]
R?sb?ck, T.; Jansson, D.S.; Johansson, K.E.; Fellstr?m, C. A novel enteropathogenic, strongly haemolytic spirochaete isolated from pig and mallard, provisionally designated “Brachyspira suanatina”sp. nov. Environ. Microbiol. 2007, 9, 983–991, doi:10.1111/j.1462-2920.2006.01220.x.
Chander, Y.; Primus, A.; Oliveira, S.; Gebhart, C.J. Phenotypic and molecular characterization of a novel strongly hemolytic Brachyspira species, provisionally designated “Brachyspira hampsonii”. J. Vet. Diagn. Invest. 2012, 24, 903–910.
[18]
Rubin, J.E.; Costa, M.O.; Hill, J.E.; Kittrell, H.E.; Fernando, C.; Huang, Y.; O’Connor, B.; Harding, J.C.S. Reproduction of mucohaemorrhagic diarrhea and colitis indistinguishable from swine dysentery following experimental inoculation with “Brachyspira hampsonii” strain 30446. PloS One 2013, 8, e57146, doi:10.1371/journal.pone.0057146.
[19]
Desrosiers, R. Transmission of swine pathogens: Different means, different needs. Anim. Health Res. Rev. 2011, 12, 1–13, doi:10.1017/S1466252310000204.
[20]
Songer, J.G.; Glock, R.D.; Schwartz, K.J.; Harris, D.L. Isolation of Treponema hyodysenteriae from sources other than swine. J. Am. Vet. Med. Assoc. 1978, 172, 464–466.
[21]
Jensen, N.S.; Stanton, T.B.; Swayne, D.E. Identification of the swine pathogen Serpulina hyodysenteriae in rheas (Rhea Americana). Vet. Microbiol. 1996, 52, 259–269, doi:10.1016/S0378-1135(96)00076-4.
[22]
Boye, M.; Baloda, S.B.; Leser, T.D.; M?ller, K. Survival of Brachyspira hyodysenteriae and B. pilosicoli in terrestrial microcosms. Vet. Microbiol. 2001, 81, 33–40, doi:10.1016/S0378-1135(01)00328-5.
[23]
Jansson, D.S.; Johansson, K.E.; Olofson, T.; Rasback, T.; Vagsholm, I.; Petterson, B.; Gunnarson, A.; Fellstrom, C. Brachyspira hyodysenteriae and other strongly betahemolytic and indole-positive spirochaetes isolated from mallards (Anas platyrhynchos). J. Vet. Microbiol. 2004, 53, 293–300.
[24]
Blunt, R.; McOrist, S. On-Farm Insect Vector Carriage of Swine Pathogens—Brachyspira and Lawsonia. In Proceedings of the 20th International Pig Veterinary Society Congress, Durban, South Africa, 22–25 June 2008; p. 291.
[25]
Feberwee, A.; Hampson, D.J.; Philips, N.D.; La, T.; van der Heijden, H.M.; Wellenberg, G.J.; Dwars, R.M.; Landman, W.J. Identification of Brachyspira hyodysenteriae and other Brachyspira species in chickens from laying flocks with diarrhea or reduced production or both. J. Clin. Microbiol. 2008, 46, 593–600, doi:10.1128/JCM.01829-07.
[26]
Gallie, A.; Chesworth, M.; Blunt, R.; McOrist, S. Identification of Harmful Dipteroid Communities on Pig Farms. In Proceedings of the American Association of Swine Veterinarians, Dallas, TX, USA, 7–10 March 2009; p. 323.
[27]
Phillips, N.D.; La, T.; Adams, P.J.; Harland, B.L.; Fenwick, S.G.; Hampson, D.J. Detection of Brachyspira hyodysenteriae, Lawsonia intracellularis and Brachyspira pilosicoli in feral pigs. Vet. Microbiol. 2009, 134, 294–299, doi:10.1016/j.vetmic.2008.08.006.
[28]
Paster, B.J.; Dewhirst, F.E. Phylogenetic foundation of spirochaetes. J. Mol. Microb. Biotech. 2000, 2, 341–344.
[29]
Ter Huurne, A.A.; Gaastra, W. Swine dysentery: More unknown than known. Vet. Microbiol. 1995, 46, 347–360, doi:10.1016/0378-1135(95)00049-G.
[30]
Bellgard, M.I.; Wanchanthuek, P.; La, T.; Ryan, K.; Moolhuijzen, P.; Albertyn, Z.; Shaban, B.; Motro, Y.; Dunn, D.S.; Schibeci, D.; et al. Genome sequence of the pathogenic intestinal spirochaete Brachyspira hyodysenteriae reveals adaptations to its lifestyle in the porcine large intestine. PLoS One 2009, 4, e4641, doi:10.1371/journal.pone.0004641.
[31]
Halter, M.R.; Joens, L.A. Lipooligosaccharides from Treponema hyodysenteriae and Treponema innocens. Infect. Immun. 1988, 56, 3152–3156.
[32]
Kennedy, M.J.; Rosnick, D.K.; Ulrich, R.G.; Yancey, R.J. Association of Treponema hyodysenteriae with porcine intestinal mucosa. J. Gen. Microbiol. 1988, 134, 1565–1576.
[33]
Ter Huurne, A.A.; Muir, S.; van Houten, M.; van der Zeijst, B.A.; Gaastra, W.; Kusters, J.G. Characterization of three putative Serpulina hyodysenteriae hemolysins. Microb. Pathog. 1994, 16, 269–282, doi:10.1006/mpat.1994.1028.
[34]
Rosey, E.L.; Kennedy, M.J.; Yancey, R.J. Dual flaA1 flaB1 mutant of Serpulina hyodysenteriae expressing periplasmic flagella is severely attenuated in a murine model of swine dysentery. Infect. Immun. 1996, 64, 4154–4162.
[35]
Wassenaar, T.M.; Gaastra, W. Bacterial virulence: Can we draw the line? FEMS Microbiol. Lett. 2001, 201, 1–7, doi:10.1111/j.1574-6968.2001.tb10724.x.
[36]
Barth, S.; Gommel, M.; Baljer, G.; Herbst, W. Demonstration of genes encoding virulence and virulence life-style factors in Brachyspira spp. isolates from pigs. Vet. Microbiol. 2012, 155, 438–443, doi:10.1016/j.vetmic.2011.09.032.
[37]
La, T.; Phillips, N.D.; Wanchanthuek, P.; Bellgard, M.I.; O’Hara, A.J.; Hampson, D.J. Evidence that the 36 kb plasmid of Brachyspira hyodysenteriae contributes to virulence. Vet. Microbiol. 2011, 153, 150–155.
[38]
Olson, L.D. Clinical and pathological observations on the experimental passage of swine dysentery. Can. J. Comp. Med. 1974, 38, 7–13.
[39]
Moreng, N.T.; Quarles, C.L.; Fagerberg, D.J.; Moeller, D.J. Pathogenesis and lesions of swine dysentery induced by artificial methods in early weaned pigs. Vet. Med. Small Anim. Clin. 1980, 75, 1841–1844.
[40]
Savage, D.C. Colonization by and survival of pathogenic bacteria on intestinal mucosal surfaces. In Adsorption of Microorganisms to Surfaces; Bitton, B., Marshall, K.C., Eds.; Wiley: New York, NY, USA, 1980; pp. 175–206.
[41]
Kinyon, J.M.; Harris, D.L.; Glock, R.D. Isolation of Treponema hyodysenteriae from Experimentally Infected Pigs at Various Intervals Post-Inoculation. In Proceedings of the 6th International Pig Veterinary Society Congress, Copenhagen, Denmark, 30 June–3 July 1980; p. 232.
[42]
Hampson, D.J.; Cutler, R.; Lee, B.J. Virulent Serpulina hyodysenteriae from a pig in a herd free of clinical swine dysentery. Vet. Rec. 1992, 131, 318–319.
[43]
Chia, S.P.; Taylor, D.J. Factors affecting the survvial of Treponema hyodysenteriae in dysenteric pig faeces. Vet. Rec. 1978, 103, 68–70.
[44]
Harris, D.L.; Hampson, D.J.; Glock, R.D. Diseases of Swine; Straw, B.E., D’Allaire, S.D., Mengelling, W.D., Taylor, D.J., Eds.; Iowa State University Press: Ames, IA, USA, 1999; pp. 579–600.
[45]
Songer, J.G.; Harris, D.L. Transmission of swine dysentery by carrier pigs. Am. J. Vet. Res. 1978, 39, 913–916.
[46]
Hidalgo, A.; Osorio, J.; Papaterra, G.J.; Llanos, A.; Marca, J.; Ferro, A.; Hernandez-Caravaca, I.; Carvajal, A.; Rubio, P. Control of Swine Dysentery with an Innactivated Autovaccine against Brachyspira hyodysenteriae in a Multiplier Herd. In Proceedings of the 20th International Pig Veterinary Society Congress, Durban, South Africa, 22–25 June 2008; p. 242.
[47]
Osorio, J.; Hidalgo, A.; Papaterra, G.J.; Llanos, A.; Marca, J.; Ferro, A.; Hernandez-Dávila, C.; Carvajal, A.; Rubio, P. Control of Swine Dysentery with An Autogenous Bacterin of Brachyspira hyodysenteriae in Iberian Pigs. In Proceedings of the 20th International Pig Veterinary Society Congress, Durban, South Africa, 22–25 June 2008; p. 249.
[48]
Kanora, A.; de Groote, S.; Fockedey, M.; Velesova, S.; Karanikolova, M. Brachyspira Causing Enteric Disorder in Young Fattening Pigs Coming from Same Reproduction Pyramid. In Proceedings of the 20th International Pig Veterinary Society Congress, Durban, South Africa, 22–25 June 2008; p. 249.
[49]
Robertson, I.D.; Mhoma, J.R.; Hampson, D.J. Risk factors associated with the occurrence of swine dysentery in Western Australia: Results of a postal survey. Aust. Vet. J. 1992, 69, 92–101, doi:10.1111/j.1751-0813.1992.tb15561.x.
[50]
Fellstr?m, C; Rasb?ck, T. How to Handle Swine Dysentery-the Swedish Approach. In Proceedings of the 5th Spiroconference, León, Spain, 8–10 June 2009; pp. 41–43.
[51]
Bano, L.; Merialdi, G.; Bonilauri, P.; Dall’Anese, G.; Capello, K.; Comin, D.; Cattoli, G.; Sanguinetti, V.; Hampson, D.J.; Agnoletti, F. Prevalence, disease associations and risk factors for colonization with intestinal spirochaetes (Brachyspira spp.) in flocks of laying hens in north-eastern Italy. Avian Pathol. 2008, 37, 281–286.
[52]
McOrist, S.; Bennett, C. Eradication of Swine Dysentery on Large-Scale Breeder Farms by Partial Depopulation/Medication. In Proceedings of the 20th International Pig Veterinary Society Congress, Durban, South Africa, 22–25 June 2008; p. 319.
[53]
Phillips, N.D.; La, T.; Hampson, D.J. Survival of intestinal spirochaete strains from chickens in the presence of disinfectants and in faeces held at different temperatures. Avian Pathol. 2003, 32, 639–643, doi:10.1080/03079450310001610677.
[54]
Pico, L.; Szancer, J.; Pique, J.; Domeneque, A.; Rodriguez-Sierra, E.; Vidal, A. Swine Dysentery Eradication Programme in a Large Farm with Three Site Production by Strategic Management and Medication. In Proceedings of the 20th International Pig Veterinary Society Congress, Durban, South Africa, 22–25 June 2008; p. 131.
[55]
Rajska, M.; Kempa, W.; Wilczynski, K. Experiences with Control Programme of Swine Dysentery in A Typical POLISH Pig Unit. In Experiences with Control Programme of Swine Dysentery in A Typical POLISH Pig Unit., Durban, South Africa, 22–25 June 2008; p. 250.
[56]
Hampson, D.J.; Combs, B.G.; Harders, S.J.; Connaughton, I.D.; Fahy, V.A. Isolation of Treponema hyodysenteriae from a wild rat living on a piggery. Aust. Vet. J. 1991, 68, 308, doi:10.1111/j.1751-0813.1991.tb03268.x.
[57]
Backhans, A.; Johansson, K.E.; Fellstr?m, C. Spirochaetes Isolated from Wild Rodents. In Proceedings of the 5th Spiroconference, León, Spain, 8–10 June 2009; pp. 58–59.
[58]
Trott, D.J.; Atyeo, R.F.; Lee, J.I.; Swayne, D.A.; Stoutenburg, J.W.; Hampson, D.J. Genetic relatedness amongst intestinal spirochaetes isolated from rats and birds. Lett. Appl. Microbiol. 1996, 23, 431–436, doi:10.1111/j.1472-765X.1996.tb01352.x.
[59]
Fellstrom, C.; Holmgren, N. Mice as reservoirs for swine dysentery in a fattening herd. Svensk Veterinartid. 2005, 57, 19–21.
[60]
Backhans, A.; Jansson, D.S.; Aspán, A.; Fellstr?m, C. Typing of Brachyspira spp. from rodents, pigs and chickens on Swedish farms., A.; Fellstr?m, C. Vet. Microbiol. 2011, 153, 156–162.
[61]
Jensen, N.S.; Stanton, T.B.; Swayne, D.E. Identification of the swine pathogen Serpulina hyodysenteriae in rheas (Rhea americana). Vet. Microbiol. 1996, 52, 259–269, doi:10.1016/S0378-1135(96)00076-4.
[62]
Swayne, D.E.; McLaren, A.J. Avian intestinal spirochaetes and avian intestinal spirochaetosis. In Intestinal Spirochaetes in Domestic Animals and Humans; Hampson, D.J., Stanton, T.B., Eds.; CAB International: New York, NY, USA, 1997; pp. 267–300.
[63]
Oxberry, S.L.; Trott, D.J.; Hampson, D.J. Serpulina pilosicoli, waterbirds and water: Potential sources of infection for humans and other animals. Epidemiol. Infect. 1998, 121, 219–225, doi:10.1017/S0950268898008863.
[64]
Duhamel, G.E. Comparative pathology and pathogenesis of naturally acquired and experimentally induced colonic spirochetosis. Anim. Health Res. Rev. 2001, 2, 3–17.
[65]
Jansson, D.S.; Rasback, T.; Fellstrom, C.; Feinstein, R. Experimental challenge of mallards (Anas platyrhynchos) with Brachyspira hyodysenteriae and “Brachyspira suanatina” isolated from pigs and mallards. J. Comp. Pathol. 2009, 141, 211–222, doi:10.1016/j.jcpa.2009.03.007.
[66]
Jansson, D.S.; Persson, M.; Zimmerman, U.; Johansson, K.E. Phenotypic and genetic diversity among intestinal spirochaetes (genus Brachyspira) in free-living wild mallards (Anas platyrhynchos) sampled in southern Sweden. Syst. Appl. Microbiol. 2011, 34, 566–575, doi:10.1016/j.syapm.2011.10.001.
[67]
Sagartz, J.E.; Swayne, D.E.; Eaton, K.A.; Hayes, J.R.; Amass, K.D.; Wack, R.; Kramer, L. Necrotizing typhlocolitis associated with a spirochaete in rheas (Rhea americana). Avian Dis. 1992, 36, 282–289.
[68]
Buckles, E.L. Inoculation of Neonatal Common Rheas (Rhea americana) and Mallard Ducklings (Anas platyrhynchos) with Three Bacterial Species Associated with Necrotizing Typhlitis. M.Sc. Thesis, Ohio State University, Columbus, OH, USA, 1996.
[69]
Buckles, E.L.; Eaton, K.A.; Swayne, D.E. Cases of spirochaete associated necrotizing typhlitis in captive common rheas (Rhea americana). Avian Dis. 1997, 41, 144–148, doi:10.2307/1592454.
[70]
Stanton, T.B.; Jensen, N.S.; Bosworth, B.T.; Kunkle, R.A. Evaluation of the Virulence of Rhea S. hyodysenteriae Strains for Swine. Brachyspira hyodysenteriae in Mallards. In Proceedings of the 1st International Virtual Conference on Infectious Diseases of Animals, National Animal Disease Center, Ames, IA, USA, 20 April–2 May 1997.
[71]
Blunt, R.; Hancox, L.; Mellits, K.; McOrist, S. Likely Carriage of Brachyspira hyodysenteriae in Cockroaches and Flies on Pig Farms. In Proceedings of the 21st International Pig Veterinary Society Congress, Vancouver, BC, Canada, 18–21 July 2010; p. 93.
[72]
Blunt, R.; McOrist, S. The Potential Transmission of Swine Dysentery by Cockroach Vectors. In Proceedings of the 5th Spiroconference, León, Spain, 8–10 June 2009; p. 14.
[73]
Fellstr?m, C.; Jacobsson, M. Screening for Brachyspira spp. and Lawsonia intracellularis in European Wild Pigs. In Proceedings of the 17th International Pig Veterinary Society Congress, Ames, IA, USA, 2–5 June 2002; p. 367.
[74]
Songer, J.G.; Glock, R.D.; Schwartz, K.J.; Harris, D.L. Isolation of Treponema hyodysenteriae from sources other than swine. J. Am. Vet. Med. Assoc. 1978, 172, 464–466.
[75]
Huisman, J.; Jansman, A.J.M. Dietary effects and some analytical aspects of antinutritional factors in pea (Pisum sativum), common beans (Phaseolus vulgaris) and soyabeans (Glycine max L.) in monogastric farm animals. A literature review. Nutr. Abstr. Rev. 1991, 61, 901–921.
[76]
Dréau, D.; Lallés, J.P.; Philouze-Romé, V.; Toullec, R.; Salmon, H. Local and systemic immune responses to soybean protein ingestion in early-weaned pigs. J. Anim. Sci. 1994, 72, 2090–2098.
[77]
Whipp, S.C.; Robinson, I.M.; Harris, D.L.; Glock, R.D.; Matthews, P.J.; Alexander, T.J. Pathogenic synergism between Treponema hyodysenteriae and other selected anaerobes in gnotobiotic pigs. Infect. Immun. 1979, 26, 1042–1047.
[78]
Dréau, D.; Lallés, J.P.; Toullec, R.; Salmon, H. B and T lymphocytes are enhanced in the gut of piglets fed heat-treated soyabean proteins. Vet. Immunol. Immunopathol. 1995, 47, 69–79, doi:10.1016/0165-2427(94)05376-4.
[79]
Neef, N.A.; McOrist, S.; Lysons, R.J.; Bland, A.P.; Miller, B.G. Development of large intestinal attaching and effacing lesions in pigs in association with the feeding of a particular diet. Infect. Immun. 1994, 62, 4325–4332.
[80]
Siba, P.M.; Pethick, D.W.; Hampson, D.J. Pigs experimentally infected with Serpulina hyodysenteriae can be protected from developing swine dysentery by feeding them a highly digestible diet. Epidemiol. Infect. 1996, 116, 207–216, doi:10.1017/S0950268800052456.
[81]
Durmic, Z.; Pethick, D.; Mullan, B.; Schulze, H.; Accioly, J.; Hampson, D. Extrusion of wheat or sorghum and/or addition of exogenous enzymes to pig diets influences the large intestinal microbiota but does not prevent development of swine dysentery following experimental challenge. J. Appl. Microbiol. 2000, 89, 678–686, doi:10.1046/j.1365-2672.2000.01166.x.
[82]
Lindecrona, R.H.; Jensen, T.K.; Jensen, B.B.; Leser, T.D.; Jiufeng, W.; M?ller, K. The influence of diet on the development of swine dysentery upon experimental infection. Anim. Sci. 2003, 76, 81–87.
[83]
Thomsen, L.E.; Bach Knudsen, K.E.; Jensen, T.K.; Christensen, A.S.; M?ller, K.; Roepstorff, A. The effect of fermentable carbohydrates on experimental swine dysentery and whip worm infections in pigs. Vet. Microbiol. 2007, 119, 152–163, doi:10.1016/j.vetmic.2006.09.004.
[84]
Hansen, C.F.; Phillips, N.D.; La, T.; Hernández, A.; Mansfield, J.; Kim, J.C.; Mullan, B.P.; Hampson, D.J.; Pluske, J.R. Diets containing inulin but not lupins help to prevent swine dysentery in experimentally challenged pigs. J. Anim. Sci. 2010, 88, 3327–3336, doi:10.2527/jas.2009-2719.
[85]
Roberfroid, M.B.; van Loo, J.A.E.; Gibson, G.R. The bifidogenic nature of chicory inulin and its hydrolysis products. J. Nutr. 1998, 128, 11–19.
[86]
Hansen, C.; Hernández, A.; Mansfield, J.; Hidalgo, A.; La, T.; Phillips, N.; Hampson, D.; Pluske, J. A high dietary concentration of inulin is necessary to reduce the incidence of swine dysentery in pigs experimentally challenged with Brachyspira hyodysenteriae. Br. J. Nutr. 2011, 106, 1506–1513, doi:10.1017/S000711451100208X.
[87]
Cummings, J.H.; Macfarlane, G.T. The control and consequences of bacterial fermentation in the human colon. J. Appl. Bacteriol. 1991, 70, 443–459, doi:10.1111/j.1365-2672.1991.tb02739.x.
[88]
M?lbak, L.; Thomsen, L.E.; Jensen, T.K.; Bach Knudsen, K.E.; Boye, M. Increased amount of Bifidobacterium thermacidophilum and Megasphaera elsdenii in the colonic microbiota of pigs fed a swine dysentery preventive diet containing chicory roots and sweet lupine. J. Appl. Microbiol. 2007, 103, 1853–1867, doi:10.1111/j.1365-2672.2007.03430.x.
[89]
Kowalski, C.; Zarí, R.; Rolinski, Z. Pleuromutilin derivatives and their usage in veterinary treatment. Med. Weter. 2004, 60, 22–26.
[90]
Molnar, L. Sensitivity of strains of Serpulina hyodysenteriae isolated in Hungary to chemotherapeutic drugs. Vet. Rec. 1996, 138, 158–160, doi:10.1136/vr.138.7.158.
[91]
Gresham, A.C.; Hunt, B.W.; Dalziel, R.W. Treatment of swine dysentery—Problems of antibiotic resistance and concurrent salmonellosis. Vet. Rec. 1998, 143, 619.
[92]
Karlsson, M.; Gunnarsson, A.; Franklin, A. Susceptibility to pleuromutilins in Brachyspira (Serpulina) hyodysenteriae. Anim. Health Res. Rev. 2001, 2, 59–65.
[93]
Karlsson, M.; Fellstrom, C.; Gunnarsson, A.; Landen, A.; Franklin, A. Antimicrobial susceptibility testing of porcine Brachyspira (Serpulina) species isolates. J. Clin. Microbiol. 2003, 41, 2596–2604, doi:10.1128/JCM.41.6.2596-2604.2003.
[94]
Lobova, D.; Smola, J.; Cizek, A. Decreased susceptibility to tiamulin and valnemulin among Czech isolates of Brachyspira hyodysenteriae. J. Med. Microbiol. 2004, 53, 287–291, doi:10.1099/jmm.0.05407-0.
[95]
Rohde, J.; Kessler, M.; Baums, C.G.; Amtsberg, G. Comparison of methods for antimicrobial susceptibility testing and MIC values for pleuromutilin drugs for Brachyspira hyodysenteriae isolated in Germany. Vet. Microbiol. 2004, 102, 25–32, doi:10.1016/j.vetmic.2004.03.023.
[96]
Hidalgo, A.; Carvajal, A.; García-Feliz, C.; Osorio, J.; Rubio, P. Antimicrobial susceptibility testing of Spanish field isolates of Brachyspira hyodysenteriae. Res. Vet. Sci. 2009, 87, 7–12, doi:10.1016/j.rvsc.2008.10.017.
[97]
Hidalgo, A.; Carvajal, A.; Vester, B.; Pringle, M.; Naharro, G.; Rubio, P. Trends towards lower antimicrobial susceptibility and characterization of acquired resistance among clinical isolates of Brachyspira hyodysenteriae in Spain. Antimicrob. Agents Ch. 2011, 55, 3330–3337, doi:10.1128/AAC.01749-10.
[98]
Ohya, T.; Sueyoshi, M. In vitro antimicrobial susceptibility of Brachyspira hyodysenteriae strains isolated in Japan from 1985 to 2009. J. Vet. Med. Sci. 2010, 72, 1651–1653, doi:10.1292/jvms.10-0271.
[99]
Karlsson, M.; Fellstrom, C.; Heldtander, M.U.; Johansson, K.E.; Franklin, A. Genetic basis of macrolide and lincosamide resistance in Brachyspira (Serpulina) hyodysenteriae. FEMS Microbiol. Lett. 1999, 172, 255–260, doi:10.1111/j.1574-6968.1999.tb13476.x.
[100]
Karlsson, M.; Fellstrom, C.; Johansson, K.E.; Franklin, A. Antimicrobial resistance in Brachyspira pilosicoli with special reference to point mutations in the 23S rRNA gene associated with macrolide and lincosamide resistance. Microb. Drug Resist. 2004, 10, 204–208.
[101]
Pringle, M.; Poehlsgaard, J.; Vester, B.; Long, K.S. Mutations in ribosomal protein L3 and 23S ribosomal RNA at the peptidyl transferase centre are associated with reduced susceptibility to tiamulin in Brachyspira spp. isolates. Mol. Microbiol. 2004, 54, 1295–1306, doi:10.1111/j.1365-2958.2004.04373.x.
[102]
Pringle, M.; Landén, A.; Unnerstad, H.E.; Molander, B.; Bengtsson, B. Antimicrobial susceptibility of porcine Brachyspira hyodysenteriae and Brachyspira pilosicoli isolated in Sweden between 1990 and 2010. Acta Vet. Scand. 2012, 54, 54, doi:10.1186/1751-0147-54-54.
[103]
R?nne, H.; Szancer, J. In Vitro Susceptibility of Danish Field Isolates of Treponema hyodysenteriae to Chemotherapeutics in Swine Dysentery (SD) Therapy. Interpretation of MICs Results Based on Pharmacokinetic Properties of the Antibacterial Agents. In Proceedings of the 11th International Pig veterinary Society Congress, Lausanne, Switerzland, 1–5 July 1990; p. 126.
[104]
Burch, D.G.S. Pharmacokinetic, pharmacodynamic and clinical correlations relating to the therapy of colonic infections in the pig and breakpoints determinations. Pig J. 2005, 56, 8–24.
[105]
Joens, L.A.; Harris, D.L.; Baum, D.H. Immunity to swine dysentery in recovered pigs. Am. J. Vet. Res. 1979, 40, 1352–1354.
[106]
Fernie, D.S.; Ripley, P.H.; Walker, P.D. Swine dysentery: Protection against experimental challenge following single dose parenteral immunisation with inactivated Treponema hyodysenteriae. Res. Vet. Sci. 1983, 35, 217–221.
[107]
Parizek, R.; Stewart, R.; Brown, K.; Blevins, D. Protection against swine dysentery with an inactivated Treponema hyodysentariae bacterin. Vet. Med. 1985, 80, 80–86.
[108]
Diego, R.; Lanza, I.; Carvajal, A.; Rubio, P.; Carmenes, P. Serpulina hyodysenteriae challenge of fattening pigs vaccinated with an adjuvanted bivalent bacterin against swine dysentery. Vaccine 1995, 13, 663–667, doi:10.1016/0264-410X(94)00018-I.
[109]
Waters, W.R.; Sacco, R.E.; Dorn, A.D.; Hontecillas, R.; Zuckermann, F.A.; Wannemuehler, M.J. Systemic and mucosal immune responses of pigs to parenteral immunization with a pepsin-digested Serpulina hyodysenteriae bacterin. Vet. Immunol. Immunopathol. 1999, 69, 75–87, doi:10.1016/S0165-2427(99)00043-4.
[110]
Hudson, M.J.; Alexander, T.L.J.; Lysons, R.J.; Wellstead, P.D. Swine dysentery: Failure of an attenuated strain of spirochaete, given orally, to protect pigs against subsequent challenge. Br. Vet. J. 1974, 130, 37–40.
[111]
Lysons, R.; Burrows, M.R.; Jones, P.W.; Collins, P. Swine dysentry, a new and effective vaccine. Proc. Int. Pig Vet. Soc. 1987, 18, 87–91.
[112]
Hyatt, D.R.; Ter Huurne, A.A.; van der Zeijst, B.A.; Joens, L.A. Reduced virulence of Serpulina hyodysenteriae hemolysin-negative mutants in pigs and their potential to protect pigs against challenge with a virulent strain. Infect. Immun. 1994, 62, 2244–2248.
Joens, L.A.; Marquez, M.R.; Halter, M. Comparison of outer-membrane fractions of Serpulina (Treponema) hyodysenteriae. Vet. Microbiol. 1993, 35, 119–132, doi:10.1016/0378-1135(93)90120-V.
[115]
La, T.; Phillips, N.D.; Reichel, M.P.; Hampson, D.J. Protection of pigs from swine dysentery by vaccination with recombinant BmpB, a 29.7 kDa outer-membrane lipoprotein of Brachyspira hyodysenteriae. Vet. Microbiol. 2004, 102, 97–109.
[116]
Witchell, T.D.; Coutts, S.A.J.; Bulach, D.M.; Adler, B. Differential expression of the Bhmp39 major outer membrane proteins of Brachyspira hyodysenteriae. Infect. Immun. 2006, 74, 3271–3276, doi:10.1128/IAI.02000-05.
[117]
Holden, J.; Coloe, P.J.; Smooker, P.M. An evaluation of the immunogenicity and protective responses to Brachyspira hyodysenteriae recombinant SmpB vaccination. Vet. Microbiol. 2008, 128, 354–363, doi:10.1016/j.vetmic.2007.10.026.
[118]
Boyden, D.A.; Albert, F.G.; Robinson, C.S. Cloning and characterization of Treponema hyodysenteriae antigens and protection in a CF-1 mouse model by immunization with a cloned endoflagellar antigen. Infect. Immun. 1989, 57, 3808–3815.
[119]
Gabe, J.D.; Chang, R.J.; Slomiany, R.; Andrews, W.H.; McCaman, M.T. Isolation of extracytoplasmic proteins from Serpulina hyodysenteriae B204 and molecular cloning of the flaB1 gene encoding a 38-kilodalton flagellar protein. Infect. Immun. 1995, 63, 142–148.
[120]
Davis, A.J.; Smith, S.C.; Moore, R.J. The Brachyspira hyodysenteriae ftnA gene: DNA vaccination and real-time PCR quantification of bacteria in a mouse model of disease. Curr. Microbiol. 2005, 50, 285–291.
[121]
Pluske, J.; Durmic, Z.; Pethick, D.; Mullan, B.; Hampson, D. Confirmation of the role of rapidly fermentable carbohydrates in the expression of swine dysentery in pigs after experimental infection. J. Nutr. 1998, 128, 1737–1744.
[122]
Durmic, Z.; Pethick, D.W.; Mullan, B.P.; Accioly, J.M.; Schulze, H.; Hampson, D.J. Evaluation of large intestinal parameters associated with dietary treatments designed to reduce the occurrence of swine dysentery. Br. J. Nutr. 2002, 88, 159–169, doi:10.1079/BJN2002607.
[123]
Gibson, G.R.; Roberfroid, M.B. Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. J. Nutr. 1995, 125, 1401–1412.
[124]
Hontecillas, R.; Wannemeulher, M.J.; Zimmerman, D.R.; Hutto, D.L.; Wilson, J.H.; Ahn, D.U.; Bassaganya-Riera, J. Nutritional regulation of porcine bacterial-induced colitis by conjugated linoleic acid. J. Nutr. 2002, 132, 2019–2027.
[125]
Bernardeau, M.; Gueguen, M.; Smith, D.G.E.; Corona-Barrera, E.; Vernoux, J.P. In vitro antagonistic activities of Lactobacillus spp. against Brachyspira hyodysenteriae and Brachyspira pilosicoli. Vet. Microbiol. 2009, 138, 184–190, doi:10.1016/j.vetmic.2009.03.020.
[126]
Klose, V.; Bayer, K.; Bruckbeck, R.; Schatzmayr, G.; Loibner, A.P. In vitro antagonistic activities of animal intestinal strains against swine-associated pathogens. Vet. Microbiol. 2010, 144, 515–521, doi:10.1016/j.vetmic.2010.02.025.
[127]
Klose, V.; Bruckbeck, R.; Henikl, S.; Schatzmayr, G.; Loibner, A.P. Identification and antimicrobial susceptibility of porcine bacteria that inhibit the growth of Brachyspira hyodysenteriae in vitro. J. Appl. Microbiol. 2010, 108, 1271–1280, doi:10.1111/j.1365-2672.2009.04521.x.
[128]
Lyoo, Y.; Park, D.; Lee, S.; Choi, Y.; Jung, J.; Jun, T.; Ahm, H.; Lee, Ch.; Lym, Y. Antibacterial compound against Pasteurella multocida and Actinobacillus pleuropneumoniae causing porcine pneumonia. J. Microbiol. Biotech. 2001, 11, 350–353.
[129]
Becker, P.M.; van Wikselaar, P.G.; Mul, M.F.; Pol, A.; Engel, B.; Wijdenes, J.W.; van der Peet-Schwering, C.M.; Wisselink, H.J.; Stockhofe-Zurwieden, N. Actinobacilluspleuropneumoniae is impaired by the garlic volatile allyl methyl sulphide (AMS) in vitro and in-feed garlic alleviates pleuropneumonia in a pig model. Vet. Microbiol. 2012, 154, 316–324, doi:10.1016/j.vetmic.2011.07.011.
[130]
Lobova, D.; Cizek, A. Bactericidal efficacy of two disinfectants against Brachyspira hyodysenteriae and one feed supplement against B. hyodysenteriae and B. pilosicoli. Vet. Med. Czech 2004, 49, 156–160.
[131]
Alvarez-Ordó?ez, A.; Carvajal, A.; Arguello, H.; Martínez-Lobo, F.J.; Naharro, G.; Rubio, P. Antibacterial activity and mode of action of a commercial citrus fruit extract. J. Appl. Microbiol. 2013, doi:10.1111/jam.12216.