- Open Access
Emergence of Brachyspira species and strains: reinforcing the need for surveillance
© Hampson et al. 2015
Received: 17 April 2015
Accepted: 5 June 2015
Published: 12 June 2015
This short review discusses the increasing complexity that has developed around the understanding of Brachyspira species that infect pigs, and their ability to cause disease. It describes the recognition of new weakly haemolytic Brachyspira species, and the growing appreciation that Brachyspira pilosicoli and some other weakly haemolytic species may be pathogenic in pigs. It discusses swine dysentery (SD) caused by the strongly haemolytic Brachyspira hyodysenteriae, particularly the cyclical nature of the disease whereby it can largely disappear as a clinical problem from a farm or region, and re-emerge years later. The review then describes the recent emergence of two newly described strongly haemolytic pathogenic species, “Brachyspira suanatina” and “Brachyspira hampsonii” both of which appear to have reservoirs in migratory waterbirds, and which may be transmitted to and between pigs. “B. suanatina” seems to be confined to Scandinavia, whereas “B. hampsonii” has been reported in North America and Europe, causes a disease indistinguishable from SD, and has required the development of new routine diagnostic tests. Besides the emergence of new species, strains of known Brachyspira species have emerged that vary in important biological properties, including antimicrobial susceptibility and virulence. Strains can be tracked locally and at the national and international levels by identifying them using multilocus sequence typing (MLST) and comparing them against sequence data for strains in the PubMLST databases. Using MLST in conjunction with data on antimicrobial susceptibility can form the basis for surveillance programs to track the movement of resistant clones. In addition some strains of B. hyodysenteriae have low virulence potential, and some of these have been found to lack the B. hyodysenteriae 36 kB plasmid or certain genes on the plasmid whose activity may be associated with colonization. Lack of the plasmid or the genes can be identified using PCR testing, and this information can be added to the MLST and resistance data to undertake detailed surveillance. Strains of low virulence are particularly important where they occur in high health status breeding herds without causing obvious disease: potentially they could be transmitted to production herds where they may colonize more effectively and cause disease under stressful commercial conditions.
Swine dysentery (SD) was first recorded in the mid-west of the USA in the 1920s but the aetiological agent was not discovered for another 50 years. Classical SD is seen mainly in grower and finisher pigs in which it manifests as an acute and severe mucohaemorrhagic colitis. On the other hand the disease may be mild and/or not clinically apparent in some herds, particularly where antimicrobial agents that may suppress the infection are used on a regular basis. SD has a worldwide distribution and is endemic in many countries where it can cause substantial financial losses through reduced and uneven growth rate, mortalities, costs of treatment and impediment to trade. It also may become a welfare issue where it is not effectively controlled.
In the early 1970s a strongly haemolytic anaerobic intestinal spirochaete named Treponema hyodysenteriae , but now known as Brachyspira hyodysenteriae , was shown to be the aetiological agent of SD. The spirochaete grows slowly and requires incubation for at least 3–5 days on specialized selective media in an anaerobic environment. Later in the 1970s a weakly haemolytic spirochaete that had been isolated from healthy pigs and did not cause disease was named Brachyspira innocens . For diagnostic purposes it was important to be able to differentiate these two species, and this was done on the basis of their phenotypic properties, with the pathogenic B. hyodysenteriae being strongly haemolytic and indole positive and B. innocens being weakly haemolytic and indole negative.
This review gives a background to how this simple understanding of two species infecting pigs changed to a more complex one, and describes the emergence of both new Brachyspira species and of new strains, and their impact on diagnosis and control of disease caused by Brachyspira species in swine. Some details about changes to the genus and species names of these spirochaetes have been covered in an earlier review .
Recognition of new weakly haemolytic Brachyspira species
From the late 1970s until the early 1990s, following examination of biochemical properties of intestinal spirochaete isolates it started to become evident that there was likely to be more than one weakly haemolytic Brachyspira species (WHBS) that colonized swine, and there was increasing awareness that sometimes WHBS could cause disease . Due to the lack of simple molecular genetics techniques at that time investigations were based on examining phenotypic properties of isolates, and it was only with the application of multilocus enzyme electrophoresis and sequencing of the 16S rRNA gene in the early 1990s that it was shown that there were at least three more WHBS that colonized swine [6–8]. Of these, Brachyspira pilosicoli was clearly confirmed as being an enteric pathogen in pigs, causing a mild colitis and a diarrhoeal disease called porcine intestinal spirochaetosis [9, 10]. Interestingly this species also was shown to colonize and cause a similar disease in a number of species, most notably in chickens [11, 12] and human beings [13, 14]. Of the other two WHBS, Brachyspira murdochii, although generally considered a commensal, occasionally has been associated with mild colitis in swine [15–17]. The significance of Brachyspira intermedia in pigs is unclear [18, 19] – although it occurs commonly in adult chickens in which it is considered to be a pathogen .
New diagnostic methods
The description of the pathogenic B. pilosicoli required the development of methods to be able to detect and differentiate it from other WHBS. Species-specific polymerase chain reactions (PCR) were developed for both B. pilosicoli and B. hyodysenteriae , even though the strong haemolysis of B. hyodysenteriae was still considered to be the gold standard for its identification. This new technology increased the speed of diagnosis, and it was further improved by development of duplex PCR systems , and later by the use of multiplex quantitative real-time PCR . The techniques could be used on DNA extracted directly from faeces, although this procedure may be less sensitive than culture . As a result of the availability of the new techniques, and because of the difficulty in isolating and identifying the anaerobic and fastidious Brachyspira species, by the mid-2000s a number of diagnostic laboratories had stopped using culture as part of the diagnostic protocol for detecting Brachyspira species in swine and simply relied on PCR techniques applied to faecal DNA.
Cyclical changes in the prevalence of swine dysentery
Although SD is an endemic disease in many countries, within regions as well as on individual farms clinical disease has been observed to occur and later wane, with the latter probably resulting from enhanced diagnostic surveillance and implementation of control measures. For example, transmission of the disease between farms can be reduced by developing improved biosecurity measures, including quarantining of introduced stock . Interestingly, it has been observed that the disease may re-emerge as a regional clinical problem in a cyclical fashion every five years or more. This phenomenon is not always explained, but one way that it can occur is through the movement of sub-clinically infected pigs from multiplier herds in apparently high health status production pyramids . Other possibilities are the acquisition of strains from potential reservoirs such as migratory birds or feral animals [27, 28]; changes in strain properties so that the infection is amplified and transmitted more readily; reduction in herd immune status; or relaxation of routine diagnostic and control measures so that the disease gains the opportunity to spread. Low-level or subclinical colonization can exist on farms for many years, and then the disease can re-emerge when there are changes in management, including changes in diet [29, 30], co-infections with other enteric pathogens, or when other stressors occur. For example, stress induces release of norepinephrine into the gut, and this hormone has been shown to enhance B. pilosicoli growth and colonization . The same is likely to apply to B. hyodysenteriae. A good example of a change in disease expression having occurred under different husbandry conditions was when an isolate from a pig in a high health status herd that had minimal antimicrobial usage and no clinical disease was shown to cause typical SD when it was used to experimentally infect pigs in a research facility . If such subclinically infected pigs were transferred to a commercial piggery they could initiate clinical SD there. New and inexpensive screening methods such as serological ELISAs that can be applied routinely to large numbers of animals are needed to allow detection of these sorts of subclinical infections on farms .
In the USA clinical SD was common and widespread in the 1980s, but by the early 1990s it had become uncommon. This change was attributed to the introduction of medicated early weaning practices, the replacement of small family farrow-to-finish piggeries in the mid-West with new large multisite piggeries, often in non-traditional pig farming areas, introduction of all-in all-out pig flow, and better farm management. It also was suspected that the regular use of antimicrobial agents, and particularly carbadox, could have been suppressing disease. SD was no longer considered to be clinically important, and research and routine surveillance in North America was scaled down. Remarkably, and perhaps predictably given the history of this disease elsewhere, in the mid-2000s SD caused by B. hyodysenteriae re-emerged in the USA and Canada, and again started to become a common problem. This re-emergence has not been completely explained, but it followed the 2001 stop sale order on carbadox by Canada and the setting of zero tolerance for carbadox residues on US pork by Canada in 2007. In addition, and as previously mentioned, the movement of subclinically infected pigs may well have been a contributing factor to spread of the disease. A multilocus sequence typing (MLST) analysis of 59 B. hyodysenteriae isolates collected from farms in the USA post-2010 identified 13 sequence types (STs), including a predominant genotype (ST93), all of which were different to those from other countries . Some of these STs showed genetic similarity to those of one or more of the 10 North American isolates from the 1970s−1990s that were analysed. These results suggest that these original strains may have persisted and been the source of the re-emergence of SD in North America, rather than completely different strains having been introduced from other sources .
New strongly haemolytic species
In the early 2000s strongly haemolytic spirochaetes were isolated from feral ducks in Scandinavia . Subsequently these spirochaetes, which formed the new proposed species “Brachyspira suanatina”, were shown to occur sporadically in pig in this region and to induce diarrhoea and changes consistent with mild SD in experimentally infected pigs . To date this spirochaete has not been found outside the region. It is likely to occasionally spill over from feral and migratory ducks into susceptible pigs where it may cause a diarrhoeal disease resembling SD. This is most likely to occur in farms where pigs are kept outside, or where lagoon water contaminated with aquatic bird faeces is recycled to clean pig houses.
Later, around 2007, outbreaks of SD started to occur in Canada and the USA from which B. hyodysenteriae could not be detected or identified by PCR. Culturing of samples eventually identified the presence of another apparently novel strongly haemolytic species that was proposed as “Brachyspira hampsonii” . Two main clades were identified and both of these were shown to be able to induce a disease indistinguishable from SD in experimentally infected pigs [37–39]. Subsequently this species was detected in lesser snow geese in arctic Canada , and then in over-wintering graylag geese and mallards in a nature reserve in Spain , as well as in pigs in Belgium and Germany (clade I) [42, 43]. A strongly haemolytic isolate designated P280/1 that had been recovered from a pig in the UK in the 1980s and had been thought to be a new species  also was shown to be closely related to “B. hampsonii” . It seems likely that this emerging species has reservoirs in migratory water birds, and that the spirochaete may be transmitted from them to pigs to cause a disease that is indistinguishable from SD caused by B. hyodysenteriae. Like “B. suanatina” this new species was not detected by the PCR techniques that were in current use. The widespread distribution of this new species makes it more significant for porcine health than “B. suanatina”, although it should be remembered that surveillance for these and potentially other new pathogenic Brachyspira species is not routinely carried out in many regions of the world. Hence there is a very incomplete understanding of the occurrence and distribution of Brachyspira species at the global level, and more surveillance is required. As another example of this, a strongly haemolytic Brachyspira isolate that was distinct from B. hyodysenteriae, “B. suanatina” and “B. hampsonii” was isolated from an Australian pig herd with suspected SD . Following treatment of the herd for SD this strain has not subsequently been isolated, nor has it been found in routine diagnostic submissions from other herds in the region. Hence the appearance of this atypical strain seems to have been a rare event, and one that easily could be overlooked.
It is interesting that these “emerging” pathogenic species have all been strongly haemolytic, and this correlation is consistent with the haemolytic activity contributing to virulence . In some ways it was fortunate that these new species were strongly haemolytic, otherwise they may have taken much longer to identify. This series of events emphasizes the need to use both culture to obtain isolates and PCR methods for diagnosing Brachyspira infections, and to keep updating molecular diagnostic techniques. PCR methods based on the NADH oxidase (nox) gene are now available for “B. hampsonii” and “B. suanatina” [46, 47], and new rapid identification methods based on Matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF MS) are being implemented for identification of isolates of Brachyspira species [48, 49].
A number of these newly described weakly and strongly haemolytic Brachyspira species infecting pigs and other species still have “candidate” species status. It is important that additional phenotypic and genetic characterization is undertaken on members of these proposed species so that they can be more clearly identified and their names officially validated.
Analysis of 16S rRNA gene sequences of the Brachyspira species has shown that they are all relatively closely related. Nevertheless all the species also show considerable strain diversity, and these strains may vary in their biological properties. Extensive genetic rearrangements have been identified within and between the species, with sequence drift also generating genetic diversity . At a farm level “microevolution” of B. hyodysenteriae strains involving small genetic changes has been recorded over relatively short periods of time [51, 52]. Besides genetic rearrangements, novel genetic information may be acquired from other Brachyspira species or strains through the activity of prophage-like gene transfer agents that are present in the genome of different Brachyspira species [53, 54]. In addition, horizontal gene transfer via bacteriophages with broad trophism is likely to be an important force in the evolution of the Brachyspira species . This knowledge has clear implications for control, as new strains, clonal groups and even new Brachyspira species are likely to emerge over time. One consequence of this emergence is that phenotypic properties that have been used to identify species may become less reliable than originally thought. For example, in the mid-1990s atypical indole-negative strains of B. hyodysenteriae were identified in Europe [56, 57], and recently atypical weakly haemolytic strains of B. hyodysenteriae that appear to have reduced virulence in pigs have been reported in Europe , and also detected in Australian pigs (Phillips ND, La T, Hampson DJ 2015. Unpublished data).
Strain variation has been studied in most detail in B. hyodysenteriae, using a variety of phenotypic and molecular methods. In recent years MLST has been used to identify new clonal groups of B. hyodysenteriae [59–61], and these can be tracked nationally and internationally by comparing their STs in the PubMLST database . Within clonal groups a reduction in tiamulin susceptibility of isolates over time has been observed , and this emphasizes the power of combining MLST and resistance data for monitoring the development and spread of resistant strains. This capacity is particularly important as the emergence of resistant and multi-resistant B. hyodysenteriae strains can seriously compromise disease control [64, 65].
It has been known since the 1980s that different strains of B. hyodysenteriae vary in their pathogenic potential, with a minority being weakly virulent or avirulent [66–68]. Such strains, particularly if present in breeding herds, could cause a serious industry problem as the pigs may appear healthy but test positive for a major pathogen. Such a result can cause substantial disruptions to trade, even though the isolates may not be highly problematic from a clinical perspective. Alternatively such strains may not cause disease on the farm of origin, but perhaps cause disease when transferred to commercial herds . Although there may be various reasons for apparent reduced virulence, including a lack of strong haemolytic activity by some strains , recently it has been demonstrated that B. hyodysenteriae strains that either lack the ~36 kB plasmid  or certain genes on the plasmid have low pathogenic potential [70, 71]. These strains, including the type strain B78T, appear to have a reduced ability to colonize, although they are capable of causing typical SD lesions if they do establish themselves sufficiently in individual pigs . Lack of the plasmid or specific plasmid genes can be identified using PCR testing on isolates, and this information can be used to help identify individual isolates that are predicted to be less able to cause disease. The unusual B. hyodysenteriae strains that have weak haemolysis also may have reduced virulence, although further work is required to confirm this. Overall, a surveillance system that included information on clonal origin, antimicrobial resistance profile and virulence potential of isolates would be very valuable to help monitor and control the spread of SD at the local, national and international levels. Similar systems are required for other pathogenic Brachyspira species.
Routine surveillance at local, national and international levels is required to monitor Brachyspira species infections in pigs, but also carriage in other species which may act as reservoirs of infection (particularly migratory water birds). Surveillance of the latter has the added benefit of increased preparedness should a new Brachyspira species spill over into pigs, as appears to have been the recent case with “B. suanatina” and possibly with “B. hampsonii”.
The various species in the genus Brachyspira have different population structures, but all are genetically quite plastic. Consequently existing non-pathogenic species may acquire determinants from other species, especially through the activity of gene transfer agents and bacteriophages, and become more virulent. Similarly new strains of the species routinely develop, and it is important to monitor their presence and potential spread.
Diagnostic methodology needs to be reviewed regularly, but should include both culture and molecular techniques. The cultural techniques have the benefit of providing isolates of the species that can be used to undertake molecular epidemiology studies, and assess antimicrobial susceptibility and virulence potential. Knowledge of these attributes and the spread of clonal groups is very important for implementing programs to control disease caused by Brachyspira species.
The authors thank the European Association of Porcine Health Management for soliciting this review.
- Harris DL, Glock RD, Christensen CR, Kinyon JM. Inoculation of pigs with Treponema hyodysenteriae (new species) and reproduction of the disease. Vet Med Small Anim Clin. 1972;67:61–4.PubMedGoogle Scholar
- Ochiai S, Adachi Y, Mori K. Unification of the genera Serpulina and Brachyspira, and proposals of Brachyspira hyodysenteriae Comb. Nov., Brachyspira innocens Comb. Nov. and Brachyspira pilosicoli Comb. Nov. Microbiol Immunol. 1997;41:445–52.PubMedView ArticleGoogle Scholar
- Kinyon JM, Harris DL. Treponema innocens, a new species of intestinal bacteria, and emended description of the type strain of Treponema hyodysenteriae Harris et al. Int J Syst Bacteriol. 1979;29:102–9.View ArticleGoogle Scholar
- Hampson DJ. The Serpulina story. In: Cargill C, McOrist S, editors. Proceedings of 16th International Pig Veterinary Society Congress; 17–20 September 2000. Melbourne, Australia: The Society; 2000. p. 1–5.Google Scholar
- Taylor DJ, Simmons JR, Laird HM. Production of diarrhoea and dysentery in pigs by feeding pure cultures of a spirochaete differing from Treponema hyodysenteriae. Vet Rec. 1980;106:326–32.PubMedView ArticleGoogle Scholar
- Lee JI, Hampson DJ, Lymbery AJ, Harders SJ. The porcine intestinal spirochaetes: identification of new genetic groups. Vet Microbiol. 1993;34:273–85.PubMedView ArticleGoogle Scholar
- Lee JI, Hampson DJ. Genetic characterisation of intestinal spirochaetes and their association with disease. J Med Microbiol. 1994;40:365–71.PubMedView ArticleGoogle Scholar
- Stanton TB, Trott DJ, Lee JI, McLaren AJ, Hampson DJ, Paster BJ, et al. Differentiation of intestinal spirochaetes by multilocus enzyme electrophoresis analysis and 16S rRNA sequence comparisons. FEMS Microbiol Lett. 1996;136:181–6.PubMedView ArticleGoogle Scholar
- Trott DJ, Stanton TB, Jensen NS, Duhamel GE, Johnson JL, Hampson DJ. Serpulina pilosicoli sp. nov., the agent of porcine intestinal spirochetosis. Int J Syst Bacteriol. 1996;46:206–15.PubMedView ArticleGoogle Scholar
- Trott DJ, Huxtable CR, Hampson DJ. Experimental infection of newly weaned pigs with human and porcine strains of Serpulina pilosicoli. Infect Immun. 1996;64:4648–54.PubMed CentralPubMedGoogle Scholar
- McLaren AJ, Trott DJ, Swayne DE, Oxberry SL, Hampson DJ. Genetic and phenotypic characterization of intestinal spirochetes colonizing chickens, and allocation of known pathogenic isolates to three distinct genetic groups. J Clin Microbiol. 1997;35:412–7.PubMed CentralPubMedGoogle Scholar
- Stephens CP, Hampson DJ. Experimental infection of broiler breeder hens with the intestinal spirochaete Brachyspira (Serpulina) pilosicoli causes reduced egg production. Avian Pathol. 2002;31:169–75.PubMedView ArticleGoogle Scholar
- Trivett-Moore NL, Gilbert GL, Law CLH, Trott DJ, Hampson DJ. Isolation of Serpulina pilosicoli from rectal biopsy specimens showing evidence of intestinal spirochetosis. J Clin Microbiol. 1998;36:261–5.PubMed CentralPubMedGoogle Scholar
- Margawani KR, Robertson ID, Brooke CJ, Hampson DJ. Prevalence, risk factors and molecular epidemiology of Brachyspira pilosicoli in humans on the island of Bali, Indonesia. J Med Microbiol. 2004;53:325–32.PubMedView ArticleGoogle Scholar
- Jensen TK, Christensen AS, Boye M. Brachyspira murdochii colitis in pigs. Vet Pathol. 2010;47:334–8.PubMedView ArticleGoogle Scholar
- Weissenböck HA, Maderner A, Herzog AM, Lussy H, Nowotny N. Amplification and sequencing of Brachyspira spp. specific portions of nox using paraffin-embedded tissue samples from clinical colitis in Austrian pigs shows frequent solitary presence of Brachyspira murdochii. Vet Microbiol. 2005;111:67–75.PubMedView ArticleGoogle Scholar
- Osorio J, Carvajal A, Naharro G, Rubio P, La T, Phillips ND, et al. Identification of weakly haemolytic Brachyspira isolates recovered from pigs with diarrhoea in Spain and Portugal and comparison with results from other countries. Res Vet Sci. 2013;95:861–9.PubMedView ArticleGoogle Scholar
- Jensen TK, Moller K, Boye M, Leser TD, Jorsal SE. Scanning electron microscopy and fluorescent in situ hybridization of experimental Brachyspira (Serpulina) pilosicoli infection in growing pigs. Vet Pathol. 2000;37:22–32.PubMedView ArticleGoogle Scholar
- Komarek V, Maderner A, Spergser J, Weissenböck H. Infections with weakly haemolytic Brachyspira species in pigs with miscellaneous chronic diseases. Vet Microbiol. 2009;34:311–7.View ArticleGoogle Scholar
- Hampson DJ, McLaren AJ. Experimental infection of layer hens with Serpulina intermedia causes reduced egg production and increased faecal water content. Avian Pathol. 1999;28:113–7.View ArticleGoogle Scholar
- Atyeo RF, Oxberry SL, Combs BG, Hampson DJ. Development and evaluation of polymerase chain reaction tests as an aid to diagnosis of swine dysentery and intestinal spirochaetosis. Lett Appl Microbiol. 1998;26:126–30.PubMedView ArticleGoogle Scholar
- La T, Phillips ND, Hampson DJ. Development of a duplex PCR assay for the detection of Brachyspira hyodysenteriae and Brachyspira pilosicoli in pig feces. J Clin Microbiol. 2003;41:3372–5.PubMed CentralPubMedView ArticleGoogle Scholar
- Song Y, Hampson DJ. Development of a multiplex qPCR for detection and quantitation of pathogenic intestinal spirochaetes in pigs and chickens. Vet Microbiol. 2009;137:129–36.PubMedView ArticleGoogle Scholar
- Råsbäck T, Fellström C, Gunnarsson A, Aspán A. Comparison of culture and biochemical tests with PCR for detection of Brachyspira hyodysenteriae and Brachyspira pilosicoli. J Microbiol Methods. 2006;66:347–53.PubMedView ArticleGoogle Scholar
- Robertson ID, Mhoma JRL, Hampson DJ. Risk factors associated with the occurrence of swine dysentery in Western Australia: results of a postal survey. Aust Vet J. 1992;69:92–3.PubMedView ArticleGoogle Scholar
- Windsor RS, Simmons JR. Investigation into the spread of swine dysentery in 25 herds in East Anglia and assessment of its economic significance in five herds. Vet Rec. 1981;109:482–4.PubMedView ArticleGoogle Scholar
- Jansson DS, Johansson KE, Olofsson T, Råsbäck T, Vågsholm I, Pettersson B, et al. Brachyspira hyodysenteriae and other strongly beta-haemolytic and indole-positive spirochaetes isolated from mallards (Anas platyrhynchos). J Med Microbiol. 2004;53:293–300.PubMedView ArticleGoogle Scholar
- Phillips ND, La T, Adams PJ, Harland BL, Fenwick SG, Hampson DJ. Detection of Lawsonia intracellularis, Brachyspira hyodysenteriae and/or Brachyspira pilosicoli in feral pigs. Vet Microbiol. 2009;134:294–9.PubMedView ArticleGoogle Scholar
- Pluske JR, Durmic Z, Pethick DW, Mullan BP, Hampson DJ. Confirmation of the role of non-starch polysaccharides and resistant starch in the expression of swine dysentery in pigs following experimental infection. J Nutr. 1998;128:1737–44.PubMedGoogle Scholar
- Durmic Z, Pethick DW, Mullan BP, Accioly JM, Schulze H, Hampson DJ. Evaluation of dietary treatments designed to reduce the occurrence of swine dysentery. Br J Nutr. 2002;88:159–69.PubMedView ArticleGoogle Scholar
- Naresh R, Hampson DJ. Exposure to norepinephrine enhances Brachyspira pilosicoli growth, attraction to mucin and attachment to Caco-2 cells. Microbiology. 2011;157:543–7.PubMedView ArticleGoogle Scholar
- Hampson DJ, Cutler R, Lee BJ. Virulent Serpulina hyodysenteriae from a pig in a herd free of clinical swine dysentery. Vet Rec. 1992;131:318–9.PubMedView ArticleGoogle Scholar
- La T, Phillips ND, Hampson DJ. Evaluation of recombinant Bhlp29.7 as an ELISA antigen for detecting pig herds with swine dysentery. Vet Microbiol. 2009;133:98–104.PubMedView ArticleGoogle Scholar
- Mirajkar NS, Gebhart CJ. Understanding the molecular epidemiology and global relationships of Brachyspira hyodysenteriae from swine herds in the United States: a multi-locus sequence typing approach. PLoS One. 2014;9(9):e107176.PubMed CentralPubMedView ArticleGoogle Scholar
- Råsbäck T, Jansson DS, Johansson KE, Fellström C. A novel enteropathogenic, strongly haemolytic spirochaete isolated from pig and mallard, provisionally designated ‘Brachyspira suanatina’ sp. nov. Environ Microbiol. 2007;9:983–91.PubMedView ArticleGoogle Scholar
- Chander Y, Primus A, Oliveira S, Gebhart CJ. Phenotypic and molecular characterization of a novel strongly hemolytic Brachyspira species, provisionally designated “Brachyspira hampsonii”. J Vet Diagn Invest. 2012;4:903–10.Google Scholar
- Rubin JE, Costa MO, Hill JE, Kittrell HE, Fernando C, Huang Y, et al. Reproduction of mucohaemorrhagic diarrhea and colitis indistinguishable from swine dysentery following experimental inoculation with “Brachyspira hampsonii” strain 30446. PLoS One. 2013;8(2):e57146.PubMed CentralPubMedView ArticleGoogle Scholar
- Burrough ER, Strait EL, Kinyon JM, Bower LP, Madson DM, Wilberts BL, et al. Comparative virulence of clinical Brachyspira spp. isolates in inoculated pigs. J Vet Diagn Invest. 2012;24:1025–34.PubMedView ArticleGoogle Scholar
- Costa MO, Hill JE, Fernando C, Lemieux HD, Detmer SE, Rubin JE, et al. Confirmation that “Brachyspira hampsonii” clade I (Canadian strain 30599) causes mucohemorrhagic diarrhea and colitis in experimentally infected pigs. BMC Vet Res. 2014;10:129.PubMed CentralPubMedView ArticleGoogle Scholar
- Rubin JE, Harms NJ, Fernando C, Soos C, Detmer SE, Harding JC, et al. Isolation and characterization of Brachyspira spp. including “Brachyspira hampsonii” from lesser snow geese (Chen caerulescens caerulescens) in the Canadian Arctic. Microb Ecol. 2013;66:813–22.PubMedView ArticleGoogle Scholar
- Martínez-Lobo FJ, Hidalgo Á, García M, Argüello H, Naharro G, Carvajal A, et al. First identification of “Brachyspira hampsonii” in wild European waterfowl. PLoS One. 2013;8(12):e82626.PubMed CentralPubMedView ArticleGoogle Scholar
- Mahu M, de Jong E, De Pauw N, Vande Maele L, Vandenbroucke V, Vandersmissen T, et al. First isolation of “Brachyspira hampsonii” from pigs in Europe. Vet Rec. 2014;174:47.PubMedView ArticleGoogle Scholar
- Rohde J, Habighorst-Blome K, Seehusen F. “Brachyspira hampsonii” clade I isolated from Belgian pigs imported to Germany. Vet Microbiol. 2014;168:432–5.PubMedView ArticleGoogle Scholar
- Atyeo RF, Stanton TB, Jensen NS, Suriyaarachichi DS, Hampson DJ. Differentiation of Serpulina species by NADH oxidase (nox) gene comparisons and nox-based polymerase chain reaction tests. Vet Microbiol. 1999;67:49–62.View ArticleGoogle Scholar
- Phillips ND, La T, Dunlop H, Hampson DJ. An unusual strongly haemolytic spirochaete isolated from an Australian herd with suspected swine dysentery. In: Smola J, Cizek A, Lobova D, Celer V, Prasek J, editors. Proceedings of the Fourth International Conference on Colonic Spirochaetal Infections of Animals and Humans: 20–22 May 2007. Prague, Czech Republic: The Society; 2007. p. 19.Google Scholar
- Rohde J, Habighorst-Blome K. An up-date on the differentiation of Brachyspira species from pigs with nox-PCR-based restriction fragment length polymorphism. Vet Microbiol. 2012;158:211–5.PubMedView ArticleGoogle Scholar
- Wilberts BL, Warneke HL, Bower LP, Kinyon JM, Burrough ER. Comparison of culture, polymerase chain reaction, and fluorescent in situ hybridization for detection of Brachyspira hyodysenteriae and “Brachyspira hampsonii” in pig feces. J Vet Diagn Invest. 2015;27:41–6.PubMedView ArticleGoogle Scholar
- Prohaska S, Pflüger V, Ziegler D, Scherrer S, Frei D, Lehmann A, et al. MALDI-TOF MS for identification of porcine Brachyspira species. Lett Appl Microbiol. 2014;58:292–8.PubMedView ArticleGoogle Scholar
- Warneke HL, Kinyon JM, Bower LP, Burrough ER, Frana TS. Matrix-assisted laser desorption ionization time-of-flight mass spectrometry for rapid identification of Brachyspira species isolated from swine, including the newly described “Brachyspira hampsonii”. J Vet Diagn Invest. 2014;26:635–9.PubMedView ArticleGoogle Scholar
- Mappley LJ, Black ML, AbuOun M, Woodward MJ, Darby A, Turner AK, et al. Comparative genomics of Brachyspira pilosicoli strains: extensive genome rearrangements and reductions, and correlation of genetic compliment with phenotypic diversity. BMC Genomics. 2012;13:454.PubMed CentralPubMedView ArticleGoogle Scholar
- Atyeo RF, Oxberry SL, Hampson DJ. Analysis of Serpulina hyodysenteriae strain variation and its molecular epidemiology using pulsed field gel electrophoresis. Epidemiol Infect. 1999;123:133–8.PubMed CentralPubMedView ArticleGoogle Scholar
- Hidalgo A, Carvajal A, Pringle M, Rubio P, Fellström C. Characterization and epidemiological relationships of Spanish Brachyspira hyodysenteriae field isolates. Epidemiol Infect. 2010;138:76–85.PubMedView ArticleGoogle Scholar
- Matson EG, Thompson MG, Humphrey SB, Zuerner RL, Stanton TB. Identification of genes of VSH-1, a prophage-like gene transfer agent of Brachyspira hyodysenteriae. J Bacteriol. 2005;187:5885–92.PubMed CentralPubMedView ArticleGoogle Scholar
- Motro Y, La T, Bellgard MI, Dunn DS, Phillips ND, Hampson DJ. Identification of genes associated with prophage-like gene transfer agents in the pathogenic intestinal spirochaetes Brachyspira hyodysenteriae, Brachyspira pilosicoli and Brachyspira intermedia. Vet Microbiol. 2009;134:340–5.PubMedView ArticleGoogle Scholar
- Håfström T, Jansson DS, Segerman B. Complete genome sequence of Brachyspira intermedia reveals unique genomic features in Brachyspira species and phage-mediated horizontal gene transfer. BMC Genomics. 2011;12:395.PubMed CentralPubMedView ArticleGoogle Scholar
- Hommez J, Castryck F, Haesebrouck F, Devriese LA. Identification of porcine Serpulina strains in routine diagnostic bacteriology. Vet Microbiol. 1998;62:163–9.PubMedView ArticleGoogle Scholar
- Fellström C, Karlsson M, Pettersson B, Zimmerman U, Gunnarsson A, Aspan A. Emended descriptions of indole negative and indole positive isolates of Brachyspira (Serpulina) hyodysenteriae. Vet Microbiol. 1999;70:225–38.PubMedView ArticleGoogle Scholar
- Mahu M, De Pauw N, Vande Maele L, Verlinden M, Boyen F, Ducatelle R, et al. Weakly hemolytic Brachyspira hyodysenteriae strains in pigs. In: Adler B, Frey J, Rood J, Inzana T, Vacquez-Boland J, Natale A, et al., editors. Proceedings of the 3rd Prato Conference on the Pathogenesis of Bacterial Diseases of Animals. 7–10 October 2014. Prato, Italy: The Society; 2014. p. 39.Google Scholar
- Råsbäck T, Johansson KE, Jansson DS, Fellström C, Alikhani MY, La T, et al. Development of a multilocus sequence typing scheme for intestinal spirochaetes within the genus Brachyspira. Microbiology. 2007;153:4074–87.PubMedView ArticleGoogle Scholar
- La T, Phillips ND, Harland BL, Wanchanthuek P, Bellgard MI, Hampson DJ. Multilocus sequence typing as a tool for studying the molecular epidemiology and population structure of Brachyspira hyodysenteriae. Vet Microbiol. 2009;138:330–8.PubMedView ArticleGoogle Scholar
- Osorio J, Carvajal A, Naharro G, La T, Phillips ND, Rubio P, et al. Dissemination of clonal groups of Brachyspira hyodysenteriae amongst pig farms in Spain, and their relationships to isolates from other countries. PLoS One. 2012;7(6):e39082.PubMed CentralPubMedView ArticleGoogle Scholar
- Brachyspira MLST databases. http://pubmlst.org/brachyspira/. Accessed 15 April 2015.
- Rugna G, Bonilauri P, Carra E, Bergamini F, Luppi A, Gherpelli Y, et al. Sequence types and pleuromutilin susceptibility of Brachyspira hyodysenteriae isolates from Italian pigs with swine dysentery: 2003–2012. Vet J. 2015;203:115–9.PubMedView ArticleGoogle Scholar
- Duinhof TF, Dierikx CM, Koene MG, van Bergen MA, Mevius DJ, Veldman KT, et al. Multiresistant Brachyspira hyodysenteriae in a Dutch sow herd. Tijdschr Diergeneeskd. 2008;133:604–8.PubMedGoogle Scholar
- Sperling D, Smola J, Cízek A. Characterisation of multiresistant Brachyspira hyodysenteriae isolates from Czech pig farms. Vet Rec. 2011;168:215.PubMedView ArticleGoogle Scholar
- Lysons RJ, Lemcke RM, Bew J, Burrows MR, Alexander TJL. An avirulent strain of Treponema hyodysenteriae isolated from herds free of swine dysentery. In: Necoechea RR, editor. Proceedings of the 7th International Pig Veterinary Society Congress: 26–31 July 1982. Mexico City, Mexico: The Society; 1982. p. 40.Google Scholar
- Jensen NS, Stanton TB. Comparison of Serpulina hyodysenteriae B78, the type strain of the species, with other S. hyodysenteriae strains using enteropathogenicity studies and restriction fragment length polymorphism analysis. Vet Microbiol. 1993;36:221–31.PubMedView ArticleGoogle Scholar
- Achacha M, Messier S, Mittal KR. Development of an experimental model allowing discrimination between virulent and avirulent isolates of Serpulina (Treponema) hyodysenteriae. Can J Vet Res. 1996;60:45–9.PubMed CentralPubMedGoogle Scholar
- Bellgard MI, Wanchanthuek P, La T, Ryan K, Moolhuijzen P, Albertyn Z, et al. Genome sequence of the pathogenic intestinal spirochete Brachyspira hyodysenteriae reveals adaptations to its lifestyle in the porcine large intestine. PLoS One. 2009;4(3):e4641.PubMed CentralPubMedView ArticleGoogle Scholar
- La T, Phillips ND, Wanchanthuek P, Bellgard MI, O’Hara AJ, Hampson DJ. Evidence that the 36 kb plasmid of Brachyspira hyodysenteriae contributes to virulence. Vet Microbiol. 2011;153:150–5.PubMedView ArticleGoogle Scholar
- La T, Phillips ND, Thomson JR, Hampson DJ. Absence of a set of plasmid-encoded genes is predictive of reduced pathogenic potential in Brachyspira hyodysenteriae. Vet Res. 2014;45:131.PubMed CentralPubMedView ArticleGoogle Scholar
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.