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porcine intestinal spirochaetosis

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porcine intestinal spirochaetosis

Summary

  • Last modified
  • 14 July 2018
  • Datasheet Type(s)
  • Animal Disease
  • Preferred Scientific Name
  • porcine intestinal spirochaetosis
  • Pathogens
  • Brachyspira pilosicoli
  • Overview
  • Brachyspira pilosicoli is an anaerobic spirochaete (bacterium) that colonizes the lumen and crypts of the large intestine of pigs, as well as a number of other animal species. The organism has been shown to be wi...

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    Compendia
    CAB International
    Wallingford
    Oxfordshire
    OX10 8DE
    UK
    compend@cabi.org
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PictureTitleCaptionCopyright
Scanning electron micrograph showing the attachment of large numbers of Brachyspira pilosicoli cells to the surface of the colonic mucosa in an experimentally-infected pig.
TitleSEM
CaptionScanning electron micrograph showing the attachment of large numbers of Brachyspira pilosicoli cells to the surface of the colonic mucosa in an experimentally-infected pig.
CopyrightDavid Hampson/Murdoch University, Western Australia
Scanning electron micrograph showing the attachment of large numbers of Brachyspira pilosicoli cells to the surface of the colonic mucosa in an experimentally-infected pig.
SEMScanning electron micrograph showing the attachment of large numbers of Brachyspira pilosicoli cells to the surface of the colonic mucosa in an experimentally-infected pig.David Hampson/Murdoch University, Western Australia

Identity

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Preferred Scientific Name

  • porcine intestinal spirochaetosis

International Common Names

  • English: porcine colonic spirochetosis, brachyspira pilosicoli; spirochaetal diarrhoea

Local Common Names

  • USA: porcine colonic spirochaetosis

English acronym

  • PIS

Pathogen/s

Top of page Brachyspira pilosicoli

Overview

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Brachyspira pilosicoli is an anaerobic spirochaete (bacterium) that colonizes the lumen and crypts of the large intestine of pigs, as well as a number of other animal species. The organism has been shown to be widespread in pig herds in a number of important pig-rearing countries. Colonization by the spirochaete can result in a mild colitis and diarrhoea, which is associated with sub-optimal growth rates in weaner and grower pigs.


History and Taxonomy


The spirochaete that is now known as B. pilosicoli was first reported in 1980 in Scotland (Taylor et al., 1980). The authors described a weakly haemolytic intestinal spirochaete that was distinct from the strongly haemolytic spirochaete that causes swine dysentery (now known as Brachyspira hyodysenteriae). The new spirochaete was isolated from pigs with diarrhoea, and caused colitis and dysentery in experimentally infected pigs. The associated disease was called 'spirochaetal diarrhoea'. A particular feature observed in infected pigs was the attachment of a dense carpet of the spirochaetes by one cell end to the colonic epithelium. The spirochaete was not fully characterized or named at this time. Over the next decade there were a number of reports of spirochaetes found attached to the colonic epithelium of pigs with diarrhoea (Andrews and Hoffman, 1982; Jacques et al., 1989). Studies using multilocus enzyme electrophoresis eventually demonstrated that the spirochaete described by Taylor and colleagues (strain P43/6/78) was genetically distinct from other species of intestinal spirochaetes that colonise pigs (Lee et al., 1981). Strain P43/6/78 was shown to be genetically similar to a collection of isolates recovered from pigs with diarrhoea in Australia and Canada, and in 1993 this group of organisms was provisionally named 'Anguillina coli' (Lee et al., 1993). Human and canine isolates of the same species were described in 1994 (Lee and Hampson, 1994). In 1996, based on further results of 16S rDNA sequencing and DNA-DNA reassociation assays, the species was officially named Serpulina pilosicoli, with the original Scottish isolate P43/6/78 being designated as the type strain (Trott et al., 1996a). The associated disease in pigs was called 'porcine intestinal spirochaetosis', in line with the name 'intestinal spirochaetosis' which has been used for a similar condition in human beings (Harland and Lee, 1967). In North America the condition also has been referred to as 'porcine colonic spirochaetosis' (Duhamel, 1998). In 1997 a proposal was made that three of the species belonging to the genus Serpulina be transferred to the genus Brachyspira, with S. pilosicoli being renamed B. pilosicoli (Ochiai et al., 1997). This change was made because; the human intestinal spirochaete Brachyspira aalborgi (Hovind-Hougen et al., 1984) had been described before the genus Serpulina was created (Stanton, 1982), it was considered that the four species of intestinal spirochaetes were sufficiently closely related to warrant them being included in a single genus, and the genus name Brachyspira had chronological priority over Serpulina. This proposal was validated in 1998 (Validation list No. 64, 1998, International Journal of Systematic Bacteriology). Nevertheless the new name for the porcine spirochaete species remained controversial, and until the year 2000 many authors continued to use the old genus name, Serpulina.


Importance


The economic importance of porcine intestinal spirochaetosis is incompletely understood. The clinical condition is mild, accurate diagnosis is difficult and the use of preventive antimicrobials may contribute to underestimation of the true prevalence of the disease (Johnston et al., 1999). Where specific surveys have been undertaken the condition appears to be widespread (Stevenson, 1999). Economic loss mainly results from reduced average daily weight gains and reduced feed efficiency in grower and finisher pigs. Uneven growth rates in groups of pigs can also disrupt efficient production, particularly in all-in-all-out management systems (Duhamel, 1998). Affected pigs may require up to 28 additional days to reach slaughter weight (Taylor and Trott, 1997).

Host Animals

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Animal nameContextLife stageSystem
GallusDomesticated hostPoultry: Mature female
Sus scrofa (pigs)Domesticated hostPigs: Weaner|Pigs/Growing-finishing pig

Hosts/Species Affected

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Besides pigs, B. pilosicoli has been isolated from the faeces or large intestines of humans (Lee and Hampson, 1994; Trivett-Moore et al., 1998), dogs (Lee and Hampson, 1994; Duhamel et al., 1998b), wild and domestic waterbirds such as ducks (Trott et al., 1997; Oxberry et al., 1998), chickens (McLaren et al., 1997; Stephens and Hampson, 1999), ring-necked pheasants (Webb et al., 1997) and guineapigs (Hélie et al., 2000).


Predispositions


Animal husbandry systems where groups of young pigs are moved into close proximity with older animals (such as following movement from weaner to grower houses in continuous flow production systems) predisposes to infection. Overcrowding and exposure to faeces in open channels also predisposes.

Some dietary interactions with disease have been observed. Feeding pelleted diets increases the risk of diarrhoea in infected pigs compared to feeding meal (Spearman et al., 1988). A rice-based diet low in soluble fibre delayed colonization of experimentally challenged pigs compared with a conventional non-pelleted wheat and lupin diet (Hampson et al., 2000).

Systems Affected

Top of page digestive diseases of pigs

Distribution

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Brachyspira pilosicoli has been identified in pigs in studies in the UK (Taylor et al., 1980; Thomson et al., 1998), continental Europe (Cizek et al., 1998; Hommez et al., 1998a; Pronost et al., 1999), Scandinavia (Fellström et al., 1996; Møller et al., 1998; Heinonen et al., 2000), Canada (Jacques et al., 1989; Girard et al., 1995), USA (Duhamel, 1998), Brazil (Barcellos et al., 2000) and Australasia (Lee et al., 1993; Hampson and Trott, 1995; Fairley, 1997). Although there are no published reports in the English language from other regions of the world, it is almost certain that the organism is both present and widespread. Until recently, easy and reliable methods of laboratory identification and diagnosis for B. pilosicoli have not been available, and consequently their have been limited numbers of publications on distribution and prevalence.

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Pathology

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At postmortem examination those affected animals which have had chronic diarrhoea may be in poor body condition and show faecal staining of the perineum. Generally, gross and histological lesions are restricted to the large intestine. In severe cases there may be oedema between the coils of the large intestine. Gross examination of the opened colon usually reveals a mild colitis with patches of reddened mucosa. Histologically a pathognomonic feature of the disease is the presence of a false brush border of spirochaetes attached to the caecal and colonic epithelium adjacent to the lumen. This feature is not present in all cases, and is usually more obvious in the early stages of the disease. More severe erosive lesions with denuding of epithelium and haemorrhage, sometimes associated with the protozoan Balantidium coli, may be found in some pigs (Hampson et al., 2000). These severe lesions are difficult to distinguish from the lesions of swine dysentery. Crypt abscesses containing spirochaetes have also been reported in experimentally infected pigs (Trott et al., 1996b).

Diagnosis

Top of page Clinical Diagnosis

Accurate diagnosis on clinical grounds alone is not possible. Affected pigs may show an intermittent mucoid grey or grey-green porridge-like diarrhoea. Characteristically there is a retardation in growth rate continuing over several weeks. The disease is rarely fatal, and subclinical infections are common.


Lesions

Lesions are restricted to the large intestine, and are usually focal. Gross lesions are not sufficient to provide a definitive diagnosis.


Differential Diagnosis

The main differential diagnoses are swine dysentery caused by Brachyspira hyodysenteriae, proliferative enteropathy caused by Lawsonia intracellularis, Salmonellosis caused by various serovars of Salmonella enterica, Yersiniasis caused by various species of Yersinia, whipworm infection by Trichuris suis, and non-specific colitis – a colitis associated with diet (Hampson and Trott, 1999; Johnston et al., 1999).


Laboratory Diagnosis and Suitability

Brachyspira pilosicoli is usually isolated on blood agar plates containing selective antibiotics. The isolation plates most usually used are Trypticase Soy agar containing 5% defibrinated ovine blood, 400 µg spectinomycin and 25 µg each of colistin and vancomycin (Jenkinson and Wingar, 1983). Plates are incubated anaerobically at 37oC for between 3 and 10 days (Muniappa et al., 1997). The spirochaetes produce a weak haemolysis on the plates. Examination of scrapings of the growth under phase contrast or dark field microscopy reveals the presence of spirochaetes with typical morphology.

A number of phenotypic and biochemical properties are then used to differentiate B. pilosicoli from other weakly haemolytic non-pathogenic intestinal spirochaetes with which they are easily confused. B. pilosicoli typically is indole negative and lacks ß-glucosidase activity, but hydrolyses hippurate (Fellström and Gunnarsson, 1995; Trott et al., 1996a; Fellström et al., 1997). Identification can be confirmed by the use of specific polymerase chain reaction tests based on the 16S rRNA, 23S rRNA or NADH oxidase genes (Park et al., 1995; Fellström et al., 1997; Leser et al., 1997; Muniappa et al., 1997; Atyeo et al., 1999). These tests are usually only available in specialized laboratories. The spirochaete has also been localized in the colon using in situ hybridization (Boyne et al., 1998; Jensen et al., 2000). Monoclonal antibodies that react specifically with B. pilosicoli have been prepared (Lee and Hampson, 1995; Tenaya et al., 1998), but these have not been widely used for diagnostic purposes.


Immunology


To date little work has been conducted on the immune response to B. pilosicoli in infected pigs. In one study, using Western blot analysis, pigs that had recovered from infection showed a serum antibody response to three outer membrane proteins of B. pilosicoli (Zhang et al., 1999). In another study, experimentally infected pigs showed no systemic antibody response to B. pilosicoli using an ELISA system with protein extracts from the organism as plate-coating antigen (Hampson et al., 2000). Local immune responses in the colon have not been evaluated.

Strain typing

The species B. pilosicoli is diverse, and shows evidence of being recombinant (Trott et al., 1998). Large numbers of distinct strains have been identified using molecular strain typing techniques, particularly pulsed field gel electrophoresis (Atyeo et al., 1996; Trott et al., 1998).

List of Symptoms/Signs

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SignLife StagesType
Digestive Signs / Anorexia, loss or decreased appetite, not nursing, off feed Sign
Digestive Signs / Bloody stools, faeces, haematochezia Sign
Digestive Signs / Diarrhoea Pigs:Weaner,Pigs:Growing-finishing pig Diagnosis
Digestive Signs / Mucous, mucoid stools, faeces Pigs:Weaner,Pigs:Growing-finishing pig Sign
General Signs / Dehydration Pigs:Weaner,Pigs:Growing-finishing pig Sign
General Signs / Fever, pyrexia, hyperthermia Sign
General Signs / Lack of growth or weight gain, retarded, stunted growth Pigs:Weaner Sign
General Signs / Trembling, shivering, fasciculations, chilling Pigs:Weaner Sign
General Signs / Underweight, poor condition, thin, emaciated, unthriftiness, ill thrift Pigs:Weaner Sign
General Signs / Weight loss Pigs:Weaner,Pigs:Growing-finishing pig Sign
Nervous Signs / Dullness, depression, lethargy, depressed, lethargic, listless Sign
Skin / Integumentary Signs / Soiling of the vent in birds Poultry:Young poultry Sign

Disease Course

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Following oral challenge the organisms can be detected in the faeces within 2-7 days, however the incubation period for disease may extend up to 20 days (Hampson and Trott, 1999). Colonization can be prolonged, with intermittent diarrhoea occurring over a period of six weeks or more.

Initial studies suggested that B. pilosicoli was not attracted to porcine mucin (Milner and Sellwood, 1994), but more recent studies indicate that it does undergo a chemotactic response, but this is modulated by the presence of certain specific substrates (Witters and Duhamel, 1999). The spirochaetes multiply close to the mucosal surface and in the crypts of the large intestine. Cells attach by one end to the colonic epithelial surface adjacent to the lumen, but do not attach to enterocytes lining the crypts. Large numbers of spirochaetes may be observed in dense mats, forming a "false brush border". Effacement of microvilli may occur, and occasionally the enterocytes may die and be sloughed into the lumen. Spirochaetes are sometimes seen in the superficial layer of the lamina propria. Mild local inflammatory responses occur, and crypt abscesses may be seen.

Epidemiology

Top of page Life Cycle

Brachyspira pilosicoli primarily resides in the lumen and crypts of the large intestine (caecum, colon, and sometimes the rectum) of pigs, and of certain other animal species. The spirochaete is known to remain viable in lake water at 4oC for up to 66 days, and it is possible that it can multiply and undergo an independent life cycle in nutrient-rich water bodies, perhaps in association with protozoa (Oxberry et al., 1998). The organism also can form resistant cyst-like structures that may aid in its survival outside the intestinal tract (Barber et al., 1995).

Transmission

Transmission is believed to be through the faecal-oral route, with young pigs being infected by ingestion of faeces from older animals which are colonized by the spirochaete. Colonization can be prolonged in individual pigs, with faecal shedding occurring for six weeks or more. The spirochaete may also survive for weeks in faeces and slurry, so contaminated boots, clothing and other fomites may be involved in indirect transmission of infection.

Vectors

S. pilosicoli frequently colonizes wild waterbirds (Oxberry et al., 1998), and mice have been experimentally infected with the spirochaete (Sacco et al., 1997). Accordingly, birds and mice could act as vectors of the spirochaete both within and between piggeries.

Distribution

Where specific surveys have been conducted, infection with B. pilosicoli has been shown to be widespread. In the UK, a study of 85 herds with diarrhoea showed that B. pilosicoli was the sole pathogen in 32.9% of farms with colitis in grower pigs (Thomson et al., 1998). In Sweden, B. pilosicoli was isolated from pigs in six of seven herds with diarrhoea, and from one of eight herds without diarrhoea (Fellström et al., 1996). In Denmark B. pilosicoli was isolated from 10 of 72 (13.9%) herds with diarrhoea but from none of 26 herds where diarrhoea was not a problem (Møller et al., 1998). In Brazil B. pilosicoli was isolated from grower pigs on seven of 17 farms where diarrhoea was a problem (Barcellos et al., 2000). Within-herd prevalence of infection also varies greatly. In a study of farms with B. pilosicoli infection in the UK, between 5-15% of different batches of pigs were estimated to be infected (Thomson et al., 1998). In a commercial herd in Papua New Guinea, 34% of 50 pigs of mixed ages sampled were found to be infected (Trott et al., 1997). Strain typing of 14 of these isolates using pulsed field gel electrophoresis showed that they belonged to nine different PFGE strain types (Trott et al., 1998). Multiple strains of the organism may cycle between batches of pigs. The most common time for infection to occur is in pigs of 8-14 weeks of age, particularly within 1-2 weeks of mixing batches of pigs.

Impact: Economic

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The economic importance and impact of porcine intestinal spirochaetosis varies from herd to herd, and can be significant in certain herds. There has been no economic analysis of the overall costs of the disease to the pig industry worldwide.

Zoonoses and Food Safety

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Brachyspira pilosicoli is capable of colonizing the large intestines of humans, and it has been associated with chronic diarrhoea and rectal bleeding (Douglas and Crucioli, 1981). In western societies, patients with immune deficiencies, such as those induced by the Human Immunodeficiency Virus (AIDS), are particularly susceptible to infection (Käsbohrer et al., 1990). Since B. pilosicoli has a wide host range it is likely that humans can be colonized by strains acquired from animals (Trott et al., 1997). The significance of this possible transmission in relation to food products of animal origin is uncertain (Higgins, 1999).

Disease Treatment

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Treatments for porcine intestinal spirochaetosis are based on those used for swine dysentery. A number of antimicrobial agents are available for use, and these may be given either in the water or by injection. In-feed medication is more generally used for prevention rather than treatment.

The most common drugs used for treatment are tiamulin and lincomycin. Resistance by porcine B. pilosicoli strains to lincomycin (Duhamel et al., 1998a) and to tiamulin (Fossi et al., 1999) has been reported.

Prevention and Control

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An experimental autogenous bacterin vaccine failed to protect experimentally infected pigs (Hampson et al., 2000). No other vaccine against B. pilosicoli has been reported.

Pigs at risk of infection, for example following movement from weaner to grower sheds in continuous flow systems, sometimes are given in-feed antibiotics as a prophylactic measure.

Management factors that predispose to infection, such as mixing and crowding of pigs, should be avoided.

Feeding of meal or mash rather than pelleted diets may reduce the occurrence of diarrhoea where there is a specific problem in a herd.

References

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Andrews JJ; Hoffman LJ, 1983. A porcine colitis caused by a weakly beta-hemolytic treponeme (Treponema innocens?). Proceedings of Annual Meeting of the American Association of Veterinary Laboratory Diagnosticians, 25:395-402; [Library: BL 6841.2207]; 14 ref.

Atyeo RF; Oxberry SL; Hampson DJ, 1996. Pulsed-field gel electrophoresis for sub-specific differentiation of Serpulina pilosicoli (formerly 'Anguillina coli'). FEMS Microbiology Letters, 141(1):77-81; 14 ref.

Atyeo RF; Stanton TB; Jensen NS; Suriyaarachichi DS; Hampson DJ, 1999. Differentiation of Serpulina species by NADH oxidase gene (nox) sequence comparisons and nox-based polymerase chain reaction tests. Veterinary Microbiology, 67(1):47-60; 37 ref.

Barber PM; Lewis GM; Barrett SP, 1995. Localisation of carbohydrate and DNA in cyst-like structures from human intestinal spirochaete. Anaerobe, 104:261-266.

Barcellos DESN; Mathiesen MR; Uzeda Mde; Kader IITA; Duhamel GE, 2000. Prevalence of Brachyspira species isolated from diarrhoeic pigs in Brazil. Veterinary Record, 146(14):398-403; 43 ref.

Boyne M; Jensen TK; Moller K; Leser TD; Jorsal SE, 1998. Specific detection of the genus Serpulina, S. hyodysenteriae and S. pilosicoli in porcine intestines by fluorescent rRNA in situ hybridization. Molecular and Cellular Probes, 12:323-330.

Castryck A; Hommez J; Miry C; Lein A, 1997. Porcine intestinal spirochaetosis caused by Serpulina pilosicoli in Belgium. Vlaams Diergeneeskundig Tijdschrift, 66(3):125-128; 25 ref.

Cizek A; Smola J; Madr P, 1998. In vitro activity of six anti-dysenteric drugs on Serpulina hyodysenteriae and S. pilosicoli strains isolated in the Czech Republic. In: Done S, Thomson J, Varley M. (eds). Proceedings of the 15th IPVS Congress, Birmingham, England. 3:135.

Douglas JG; Crucioli V, 1981. Spirochaetosis: a remediable cause of diarrhoea and rectal bleeding? British Medical Journal, 283:1362.

Duhamel GE, 1998. Colonic spirochetosis caused by Serpulina pilosicoli. Large Animal Practice, 19(1):14-22; 24 ref.

Duhamel GE; Kinyon JM; Mathiesen MR; Murphy DP; Walter D, 1998. In vitro activity of four antimicrobial agents against North American isolates of porcine Serpulina pilosicoli. Journal of Veterinary Diagnostic Investigation, 10(4):350-356; 39 ref.

Duhamel GE; Trott DJ, Muniappa N et al. , 1998. Canine intestinal spirochetes consist of Serpulina pilosicoli and a newly identified group provisionally designated "Serpulina canis" sp. nov. Journal of Clinical Microbiology 36:2264-2270.

Dünser M; Scheighardt H; Pangerl R; Awad-Masalmeh M; Schuh M, 1997. Swine dysentery and spirochaetal diarrhoea - a comparative study of enteritis cases caused by Serpulina.. Wiener Tierärztliche Monatsschrift, 84(6):151-161; 46 ref.

Fairley R, 1997. Infectious diseases of pigs in New Zealand. Surveillance-Wellington, 24:5-7.

Fellström C; Gunnarsson A, 1995. Phenotypical characterisation of intestinal spirochaetes isolated from pigs. Research in Veterinary Science, 59(1):1-4; 28 ref.

Fellström C; Pettersson B; Johansson KE; Lundeheim N; Gunnarsson A, 1996. Prevalence of Serpulina species in relation to diarrhea and feed medication in pig-rearing herds in Sweden. American Journal of Veterinary Research, 57(6):807-811; 42 ref.

Fellström C; Pettersson B; Thomson J; Gunnarsson A; Persson M; Johansson KE, 1997. Identification of Serpulina species associated with porcine colitis by biochemical analysis and PCR. Journal of Clinical Microbiology, 35(2):462-467; 30 ref.

Fossi M; Saranpaa T; Rautiainen E, 1999. In vitro sensitivity of the swine Brachyspira species to tiamulin in Finland. Acta Vet. Scand., 40(4):355-358.

Girard C; Lemarchand T; Higgins R, 1995. Porcine colonic spirochetosis: a retrospective study of eleven cases. Canadian Veterinary Journal, 36(5):291-294; 17 ref.

Hampson DJ; Trott DJ, 1995. A review - intestinal spirochaetal infections of pigs: an overview with an Australian perspective. Manipulating pig production 5. Proceedings of the Fifth Biennial Conference of the Australasian Pig Science Association (APSA) held in Canberra, ACT on November 26 to 29, 1995., 139-169; many ref.

Hampson DJ; Trott DJ, 1999. Spirochetal diarrhea/porcine intestinal spirochetosis. In: Straw BE, D'Allaire S, Mengeling WL, Taylor DJ (eds), Diseases of Swine, 8th Ed. Ames, Iowa: Iowa State university Press, 553-562.

Hampson; DJ; Robertson ID, La T et al. , 2000. Influences of diet and vaccination on colonisation of pigs with the intestinal spirochaete Brachyspira (Serpulina) pilosicoli. Veterinary Microbiology, 73:75-84.

Harland WA; Lee FD, 1967. Intestinal spirochaetosis. British Medical Journal, 3:718-719.

Heinonen M; Fossi M, Jalli J-P et al. , 2000. Detectability and prevalence of Brachyspira species in herds rearing health class feeder pigs in Finland. Veterinary Record, 146:343-347.

Hélie P; Harel J; Higgins R, 2000. Intestinal spirochaetosis in a guinea pig with colorectal prolapse. Canadian Veterinary Journal, 41:134.

Higgins R, 1999. Infections of uncertain zoonotic origin. Médecin Vétérinaire du Québec, 29(1):29, 32-35; 2 pp. of ref.

Hommez J; Castryck F; Haesebrouck F; Devriese LA, 1998. Identification of porcine Serpulina strains in routine diagnostic bacteriology. Veterinary Microbiology, 62(2):163-169; 19 ref.

Hommez J; Devriese LA; Castryck F; Miry C; Lein A; Haesebrouck F, 1998. Susceptibility of different Serpulina species in pigs to antimicrobial agents. Vlaams Diergeneeskundig Tijdschrift, 67(1):32-35; 7 ref.

Hovind-Hougen K, Birch-Andersen A et al. , 1984. Intestinal spirochaetosis: morphological characterization and cultivation of the spirochete Brachyspira aalborgi gen. nov. sp. nov. Journal of Clinical Microbiology, 16:1127-1136.

Jacques M; Girard C; Higgins R; Goyette G, 1989. Extensive colonization of the porcine colonic epithelium by a spirochete similar to Treponema innocens.. Journal of Clinical Microbiology, 27(5):1139-1141; 16 ref.

Jenkinson SR; Wingar CR, 1983. Sensitivity to dimetridazole of field isolates of Treponema hyodysenteriae. Veterinary Record, 112: 58.

Jensen TK; MOller K; Boye M; Leser TD; Jorsal SE, 2000. Scanning electron microscopy and fluorescent in situ hybridization of experimental Brachyspira (Serpulina) pilosicoli infection in growing pigs. Veterinary Pathology, 37(1):22-32; 43 ref.

Johnston T; Dewey C; Walter D; Duhamel GE; Mathiesen MR; Smart N, 1999. Recent advances in diagnosing and controlling porcine colonic spirochetosis. Compendium on Continuing Education for the Practicing Veterinarian, 21(Supplement 9):S198-S231; 46 ref.

Käsbohrer A; Gelderblom HR, Arasteh K et al. , 1990. Intestinal spirochaetosis in HIV infection: prevalence, isolation and morphology of spirochaetes. Deutsche Medizinische Wochenschrift, 115:1499-1506.

Lee BJ; Hampson DJ, 1995. A monoclonal antibody reacting with the cell envelope of spirochaetes isolated from cases of intestinal spirochaetosis in pigs and humans. FEMS Microbiology Letters, 131(2):179-184; 16 ref.

Lee JI; Hampson DJ, 1994. Genetic characterisation of intestinal spirochaetes and their association with disease. Journal of Medical Microbiology, 40:365-371.

Lee JI; Hampson DJ; Lymbery AJ, 1991. The intestinal spirochaetes: genetic diversity and disease associations. Manipulating pig production III., 140; [Proceedings, 3rd Biennial Conference, Australasian Pig Science Association, Albury, NSW, Nov. 24-27, 1991]; 5 ref.

Lee JI; Hampson DJ; Lymbery AJ; Harders SJ, 1993. The porcine intestinal spirochaetes: identification of new genetic groups. Veterinary Microbiology, 34(3):273-285; 27 ref.

Leser TD; Moller K; Jensen TK; Jorsal SE, 1997. Specific detection of Serpulina hyodysenteriae and potentially pathogenic weakly haemolytic porcine intestinal spirochaetes by polymerase chain reaction targeting 23S rDNA. Molecular and Cellular Probes, 11:363-372.

McLaren AJ; Trott DJ; Swayne DE; Oxberry SL; Hampson DJ, 1997. Genetic and phenotypic characterization of intestinal spirochetes colonizing chickens and allocation of known pathogenic isolates to three distinct genetic groups. Journal of Clinical Microbiology, 35(2):412-417; 32 ref.

Milner JA; Sellwood R, 1994. Chemotactic response to mucin by Serpulina hyodysenteriae and other porcine spirochetes: potential role in intestinal colonization. Infection and Immunity, 62(9):4095-4099; 38 ref.

Mohan Ramanathan; Duhamel GE; Mathiesen MR; Messier S, 1993. Identification and partial characterization of a group of weakly -hemolytic intestinal spirochetes of swine distinct from Serpulina innocens isolate B256. Veterinary Microbiology, 37(1/2):53-64; 27 ref.

Montanari L, 1998. Colitis caused by Serpulina pilosicoli. Obiettivi e Documenti Veterinari, 19(Supp):23-26; 20 ref.

Muniappa N; Duhamel GE, 1997. Outer membrane-associated serine protease of intestinal spirochaetes. FEMS Microbiology Letters, 154(1):159-164; 26 ref.

Muniappa N; Mathiesen MR; Duhamel GE, 1997. Laboratory identification and enteropathogenicity testing of Serpulina pilosicoli associated with porcine colonic spirochaetosis. Journal of Veterinary Diagnostic Investigation, 9(2):165-171; 36 ref.

Møller K; Jensen TK; Jorsal SE; Leser TD; Carstensen B, 1998. Detection of Lawsonia intracellularis, Serpulina hyodysenteriae, weakly beta-haemolytic intestinal spirochaetes, Salmonella enterica, and haemolytic Escherichia coli from swine herds with and without diarrhoea among growing pigs. Veterinary Microbiology, 62(1):59-72; 28 ref.

Ochiai S; Adachi Y; Mori K, 1997. Unification of the genera Serpulina and Brachyspira, and proposals of Brachyspira hyodysenteriae comb. nov., Brachyspira innocens comb. nov. and Brachyspira pilosicoli comb. nov. Microbiology and Immunology, 41(6):445-452; 26 ref.

Oxberry SL; Trott DJ; Hampson DJ, 1998. Serpulina pilosicoli, water birds and water: potential sources of infection for humans and other animals. Epidemiology and Infection, 121:219-225.

Park NY; Chung CY; McLaren AJ; Atyeo RF; Hampson DJ, 1995. Polymerase chain reaction for identification of human and porcine spirochaetes recovered from cases of intestinal spirochaetosis. FEMS Microbiology Letters, 125(2/3):225-230; 22 ref.

Pronost S; Baluti-Osako M; Dumontier S; Leguennec J; Fortier G; Moalic PY, 1999. Advantages of PCR for pathogenic Brachyspira strains identification in swine. Revue de Médecine Vétérinaire, 150(10):803-808; 14 ref.

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