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==Lifecycle and pathogenesis==
==Lifecycle and pathogenesis==
Infection of ''B. pilosicoli'' is acquired the [[faecal-oral route]]. Once in the alimentary tract, the bacterium invades its target cells in the [[large intestine]] causing [[oedema]], [[haemorrhage]] and the infiltration by inflammatory cells. The consequences of this are the sloughing of cells into the intestinal lumen, [[malabsorption]] and secretory diarrhea which could last up to 2 weeks.<ref name=":0" />
Infection of ''Brachyspira pilosicoli'' is acquired via the [[faecal-oral route]]. Once in the alimentary tract, the bacterium invades its target cells in the [[large intestine]] causing [[oedema]], [[haemorrhage]] and the infiltration by inflammatory cells. The consequences of this are the sloughing of cells into the intestinal lumen, [[malabsorption]] and secretory diarrhea which could last up to two weeks.<ref name=":0" />


==Diseases==
==Diseases==
''B. pilosicoli'' is the cause of [[porcine intestinal spirochaetosis]]. The presence of the spirochaetes in grey-pink diarrhoea is diagnostic.
''Brachyspira pilosicoli'' is the cause of [[porcine intestinal spirochaetosis]]. The presence of the spirochaetes in grey-pink diarrhoea is diagnostic.

== Zoonotic potential ==
Anaerobic host-associated spirochetes of the genus ''Brachyspira'' colonize the oral cavity, intestinal tract, and genital region of animals and humans.<ref>{{Cite journal|last=Mappley|first=Luke J.|last2=Black|first2=Michael L.|last3=AbuOun|first3=Manal|last4=Darby|first4=Alistair C.|last5=Woodward|first5=Martin J.|last6=Parkhill|first6=Julian|last7=Turner|first7=A. Keith|last8=Bellgard|first8=Matthew I.|last9=La|first9=Tom|last10=Phillips|first10=Nyree D.|last11=La Ragione|first11=Roberto M.|date=2012-09-05|title=Comparative genomics of Brachyspira pilosicoli strains: genome rearrangements, reductions and correlation of genetic compliment with phenotypic diversity|url=https://doi.org/10.1186/1471-2164-13-454|journal=BMC Genomics|volume=13|issue=1|pages=454|doi=10.1186/1471-2164-13-454|issn=1471-2164|pmc=PMC3532143|pmid=22947175}}</ref>  The principal species of veterinary significance is ''Brachyspira hyodysenteriae'', the causative agent of swine dysentery.<ref name=":1">{{Cite journal|last=Casas|first=Vanessa|last2=Rodríguez-Asiain|first2=Arantza|last3=Pinto-Llorente|first3=Roberto|last4=Vadillo|first4=Santiago|last5=Carrascal|first5=Montserrat|last6=Abian|first6=Joaquin|date=2017|title=Brachyspira hyodysenteriae and B. pilosicoli Proteins Recognized by Sera of Challenged Pigs|url=https://www.frontiersin.org/articles/10.3389/fmicb.2017.00723/full|journal=Frontiers in Microbiology|language=English|volume=8|doi=10.3389/fmicb.2017.00723|issn=1664-302X}}</ref> However, other organisms in this group have been associated with disease in animals, including ''Brachyspira pilosicoli'', a causative agent of porcine intestinal spirochaetosis.<ref name=":1" /> Whereas most ''Brachyspira'' have a restricted host range, ''B. pilosicoli'' colonizes a variety of domestic animals, including pigs, chickens, and dogs, as well as wild birds, rodents, and humans.<ref name=":2">{{Cite journal|last=Hampson|first=David J.|date=2017-11-29|title=The Spirochete Brachyspira pilosicoli, Enteric Pathogen of Animals and Humans|url=https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5740978/|journal=Clinical Microbiology Reviews|volume=31|issue=1|doi=10.1128/CMR.00087-17|issn=0893-8512|pmc=5740978|pmid=29187397}}</ref>  In particular, ''B. pilosicoli'' has been described as an important colonic pathogen of pigs and chickens, causing colitis and diarrhea resulting in depressed rates of growth and impaired production on farms where infections with ''B. pilosicoli'' may be endemic.<ref name=":1" /><ref name=":3">{{Cite journal|last=Le Roy|first=Caroline I.|last2=Mappley|first2=Luke J.|last3=La Ragione|first3=Roberto M.|last4=Woodward|first4=Martin J.|last5=Claus|first5=Sandrine P.|date=2015-12-15|title=Brachyspira pilosicoli-induced avian intestinal spirochaetosis|url=https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4683989/|journal=Microbial Ecology in Health and Disease|volume=26|doi=10.3402/mehd.v26.28853|issn=0891-060X|pmc=4683989|pmid=26679774}}</ref>  In addition, ''B. pilosicoli'' is associated with clinical disease in human infections, thus possessing public health implications.<ref name=":4">{{Cite journal|last=Neo|first=Eugene|last2=La|first2=Tom|last3=Phillips|first3=Nyree Dale|last4=Alikani|first4=Mohammad Yousef|last5=Hampson|first5=David J|date=2013-12|title=The pathogenic intestinal spirochaete Brachyspira pilosicoli forms a diverse recombinant species demonstrating some local clustering of related strains and potential for zoonotic spread|url=https://gutpathogens.biomedcentral.com/articles/10.1186/1757-4749-5-24|journal=Gut Pathogens|language=en|volume=5|issue=1|pages=24|doi=10.1186/1757-4749-5-24|issn=1757-4749|pmc=PMC3751851|pmid=23957888}}</ref>  


Interspecies transmission of ''B. pilosicoli'' has been demonstrated;<ref name=":2" /> zoonotic transmission is highly likely, although it has not been conclusively shown.<ref name=":4" />  A number of studies that have isolated ''B. pilosicoli'' from fecal carriage have identified environmental factors that may be important in transmission.<ref name=":5">{{Cite journal|last=Trott|first=Darren J.|last2=Mikosza|first2=Andrew S. J.|last3=Combs|first3=Barry G.|last4=Oxberry|first4=Sophy L.|last5=Hampson|first5=David J.|date=1998|title=Population genetic analysis of Serpulina pilosicoli and its molecular epidemiology in villages in the Eastern Highlands of Papua New Guinea|url=https://www.microbiologyresearch.org/content/journal/ijsem/10.1099/00207713-48-3-659|journal=International Journal of Systematic and Evolutionary Microbiology,|volume=48|issue=3|pages=659–668|doi=10.1099/00207713-48-3-659|issn=1466-5026}}</ref>  Specifically, the spirochete is passed in feces and may survive for prolonged periods in natural water systems such as lakes and ponds, from which it can be isolated.<ref name=":6">{{Cite journal|last=Hampson|first=David J.|date=2018-01-01|title=The Spirochete Brachyspira pilosicoli, Enteric Pathogen of Animals and Humans|url=https://cmr.asm.org/content/31/1/e00087-17|journal=Clinical Microbiology Reviews|language=en|volume=31|issue=1|doi=10.1128/CMR.00087-17|issn=0893-8512|pmid=29187397}}</ref>  Therefore, it is presumed that infection occurs in humans via the oral route following exposure to infected fecal material of either human or animal origin.<ref name=":6" />  Colonization of the intestinal tract and consequential spirochaetosis, the presence of spirochetes forming a dense fringe or brush border on the colonic epithelium, is more commonly described.<ref name=":6" />  Incidences of blood-borne infections have been observed, however, cases of spirochetemia with ''B. pilosicoli'' are relatively uncommon.<ref name=":7">{{Cite journal|last=Prim|first=Núria|last2=Pericas|first2=Roser|last3=Español|first3=Montse|last4=Rivera|first4=Alba|last5=Mirelis|first5=Beatriz|last6=Coll|first6=Pere|date=2011-10|title=Bloodstream Infection Due to Brachyspira pilosicoli in a Patient with Multiorgan Failure▿|url=https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3187341/|journal=Journal of Clinical Microbiology|volume=49|issue=10|pages=3697–3699|doi=10.1128/JCM.00680-11|issn=0095-1137|pmc=3187341|pmid=21832021}}</ref>  The incidence of intestinal colonization with ''B. pilosicoli'' and consequential spirochaetosis is associated with crowded and unhygienic conditions in developing countries.<ref name=":5" /><ref name=":8">{{Cite journal|last=Margawani|first=K. Rini|last2=Robertson|first2=Ian D.|last3=Brooke|first3=C. Josephine|last4=Hampson|first4=David J.|date=2004-04|title=Prevalence, risk factors and molecular epidemiology of Brachyspira pilosicoli in humans on the island of Bali, Indonesia|url=https://pubmed.ncbi.nlm.nih.gov/15017290/|journal=Journal of Medical Microbiology|volume=53|issue=Pt 4|pages=325–332|doi=10.1099/jmm.0.05415-0|issn=0022-2615|pmid=15017290}}</ref>  As a consequence of the spirochete’s ability to survive for long periods of time in stagnant water, there is conclusive evidence that suggests contaminated water sources may account for the high rates of intestinal carriage with ''B. pilosicoli'' found in developing communities.<ref name=":2" />  Studies investigating the prevalence of ''B. pilosicoli'' in human fecal carriage in Latin America demonstrate that human colonization with ''B. pilosicoli'' is significantly more common in individuals living in villages than in those living in an urban area.<ref name=":5" />  Specifically, if hygiene in a village is poor due to lack of modern sanitation and reliance on nearby streams as a sole source of water, fecal-oral transmission of ''B. pilosicoli'' is favoured.<ref name=":5" />  Similarly, the prevalence of ''B. pilosicoli'' in human fecal carriage is greater in crowded periurban areas that contain pigs and other animal species, where water is collected from shallow wells rather than having a supply of clean tap water as seen in urban areas.<ref name=":8" />  Opportunities for interspecies transmission of ''B. pilosicoli'' is more likely to occur in households where animals and humans live in close proximity, thus individuals working with intensively farmed pigs, chickens, or other farmed species may be at increased risk of exposure.<ref name=":8" />  In addition, it has been suggested that ''B. pilosicoli'' is able to survive meat processing and thus serves as a potential risk to consumers via contaminated raw meat.<ref name=":3" />  Largely as a consequence of the considerable genetic similarities between strains of ''B. pilosicoli'' infecting humans, swine, and poultry, the potential to adapt to various hosts exists.<ref name=":3" />


Human case reports of ''B. pilosicoli'' spirochaetosis have been described, suggesting that individuals colonized with ''B. pilosicoli'' may develop focal colitis and chronic diarrhoea, with abdominal pain, flatulence, gastrointestinal bleeding, rectal discharge, watery diarrhea, and pseudoappendicitis.<ref name=":9">{{Cite journal|last=Kanavaki|first=S.|last2=Mantadakis|first2=E.|last3=Thomakos|first3=N.|last4=Pefanis|first4=A.|last5=Matsiota-Bernard|first5=P.|last6=Karabela|first6=S.|last7=Samonis|first7=G.|date=2002-06-01|title=Brachyspira (Serpulina) pilosicoli Spirochetemia in an Immunocompromised Patient|url=https://doi.org/10.1007/s15010-002-2175-1|journal=Infection|language=en|volume=30|issue=3|pages=175–177|doi=10.1007/s15010-002-2175-1|issn=1439-0973}}</ref>  Colonoscopic examination often reveals a normal-appearing mucosa.<ref name=":2" /> However, edematous and erythematous mucosal changes have been reported.<ref name=":2" />  Following the apparition of any symptoms, intestinal spirochaetosis is confirmed by biopsy.<ref name=":2" />  Overall, human intestinal spirochaetosis with ''B. pilosicoli'' is relatively uncommon and there is debate in regards to its clinical significance as most cases are asymptomatic.<ref name=":2" />  Incidence of colonization is associated with crowded and unhygienic conditions in developing countries and in specific populations such as Australian Aborigines, as well as amongst homosexual males and HIV+ patients in western countries.<ref name=":7" />  Of those already colonized, spirochetemia has been observed in individuals with impaired immune defence or injury of the gastrointestinal mucosa.<ref>{{Cite journal|last=Erlandson|first=Kristine Mace|last2=Klingler|first2=Edna Toubes|date=2005-06-15|title=Intestinal spirochetosis: epidemiology, microbiology, and clinical significance|url=http://www.sciencedirect.com/science/article/pii/S0196439905000243|journal=Clinical Microbiology Newsletter|language=en|volume=27|issue=12|pages=91–96|doi=10.1016/j.clinmicnews.2005.05.002|issn=0196-4399}}</ref>  Further evidence of ''B. pilosicoli'' pathogenicity includes human cases of invasive hepatic infection and hepatitis in chronically ill or immunocompromised individuals where the spirochetemia is likely to have been secondary to the immunosuppression.<ref name=":9" />  These cases are likely examples of human infections of pathogenic ''B. pilosicoli'' from enteric commensal populations as a consequence of increased microorganism virulence or diminished host defences.<ref name=":9" />  It remains unclear as to what extent spirochetemia may contribute to clinical signs in these patients, although some patients have shown multiorgan failure.<ref name=":7" />  Nevertheless, spirochetemia also appears to be a relatively rare phenomenon in individuals where fecal carriage has been observed.<ref name=":2" />  


== See also ==
== See also ==

Revision as of 22:34, 12 October 2020

Brachyspira pilosicoli
Scientific classification Edit this classification
Domain: Bacteria
Phylum: Spirochaetota
Class: Spirochaetia
Order: Brachyspirales
Family: Brachyspiraceae
Genus: Brachyspira
Species:
B. pilosicoli
Binomial name
Brachyspira pilosicoli
Brandt and Ingvorsen, 1998" [1]
Synonyms[1]

Brachyspira pilosicoli is a Gram-negative, spiral-shaped, obligate anaerobe bacterium. It is a member of the Spirochaete family. The bacterium is loosely coiled and is 6–11 µm long. It has several flagellae, inserted at either pole of the cell, and a lipopolysaccharide cell wall. It causes intestinal spirochetosis in pigs, chickens, and people, and has been isolated from other species such as dogs, rodents and horses as well.[2] It causes zoonotic infection in humans, with infection thought to originate from dogs.

Lifecycle and pathogenesis

Infection of Brachyspira pilosicoli is acquired via the faecal-oral route. Once in the alimentary tract, the bacterium invades its target cells in the large intestine causing oedema, haemorrhage and the infiltration by inflammatory cells. The consequences of this are the sloughing of cells into the intestinal lumen, malabsorption and secretory diarrhea which could last up to two weeks.[2]

Diseases

Brachyspira pilosicoli is the cause of porcine intestinal spirochaetosis. The presence of the spirochaetes in grey-pink diarrhoea is diagnostic.

Zoonotic potential

Anaerobic host-associated spirochetes of the genus Brachyspira colonize the oral cavity, intestinal tract, and genital region of animals and humans.[3]  The principal species of veterinary significance is Brachyspira hyodysenteriae, the causative agent of swine dysentery.[4] However, other organisms in this group have been associated with disease in animals, including Brachyspira pilosicoli, a causative agent of porcine intestinal spirochaetosis.[4] Whereas most Brachyspira have a restricted host range, B. pilosicoli colonizes a variety of domestic animals, including pigs, chickens, and dogs, as well as wild birds, rodents, and humans.[5]  In particular, B. pilosicoli has been described as an important colonic pathogen of pigs and chickens, causing colitis and diarrhea resulting in depressed rates of growth and impaired production on farms where infections with B. pilosicoli may be endemic.[4][6]  In addition, B. pilosicoli is associated with clinical disease in human infections, thus possessing public health implications.[7]  


Interspecies transmission of B. pilosicoli has been demonstrated;[5] zoonotic transmission is highly likely, although it has not been conclusively shown.[7]  A number of studies that have isolated B. pilosicoli from fecal carriage have identified environmental factors that may be important in transmission.[8]  Specifically, the spirochete is passed in feces and may survive for prolonged periods in natural water systems such as lakes and ponds, from which it can be isolated.[9]  Therefore, it is presumed that infection occurs in humans via the oral route following exposure to infected fecal material of either human or animal origin.[9]  Colonization of the intestinal tract and consequential spirochaetosis, the presence of spirochetes forming a dense fringe or brush border on the colonic epithelium, is more commonly described.[9]  Incidences of blood-borne infections have been observed, however, cases of spirochetemia with B. pilosicoli are relatively uncommon.[10]  The incidence of intestinal colonization with B. pilosicoli and consequential spirochaetosis is associated with crowded and unhygienic conditions in developing countries.[8][11]  As a consequence of the spirochete’s ability to survive for long periods of time in stagnant water, there is conclusive evidence that suggests contaminated water sources may account for the high rates of intestinal carriage with B. pilosicoli found in developing communities.[5]  Studies investigating the prevalence of B. pilosicoli in human fecal carriage in Latin America demonstrate that human colonization with B. pilosicoli is significantly more common in individuals living in villages than in those living in an urban area.[8]  Specifically, if hygiene in a village is poor due to lack of modern sanitation and reliance on nearby streams as a sole source of water, fecal-oral transmission of B. pilosicoli is favoured.[8]  Similarly, the prevalence of B. pilosicoli in human fecal carriage is greater in crowded periurban areas that contain pigs and other animal species, where water is collected from shallow wells rather than having a supply of clean tap water as seen in urban areas.[11]  Opportunities for interspecies transmission of B. pilosicoli is more likely to occur in households where animals and humans live in close proximity, thus individuals working with intensively farmed pigs, chickens, or other farmed species may be at increased risk of exposure.[11]  In addition, it has been suggested that B. pilosicoli is able to survive meat processing and thus serves as a potential risk to consumers via contaminated raw meat.[6]  Largely as a consequence of the considerable genetic similarities between strains of B. pilosicoli infecting humans, swine, and poultry, the potential to adapt to various hosts exists.[6]


Human case reports of B. pilosicoli spirochaetosis have been described, suggesting that individuals colonized with B. pilosicoli may develop focal colitis and chronic diarrhoea, with abdominal pain, flatulence, gastrointestinal bleeding, rectal discharge, watery diarrhea, and pseudoappendicitis.[12]  Colonoscopic examination often reveals a normal-appearing mucosa.[5] However, edematous and erythematous mucosal changes have been reported.[5]  Following the apparition of any symptoms, intestinal spirochaetosis is confirmed by biopsy.[5]  Overall, human intestinal spirochaetosis with B. pilosicoli is relatively uncommon and there is debate in regards to its clinical significance as most cases are asymptomatic.[5]  Incidence of colonization is associated with crowded and unhygienic conditions in developing countries and in specific populations such as Australian Aborigines, as well as amongst homosexual males and HIV+ patients in western countries.[10]  Of those already colonized, spirochetemia has been observed in individuals with impaired immune defence or injury of the gastrointestinal mucosa.[13]  Further evidence of B. pilosicoli pathogenicity includes human cases of invasive hepatic infection and hepatitis in chronically ill or immunocompromised individuals where the spirochetemia is likely to have been secondary to the immunosuppression.[12]  These cases are likely examples of human infections of pathogenic B. pilosicoli from enteric commensal populations as a consequence of increased microorganism virulence or diminished host defences.[12]  It remains unclear as to what extent spirochetemia may contribute to clinical signs in these patients, although some patients have shown multiorgan failure.[10]  Nevertheless, spirochetemia also appears to be a relatively rare phenomenon in individuals where fecal carriage has been observed.[5]  

See also

References

  1. ^ a b c Brandt KK, Ingvorsen K (1998). "Validation of the publication of new names and new combinations previously effectively published outside the IJSB. List No. 64". Int. J. Syst. Bacteriol.. 48: 327–8. doi:10.1099/00207713-48-1-327.
  2. ^ a b Hampson DJ (January 2018). "The Spirochete Brachyspira pilosicoli, Enteric Pathogen of Animals and Humans". Clinical Microbiology Reviews. 31 (1): e00087–17, /cmr/31/1/e00087–17.atom. doi:10.1128/CMR.00087-17. PMC 5740978. PMID 29187397.
  3. ^ Mappley, Luke J.; Black, Michael L.; AbuOun, Manal; Darby, Alistair C.; Woodward, Martin J.; Parkhill, Julian; Turner, A. Keith; Bellgard, Matthew I.; La, Tom; Phillips, Nyree D.; La Ragione, Roberto M. (2012-09-05). "Comparative genomics of Brachyspira pilosicoli strains: genome rearrangements, reductions and correlation of genetic compliment with phenotypic diversity". BMC Genomics. 13 (1): 454. doi:10.1186/1471-2164-13-454. ISSN 1471-2164. PMC 3532143. PMID 22947175.{{cite journal}}: CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
  4. ^ a b c Casas, Vanessa; Rodríguez-Asiain, Arantza; Pinto-Llorente, Roberto; Vadillo, Santiago; Carrascal, Montserrat; Abian, Joaquin (2017). "Brachyspira hyodysenteriae and B. pilosicoli Proteins Recognized by Sera of Challenged Pigs". Frontiers in Microbiology. 8. doi:10.3389/fmicb.2017.00723. ISSN 1664-302X.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  5. ^ a b c d e f g h Hampson, David J. (2017-11-29). "The Spirochete Brachyspira pilosicoli, Enteric Pathogen of Animals and Humans". Clinical Microbiology Reviews. 31 (1). doi:10.1128/CMR.00087-17. ISSN 0893-8512. PMC 5740978. PMID 29187397.
  6. ^ a b c Le Roy, Caroline I.; Mappley, Luke J.; La Ragione, Roberto M.; Woodward, Martin J.; Claus, Sandrine P. (2015-12-15). "Brachyspira pilosicoli-induced avian intestinal spirochaetosis". Microbial Ecology in Health and Disease. 26. doi:10.3402/mehd.v26.28853. ISSN 0891-060X. PMC 4683989. PMID 26679774.
  7. ^ a b Neo, Eugene; La, Tom; Phillips, Nyree Dale; Alikani, Mohammad Yousef; Hampson, David J (2013-12). "The pathogenic intestinal spirochaete Brachyspira pilosicoli forms a diverse recombinant species demonstrating some local clustering of related strains and potential for zoonotic spread". Gut Pathogens. 5 (1): 24. doi:10.1186/1757-4749-5-24. ISSN 1757-4749. PMC 3751851. PMID 23957888. {{cite journal}}: Check date values in: |date= (help)CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
  8. ^ a b c d Trott, Darren J.; Mikosza, Andrew S. J.; Combs, Barry G.; Oxberry, Sophy L.; Hampson, David J. (1998). "Population genetic analysis of Serpulina pilosicoli and its molecular epidemiology in villages in the Eastern Highlands of Papua New Guinea". International Journal of Systematic and Evolutionary Microbiology,. 48 (3): 659–668. doi:10.1099/00207713-48-3-659. ISSN 1466-5026.{{cite journal}}: CS1 maint: extra punctuation (link)
  9. ^ a b c Hampson, David J. (2018-01-01). "The Spirochete Brachyspira pilosicoli, Enteric Pathogen of Animals and Humans". Clinical Microbiology Reviews. 31 (1). doi:10.1128/CMR.00087-17. ISSN 0893-8512. PMID 29187397.
  10. ^ a b c Prim, Núria; Pericas, Roser; Español, Montse; Rivera, Alba; Mirelis, Beatriz; Coll, Pere (2011-10). "Bloodstream Infection Due to Brachyspira pilosicoli in a Patient with Multiorgan Failure▿". Journal of Clinical Microbiology. 49 (10): 3697–3699. doi:10.1128/JCM.00680-11. ISSN 0095-1137. PMC 3187341. PMID 21832021. {{cite journal}}: Check date values in: |date= (help)
  11. ^ a b c Margawani, K. Rini; Robertson, Ian D.; Brooke, C. Josephine; Hampson, David J. (2004-04). "Prevalence, risk factors and molecular epidemiology of Brachyspira pilosicoli in humans on the island of Bali, Indonesia". Journal of Medical Microbiology. 53 (Pt 4): 325–332. doi:10.1099/jmm.0.05415-0. ISSN 0022-2615. PMID 15017290. {{cite journal}}: Check date values in: |date= (help)
  12. ^ a b c Kanavaki, S.; Mantadakis, E.; Thomakos, N.; Pefanis, A.; Matsiota-Bernard, P.; Karabela, S.; Samonis, G. (2002-06-01). "Brachyspira (Serpulina) pilosicoli Spirochetemia in an Immunocompromised Patient". Infection. 30 (3): 175–177. doi:10.1007/s15010-002-2175-1. ISSN 1439-0973.
  13. ^ Erlandson, Kristine Mace; Klingler, Edna Toubes (2005-06-15). "Intestinal spirochetosis: epidemiology, microbiology, and clinical significance". Clinical Microbiology Newsletter. 27 (12): 91–96. doi:10.1016/j.clinmicnews.2005.05.002. ISSN 0196-4399.

Further reading

  • Hirsh DC, Maclachan NJ, Walker RL (2004). Veterinary Microbiology (2nd ed.). London: Wiley-Blackwell. pp. 131–133.