Brachyspira

Brachyspira
Scientific classification
Kingdom:
Bacteria
Phylum:
Spirochaetes
Class:
Spirochaetes
Order:
Brachyspirales
Family:
Brachyspiraceae
Genus:
Brachyspira Hovind-Hougen et al. 1983
Species
  • Brachyspira aalborgi Hovind-Hougen et al. 1983 emend. Ochiai, Adachi & Mori 1998 non Foliella non Pfeiffer 1855
  • Brachyspira alvinipulli Stanton et al. 1998
  • Brachyspira canis ♠ (Duhamel et al. 1998) Oxberry & Hampson 2003
  • Brachyspira corvi ♠ Jansson et al. 2008
  • Brachyspira hampsonii ♠ Chander et al. 2012
  • Brachyspira hyodysenteriae (Harris et al. 1972) Ochiai et al. 1998
  • Brachyspira ibaraki ♠ (presumably an 16S-rDNA variant of B. aalborgi)[1] ♠ Tachibana et al. 2003
  • Brachyspira innocens (Kinyon and Harris 1979) Ochiai et al. 1998
  • Brachyspira intermedia (Stanton et al. 1997) Hampson and La 2006
  • Brachyspira murdochii (Stanton et al. 1997) Hampson and La 2006
  • Brachyspira pilosicoli (Trott et al. 1996) Ochiai et al. 1998
  • Brachyspira muridarum ♠ Backhans et al. 2010
  • Brachyspira muris ♠ Backhans et al. 2010
  • Brachyspira pulli ♠ Stephens and Hampson 2001
  • Brachyspira rattus ♠ Backhans et al. 2010
  • Brachyspira suanatina ♠ Rasback et al. 2007
Synonyms
  • Serpula Stanton et al. 1991 non (Persson 1801) Gray 1821 non Linnaeus 1758
  • Serpulina Stanton 1992 non Zborzevski 1834

Brachyspira is a genus of bacteria classified within the phylum Spirochaetes.[2][3] [4]

Brachyspira species include pathogens in pigs, birds, dogs, and humans.

B. pilosicoli colonizes millions of humans worldwide, leading to human intestinal spirochaetosis, a chronic, intermittent watery diarrhea vastly underdiagnosed [5] because of the lack of a simple diagnostic tool for clinicians. Multiplex qPCRs are promising diagnostic tools, as Brachyspira do not grow on conventional media.[6]

B. pilosicoli also cause avian spirochetosis:[2] birds might be considered as the natural reservoir.

B. hyodysenteriae leads to diarrheal disease in growing pigs worldwide, causing the so-called swine dysentery, typhlocolitis or porcine intestinal spirochaetosis, which contributes to major "production losses" in agrobusiness.

Some species like B. innocens or B. intermedia seem to be less virulent.

Phylogeny

The currently accepted taxonomy is based on the List of Prokaryotic names with Standing in Nomenclature (LPSN)[7] and National Center for Biotechnology Information (NCBI),[8] and the phylogeny is based on 16S rRNA-based LTP release 123 by 'The All-Species Living Tree' Project.[9]

 
 

B. aalborgi Hovind-Hougen et al. 1983 (type sp.)

 
 
 

B. hyodysenteriae (Harris et al. 1972) Ochiai et al. 1998

 
 
 

B. innocens (Kinyon and Harris 1979) Ochiai et al. 1998

 
 

B. murdochii (Stanton et al. 1997) Hampson and La 2006

 
 
 
 

B. intermedia (Stanton et al. 1997) Hampson and La 2006

 
 
 

B. alvinipulli Stanton et al. 1998

 
 

B. pilosicoli (Trott et al. 1996) Ochiai et al. 1998

 
 
 
 
 

♠ Strains found at the National Center for Biotechnology Information (NCBI) but not listed in the List of Prokaryotic names with Standing in Nomenclature (LSPN).

Evolutionary hypothesis

It is interesting to consider that Brachyspira could be the missing link between independent gram-negatives and eventually internalized organisms like Mitochondria. One could imagine the following phylogenetic pathway: gram-negative free dwellers -> spirochetes attached to cell cytoskeleton and expressing porins creating cytoplasmic bridges and genome complementarity between parasite and mother cell -> rickettsia with full internalization --> permanent intracellular host = mitochondrion

Pathogenesis of human intestinal spirochetosis (HIS)

Brachyspira bacteria have evolved a parasitic lifestyle through genomic reduction (~2.5 to 3.3 Mb) [10] compared to other gram negative bacteria (~5 Mb).

Humans become infected through dirty water ingestion, possibly by swimming in waters containing the bacteria or by direct oral exposure to contaminated feces (outdoor tribes, raw egg eaters, slum inhabitants with no sanitation, MSM).

Genome homologies between Borellia, Treponema and Brachyspira imply that Brachyspira is expected to:

  • import carbohydrates and short fatty acids (6->3 carbons) for its energetic needs from the colon lumen,
  • swim to (viscophily[11]) and through (viscotaxy) mucin layers thanks to its spiroid shape and flagellum (see film [12]),
  • attach to colonocytes apically and to each other laterally,
  • thereby creating a continuous layer of bacterial cells[13] which can withstand feces movement in vivo: this is the pathognomonic brush border seen in histology on colonic biopsies
  • its is still to be elucidated if Brachyspira is, as Borrelia, able to attach to decorin and progress in loose connective tissue and invade other tissues,[14]
  • as for borrelia and syphilis,[15] Brachyspira may be able to translocate to seminal vesicles where it would find another niche "outside" the body with mucins to invade, epithelia to attach and glucose available. Chapot F. (2020) hypothesises that Brachyspira may be a sexually transmittable disease in MSM communities via ano-oral route but also penetrative route.

Once attached apically to the enterocyte, hidden to the natural and acquired immunity by the mucous layer and occupying a niche that other bacteria cannot use, Brachyspira most likely expresses at its apex porins allowing it to import from the colonocyte's cytoplasm the amino acids and nucleic acids necessary to replicate.

It has also been demonstrated that Brachyspira creates an environment which is favorable to its locomotion by upregulating mucin expression:[16] it creates its own niche.

Clinical manifestations in human medicine

Publications now tend to point out that Brachyspira colonization should not be considered harmless commensalism:

  • Chronic diarrhea [17]
  • Irritable bowel syndrome [18]
  • Acute intestinal pain [19]
  • Ulcerative colitis [20]
  • Post translocation spirochetemia and cardiogenic shock [21]

Antibiotic treatment and resistances in human medicine

Treament with 10 days co-amoxicilline 1g bid + metronidazole 500 tid seems to have very good results on abdominal symptoms.[22] It is advised to administer Saccharomyces boulardii once a day during this course of antibiotherapy.[23]

Doxycycline resistance has been documented and should be avoided.

Antibiotic treatment and resistance in veterinary medicine

Veterinary antibiotics used to treat pigs with dysentery due to Brachyspira species include the lincosamide lincomycin, the ionophore salinomycin, the quinoxaline carbadox, the pleuromodulins tiamulin and valnemulin, as well as the aminoglycoside gentamicin, an important antibiotic used in humans.

Brachyspira resistance to the above antibiotics has been increasingly reported. While no Clinical and Laboratory Standards Institute (CLSI) antimicrobial breakpoints for Brachyspira have been established, resistance to the pleuromodulins tiamulin and valnemulin is considered at MIC ≥ 2 µg/ml.[24] Resistance to pleuromodulins is important, because they are antibiotics of "last resort"; as of 2001, they were the only antibiotics with sufficient minimum inhibitory concentration (MIC) values left to treat swine dysentery in Sweden, per the National Veterinary Institute in Uppsala.[25]

Antibiotic resistance varies by geographic region and is not developing as rapidly in U.S. isolates as has been seen in isolates from other countries.[26] Tiamulin resistance was first described in 1996 in Hungary,[27] and subsequently reported from other countries in Europe and Asia,.[28][29][30][31][32][33] In Spain, 7.4% of Brachyspira isolates were reported to be venamulin-resistant and 17.6% were tiamulin-resistant in 2009.[34] In Sweden, 10-15% of B. pilosicoli isolates between 2002 and 2010 were resistant to tiamulin (MICs >4 μg/ml), and a gradual increase in tiamulin MICs was seen in B. hyodysenteriae between 1990 and 2003, which has since plateaued.[35]

Decreased susceptibility to lincomycin, but not to tiamulin was found among Polish isolates.[36]

In the USA, resistance of Brachyspira species collected 2008–2010 was common only against lincomycin (80% had MIC of 32 or 64), MIC's were moderately high against gentamicin, while resistance to valnemulin(4.7%) and tiamulin (3.2% of isolates) was yet uncommon, as reported in the only U.S. study to date, from Iowa.[26]

The use of pleuromodulins in U.S. food animals is not separately reported in the U.S. Food and Drug Administration's annual Animal Drug User Fee Act (ADUFA) report, "Antimicrobials Sold or Distributed for Use in Food-Producing Animals".[37] However, the amount of 190 tonnes of lincosamides used is substantial per ADUFA; antibiotics used in the U.S. in food animals in 2011 was: Ionophores 4,123,259 kg, aminoglycosides 214,895 kg, and Lincosamides 190,101 kg.

Microbiologic identification

Brachyspira are capable of hemolysis, the degree of which has been used to characterize them, with B. hyodysenteriae showing strong beta hemolysis while B. pilosicoli, B. intermedia, B. murdochii, and B. innocens have been described as weakly hemolytic.[38] However, in a recent study from Iowa State University, all (10/10) B. intermedia isolates, 91% (9/11) of Brachyspira spp. isolates, and 20% (2/6) of B. pilosicoli isolates from farms in North Carolina (36), Iowa (23), Minnesota (9), Nebraska (3), Michigan (2), Illinois (2), Missouri (1), North Dakota (1), South Dakota (1), and Ohio (1), demonstrated strong beta-hemolysis.[26]

Recently quantitative PCR seems to be a more sensitive way to identify Brachyspira, which is globally a very fastidious bacterium to grow.

Change in ecology

In the U.S.A. Brachyspira-associated pig disease and isolation of Brachyspira species from swine with diarrheal disease largely disappeared from swine herds in the late 1990s and early 2000s, but returned in the mid-2000s for unknown reasons.

A 2011 study of isolates from Midwestern swine herds described major changes in Brachyspira spp frequency and hemolysis, i.e. pathogenicity: the majority of isolated Brachyspira species were previously considered minimally pathogenic or commensal, like Brachyspira murdochi (27%)or novel/unclassifiable Brachyspira species (25%), while only 40.5% of 79 isolates from diseased pigs could be confirmed as the classic pathogens B. hyodysenteriae or Brachyspira pilosicoli by PCR.[39] Brachyspira species previously capable of weak hemolysis only, like B. intermedia and B. pilosicoli were found to produce strong hemolysis. They were also frequently identified from diseased swine which suggests they are emerging pathogens.

A compelling explanation for this change in epidemiology and ecology is selection by the increasing use of antibiotics in pigs (e.g. as growth promoters), since B. murdochii and unclassifiable Brachyspira spp. are less susceptible to antimicrobials than the previously established Brachyspira pathogens.

References

  1. ↑ Westerman, L. J. (2013). Human Intestinal Spirochaetosis (PhD thesis).
  2. 1 2 Le Roy, Caroline I.; Mappley, Luke J.; La Ragione, Roberto M.; Woodward, Martin J.; Claus, Sandrine P. (5 March 2019). "Brachyspira pilosicoli-induced avian intestinal spirochaetosis". Microbial Ecology in Health and Disease. 26: 28853. doi:10.3402/mehd.v26.28853. PMC 4683989. PMID 26679774.
  3. ↑ See the List of Prokaryotic names with Standing in Nomenclature. Data extracted from J.P. Euzéby. "Spirochaetes". Archived from the original on 2011-06-13. Retrieved 2011-11-17.
  4. ↑ See the NCBI webpage on Spirochaetes Data extracted from Sayers; et al. "NCBI Taxonomy Browser". National Center for Biotechnology Information. Retrieved 2011-06-05.
  5. ↑ Hampson, David J. (2017). "The Spirochete Brachyspira pilosicoli, Enteric Pathogen of Animals and Humans". Clinical Microbiology Reviews. 31 (1). doi:10.1128/CMR.00087-17. PMC 5740978. PMID 29187397.
  6. ↑ Borgström, Anna; Scherrer, Simone; Kirchgässner, Constanze; Schmitt, Sarah; Frei, Daniel; Wittenbrink, Max M. (7 February 2017). "A novel multiplex qPCR targeting 23S rDNA for diagnosis of swine dysentery and porcine intestinal spirochaetosis". BMC Veterinary Research. 13 (1): 42. doi:10.1186/s12917-016-0939-6. PMC 5297149. PMID 28173799.
  7. ↑ J.P. Euzéby. "Brachyspira". List of Prokaryotic names with Standing in Nomenclature (LPSN). Retrieved 2016-03-30.
  8. ↑ Sayers; et al. "Brachyspira". National Center for Biotechnology Information (NCBI) taxonomy database. Retrieved 2016-03-30.
  9. ↑ 'The All-Species Living Tree' Project."16S rRNA-based LTP release 123 (full tree)" (PDF). Silva Comprehensive Ribosomal RNA Database. Retrieved 2013-03-20.
  10. ↑ Hampson, D. J.; Wang, P. (2018). "Colonic Spirochetes: What Has Genomics Taught Us?". Current Topics in Microbiology and Immunology. 415: 273–294. doi:10.1007/82_2017_48. ISBN 978-3-319-89637-3. PMID 28879525.
  11. ↑ Naresh, Ram; Hampson, David J. (1 January 2010). "Attraction of Brachyspira pilosicoli to mucin". Microbiology (Reading, England). 156 (Pt 1): 191–197. doi:10.1099/mic.0.030262-0. PMID 19833772.
  12. ↑
  13. ↑ "FIG. 1. Transmission electron microscopic view of sectioned rectal..." ResearchGate. Retrieved 5 March 2019.
  14. ↑ Salo, Jemiina; Jaatinen, Annukka; Söderström, Mirva; Viljanen, Matti K.; Hytönen, Jukka (2015). "Decorin binding proteins of Borrelia burgdorferi promote arthritis development and joint specific post-treatment DNA persistence in mice". PLOS ONE. 10 (3): e0121512. Bibcode:2015PLoSO..1021512S. doi:10.1371/journal.pone.0121512. ISSN 1932-6203. PMC 4376631. PMID 25816291.
  15. ↑ Middelveen, Marianne J.; Burke, Jennie; Sapi, Eva; Bandoski, Cheryl; Filush, Katherine R.; Wang, Yean; Franco, Agustin; Timmaraju, Arun; Schlinger, Hilary A.; Mayne, Peter J.; Stricker, Raphael B. (2014). "Culture and identification of Borrelia spirochetes in human vaginal and seminal secretions". F1000Research. 3: 309. doi:10.12688/f1000research.5778.3. ISSN 2046-1402. PMC 5482345. PMID 28690828.
  16. ↑ Ogata, Sho; Shimizu, Ken; Tominaga, Susumu; Nakanishi, Kuniaki (2017). "Immunohistochemical study of mucins in human intestinal spirochetosis". Human Pathology. 62: 126–133. doi:10.1016/j.humpath.2017.01.013. PMID 28188751.
  17. ↑ Tsinganou, Efstathia; Gebbers, Jan-Olaf (7 January 2010). "Human intestinal spirochetosis--a review". GMS German Medical Science. 8: Doc01. doi:10.3205/000090. PMC 2830567. PMID 20200654.
  18. ↑ Walker, Marjorie M.; Talley, Nicholas J.; Inganäs, Linn; Engstrand, Lars; Jones, Michael P.; Nyhlin, Henry; Agréus, Lars; Kjellstrom, Lars; Öst, Åke; Andreasson, Anna (1 February 2015). "Colonic spirochetosis is associated with colonic eosinophilia and irritable bowel syndrome in a general population in Sweden". Human Pathology. 46 (2): 277–283. doi:10.1016/j.humpath.2014.10.026. PMID 25540866.
  19. ↑ Gan, Jason; Bryant, Catherine; Arul, Dhili; Parmar, Chetan (4 November 2017). "Intestinal spirochaetosis mimicking acute appendicitis with review of the literature". BMJ Case Reports. 2017: bcr–2017–221574. doi:10.1136/bcr-2017-221574. PMC 5747739. PMID 29103010.
  20. ↑ Nishii, Shin; Higashiyama, Masaaki; Ogata, Sho; Komoto, Shunsuke; Ito, Suguru; Mizoguchi, Akinori; Terada, Hisato; Furuhashi, Hirotaka; Takajo, Takeshi; Shirakabe, Kazuhiko; Watanabe, Chikako; Tomita, Kengo; Nagao, Shigeaki; Miura, Soichiro; Hokari, Ryota (1 April 2018). "Human intestinal spirochetosis mimicking ulcerative colitis". Clinical Journal of Gastroenterology. 11 (2): 145–149. doi:10.1007/s12328-017-0807-3. PMID 29204849. S2CID 4673959.
  21. ↑ Bait-Merabet, Lilia; Thille, Arnaud; Legrand, Patrick; Brun-Buisson, Christian; Cattoir, Vincent (25 September 2008). "Brachyspira pilosicoli bloodstream infections: case report and review of the literature". Annals of Clinical Microbiology and Antimicrobials. 7: 19. doi:10.1186/1476-0711-7-19. PMC 2561035. PMID 18817558.
  22. ↑ Helbling, Rossana; Osterheld, Maria-Chiara; Vaudaux, Bernard; Jaton, Katia; Nydegger, Andreas (16 October 2012). "Intestinal Spirochetosis mimicking inflammatory bowel disease in children". BMC Pediatrics. 12: 163. doi:10.1186/1471-2431-12-163. PMC 3480841. PMID 23066991.
  23. ↑ Kelesidis, Theodoros; Pothoulakis, Charalabos (1 March 2012). "Efficacy and safety of the probiotic Saccharomyces boulardii for the prevention and therapy of gastrointestinal disorders". Therapeutic Advances in Gastroenterology. 5 (2): 111–125. doi:10.1177/1756283X11428502. PMC 3296087. PMID 22423260.
  24. ↑ Karlsson M,Fellström C, Johansson KE,Franklin A. Antimicrobial resistance in Brachyspira pilosicoli with special reference to point mutations in the 23S rRNA gene associated with macrolide and lincosamide resistance. Microb Drug Resist 2004. 10:204–208
  25. ↑ Karlsson M, Gunnarsson A, Franklin A. Susceptibility to pleuromutilins in Brachyspira (Serpulina) hyodysenteriae. Anim Health Res Rev. 2001 Jun;2(1):59-65.
  26. 1 2 3 Clothier KA, Kinyon JM, Frana TS, Naberhaus N, Bower L, Strait EL, Schwartz K.Species characterization and minimum inhibitory concentration patterns of Brachyspira species isolates from swine with clinical disease.J Vet Diagn Invest. 2011 Nov;23(6):1140-5.
  27. ↑ Molnàr, L. (1996). Vet. Rec. 138:158-160.
  28. ↑ Gresham AC, Hunt BW, Dalziel RW.Treatment of swine dysentery--problems of antibiotic resistance and concurrent salmonellosis. Vet Rec. 1998 Nov 28;143(22):619.
  29. ↑ Italy http://www.ivis.org/proceedings/ipvs/2006/TREATMENT/P_31-22.pdf?LA=1
  30. ↑ Germany: Rohde J,Kessler M,Baums CG, Amtsberg G.Comparison of methods for antimicrobial susceptibility testing and MIC values for pleuromutilin drugs for Brachyspira hyodysenteriae isolated in Germany. Vet Microbiol 2004. 102:25–32.
  31. ↑ Pringle M,Landén A,Franklin A. Tiamulin resistance in porcine Brachyspira pilosicoli isolates. Res Vet Sci 2006. 80:1–4.
  32. ↑ Czech Republic: Lobová D, Smola J, Cizek A. Decreased susceptibility to tiamulin and valnemulin among Czech isolates of Brachyspira hyodysenteriae. J Med Microbiol 2004. 53:287–291.
  33. ↑ Karlsson M. et al (2002). Proc. 17th IPVS Congr, p.189
  34. ↑ Hidalgo A,Carvajal A, García-Feliz C,et al. Antimicrobial susceptibility testing of Spanish field isolates of Brachyspira hyodysenteriae. Res Vet Sci 2009. 87:7–12.
  35. ↑ Pringle M, Landén A, Unnerstad HE, Molander B, Bengtsson B. Antimicrobial susceptibility of porcine Brachyspira hyodysenteriae and Brachyspira pilosicoli isolated in Sweden between 1990 and 2010.Acta Vet Scand. 2012 Sep 21;54:54.
  36. ↑ Zmudzki J, Szczotka A, Nowak A, Strzelecka H, Grzesiak A, Pejsak Z.Antimicrobial susceptibility of Brachyspira hyodysenteriae isolated from 21 Polish farms.Pol J Vet Sci. 2012;15(2):259-65.
  37. ↑ "Antimicrobials Sold or Distributed for Use in Food-Producing Animals". FDA.gov. Retrieved 5 March 2019.
  38. ↑ Komarek V,Maderner A,Spergser J,Weissenböck H. Infections with weakly haemolytic Brachyspira species in pigs with miscellaneous chronic diseases. Vet Microbiol 134: 311–317.
  39. ↑ Clothier KA, Kinyon JM, Frana TS, Naberhaus N, Bower L, Strait EL, Schwartz K.Species characterization and minimum inhibitory concentration patterns of Brachyspira species isolates from swine with clinical disease.J Vet Diagn Invest. 2011 Nov;23(6):1140-5.
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