Streptococcus dysgalactiae

Streptococcus dysgalactiae
Scientific classification
Kingdom: Bacteria
Phylum: Firmicutes
Class: Bacilli
Order: Lactobacillales
Family: Streptococcaceae
Genus: Streptococcus
Species: S. dysgalactiae

Streptococcus dysgalactiae is a gram positive, beta-haemolytic, coccal bacterium belonging to the family Streptococcaceae. It is capable of infecting both humans and animals, but is most frequently encountered as a commensal of the alimentary tract, genital tract, or less commonly, as a part of the skin flora. The clinical manifestations in human disease range from superficial skin-infections and tonsillitis, to severe necrotising fasciitis and bacteraemia.[1] The incidence of invasive disease has been reported to be rising.[2][3][4] Several different animal species are susceptible to infection by S.dysgalactiae, but bovine mastitis and infectious arthritis in lambs (joint ill) have been most frequently reported.[5][6]

Streptococcus dysgalactiae is currently divided into the subspecies Streptococcus dysgalactiae subspecies equisimilis (SDSE) and Streptococcus dysgalactiae subspecies dysgalactiae (SDSD); the former mostly associated with human disease, and the latter almost exclusively encountered in veterinary medicine.[7] Their exact taxonomic delineation, however, is a matter of ongoing debate (See taxonomy).

The names are derived from Greek; Streptococcus meaning chain forming (Streptos) rounded berry-like bodies (kokkos), referring to their usual appearance under a light-microscope. Dys (bad) galactiae (milk) alludes to their propensity to cause bovine mastitis. Equi (horse) similis (like) infers similarity to the closely related species, Streptococcus equi.

Epidemiology

Streptococcus dysgalactiae was long believed to be non-pathogenic to humans. However, an increasing incidence of S.dysgalactiae infections has been documented, and in some geographic regions, the rate of invasive infection has even surpassed that of Streptococcus pyogenes.[2][3][4][8][9] The age distribution of invasive cases among humans is clearly skewed towards the elderly, whereas the healthy carrier state appears to have the inverse relation to age. People with chronic maladies, including cancer and diabetes, are also especially susceptible to infection.[1][10] These opportunistic traits have been proposed as one of the mechanisms underlying the observed increasing frequency of invasive disease. Furthermore, a male predominance has been noted, presumably due to a higher burden of comorbidity. The incidence of non-invasive disease in human does not appear to be increasing.[2]

Role in human disease

Streptococcus dysgalactiae subspecies equisimilis (SDSE) is a commensal in human alimentary tract and genital tract. Occasionally it is isolated from skin, but usually in relation to a chronic skin condition or some breach of the epithelial barrier.[11]

Non-invasive disease manifestations include predominantly tonsillitis and superficial skin infections.[1][2] Additionally, it has long been recognized as a potential cause of cellulitis/erysipelas. However, the role of SDSE in cellulitis might have been previously underestimated, and it was linked to a majority of the cellulitis cases in a recent study.[11]

The clinical presentation among invasive disease is also dominated by skin and soft tissue infections, including a small subset of patients presenting with severe necrotizing fasciitis.[1][2] Moreover, it is an important cause of bone and joint infections, and this disease manifestation is reported to be increasing.[12] Less commonly it can present as pneumonia, endocarditis, genital or intraabdominal infections. Primary bacteraemia, infection without identifiable focal origin, comprises approximately 20% of the reported cases.[1][2][13]

Recently, SDSE has been linked to post-streptococcal glomerulonephritis and acute rheumatic fever.[14][15] These immunologic sequelae have previously only been associated with Streptococcus pyogenes. Streptococcus dysgalactiae subspecies dysgalactiae (SDSD) is almost exclusively an animal pathogen. However, a few casuistic reports of human zoonotic infection have been documented.[16][17]

Role in animal disease

Streptococcus dysgalactiae can infect a range of animal hosts, and both subspecies are of importance. However, the bacterium is frequently encountered as a colonizer of healthy animals, especially in the alimentary tract and genital region.[6]

In veterinary medicine, it is a well-recognized cause of bovine mastitis, hence the name dys-galactiae. In some geographic regions, it is reported only second to Staphylococcus aureus as a cause of both clinical and subclinical mastitis.[5] S. dysgalactiae has been particularly linked to mastitis occurring during the summer time (“Summer mastitis”), and bacterial spreading by flying insects has been suggested.[18] Mastitis in other animals has also been documented.[19]

S.dysgalactiae has been isolated from infectious polyarthritis in several animal species, including piglets, lambs, calves and goats.[6][20] Furthermore, it has been implicated in neonatal mortality among puppies.[21] Recently, SDSD has been described as an emerging pathogen in fish, causing fulminant necrotic ulcers of the caudal peduncle, with ensuing high mortality rates.[22] The clinical presentation is dominated by severe sepsis and the formation of microabscesses, and a relationship between disease severity and the expression of the virulence factors Streptolysin S and SPEGdys has been inferred.[20]

Treatment and Antimicrobial susceptibility

Penicillin remains the drug of choice for treating streptococcal infections, and S.dysgalactiae strains with reduced susceptibility to penicillin have never been reported. Treatment duration varies from 5 days to 3 months, depending on the clinical diagnosis. Second-line agents include macrolides and clindamycin, although increasing resistance, due to both efflux and target modification, has been documented in some geographic regions.[13][23][24] Aminoglycosides are not active against streptococci due to their lacking respiratory metabolism. However, administered in combination with a beta-lactam antibiotic, aminoglycosides appear to produce a synergistic effect towards streptococci.[25] Streptococcus dysgalactiae is uniformly susceptible to glycopeptides and oxazolidones.

Taxonomy

Diernhofer first used the name Streptococcus dysgalactiae in 1932, describing a streptococcus of veterinary origin.[26] Subsequently, Frost reported the discovery of the human pathogen Streptococcus equisimilis in 1936.[27] Contemporarily, though, Rebecca Lancefield devised a classification of streptococci based on their carbohydrate-antigens, and successively described streptococci belonging to group C (1933) and group G (1935).[28][29] The correlation of group carbohydrate specificity with the proposed species S.dysgalactiae and S.equisimilis, however, were not explored in detail. The Lancefield classification soon became the preferred laboratory identification method for streptococci, and the names S.dysgalactiae and S.equisimilis fell into disuse. In 1980, they were even removed from the List of Approved Bacterial species.[30] Three years later, though, DNA hybridization studies revealed extensive similarities between the entities Streptococcus dysgalactiae, Streptococcus equisimilis, large-colony-forming group C and group G streptococcus of human origin, and certain large-colony-forming group C, G and L streptococci of animal origin.[31][32] Accordingly, they were fused to one species, Streptococcus dysgalactiae. However, subsequent molecular investigations indicated heterogeneity within this new species, and in 1996 it was divided into S.dysgalactiae subspecies equisimilis and S.dysgalactiae subspecies dysgalactiae.[33]

The taxonomic division of Streptococcus dysgalactiae into its two subspecies has been the origin of much confusion, and a matter of ongoing debate. Although no official taxonomic gold standard exists, the most current and widely supported definition was published by Vieira et al in 1998.[7] It defines S.dysgalactiae subspecies dysgalactiae solely as the alpha-haemolytic phenotype harbouring the Lancefield group C antigen. The rest are classified as S.dysgalactiae subspecies equisimilis, are (mostly) beta-haemolytic and can harbour carbohydrate antigens of Lancefield group A, C, G or L. However, a recent study indicates that the SDSE strains of animal and human origin are genetically divergent, and future taxonomic reclassifications are conceivable.[34]

Laboratory identification

Streptococcus dysgalactiae form large colonies (>0.5 cm) after 24 hours of incubation, and produce haemolysis on blood agar; SDSD is alpha-haemolytic, whereas SDSE is predominantly beta-haemolytic. They are facultative anaerobic, incapable of respiratory metabolism, but are aerotolerant. Growth is enhanced by incubation in 5% CO2 atmosphere, but they usually grow adequately in ambient air. The optimum temperature for growth is approximately 37° Celsius. Lancefield group C and G carbohydrate antigens are predominantly expressed, but group A and L have been documented.[34] However, the above characteristics are not unique to S.dysgalactiae, and further testing is required to confirm the species identity. Although many laboratories currently identify bacteria by mass-spectrometry (Matrix Assisted Laser Desorption/ionization Time Of Flight (MALDI TOF MS), phenotypic testing is still widely used. Unlike Streptococcus pyogenes (harbouring Lancefield group A antigen), S.dysgalactiae is PYR-negative and Bacitracin resistant. The distinction from the Streptococcus anginosus group (Lancefield A, C, G or F) can be made by colony size and Voges Proskauer test (VP); the S.anginosus group being VP positive. Streptococcus equi contains Lancefield group C, and Streptococcus canis harbours group G, but unlike S.dysgalactiae, they are both Hyaluronidase negative.[34]

The identification of S.dysgalactiae to the subspecies level is most reliably performed by MultiLocus Sequence Typing (MLST).[35] MALDI TOF MS does currently not possess taxonomic resolution beyond the species level.

Molecular typing

Several different typing systems for Streptococcus dysgalactiae have been used, the majority originally devised for the closely related species Streptococcus pyogenes. The most widely employed method is emm-typing. The emm-gene encodes the M-protein, a major virulence factor in both S.pyogenes and Streptococcus dysgalactiae. It is ubiquitous in SDSE of human origin, and its hypervariability in the 5’-terminal region forms the basis for categorization into separate emm-types.[36] To date, more than 100 SDSE emm-types have been described (CDC Strep Lab). The prevailing emm-types vary in different geographical regions, and clonal outbreaks have been reported.[37] Unlike for S.pyogenes, a correlation between emm-type and disease manifestation or severity has not been established for S. dysgalactiae.[13][38] Pulsed Field Gel Electrophoresis (PFGE) has historically been employed for the exploration of clonal relationships among S.dysgalactiae, but with the increased availability and reduced costs of sequencing, it is likely to be replaced by MLST and Single Nucleotide Polymorphism-analysis (SNP).

Pathogenesis and virulence factors

The pathogenetic pathways of Streptococcus dysgalactiae have not been explored in detail. Several virulence factors have been identified, but predominantly by screening S.dysgalactiae isolates for homologues of well-characterized S.pyogenes virulence genes. In a study of 216 S.pyogenes virulence genes, S.dysgalactiae was found to harbour approximately half of them.[39] Indeed, whole-genome comparisons reveal a 70% -genetic similarity between the two species, indicating a common genetic ancestry.[40] However, evidence of horizontal genetic transfer has also been reported.[41]

The first pivotal step in infectious pathogenesis is the attachment to the host tissues. The M-protein, the most extensively studied SDSE virulence factor, has been documented to facilitate both adherence to and internalization into host cells.[1][42] Other adhesins have also been described, including the genes gfba, fnB, fbBA, fnBB, lmb and gapC; all mediating binding to fibronectin.[43][44][45][46] gfba was recently shown contribute to bacterial internalization into endothelial cells and intracellular persistence.[47][48] These properties may explain the tendency of recurrent bacteraemia observed in human SDSE-cases.

In order to establish infection, the bacteria need to escape the host immune response, and in streptococci, a varied arsenal of bacterial strategies have been described. The M-protein aids in immune evasion by inhibiting phagocytosis and inactivating the complement system.[1] Furthermore, Streptococcus dysgalactiae possesses Protein G, a virulence factor binding circulating immunoglobulins, and thus interfering with the host antibody response.[49] DrsG, a virulence protein abrogating the effect of antimicrobial peptides secreted by human immune cells, is also harboured by a subset of SDSE-strains.[50][51]

Several toxins and secreted enzymes have been identified in Streptococcus dysgalactiae, including the haemolysins Streptolysin O (SLO) and Streptolysin S (SLS), and a correlation between the expression of SLO and SLS and disease severity has been inferred.[52] speGdys, a homolog of the S.pyogenes superantigen speG, has been documented in some S.dysgalactiae strains.[38][53] However, it only appears to possess superantigen-capabilities in animals, and its relevance in human disease has yet to be elucidated.[54] Streptokinase appears to be ubiquitous in S.dysgalactiae, enabling fibrinolysis and aiding in bacterial spreading through tissues.[1][39]

Recently, a capacity to form biofilm was reported, facilitating survival and proliferation in hostile environments.[55] Although this potentially could have implications for the treatment of S.dysgalactiae-infections, its clinical significance has not yet been determined.

References

  1. 1 2 3 4 5 6 7 8 Brandt, CM; Spellerberg, B (1 September 2009). "Human infections due to Streptococcus dysgalactiae subspecies equisimilis.". Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 49 (5): 766–72. doi:10.1086/605085. PMID 19635028.
  2. 1 2 3 4 5 6 Oppegaard, O; Mylvaganam, H; Kittang, BR (February 2015). "Beta-haemolytic group A, C and G streptococcal infections in Western Norway: a 15-year retrospective survey.". Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases. 21 (2): 171–8. doi:10.1016/j.cmi.2014.08.019. PMID 25658557.
  3. 1 2 Sylvetsky, N; Raveh, D; Schlesinger, Y; Rudensky, B; Yinnon, AM (1 June 2002). "Bacteremia due to beta-hemolytic Streptococcus group G: increasing incidence and clinical characteristics of patients.". The American journal of medicine. 112 (8): 622–6. PMID 12034411.
  4. 1 2 Anonymous (November 2015). "Voluntary surveillance of pyogenic and non-pyogenic streptococcal bacteraemia in England, Wales and Northern Ireland: 2014" (PDF). Health Protection Report: Weekly Report. 9.
  5. 1 2 Whist, A. C.; Østerås, O.; Sølverød, L. (2007-02-01). "Streptococcus dysgalactiae isolates at calving and lactation performance within the same lactation". Journal of Dairy Science. 90 (2): 766–778. doi:10.3168/jds.S0022-0302(07)71561-8. ISSN 1525-3198. PMID 17235154.
  6. 1 2 3 Rutherford, S. J.; Rycroft, A. N.; Ridler, A. L. (2014-06-07). "Sources of Streptococcus dysgalactiae in English and Welsh sheep flocks affected by infectious arthritis (joint ill)". The Veterinary Record. 174 (23): 579. doi:10.1136/vr.101753. ISSN 2042-7670. PMID 24619629.
  7. 1 2 VIEIRA, VERNICA V.; TEIXEIRA, LÚCIA M.; ZAHNER, VIVIANE; MOMEN, HOOMAN; FACKLAM, RICHARD R.; STEIGERWALT, ARNOLD G.; BRENNER, DON J.; CASTRO, ANGELA C. D. (1998-01-01). "Genetic relationships among the different phenotypes of Streptococcus dysgalactiae strains". International Journal of Systematic and Evolutionary Microbiology. 48 (4): 1231–1243. doi:10.1099/00207713-48-4-1231.
  8. ↑ Bramhachari, Pallaval V.; Kaul, Santosh Y.; McMillan, David J.; Shaila, Melkote S.; Karmarkar, Mohan G.; Sriprakash, Kadaba S. (2010-02-01). "Disease burden due to Streptococcus dysgalactiae subsp. equisimilis (group G and C streptococcus) is higher than that due to Streptococcus pyogenes among Mumbai school children". Journal of Medical Microbiology. 59 (Pt 2): 220–223. doi:10.1099/jmm.0.015644-0. ISSN 1473-5644. PMID 19833781.
  9. ↑ Wong, San S.; Lin, Yu S.; Mathew, Liby; Rajagopal, Latha; Sepkowitz, Douglas (2009-06-01). "Increase in group G streptococcal infections in a community hospital, New York, USA". Emerging Infectious Diseases. 15 (6): 991–993. doi:10.3201/eid1506.080666. ISSN 1080-6059. PMC 2727315Freely accessible. PMID 19523319.
  10. ↑ Broyles, Laura N.; Van Beneden, Chris; Beall, Bernard; Facklam, Richard; Shewmaker, P. Lynn; Malpiedi, Paul; Daily, Pamala; Reingold, Arthur; Farley, Monica M. (2009-03-15). "Population-based study of invasive disease due to beta-hemolytic streptococci of groups other than A and B". Clinical Infectious Diseases: An Official Publication of the Infectious Diseases Society of America. 48 (6): 706–712. doi:10.1086/597035. ISSN 1537-6591. PMID 19187026.
  11. 1 2 Bruun, Trond; Oppegaard, Oddvar; Kittang, Bård R.; Mylvaganam, Haima; Langeland, Nina; Skrede, Steinar (2016-01-01). "Etiology of Cellulitis and Clinical Prediction of Streptococcal Disease: A Prospective Study". Open Forum Infectious Diseases. 3 (1): ofv181. doi:10.1093/ofid/ofv181. ISSN 2328-8957. PMC 4699398Freely accessible. PMID 26734653.
  12. ↑ Oppegaard, Oddvar; Skrede, Steinar; Mylvaganam, Haima; Kittang, Bård Reiakvam (2016-10-04). "Temporal trends of β-haemolytic streptococcal osteoarticular infections in western Norway". BMC infectious diseases. 16 (1): 535. doi:10.1186/s12879-016-1874-7. ISSN 1471-2334. PMC 5050853Freely accessible. PMID 27716100.
  13. 1 2 3 Loubinoux, Julien; Plainvert, Céline; Collobert, Gislène; Touak, Gérald; Bouvet, Anne; Poyart, Claire; CNR-Strep Network (2013-08-01). "Adult invasive and noninvasive infections due to Streptococcus dysgalactiae subsp. equisimilis in France from 2006 to 2010". Journal of Clinical Microbiology. 51 (8): 2724–2727. doi:10.1128/JCM.01262-13. ISSN 1098-660X. PMC 3719644Freely accessible. PMID 23698531.
  14. ↑ Haidan, A.; Talay, S. R.; Rohde, M.; Sriprakash, K. S.; Currie, B. J.; Chhatwal, G. S. (2000-09-30). "Pharyngeal carriage of group C and group G streptococci and acute rheumatic fever in an Aboriginal population". Lancet (London, England). 356 (9236): 1167–1169. doi:10.1016/S0140-6736(00)02765-3. ISSN 0140-6736. PMID 11030302.
  15. ↑ Reid, H. F.; Bassett, D. C.; Poon-King, T.; Zabriskie, J. B.; Read, S. E. (1985-02-01). "Group G streptococci in healthy school-children and in patients with glomerulonephritis in Trinidad". The Journal of Hygiene. 94 (1): 61–68. ISSN 0022-1724. PMC 2129394Freely accessible. PMID 3882827.
  16. ↑ Jordal, Stina; Glambek, Marte; Oppegaard, Oddvar; Kittang, Bård Reiakvam (2015-02-01). "New tricks from an old cow: infective endocarditis caused by Streptococcus dysgalactiae subsp. dysgalactiae". Journal of Clinical Microbiology. 53 (2): 731–734. doi:10.1128/JCM.02437-14. ISSN 1098-660X. PMC 4298539Freely accessible. PMID 25472489.
  17. ↑ Koh, T. H.; Sng, L.-H.; Yuen, S. M.; Thomas, C. K.; Tan, P. L.; Tan, S. H.; Wong, N. S. (2009-05-01). "Streptococcal cellulitis following preparation of fresh raw seafood". Zoonoses and Public Health. 56 (4): 206–208. doi:10.1111/j.1863-2378.2008.01213.x. ISSN 1863-1959. PMID 19309483.
  18. ↑ Chirico, J.; Jonsson, P.; Kjellberg, S.; Thomas, G. (1997-04-01). "Summer mastitis experimentally induced by Hydrotaea irritans exposed to bacteria". Medical and Veterinary Entomology. 11 (2): 187–192. ISSN 0269-283X. PMID 9226651.
  19. ↑ Scott, P. R. (2000-03-18). "Extensive fibrinous pleurisy associated with Streptococcus dysgalactiae mastitis in two ewes". The Veterinary Record. 146 (12): 347–349. ISSN 0042-4900. PMID 10777043.
  20. 1 2 Abdelsalam, M.; Eissa, A. E.; Chen, S.-C. (2015-03-01). "Genetic diversity of geographically distinct Streptococcus dysgalactiae isolates from fish". Journal of Advanced Research. 6 (2): 233–238. doi:10.1016/j.jare.2013.12.003. ISSN 2090-1232. PMC 4348444Freely accessible. PMID 25750757.
  21. ↑ Vela, Ana I.; Falsen, Enevold; Simarro, Isabel; Rollan, Eduardo; Collins, Matthew D.; Domínguez, Lucas; Fernandez-Garayzabal, Jose F. (2006-02-01). "Neonatal mortality in puppies due to bacteremia by Streptococcus dysgalactiae subsp. dysgalactiae". Journal of Clinical Microbiology. 44 (2): 666–668. doi:10.1128/JCM.44.2.666-668.2006. ISSN 0095-1137. PMC 1392640Freely accessible. PMID 16455943.
  22. ↑ Nomoto, R.; Munasinghe, L. I.; Jin, D.-H.; Shimahara, Y.; Yasuda, H.; Nakamura, A.; Misawa, N.; Itami, T.; Yoshida, T. (2004-12-01). "Lancefield group C Streptococcus dysgalactiae infection responsible for fish mortalities in Japan". Journal of Fish Diseases. 27 (12): 679–686. doi:10.1111/j.1365-2761.2004.00591.x. ISSN 0140-7775. PMID 15575875.
  23. ↑ Lo, Hsueh-Hsia; Nien, Hao-Hsiang; Cheng, Ya-Yu; Su, Fang-Yi (2015-12-01). "Antibiotic susceptibility pattern and erythromycin resistance mechanisms in beta-hemolytic group G Streptococcus dysgalactiae subspecies equisimilis isolates from central Taiwan". Journal of Microbiology, Immunology, and Infection = Wei Mian Yu Gan Ran Za Zhi. 48 (6): 613–617. doi:10.1016/j.jmii.2014.04.003. ISSN 1995-9133. PMID 24856419.
  24. ↑ de Souza, José Paulo; Santos, Amanda Ribeiro; de Paula, Geraldo Renato; Barros, Rosana Rocha (2016-09-01). "Antimicrobial susceptibility and genetic relationships among Streptococcus dysgalactiae subsp. equisimilis isolates in Rio de Janeiro". Infectious Diseases (London, England). 48 (9): 676–681. doi:10.1080/23744235.2016.1192680. ISSN 2374-4243. PMID 27301015.
  25. ↑ Baker, C. N.; Thornsberry, C.; Facklam, R. R. (1981-05-01). "Synergism, killing kinetics, and antimicrobial susceptibility of group A and B streptococci". Antimicrobial Agents and Chemotherapy. 19 (5): 716–725. ISSN 0066-4804. PMC 181512Freely accessible. PMID 7027921.
  26. ↑ Diernhofer, K (1932). "Aesculinbouillon als Hilfsmittel für die Differenzierung von Euter- und Milchstreptokokken bei Massenuntersuchungen". Milchwirtschaftliche Forschung. 13: 368–374.
  27. ↑ Frost, W.D.E. (1940). The streptococci. Willdorf Co.
  28. ↑ Lancefield, R. C. (1933-03-31). "A SEROLOGICAL DIFFERENTIATION OF HUMAN AND OTHER GROUPS OF HEMOLYTIC STREPTOCOCCI". The Journal of Experimental Medicine. 57 (4): 571–595. ISSN 0022-1007. PMC 2132252Freely accessible. PMID 19870148.
  29. ↑ Lancefield, R. C.; Hare, R. (1935-02-28). "THE SEROLOGICAL DIFFERENTIATION OF PATHOGENIC AND NON-PATHOGENIC STRAINS OF HEMOLYTIC STREPTOCOCCI FROM PARTURIENT WOMEN". The Journal of Experimental Medicine. 61 (3): 335–349. ISSN 0022-1007. PMC 2133228Freely accessible. PMID 19870362.
  30. ↑ Skerman, V.B.D.M.; Sneath, P.H.A. (1980). "Approved list of bacterial names". Int J Syst Bacteriol. 30: 225–420.
  31. ↑ Garvie, E.I.F.; Collins, M.D. (1983). "Streptococcus dysgalactiae (Diernhofer) nom. Rev". Int J Syst Bacteriol. 33: 404–405.
  32. ↑ Farrow, J.A.E.C.; Collins, M.D. (1984). "Taxonimic studies on streptococci of serological groups C, G and L and possibly related taxa". Syst Appl Microbiol. 5: 840–842.
  33. ↑ Vandamme P, Pot B, Falsen E, Kersters K, Devriese LA (July 1996). "Taxonomic study of lancefield streptococcal groups C, G, and L (Streptococcus dysgalactiae) and proposal of S. dysgalactiae subsp. equisimilis subsp. nov". Int. J. Syst. Bacteriol. 46 (3): 774–81. doi:10.1099/00207713-46-3-774. PMID 8782689.
  34. 1 2 3 Jensen, Anders; Kilian, Mogens (2012-01-01). "Delineation of Streptococcus dysgalactiae, its subspecies, and its clinical and phylogenetic relationship to Streptococcus pyogenes". Journal of Clinical Microbiology. 50 (1): 113–126. doi:10.1128/JCM.05900-11. ISSN 1098-660X. PMC 3256718Freely accessible. PMID 22075580.
  35. ↑ Bishop, Cynthia J.; Aanensen, David M.; Jordan, Gregory E.; Kilian, Mogens; Hanage, William P.; Spratt, Brian G. (2009-01-01). "Assigning strains to bacterial species via the internet". BMC biology. 7: 3. doi:10.1186/1741-7007-7-3. ISSN 1741-7007. PMC 2636762Freely accessible. PMID 19171050.
  36. ↑ Beall, B.; Facklam, R.; Thompson, T. (1996-04-01). "Sequencing emm-specific PCR products for routine and accurate typing of group A streptococci". Journal of Clinical Microbiology. 34 (4): 953–958. ISSN 0095-1137. PMC 228924Freely accessible. PMID 8815115.
  37. ↑ Wang, Xiaohui; Zhang, Xiaoxia; Zong, Zhiyong (2016-01-01). "Genome sequence and virulence factors of a group G Streptococcus dysgalactiae subsp. equisimilis strain with a new element carrying erm(B)". Scientific Reports. 6: 20389. doi:10.1038/srep20389. ISSN 2045-2322. PMC 4740735Freely accessible. PMID 26843282.
  38. 1 2 Kittang, B. R.; Skrede, S.; Langeland, N.; Haanshuus, C. G.; Mylvaganam, H. (2011-03-01). "emm gene diversity, superantigen gene profiles and presence of SlaA among clinical isolates of group A, C and G streptococci from western Norway". European Journal of Clinical Microbiology & Infectious Diseases: Official Publication of the European Society of Clinical Microbiology. 30 (3): 423–433. doi:10.1007/s10096-010-1105-x. ISSN 1435-4373. PMC 3034890Freely accessible. PMID 21103900.
  39. 1 2 Davies, Mark R.; McMillan, David J.; Beiko, Robert G.; Barroso, Vanessa; Geffers, Robert; Sriprakash, Kadaba S.; Chhatwal, Gursharan S. (2007-06-01). "Virulence profiling of Streptococcus dysgalactiae subspecies equisimilis isolated from infected humans reveals 2 distinct genetic lineages that do not segregate with their phenotypes or propensity to cause diseases". Clinical Infectious Diseases: An Official Publication of the Infectious Diseases Society of America. 44 (11): 1442–1454. doi:10.1086/516780. ISSN 1537-6591. PMID 17479940.
  40. ↑ Shimomura, Yumi; Okumura, Kayo; Murayama, Somay Yamagata; Yagi, Junji; Ubukata, Kimiko; Kirikae, Teruo; Miyoshi-Akiyama, Tohru (2011-01-01). "Complete genome sequencing and analysis of a Lancefield group G Streptococcus dysgalactiae subsp. equisimilis strain causing streptococcal toxic shock syndrome (STSS)". BMC genomics. 12: 17. doi:10.1186/1471-2164-12-17. ISSN 1471-2164. PMC 3027156Freely accessible. PMID 21223537.
  41. ↑ McNeilly, Celia L.; McMillan, David J. (2014-01-01). "Horizontal gene transfer and recombination in Streptococcus dysgalactiae subsp. equisimilis". Frontiers in Microbiology. 5: 676. doi:10.3389/fmicb.2014.00676. ISSN 1664-302X. PMC 4266089Freely accessible. PMID 25566202.
  42. ↑ Bisno, A. L.; Craven, D. E.; McCabe, W. R. (1987-03-01). "M proteins of group G streptococci isolated from bacteremic human infections". Infection and Immunity. 55 (3): 753–757. ISSN 0019-9567. PMC 260406Freely accessible. PMID 3102380.
  43. ↑ Kline, J. B.; Xu, S.; Bisno, A. L.; Collins, C. M. (1996-06-01). "Identification of a fibronectin-binding protein (GfbA) in pathogenic group G streptococci". Infection and Immunity. 64 (6): 2122–2129. ISSN 0019-9567. PMC 174045Freely accessible. PMID 8675316.
  44. ↑ Lindgren, P. E.; McGavin, M. J.; Signäs, C.; Guss, B.; Gurusiddappa, S.; Höök, M.; Lindberg, M. (1993-06-15). "Two different genes coding for fibronectin-binding proteins from Streptococcus dysgalactiae. The complete nucleotide sequences and characterization of the binding domains". European journal of biochemistry / FEBS. 214 (3): 819–827. ISSN 0014-2956. PMID 8319691.
  45. ↑ Lindgren, P. E.; Signäs, C.; Rantamäki, L.; Lindberg, M. (1994-08-01). "A fibronectin-binding protein from Streptococcus equisimilis: characterization of the gene and identification of the binding domain". Veterinary Microbiology. 41 (3): 235–247. ISSN 0378-1135. PMID 7975149.
  46. ↑ Lo, Hsueh-Hsia; Cheng, Wei-Shan (2015-01-01). "Distribution of virulence factors and association with emm polymorphism or isolation site among beta-hemolytic group G Streptococcus dysgalactiae subspecies equisimilis". APMIS: acta pathologica, microbiologica, et immunologica Scandinavica. 123 (1): 45–52. doi:10.1111/apm.12305. ISSN 1600-0463. PMID 25244428.
  47. ↑ Rohde, Manfred; Talay, Susanne R.; Rasmussen, Magnus (2012-04-01). "Molecular mechanisms of Streptococcus dysgalactiae subsp equisimilis enabling intravascular persistence". Microbes and Infection / Institut Pasteur. 14 (4): 329–334. doi:10.1016/j.micinf.2011.10.008. ISSN 1769-714X. PMID 22100875.
  48. ↑ Gherardi, Giovanni; Imperi, Monica; Palmieri, Claudio; Magi, Gloria; Facinelli, Bruna; Baldassarri, Lucilla; Pataracchia, Marco; Creti, Roberta (2014-01-01). "Genetic diversity and virulence properties of Streptococcus dysgalactiae subsp. equisimilis from different sources". Journal of Medical Microbiology. 63 (Pt 1): 90–98. doi:10.1099/jmm.0.062109-0. ISSN 1473-5644. PMID 24149625.
  49. ↑ Sjöbring, U.; Björck, L.; Kastern, W. (1991-01-05). "Streptococcal protein G. Gene structure and protein binding properties". The Journal of Biological Chemistry. 266 (1): 399–405. ISSN 0021-9258. PMID 1985908.
  50. ↑ Smyth, Danielle; Cameron, Ainslie; Davies, Mark R.; McNeilly, Celia; Hafner, Louise; Sriprakash, Kadaba S.; McMillan, David J. (2014-06-01). "DrsG from Streptococcus dysgalactiae subsp. equisimilis inhibits the antimicrobial peptide LL-37". Infection and Immunity. 82 (6): 2337–2344. doi:10.1128/IAI.01411-13. ISSN 1098-5522. PMC 4019180Freely accessible. PMID 24664506.
  51. ↑ Oppegaard, O.; Mylvaganam, H.; Skrede, S.; Langeland, N.; Kittang, B. R. (2014-02-01). "Sequence diversity of sicG among group C and G Streptococcus dysgalactiae subspecies equisimilis isolates associated with human infections in western Norway". European Journal of Clinical Microbiology & Infectious Diseases: Official Publication of the European Society of Clinical Microbiology. 33 (2): 273–277. doi:10.1007/s10096-013-1955-0. ISSN 1435-4373. PMID 24019161.
  52. ↑ Watanabe, Shinya; Shimomura, Yumi; Ubukata, Kimiko; Kirikae, Teruo; Miyoshi-Akiyama, Tohru (2013-11-01). "Concomitant regulation of host tissue-destroying virulence factors and carbohydrate metabolism during invasive diseases induced by group g streptococci". The Journal of Infectious Diseases. 208 (9): 1482–1493. doi:10.1093/infdis/jit353. ISSN 1537-6613. PMID 23901096.
  53. ↑ Sachse, Svea; Seidel, Peter; Gerlach, Dieter; Günther, Elisabeth; Rödel, Jürgen; Straube, Eberhard; Schmidt, Karl-Hermann (2002-10-11). "Superantigen-like gene(s) in human pathogenic Streptococcus dysgalactiae, subsp equisimilis: genomic localisation of the gene encoding streptococcal pyrogenic exotoxin G (speG(dys))". FEMS immunology and medical microbiology. 34 (2): 159–167. ISSN 0928-8244. PMID 12381468.
  54. ↑ Zhao, Jizi; Hayashi, Tomohito; Saarinen, Susanna; Papageorgiou, Anastassios C.; Kato, Hidehito; Imanishi, Ken'ichi; Kirikae, Teruo; Abe, Ryo; Uchiyama, Takehiko (2007-04-01). "Cloning, expression, and characterization of the superantigen streptococcal pyrogenic exotoxin G from Streptococcus dysgalactiae". Infection and Immunity. 75 (4): 1721–1729. doi:10.1128/IAI.01183-06. ISSN 0019-9567. PMC 1865666Freely accessible. PMID 17283088.
  55. ↑ Genteluci, Gabrielle Limeira; Silva, Ligia Guedes; Souza, Maria Clara; Glatthardt, Thaís; de Mattos, Marcos Corrêa; Ejzemberg, Regina; Alviano, Celuta Sales; Figueiredo, Agnes Marie Sá; Ferreira-Carvalho, Bernadete Teixeira (2015-12-01). "Assessment and characterization of biofilm formation among human isolates of Streptococcus dysgalactiae subsp. equisimilis". International journal of medical microbiology: IJMM. 305 (8): 937–947. doi:10.1016/j.ijmm.2015.10.004. ISSN 1618-0607. PMID 26558847.

External links

This article is issued from Wikipedia - version of the 11/8/2016. The text is available under the Creative Commons Attribution/Share Alike but additional terms may apply for the media files.