Advertisement

Medical Microbiology and Immunology

, Volume 208, Issue 1, pp 25–32 | Cite as

Legionella feeleii: pneumonia or Pontiac fever? Bacterial virulence traits and host immune response

  • Changle WangEmail author
  • Xia Chuai
  • Mei Liang
Review

Abstract

Gram-negative bacterium Legionella is able to proliferate intracellularly in mammalian host cells and amoeba, which became known in 1976 since they caused a large outbreak of pneumonia. It had been reported that different strains of Legionella pneumophila, Legionella micdadei, Legionella longbeachae, and Legionella feeleii caused human respiratory diseases, which were known as Pontiac fever or Legionnaires’ disease. However, the differences of the virulence traits among the strains of the single species and the pathogenesis of the two diseases that were due to the bacterial virulence factors had not been well elucidated. L. feeleii is an important pathogenic organism in Legionellae, which attracted attention due to cause an outbreak of Pontiac fever in 1981 in Canada. In published researches, it has been found that L. feeleii serogroup 2 (ATCC 35849, LfLD) possess mono-polar flagellum, and L. feeleii serogroup 1 (ATCC 35072, WRLf) could secrete some exopolysaccharide (EPS) materials to the surrounding. Although the virulence of the L. feeleii strain was evidenced that could be promoted, the EPS might be dispensable for the bacteria that caused Pontiac fever. Based on the current knowledge, we focused on bacterial infection in human and murine host cells, intracellular growth, cytopathogenicity, stimulatory capacity of cytokines secretion, and pathogenic effects of the EPS of L. feeleii in this review.

Keywords

Legionella feeleii Pontiac fever Legionnaires’ disease Flagellum Exopolysaccharide Bacterial infection 

Notes

Acknowledgements

We are deeply indebted Dr. Shin-ichi Yoshida, Dr. Mitsumasa Saito, Dr. Kazunobu Amako, Hideko Kameyama for the kind guidance and help, scientific discussion and technical assistance of previous studies. We also want to thank all the members for the kind support when the first author studied at the Department of Bacteriology, Kyushu University, Japan as a Ph.D. candidate. This work was supported by a Grant from Natural Science Foundation of Hebei Province, China (No. H2018206259).

References

  1. 1.
    Newton HJ, Ang DK, van Driel IR, Hartland EL (2010) Molecular pathogenesis of infections caused by Legionella pneumophila. Clin Microbiol Rev 23(2):274–298.  https://doi.org/10.1128/CMR.00052-09 PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Steele TW, Moore CV, Sangster N (1990) Distribution of Legionella longbeachae serogroup 1 and other Legionellae in potting soils in Australia. Appl Environ Microbiol 56(10):2984–2988PubMedPubMedCentralGoogle Scholar
  3. 3.
    Appelt S, Heuner K (2017) The flagellar regulon of Legionella—a review. Front Cell Infect Microbiol 7:454.  https://doi.org/10.3389/fcimb.2017.00454 PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Fields BS, Benseton RF, Besser RE (2002) Legionella and Legionnaires’ disease: 25 years of investigation. Clin Microbiol Rev 15(3):506–526PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Skaliy P, McEachern HV (1979) Survival of the Legionnaires’ disease bacterium in water. Ann Intern Med 90(4):662–663PubMedCrossRefGoogle Scholar
  6. 6.
    Rowbotham TJ (1980) Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J Clin Pathol 33(12):1179–1183PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Anand CM, Skinner AR, Malic A, Kurtz JB (1983) Interaction of L. pneumophilia and a free living amoeba (Acanthamoeba palestinensis). J Hyg (Lond) 91(2):167–178CrossRefGoogle Scholar
  8. 8.
    King CH, Shotts EB Jr, Wooley RE, Porter KG (1988) Survival of coliforms and bacterial pathogens within protozoa during chlorination. Appl Environ Microbiol 54(12):3023–3033PubMedPubMedCentralGoogle Scholar
  9. 9.
    Barker J, Brown MR, Collier PJ, Farrell I, Gilbert P (1992) Relationship between Legionella pneumophila and Acanthamoeba polyphaga: physiological status and susceptibility to chemical inactivation. Appl Environ Microbiol 58(12):2420–2425PubMedPubMedCentralGoogle Scholar
  10. 10.
    Maruta K, Miyamoto H, Hamada T, Ogawa M, Taniguchi H, Yoshida S (1988) Entry and intracellular growth of Legionella dumoffii in alveolar epithelial cells. Am J Respir Crit Care Med 157(6 Pt 1):1967–1974.  https://doi.org/10.1164/ajrccm.157.6.9710108 CrossRefGoogle Scholar
  11. 11.
    Alli OA, Zink S, von Lackum NK, Abu-Kwaik Y (2003) Comparative assessment of virulence traits in Legionella spp. Microbiology 149(Pt 3):631–641.  https://doi.org/10.1099/mic.0.25980-0 PubMedCrossRefGoogle Scholar
  12. 12.
    Ohnishi H, Mizunoe Y, Takade A, Tanaka Y, Miyamoto H, Harada M, Yoshida S (2004) Legionella dumoffii DjlA, a member of the DnaJ family, is required for intracellular growth. Infect Immun 72(6):3592–3603.  https://doi.org/10.1128/IAI.72.6.3592-3603.2004 PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Takekawa Y, Saito M, Wang C, Qin T, Ogawa M, Kanemaru T, Yoshida S (2012) Characteristic morphology of intracellular microcolonies of Legionella oakridgensis OR-10. Can J Microbiol 58(2):179–183.  https://doi.org/10.1139/w11-126 PubMedCrossRefGoogle Scholar
  14. 14.
    Wang C, Saito M, Tanaka T, Amako K, Yoshida S (2015) Comparative analysis of virulence traits between a Legionella feeleii strain implicated in Pontiac Fever and a strain that caused Legionnaires’ disease. Microb Pathog 89:79–86.  https://doi.org/10.1016/j.micpath.2015.09.004 PubMedCrossRefGoogle Scholar
  15. 15.
    Isberg RR, O’Connor TJ, Heidtman M (2009) The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat Rev Microbiol 7(1):13–24.  https://doi.org/10.1038/nrmicro1967 PubMedCrossRefGoogle Scholar
  16. 16.
    Vogel JP, Isberg RR (1999) Cell biology of Legionella pneumophila. Curr Opin Microbiol 2(1):30–34.  https://doi.org/10.1016/S1369-5274(99)80005-8 PubMedCrossRefGoogle Scholar
  17. 17.
    Hilbi H, Segal G, Shuman HA (2001) Icm/dot-dependent upregulation of phagocytosis by Legionella pneumophila. Mol Microbiol 42(3):603–617.  https://doi.org/10.1046/j.1365-2958.2001.02645.x PubMedCrossRefGoogle Scholar
  18. 18.
    Ogawa M, Takade A, Miyamoto H, Taniguchi H, Yoshida S (2001) Morphological variety of intracellular microcolonies of Legionella species in Vero cells. Microbiol Immunol 45(7):557–562.  https://doi.org/10.1111/j.1348-0421.2001.tb02658.x PubMedCrossRefGoogle Scholar
  19. 19.
    Herwaldt LA, Gorman GW, McGrath T, Toma S, Brake B, Hightower AW, Jones J, Reingold AL, Boxer PA, Tang PW et al (1984) A new Legionella species, Legionella feeleii species nova, causes Pontiac fever in an automobile plant. Ann Intern Med 100(3):333–338.  https://doi.org/10.7326/0003-4819-100-3-333 PubMedCrossRefGoogle Scholar
  20. 20.
    Palutke WA, Crane LR, Wentworth BB, Geiger JG, Cardozo L, Singhakowinta A, Bartley J, Robinson BE (1986) Legionella feeleii-associated pneumonia in humans. Am J Clin Pathol 86(3):348–351PubMedCrossRefGoogle Scholar
  21. 21.
    Thacker WL, Wilkinson HW, Plikaytis BB, Steigerwalt AG, Mayberry WR, Moss CW, Brenner DJ (1985) Second serogroup of Legionella feeleii strains isolated from humans. J Clin Microbiol 22(1):1–4PubMedPubMedCentralGoogle Scholar
  22. 22.
    Moffat JF, Tompkins LS (1992) A quantitative model of intracellular growth of Legionella pneumophila in Acanthamoeba castellanii. Infect Immun 60(1):296–301PubMedPubMedCentralGoogle Scholar
  23. 23.
    Moss CW, Bibb WF, Karr DE, Guerrant GO, Lambert MA (1983) Cellular fatty acid composition and ubiquinone content of Legionella feeleii sp. nov. J Clin Microbiol 18(4):917–919PubMedPubMedCentralGoogle Scholar
  24. 24.
    Fields BS, Barbaree JM, Shotts EB Jr, Feeley JC, Morrill WE, Sanden GN, Dykstra MJ (1986) Comparison of guinea pig and protozoan models for determining virulence of Legionella species. Infect Immun 53(3):553–559PubMedPubMedCentralGoogle Scholar
  25. 25.
    Macnab RM (2003) How bacteria assemble flagella. Annu Rev Microbiol 57:77–100.  https://doi.org/10.1146/annurev.micro.57.030502.090832 PubMedCrossRefGoogle Scholar
  26. 26.
    Fujii T, Kato T, Hiraoka KD, Miyata T, Minamino T, Chevance FF, Hughes KT, Namba K (2017) Identical folds used for distinct mechanical functions of the bacterial flagellar rod and hook. Nat Commun 8:14276.  https://doi.org/10.1038/ncomms14276 PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Aldridge P, Hughes KT (2002) Regulation of flagellar assembly. Curr Opin Microbiol 5(2):160–165.  https://doi.org/10.1016/S1369-5274(02)00302-8 PubMedCrossRefGoogle Scholar
  28. 28.
    Molofsky AB, Shetron-Rama LM, Swanson MS (2005) Components of the Legionella pneumophila flagellar regulon contribute to multiple virulence traits, including lysosome avoidance and macrophage death. Infect Immun 73(9):5720–5734.  https://doi.org/10.1128/IAI.73.9.5720-5734.2005 PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Giron JA, Torres AG, Freer E, Kaper JB (2002) The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol Microbiol 44(2):361–379.  https://doi.org/10.1046/j.1365-2958.2002.02899.x PubMedCrossRefGoogle Scholar
  30. 30.
    Tomich M, Herfst CA, Golden JW, Mohr CD (2002) Role of flagella in host cell invasion by Burkholderia cepacia. Infect Immun 70(4):1799–1806.  https://doi.org/10.1128/IAI.70.4.1799-1806.2002 PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Inglis TJ, Robertson T, Woods DE, Dutton N, Chang BJ (2003) Flagellum-mediated adhesion by Burkholderia pseudomallei precedes invasion of Acanthamoeba astronyxis. Infect Immun 71(4):2280–2282.  https://doi.org/10.1128/IAI.71.4.2280-2282.2003 PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Young GM, Schmiel DH, Miller VL (1999) A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc Natl Acad Sci USA 96(11):6456–6461.  https://doi.org/10.1073/pnas.96.11.6456 PubMedCrossRefGoogle Scholar
  33. 33.
    Ghelardi E, Celandroni F, Salvetti S, Beecher DJ, Gominet M, Lereclus D, Wong AC, Senesi S (2002) Requirement of flhA for swarming differentiation, flagellin export, and secretion of virulence-associated proteins in Bacillus thuringiensis. J Bacteriol 184(23):6424–6433.  https://doi.org/10.1128/JB.184.23.6424-6433.2002 PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Bornstein N, Marmet D, Dumaine MH, Surgot M, Fleurette J (1991) Detection of flagella in 278 Legionella strains by latex reagent sensitized with antiflagellum immunoglobulins. J Clin Mirobiol 29(5):953–956Google Scholar
  35. 35.
    Dietrich C, Heuner K, Brand BC, Hacker J, Steinert M (2001) Flagellum of Legionella pneumophila positively affects the early phase of infection of eukaryotic host cells. Infect Immun 69(4):2116–2122.  https://doi.org/10.1128/IAI.69.4.2116-2122.2001 PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Silveira TN, Zamboni DS (2010) Pore Formation triggered by Legionella spp. is an Nlrc4 inflammasome-dependent host cell response that precedes pyroptosis. Infect Immun 78(3):1403–1413.  https://doi.org/10.1128/IAI.00905-09 PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Pereira MS, Marques GG, Dellama JE, Zamboni DS (2011) The Nlrc4 inflammasome contributes to restriction of pulmonary infection by flagellated Legionella spp. that trigger pyroptosis. Front Microbiol 2:33.  https://doi.org/10.3389/fmicb.2011.00033 PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Heuner K, Steinert M (2003) The flagellum of Legionella pneumophila and its link to the expression of the virulent phenotype. Int J Med Microbiol 293(2–3):133–143.  https://doi.org/10.1078/1438-4221-00259 PubMedCrossRefGoogle Scholar
  39. 39.
    Heuner K, Bender-Beck L, Brand BC, Lück PC, Mann KH, Marre R, Ott M, Hacker J (1995) Cloning and genetic characterization of the flagellum subunit gene (flaA) of Legionella pneumophila serogroup 1. Infect Immun 63(7):2499–2507PubMedPubMedCentralGoogle Scholar
  40. 40.
    Ott M, Messner P, Heesemann J, Marre R, Hacker J (1991) Temperature-dependent expression of flagella in Legionella. J Gen Microbiol 137(8):1955–1961.  https://doi.org/10.1099/00221287-137-8-1955 PubMedCrossRefGoogle Scholar
  41. 41.
    Whitfield NN, Byrne BG, Swanson MS (2010) Mouse macrophages are permissive to motile Legionella species that fail to trigger pyroptosis. Infect Immun 78(1):423–432.  https://doi.org/10.1128/IAI.00070-09 PubMedCrossRefGoogle Scholar
  42. 42.
    Case CL, Shin S, Roy CR (2009) Asc and Ipaf inflammasomes direct distinct pathways for Caspase-1 activation in response to Legionella pneumophila. Infect Immun 77(5):1981–1991.  https://doi.org/10.1128/IAI.01382-08 PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124(4):783–801.  https://doi.org/10.1016/j.cell.2006.02.015 PubMedCrossRefGoogle Scholar
  44. 44.
    Mariathasan S, Monack DM (2007) Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat Rev Immunol 7(1):31–40.  https://doi.org/10.1038/nri1997 PubMedCrossRefGoogle Scholar
  45. 45.
    Molofsky AB, Byrne BG, Whitfield NN, Madigan CA, Fuse ET, Tateda K, Swanson MS (2006) Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J Exp Med 203(4):1093–1104.  https://doi.org/10.1084/jem.20051659 PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Casson CN, Copenhaver AM, Zwack EE, Nguyen HT, Strowig T, Javdan B, Bradley WP, Fung TC, Flavell RA, Brodsky IE, Shin S (2013) Caspase-11 activation in response to bacterial secretion systems that access the host cytosol. PLoS Pathog 9(6):e1003400.  https://doi.org/10.1371/journal.ppat.1003400 PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Lightfield KL, Persson J, Trinidad NJ, Brubaker SW, Kofoed EM, Sauer JD, Dunipace EA, Warren SE, Miao EA, Vance RE (2011) Differential requirements for NAIP5 in activation of the NLRC4 inflammasome. Infect Immun 79(4):1606–1614.  https://doi.org/10.1128/IAI.01187-10 PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Franchi L, Muñoz-Planillo R, Núñez G (2012) Sensing and reacting to microbes through the inflammasomes. Nat Immunol 13(4):325–332.  https://doi.org/10.1038/ni.2231 PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Zhao Y, Shao F (2016) Diverse mechanisms for inflammasome sensing of cytosolic bacteria and bacterial virulence. Curr Opin Microbiol 29:37–42.  https://doi.org/10.1016/j.mib.2015.10.003 PubMedCrossRefGoogle Scholar
  50. 50.
    Zhao Y, Shi J, Shi X, Wang Y, Wang F, Shao F (2016) Genetic functions of the NAIP family of inflammasome receptors for bacterial ligands in mice. J Exp Med 213(5):647–656.  https://doi.org/10.1084/jem.20160006 PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Hawn TR, Verbon A, Lettinga KD, Zhao LP, Li SS, Laws RJ, Skerrett SJ, Beutler B, Schroeder L, Nachman A, Ozinsky A, Smith KD, Aderem A (2003) A common dominant TLR5 stop codon polymorphism abolishes flagellin signaling and is associated with susceptibility to Legionnaires’ disease. J Exp Med 198(10):1563–1572.  https://doi.org/10.1084/jem.20031220 PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Schmeck B, N’Guessan PD, Ollomang M, Lorenz J, Zahlten J, Opitz B, Flieger A, Suttorp N, Hippenstiel S (2007) Legionella pneumophila-induced NF-kappaB- and MAPK-dependent cytokine release by lung epithelial cells. Eur Respir J 29(1):25–33.  https://doi.org/10.1183/09031936.00141005 PubMedCrossRefGoogle Scholar
  53. 53.
    Lorenz J, Zahlten J, Pollok I, Lippmann J, Scharf S, N’Guessan PD, Opitz B, Flieger A, Suttorp N, Hippenstiel S, Schmeck B (2011) Legionella pneumophila-induced IκBζ-dependent expression of interleukin-6 in lung epithelium. Eur Respir J 37(3):648–657.  https://doi.org/10.1183/09031936.00200009 PubMedCrossRefGoogle Scholar
  54. 54.
    Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140(6):805–820.  https://doi.org/10.1016/j.cell.2010.01.022 PubMedCrossRefGoogle Scholar
  55. 55.
    Medzhitov R (2007) Recognition of microorganisms and activation of the immune response. Nature 449(7164):819–826.  https://doi.org/10.1038/nature06246 PubMedCrossRefGoogle Scholar
  56. 56.
    Eisele NA, Anderson DM (2011) Host defense and the airway epithelium: frontline responses that protect against bacterial invasion and pneumonia. J Pathog.  https://doi.org/10.4061/2011/249802 PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Wai SN, Mizunoe Y, Takade A, Kawabata SI, Yoshida SI (1998) Vibrio cholerae O1 strain TSI-4 produces the exopolysaccharide materials that determine colony morphology, stress resistance, and biofilm formation. Appl Environ Microbiol 64(10):3648–3655PubMedPubMedCentralGoogle Scholar
  58. 58.
    Torres-Cabassa A, Gottesman S, Frederick RD, Dolph PJ, Coplin DL (1987) Control of extracellular polysaccharide synthesis in Erwinia stewartii and Escherichia coli K-12: a common regulatory function. J Bacteriol 169(10):4525–4531.  https://doi.org/10.1128/jb.169.10.4525-4531.1987 PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Yoshida S, Ogawa M, Mizuguchi Y (1985) Relation of capsular materials and colony opacity to virulence of Vibrio vulnificus. Infect Immun 47(2):446–451PubMedPubMedCentralGoogle Scholar
  60. 60.
    Martin DW, Schurr MJ, Mudd MH, Govan JR, Holloway BW, Deretic V (1993) Mechanism of conversion to mucoidy in Pseudomonas aeruginosa infecting cystic fibrosis patients. Proc Natl Acad Sci USA 90(18):8377–8381.  https://doi.org/10.1073/pnas.90.18.8377 PubMedCrossRefGoogle Scholar
  61. 61.
    Wang C, Saito M, Ogawa M, Yoshida S (2016) Colony types and virulence traits of Legionella feeleii determined by exopolysacchride materials. FEMS Microbiol Lett 363(10):fnw098.  https://doi.org/10.1093/femsle/fnw098 PubMedCrossRefGoogle Scholar
  62. 62.
    Edelstein PH (2007) Urine antigen tests positive for Pontiac fever: implications for diagnosis and pathogenesis. Clin Infect Dis 44(2):229–231.  https://doi.org/10.1086/510394 PubMedCrossRefGoogle Scholar
  63. 63.
    Mangione EJ, Remis RS, Tait KA, Gee HB, Gorman GW, Wentworth BB, Baron PA, Hightower AW, Barbaree JM, Broome CV (1985) An outbreak of Pontiac fever related to whirlpool use, Michigan 1982. JAMA 253(4):535–539.  https://doi.org/10.1001/jama.1985.03350280091026 PubMedCrossRefGoogle Scholar
  64. 64.
    Fallon RJ, Rowbotham TJ (1990) Microbiological investigations into an outbreak of Pontiac fever due to Legionella micdadei associated with use of a whirlpool. J Clin Pathol 43(6):479–483.  https://doi.org/10.1136/jcp.43.6.479 PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Fields BS, Barbaree JM, Sanden GN, Morrill WE (1990) Virulence of a Legionella anisa strain associated with Pontiac fever: an evaluation using protozoan, cell culture, and guinea pig models. Infect Immun 58(9):3139–3142PubMedPubMedCentralGoogle Scholar
  66. 66.
    Cramp GJ, Harte D, Douglas NM, Graham F, Schousboe M, Sykes K (2010) An outbreak of Pontiac fever due to Legionella longbeachae serogroup 2 found in potting mix in a horticultural nursery in New Zealand. Epidemiol Infect 138(1):15–20.  https://doi.org/10.1017/S0950268809990835 PubMedCrossRefGoogle Scholar
  67. 67.
    Huhn GD, Adam B, Ruden R, Hilliard L, Kirkpatrick P, Todd J, Crafts W, Passaro D, Dworkin MS (2005) Outbreak of travel-related pontiac fever among hotel guests illustrating the need for better diagnostic tests. J Travel Med 12(4):173–179.  https://doi.org/10.2310/7060.2005.12401 PubMedCrossRefGoogle Scholar
  68. 68.
    Diederen BM (2008) Legionella spp. and Legionnaires’ disease. J Infect 56(1):1–12.  https://doi.org/10.1016/j.jinf.2007.09.010 PubMedCrossRefGoogle Scholar
  69. 69.
    Swanson MS, Hammer BK (2000) Legionella pneumophila pathogenesis: a fateful journey from amoebae to macrophages. Annu Rev Microbiol 54:567–613.  https://doi.org/10.1146/annurev.micro.54.1.567 PubMedCrossRefGoogle Scholar
  70. 70.
    Fraser DW, Tsai TR, Orenstein W, Parkin WE, Beecham HJ, Sharrar RG, Harris J, Mallison GF, Martin SM, McDade JE, Shepard CC, Brachman PS (1977) Legionnaires’ disease: description of an epidemic of pneumonia. N Engl J Med 297(22):1189–1197.  https://doi.org/10.1056/NEJM197712012972201 PubMedCrossRefGoogle Scholar
  71. 71.
    Fiumefreddo R, Zaborsky R, Haeuptle J, Christ-Crain M, Trampuz A, Steffen I, Frei R, Müller B, Schuetz P (2009) Clinical predictors for Legionella in patients presenting with community-acquired pneumonia to the emergency department. BMC Pulm Med 9:4.  https://doi.org/10.1186/1471-2466-9-4 PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Muder RR, Yu VL (2002) Infection due to Legionella species other than L. pneumophila. Clin Infect Dis 35(8):990–998.  https://doi.org/10.1086/342884 PubMedCrossRefGoogle Scholar
  73. 73.
    Yu VL, Plouffe JF, Pastoris MC, Stout JE, Schousboe M, Widmer A, Summersgill J, File T, Heath CM, Paterson DL, Chereshsky A (2002) Distribution of Legionella species and serogroups isolated by culture in patients with sporadic community-acquired legionellosis: an international collaborative survey. J Infect Dis 186(1):127–128.  https://doi.org/10.1086/341087 PubMedCrossRefGoogle Scholar
  74. 74.
    Weiss D, Boyd C, Rakeman JL, Greene SK, Fitzhenry R, McProud T, Musser K, Huang L, Kornblum J, Nazarian EJ, Fine AD, Braunstein SL, Kass D, Landman K, Lapierre P, Hughes S, Tran A, Taylor J, Baker D, Jones L, Kornstein L, Liu B, Perez R, Lucero DE, Peterson E, Benowitz I, Lee KF, Ngai S, Stripling M, Varma JK (2017) A large community outbreak of Legionnaires’ disease associated with a cooling tower in New York City, 2015. Public Health Rep 132(2):241–250.  https://doi.org/10.1177/0033354916689620 PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Personnic N, Striednig B, Hilbi H (2017) Legionella quorum sensing and its role in pathogen–host interactions. Curr Opin Microbiol 41:29–35.  https://doi.org/10.1016/j.mib.2017.11.010 PubMedCrossRefGoogle Scholar
  76. 76.
    Correia AM, Ferreira JS, Borges V, Nunes A, Gomes B, Capucho R, Gonçalves J, Antunes DM, Almeida S, Mendes A, Guerreiro M, Sampaio DA, Vieira L, Machado J, Simões MJ, Gonçalves P, Gomes JP (2016) Probable person-to-person transmission of Legionnaires’ disease. N Engl J Med 374(5):497–498.  https://doi.org/10.1056/NEJMc1505356 PubMedCrossRefGoogle Scholar
  77. 77.
    Lee J, Caplivski D, Wu M, Huprikar S (2009) Pneumonia due to Legionella feeleii: case report and review of the literature. Transpl Infect Dis 11(4):337–340.  https://doi.org/10.1111/j.1399-3062.2009.00390.x PubMedCrossRefGoogle Scholar
  78. 78.
    Keen MG, Hoffman PS (1989) Characterization of a Legionella pneumophila extracellular protease exhibiting hemolytic and cytotoxic activities. Infect Immun 57(3):732–738PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Pathogenic BiologyHebei Medical UniversityShijiazhuangPeople’s Republic of China
  2. 2.School of Basic Medical ScienceHebei Medical UniversityShijiazhuangPeople’s Republic of China

Personalised recommendations