Share This Article:
Review Paper

Borrelia burgdorferi: Cell Biology and Clinical Manifestations in Latent Chronic Lyme

Full-Text HTML XML Download Download as PDF (Size:2646KB) PP. 210-223
DOI: 10.4236/ojmm.2014.44023    7,364 Downloads   18,371 Views   Citations

ABSTRACT

Chronic Lyme disease is predicated by an infection with Borrelia burgdorferi via tick vector. B. burgdorferi has been extensively researched with regard to its genome and cell biology. There are many unique characteristics to the bacteria itself; however, serological diagnostics and diagnosis based on symptoms can be complicated and potentially misleading. Other promising diagnostics were also evaluated in this review. Treatment of the chronic Lyme disease can be complicated and at times ineffective. The purpose of this review is to examine B. burgdorferi from a biological and clinical perspective.

Cite this paper

Smith, A. , Oertle, J. and Prato, D. (2014) Borrelia burgdorferi: Cell Biology and Clinical Manifestations in Latent Chronic Lyme. Open Journal of Medical Microbiology, 4, 210-223. doi: 10.4236/ojmm.2014.44023.

References

[1] Garin, C. and Bujadoux, A. (1922) Paralysie par les tiques. J Med Lyon, 71, 765-767.
[2] Steere, A.C., Malawista, S.E., Hardin, J.A., Ruddy, S., Askenase, W. and Andiman, W.A. (1977) Erythema Chronicum Migrans and Lyme Arthritis. The Enlarging Clinical Spectrum. Annals of Internal Medicine, 86, 685-698.
http://dx.doi.org/10.7326/0003-4819-86-6-685
[3] Qiu, W. and Martin, C. (2014) Evolutionary Genomics of Borrelia burgdorferi Sensu Lato: Findings, Hypotheses, and the Rise of Hybrids. Infection, Genetics and Evolution, 27, 576-593.
http://dx.doi.org/10.1016/j.meegid.2014.03.025
[4] Casjens, S., Palmer, N., van Vugt, R., Huang, W.M., Stevenson, B., et al. (2000) A Bacterial Genome in Flux: The Twelve Linear and Nine Circular Extrachromosomal DNAs in an Infectious Isolate of the Lyme Disease Spirochete Borrelia burgdorferi. Molecular Microbiology, 35, 490-516.
http://dx.doi.org/10.1046/j.1365-2958.2000.01698.x
[5] Casjens, S.R., Mongodin, E.F., Qiu, W.-G., Luft, B.J., Schutzer, S.E., et al. (2012) Genome Stability of Lyme Disease Spirochetes: Comparative Genomics of Borrelia burgdorferi Plasmids. PLoS ONE, 7.
http://dx.doi.org/10.1371/journal.pone.0033280
[6] Chaconas, G. and Kobryn, K. (2010) Structure, Function, and Evolution of Linear Replicons in Borrelia. Annual Review of Microbiology, 64, 185-202.
http://dx.doi.org/10.1146/annurev.micro.112408.134037
[7] Fraser, C.M., Casjens, S., Huang, W.M., Sutton, G.G., Clayton, R., et al. (1997) Genomic Sequence of a Lyme Disease Spirochete, Borrelia burgdorferi. Nature, 390, 580-586.
http://dx.doi.org/10.1038/37551
[8] Barbour, A.G. and Garon, C.F. (1987) Linear Plasmids of the Bacterium Borrelia burgdorferi Have Covalently Closed Ends. Science, 237, 409-411.
http://dx.doi.org/10.1126/science.3603026
[9] Kobryn, K. and Chaconas, G. (2002) ResT, a Telomere Resolvase Encoded by the Lyme Disease Spirochete. Molecular Cells, 9, 195-201.
http://dx.doi.org/10.1016/S1097-2765(01)00433-6
[10] Radolf, J.D., Caimano, M.J., Stevenson, B. and Hu, L.T. (2012) Of Ticks, Mice and Men: Understanding the Dualhost Lifestyle of Lyme Disease Spirochaetes. Nature Reviews Microbiology, 10, 87-99.
[11] Samuels, D.S. (2011) Gene Regulation in Borrelia burgdorferi. Annual Review of Microbiology, 65, 479-499.
http://dx.doi.org/10.1146/annurev.micro.112408.134040
[12] Singh, S.K. and Girschick, H.J. (2004) Molecular Survival Strategies of the Lyme Disease Spirochete Borrelia burgdorferi. The Lancet Infectious Diseases, 4, 575-583.
http://dx.doi.org/10.1016/S1473-3099(04)01132-6
[13] Gherardini, F., Boylan, J., Lawrence, K. and Skare, J. (2010) Metabolism and Physiology of Borrelia. Borrelia: Molecular Biology, Host Interaction and Pathogenesis. Caister Academic Press, Norfolk, 103-138.
[14] Saier Jr., M.H. and Paulsen, I.T. (2000) Whole Genome Analyses of Transporters in Spirochetes: Borrelia burgdorferi and Treponema pallidum. Journal of Molecular Microbiology and Biotechnology, 2, 393-399.
[15] Zhang, J.-R., Hardham, J.M., Barbour, A.G. and Norris, S.J. (1997) Antigenic Variation in Lyme Disease Borreliae by Promiscuous Recombination of VMP-Like Sequence Cassettes. Cell, 89, 275-285.
http://dx.doi.org/10.1016/S0092-8674(00)80206-8
[16] Zhang, J.-R. and Norris, S.J. (1998) Genetic Variation of the Borrelia burgdorferi Gene vlsE Involves Cassette-Specific, Segmental Gene Conversion. Infection and Immunity, 66, 3698-3704.
[17] Barbour, A.G. (1984) Isolation and Cultivation of Lyme Disease Spirochetes. Yale Journal of Biology and Medicine, 57, 521-525.
[18] Corbin, B.D., Seeley, E.H., Raab, A., Feldmann, J., Miller, M.R., Torres, V.J., et al. (2008) Metal Chelation and Inhibition of Bacterial Growth in Tissue Abscesses. Science, 319, 962-965.
http://dx.doi.org/10.1126/science.1152449
[19] Papp-Wallace, K.M. and Maguire, M.E. (2006) Manganese Transport and the Role of Manganese in Virulence. Annual Review of Microbiology, 60, 187-209.
http://dx.doi.org/10.1146/annurev.micro.60.080805.142149
[20] Wandersman, C. and Delepelaire, P. (2004) Bacterial Iron Sources: From Siderophores to Hemophores. Annual Review of Microbiology, 58, 611-647.
http://dx.doi.org/10.1146/annurev.micro.58.030603.123811
[21] Overbeek, R., Larsen, N., Walunas, T., D’Souza, M., Pusch, G., Selkov Jr., E., et al. (2003) The ERGO Genome Analysis and Discovery System. Nucleic Acids Research, 31, 164-171.
http://dx.doi.org/10.1093/nar/gkg148
[22] Wang, X.G., Lin, B., Kidder, J.M., Telford, S. and Hu, L.T. (2002) Effects of Environmental Changes on Expression of the Oligopeptide Permease (opp) Genes of Borrelia burgdorferi. Journal of Bacteriology, 184, 6198-6206.
http://dx.doi.org/10.1128/JB.184.22.6198-6206.2002
[23] von Lackum, K. and Stevenson, B. (2005) Carbohydrate Utilization by the Lyme borreliosis Spirochete, Borrelia burgdorferi. FEMS Microbiology Letters, 243, 173-179.
http://dx.doi.org/10.1016/j.femsle.2004.12.002
[24] Tilly, K., Elias, A.F., Errett, J., Fischer, E., Iyer, R., Schwartz, I., et al. (2001) Genetics and Regulation of Chitobiose Utilization in Borrelia burgdorferi. Journal of Bacteriology, 183, 5544-5553.
http://dx.doi.org/10.1128/JB.183.19.5544-5553.2001
[25] He, M., Ouyang, Z., Troxell, B., Xu, H., Moh, A., Piesman, J., et al. (2011) Cyclic di-GMP Is Essential for the Survival of the Lyme Disease Spirochete in Ticks. PLoS Pathogens, 7, e1002133.
http://dx.doi.org/10.1371/journal.ppat.1002133
[26] Pappas, C.J., Iyer, R., Petzke, M.M., Caimano, M.J., Radolf, J.D. and Schwartz, I. (2011) Borrelia burgdorferi Requires Glycerol for Maximum Fitness during the Tick Phase of the Enzootic Cycle. PLoS Pathogens, 7, e1002102.
http://dx.doi.org/10.1371/journal.ppat.1002102
[27] Barbour, A.G. and Hayes, S.F. (1986) Biology of Borrelia Species. Microbiological Reviews, 50, 381-400.
[28] Boylan, J.A., Lawrence, K.A., Downey, J.S. and Gherardini, F.C. (2008) Borrelia burgdorferi Membranes Are the Pri- mary Targets of Reactive Oxygen Species. Molecular Microbiology, 68, 786-799.
http://dx.doi.org/10.1111/j.1365-2958.2008.06204.x
[29] Ostberg, Y., Berg, S., Comstedt, P., Wieslander, A. and Bergstrom, S. (2007) Functional Analysis of a Lipid Galactosyltransferase Synthesizing the Major Envelope Lipid in the Lyme Disease Spirochete Borrelia burgdorferi. FEMS Microbiology Letters, 272, 22-29.
http://dx.doi.org/10.1111/j.1574-6968.2007.00728.x
[30] Wang, X.G., Scagliotti, J.P. and Hu, L.T. (2004) Phospholipid Synthesis in Borrelia burgdorferi: BB0249 and BB0721 Encode Functional Phosphatidylcholine Synthase and Phosphatidylglycerolphosphate Synthase Proteins. Microbiology, 150, 391-397.
http://dx.doi.org/10.1099/mic.0.26752-0
[31] Sambir, M., Ivanova, L.B., Bryksin, A.V., Godfrey, H.P. and Cabello, F.C. (2011) Functional Analysis of Borrelia burgdorferi uvrA in DNA Damage Protection. FEMS Microbiology Letters, 317, 172-180.
http://dx.doi.org/10.1111/j.1574-6968.2011.02226.x
[32] Hardy, P.O. and Chaconas, G. (2013) The Nucleotide Excision Repair System of Borrelia burgdorferi Is the Sole Pathway Involved in Repair of DNA Damage by UV Light. Journal of Bacteriology, 195, 2220-2231.
http://dx.doi.org/10.1128/JB.00043-13
[33] Johnson, L. and Stricker, R. (2010) The Infectious Diseases Society of America Lyme Guidelines: A Cautionary Tale about the Development of Clinical Practice Guidelines. Philosophy, Ethics, and Humanities in Medicine, 5, 9.
http://dx.doi.org/10.1186/1747-5341-5-9
[34] Sal, M.S., Li, C., Motalab, M.A., Shibata, S., Aizawa, S. and Charon, N.W. (2008) Borrelia burgdorferi Uniquely Regulates Its Motility Genes and Has an Intricate Flagellar Hook-Basal Body Structure. Journal of Bacteriology, 190, 1912-1921.
http://dx.doi.org/10.1128/JB.01421-07
[35] Charon, N.W., Goldstein, S.F., Marko, M., et al. (2009) The Flat Ribbon Configuration of the Periplasmic Flagella of Borrelia burgdorferi and Its Relationship to Motility and Morphology. Journal of Bacteriology, 191, 600-607.
http://dx.doi.org/10.1128/JB.01288-08
[36] Berende, A., Oosting, M., Kullberg, B.J., Netea, M.G. and Joosten, L.A. (2010) Activation of Innate Host Defense Mechanisms by Borrelia. European Cytokine Network, 21, 7-18.
[37] Weis, J.J. and Bockenstedt, L.K. (2010) Host Response. In: Samuels, D.S. and Radolf, J., Eds., Borrelia—Molecular biology, Host Interaction and Pathogenesis, Caister Academic Press, Norfolk, 413-441.
[38] Posey, J.E. and Gherardini, F.C. (2000) Lack of a Role for Iron in the Lyme Disease Pathogen. Science, 288, 1651- 1653.
http://dx.doi.org/10.1126/science.288.5471.1651
[39] Iuchi, S. and Weiner, L. (1996) Cellular and Molecular Physiology of Escherichia coli in the Adaptation to Aerobic Environments. Journal of Biochemistry, 120, 1055-1063.
http://dx.doi.org/10.1093/oxfordjournals.jbchem.a021519
[40] Boylan, J.A., Hummel, C.S., Benoit, S., Garcia-Lara, J., Treglown-Downey, J., Crane, E.J., et al. (2006) Borrelia burgdorferi bb0728 Encodes a Coenzyme A Disulphide Reductase Whose Function Suggests a Role in Intracellular Redox and the Oxidative Stress Response. Molecular Microbiology, 59, 475-486.
http://dx.doi.org/10.1111/j.1365-2958.2005.04963.x
[41] Boylan, J.A., Posey, J.E. and Gherardini, F.C. (2003) Borrelia Oxidative Stress Response Regulator, BosR: A Distinctive Zn-Dependent Transcriptional Activator. Proceedings of the National Academy of Sciences of the United States of America, 100, 11684-91168.
http://dx.doi.org/10.1073/pnas.2032956100
[42] Hyde, J.A., Seshu, J. and Skare, J.T. (2006) Transcriptional Profiling of Borrelia burgdorferi Containing a Unique bosR Allele Identifies a Putative Oxidative Stress Regulon. Microbiology, 152, 2599-2609.
http://dx.doi.org/10.1099/mic.0.28996-0
[43] Ouyang, Z., Deka, R.K. and Norgard, M.V. (2011) BosR (BB0647) Controls the RpoN-RpoS Regulatory Pathway and Virulence Expression in Borrelia burgdorferi by a Novel DNA-Binding Mechanism. PLoS Pathogens, 7, e1001272.
http://dx.doi.org/10.1371/journal.ppat.1001272
[44] Seshu, J., Boylan, J.A., Hyde, J.A., Swingle, K.L., Gherardini, F.C. and Skare, J.T. (2004) A Conservative Amino Acid Change Alters the Function of BosR, the Redox Regulator of Borrelia burgdorferi. Molecular Microbiology, 54, 1352- 1363.
http://dx.doi.org/10.1111/j.1365-2958.2004.04352.x
[45] Zhao, G., Ceci, P., Ilari, A., Giangiacomo, L., Laue, T.M., Chiancone, E., et al. (2002) Iron and Hydrogen Peroxide Detoxification Properties of DNA-Binding Protein from Starved Cells. A Ferritin-Like DNA-Binding Protein of Esche- richia coli. The Journal of Biological Chemistry, 277, 27689-27696.
http://dx.doi.org/10.1074/jbc.M202094200
[46] Aguirre, J.D., Clark, H.M., McIlvin, M., Vazquez, C., Palmere, S.L., Grab, D.J., et al. (2013) A Manganese-Rich Environment Supports Superoxide Dismutase Activity in a Lyme Disease Pathogen, Borrelia burgdorferi. The Journal of Biological Chemistry, 288, 8468-8478.
http://dx.doi.org/10.1074/jbc.M112.433540
[47] Esteve-Gassent, M.D., Elliott, N.L. and Seshu, J. (2009) sodA Is Essential for Virulence of Borrelia burgdorferi in the Murine Model of Lyme Disease. Molecular Microbiology, 71, 594-612.
http://dx.doi.org/10.1111/j.1365-2958.2008.06549.x
[48] Troxell, B., Xu, H. and Yang, X.F. (2012) Borrelia burgdorferi, Pathogen That Lacks Iron, Encodes Manganese-Dependent Superoxide Dismutase Essential for Resistance to Streptonigrin. The Journal of Biological Chemistry, 287, 19284-19293.
http://dx.doi.org/10.1074/jbc.M112.344903
[49] Whitehouse, C.A., Williams, L.R. and Austin, F.E. (1997) Identification of Superoxide Dismutase Activity in Borrelia burgdorferi. Infection and Immunity, 65, 4865-4868.
[50] Barbour, A.G. (1990) Antigenic Variation of a Relapsing Fever Borrelia Species. Annual Review of Microbiology, 44, 155-171.
http://dx.doi.org/10.1146/annurev.mi.44.100190.001103
[51] Barbour, A.G. and Restrepo, B.I. (2000) Antigenic Variation in Vector-Borne Pathogens. Emerging Infectious Diseases, 6, 449-457.
http://dx.doi.org/10.3201/eid0605.000502
[52] Deitsch, K.W., Moxon, E.R. and Wellems, T.E. (1997) Shared Themes of Antigenic Variation and Virulence in Bacterial, Protozoal, and Fungal Infections. Microbiology and Molecular Biology Reviews, 61, 281-293.
[53] Palmer, G.H. and Brayton, K.A. (2007) Gene Conversion Is a Convergent Strategy for Pathogen Antigenic Variation. Trends in Parasitology, 23, 408-413.
http://dx.doi.org/10.1016/j.pt.2007.07.008
[54] Vink, C., Rudenko, G. and Seifert, H.S. (2011) Microbial Antigenic Variation Mediated by Homologous DNA Recombination. FEMS Microbiology Reviews, 5, 917-948.
[55] Eicken, C., Sharma, V., Klabunde, T., Lawrenz, M.B., Hardham, J.M., Norris, S.J., et al. (2002) Crystal Structure of Lyme Disease Variable Surface Antigen VlsE of Borrelia burgdorferi. The Journal of Biological Chemistry, 277, 21691-2166.
http://dx.doi.org/10.1074/jbc.M201547200
[56] Liang, F.T., Alvarez, A.L., Gu, Y., Nowling, J.M., Ramamoorthy, R. and Philipp, M.T. (1999) An Immunodominant Conserved Region within the Variable Domain of VlsE, the Variable Surface Antigen of Borrelia burgdorferi. The Journal of Immunology, 163, 5566-5573.
[57] Liang, F.T., Nowling, J.M. and Philipp, M.T. (2000) Cryptic and Exposed Invariable Regions of VlsE, the Variable Surface Antigen of Borrelia burgdorferi sl. Journal of Bacteriology, 182, 3597-3601.
http://dx.doi.org/10.1128/JB.182.12.3597-3601.2000
[58] Kraiczy, P., Peters, S., Seitz, C., Wurzner, R., Oschmann, P. and Brade, V. (1998) Growth Inhibitory and Bactericidal Efficacy of Sera from Lyme borreliosis Patients on Borrelia burgdorferi Strains. Wiener Klinische Wochenschrift, 110, 886-893.
[59] Kraiczy, P., Skerka, C., Kirschfink, M., Brade, V. and Zipfel, P.F. (2001) Immune Evasion of Borrelia burgdorferi by Acquisition of Human Complement Regulators FHL-1/Reconectin and Factor H. European Journal of Immunology, 31, 1674-1684.
http://dx.doi.org/10.1002/1521-4141(200106)31:6<1674::AID-IMMU1674>3.0.CO;2-2
[60] Gordon, D.L., Kaufman, R.M., Blackmore, T.K., Kwong, J. and Lublin, D.M. (1995) Identification of Complement Regulatory Domains in Human Factor H. The Journal of Immunology, 155, 348-356.
[61] Kraiczy, P., Skerka, C., Brade, V. and Zipfel, P.F. (2001) Further Characterization of Complement Regulator-Acquir- ing Surface Proteins of Borrelia burgdorferi. Infection and Immunity, 69, 7800-7809.
http://dx.doi.org/10.1128/IAI.69.12.7800-7809.2001
[62] Kuhn, S., Skerka, C. and Zipfel, P.F. (1995) Mapping of the Complement Regulatory Domains in the Human Factor H-Like Protein 1 and in Factor H1. The Journal of Immunology, 155, 5663-5670.
[63] Kuhn, S. and Zipfel, P.F. (1996) Mapping of the Domains Required for Decay Acceleration Activity of the Human Factor H-Like Protein 1 and Factor H. European Journal of Immunology, 26, 2383-2387.
http://dx.doi.org/10.1002/eji.1830261017
[64] Lindahl, G., Sjobring, U. and Johnsson, E. (2000) Human Complement Regulators: A Major Target for Pathogenic Microorganisms. Current Opinion in Immunology, 12, 44-51.
http://dx.doi.org/10.1016/S0952-7915(99)00049-7
[65] Kurtenbach, K., De Michelis, S., Etti, S., Schafer, S.M., Sewell, H.S., Brade, V., et al. (2002) Host Association of Borrelia burgdorferi Sensu Lato—The Key Role of Host Complement. Trends in Microbiology, 10, 74-79.
http://dx.doi.org/10.1016/S0966-842X(01)02298-3
[66] Stevenson, B., El-Hage, N., Hines, M.A., Miller, J.C. and Babb, K. (2002) Differential Binding of Host Complement Inhibitor Factor H by Borrelia burgdorferi Erp Surface Proteins: A Possible Mechanism Underlying the Expansive Host Range of Lyme Disease Spirochetes. Infection and Immunity, 70, 491-497.
http://dx.doi.org/10.1128/IAI.70.2.491-497.2002
[67] Xu, H., Raddi, G., Liu, J., Charon, N.W. and Li, C. (2011) Chemoreceptors and Flagellar Motors Are Subterminally Located in Close Proximity at the Two Cell Poles in Spirochetes. Journal of Bacteriology, 193, 2652-2656.
http://dx.doi.org/10.1128/JB.01530-10
[68] Zhang, K., Liu, J., Tu, Y., Xu, H., Charon, N.W. and Li, C. (2012) Two CheW Coupling Proteins Are Essential in a Chemosensory Pathway of Borrelia burgdorferi. Molecular Microbiology, 85, 782-794.
http://dx.doi.org/10.1111/j.1365-2958.2012.08139.x
[69] Parveen, N. and Leong, J.M. (1998) Identification of a Candidate Glycosaminoglycan-Binding Adhesin of the Lyme Disease Spirochete Borrelia burgdorferi. Molecular Microbiology, 35, 1220-1234.
http://dx.doi.org/10.1046/j.1365-2958.2000.01792.x
[70] Guo, B.P., Brown, E.L., Dorward, D.W., Rosenberg, L.C. and Hook, M. (1998) Decorin-Binding Adhesins from Borrelia burgdorferi. Molecular Microbiology, 30, 711-723.
http://dx.doi.org/10.1046/j.1365-2958.1998.01103.x
[71] Probert, W.S. and Johnson, B.J. (1998) Identification of a 47 kDa Fibrinonectin-Binding Protein Expressed by Borrelia burgdorferi Isolate B31. Molecular Microbiology, 30, 1003-1015.
http://dx.doi.org/10.1046/j.1365-2958.1998.01127.x
[72] Sze, C.S., Zhang, K., Kariu, T., Pal, U. and Li, C. (2012) Borrelai burgdorferi Needs Chemotaxis to Establish Infection in Mammals and to Accomplish Its Enzootic Cycle. Infection and Immunity, 80, 2485-2492.
http://dx.doi.org/10.1128/IAI.00145-12
[73] Rutherford, S.T. and Bassler, B.L. (2012) Bacterial Quorum Sensing: Its Role in Virulence and Possibilities for Its Control. Cold Spring Harb Perspect Med., 2, Article ID: a012427.
[74] Surette, M.G., Miller, M.B. and Bassler, B.L. (1999) Quorum Sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: A New Family of Genes Responsible for Autoinducer Production. Proceedings of the National Academy of Sciences of the United States of America, 96, 1639-1644.
http://dx.doi.org/10.1073/pnas.96.4.1639
[75] Kilpatrick, A.M. and Randolph, S.E. (2012) Drivers, Dynamics, and Control of Emerging Vector-Borne Zoonotic Diseases. The Lancet, 380, 1946-1955.
http://dx.doi.org/10.1016/S0140-6736(12)61151-9
[76] Lindgren, E., Talleklint, L. and Polfeldt, T. (2000) Impact of Climatic Change on the Northern Latitude Limit and Population Density of the Disease-Transmitting European Tick Ixodes ricinus. Environmental Health Perspectives, 108, 119-123.
http://dx.doi.org/10.1289/ehp.00108119
[77] Ogden, N.H., Lindsay, R.L., Sockett, P.N., Morshed, M. and Artsob, H. (2009) Emergence of Lyme Disease in Canada. Canadian Medical Association Journal, 180, 1221-1224.
http://dx.doi.org/10.1503/cmaj.080148
[78] Léger, E., Vourc’h, G., Vial, L., Chevillon, C. and McCoy, K.D. (2013) Changing Distributions of Ticks: Causes and Consequences. Experimental and Applied Acarology, 59, 219-244.
http://dx.doi.org/10.1007/s10493-012-9615-0
[79] Medlock, J.M., Hansford, K.M., Bormane, A., Derdakova, M., Estrada-Pena, A., George, J.C., et al. (2013) Driving Forces for Changes in Geographical Distribution of Ixodes ricinus Ticks in Europe. Parasites & Vectors, 6, 1.
http://dx.doi.org/10.1186/1756-3305-6-1
[80] Ogden, N.H., Margos, G., Aanensen, D.M., Drebot, M.A., Feil, E.J., Hanincová, K., et al. (2011) Investigation of Genotypes of Borrelia burgdorferi in Ixodes scapularis Ticks Collected in Surveillance in Canada. Applied and Environmental Microbiology, 77, 3244-3254.
http://dx.doi.org/10.1128/AEM.02636-10
[81] Norman, R., Bowers, R.G., Begon, M. and Hudson, P.J. (1999) Persistence of Tick-Borne Virus in the Presence of Multiple Host Species: Tick Reservoirs and Parasite Mediated Competition. Journal of Theoretical Biology, 200, 111- 118.
http://dx.doi.org/10.1006/jtbi.1999.0982
[82] Ogden, N.H., Bigras-Poulin, M., O’Callaghan, C.J., Barker, I.K., Lindsay, L.R., Maarouf, A., et al. (2007) Tick Seasonality, Host Infection Dynamics and Fitness of Ixodes scapularis-Borne Pathogens. Parasitology, 134, 209-227.
http://dx.doi.org/10.1017/S0031182006001417
[83] Lindsay, L.R., Barker, I.K., Surgeoner, G.A., McEwen, S.A., Gillespie, T.J. and Addison, E.M. (1998) Survival and Development of the Different Life Stages of Ixodes scapularis (Acari: Ixodidae) Held within Four Habitats on Long Point, Ontario, Canada. Journal of Medical Entomology, 35, 189-199.
[84] Lindsay, L.R., Barker, I.K., Surgeoner, G.A., McEwen, S.A., Gillespie, T.J. and Robinson, J.T. (1995) Survival and Development of Ixodes scapularis (Acari: Ixodidae) under Various Climatic Conditions in Ontario, Canada. Journal of Medical Entomology, 32, 143-152.
[85] Ogden, N.H., Barker, I.K., Beauchamp, G., Brazeau, S., Charron, D., Maarouf, A., et al. (2006) Investigation of Ground Level and Remote-Sensed Data for Habitat Classification and Prediction of Survival of Ixodes scapularis Ticks in Habitats of Southeastern Canada. Journal of Medical Entomology, 43, 403-414.
http://dx.doi.org/10.1603/0022-2585(2006)043[0403:IOGLAR]2.0.CO;2
[86] Gatewood, A.G., Liebman, K.A., Vourc’h, G., Bunikis, J., Hamer, S.A., Cortinas, R., et al. (2009) Climate and Tick Seasonality Are Predictors of Borrelia burgdorferi Genotype Distribution. Applied and Environmental Microbiology, 75, 2476-2483.
http://dx.doi.org/10.1128/AEM.02633-08
[87] Rauter, C. and Hartung, T. (2005) Prevalence of Borrelia burgdorferi Sensu Lato Genospecies in Ixodes ricinus Ticks in Europe: A Metaanalysis. Applied and Environmental Microbiology, 71, 7203-7216.
http://dx.doi.org/10.1128/AEM.71.11.7203-7216.2005
[88] Estrada-Pena, A., Venzal, J.M. and Sanchez Acedo, C. (2006) The Tick Ixodes ricinus: Distribution and Climate Preferences in the Western Palaearctic. Medical and Veterinary Entomology, 20, 189-197.
http://dx.doi.org/10.1111/j.1365-2915.2006.00622.x
[89] Jaenson, T.G., Eisen, L., Comstedt, P., Mejlon, H.A., Lindgren, E., Bergstrom, S., et al. (2009) Risk Indicators for the Tick Ixodes ricinus and Borrelia burgdorferi Sensu Lato in Sweden. Medical and Veterinary Entomology, 23, 226-237.
http://dx.doi.org/10.1111/j.1365-2915.2009.00813.x
[90] Pejchalová, K., Zákovská, A., Mejzlíková, M., Halouzka, J. and Dendis, M. (2007) Isolation, Cultivation and Identification of Borrelia burgdorferi Genospecies from Ixodes ricinus Ticks from the City of Brno, Czech Republic. Annals of Agricultural and Environmental Medicine, 14, 75-79.
[91] Haemig, P.D., Waldenstrom, J. and Olsen, B. (2008) Roadside Ecology and Epidemiology of Tick-Borne Diseases. Scandinavian Journal of Infectious Diseases, 40, 853-858.
[92] Ljostad, U., Skogvoll, E., Eikeland, R., et al. (2008) Oral Doxycycline versus Intravenous Ceftriaxone for European Lyme Neuroborreliosis: A Multicentre, Non-Inferiority, Doubleblind, Randomised Trial. The Lancet Neurology, 7, 690-695.
http://dx.doi.org/10.1016/S1474-4422(08)70119-4
[93] Kruger, H., Kohlhepp, W. and Konig, S. (1990) Follow-Up of Antibiotically Treated and Untreated Neuroborreliosis. Acta Neurologica Scandinavica, 82, 59-67.
http://dx.doi.org/10.1111/j.1600-0404.1990.tb01588.x
[94] Kruger, H., Reuss, K., Pulz, M., et al. (1989) Meningoradiculitis and Encephalomyelitis due to Borrelia burgdorferi: A Follow-Up Study of 72 Patients over 27 Years. Journal of Neurology, 236, 322-328.
http://dx.doi.org/10.1007/BF00314373
[95] Ljostad, U. and Henriksen, T.H. (2008) Management of Neuroborreliosis in European Adult Patients. Acta Neurologica Scandinavica, 188, 22-28.
http://dx.doi.org/10.1111/j.1600-0404.2008.01027.x
[96] Hansen, K. and Lebech, A.M. (1992) The Clinical and Epidemiological Profile of Lyme Neuroborreliosis in Denmark 1985-1990. A Prospective Study of 187 Patients with Borrelia burgdorferi Specific Intrathecal Antibody Production. Brain, 115, 399-423.
http://dx.doi.org/10.1093/brain/115.2.399
[97] Topakian, R., Stieglbauer, K., Nussbaumer, K. and Aichner, F.T. (2008) Cerebral Vasculitis and stRoke in Lyme Neuroborreliosis. Two Case Reports and Review of Current Knowledge. Cerebrovascular Diseases, 26, 455-461.
http://dx.doi.org/10.1159/000155982
[98] Oschmann, P., Dorndorf, W., Hornig, C., Schafer, C., Wellensiek, H.J. and Pflughaupt, K.W. (1998) Stages and Syndromes of Neuroborreliosis. Journal of Neurology, 245, 262-272.
http://dx.doi.org/10.1007/s004150050216
[99] Pfister, H.W. and Rupprecht, T.A. (2006) Clinical Aspects of Neuroborreliosis and Post-Lyme Disease Syndrome in Adult Patients. International Journal of Medical Microbiology, 296, 11-16.
http://dx.doi.org/10.1016/j.ijmm.2005.12.003
[100] Gorson, K.C., Kolb, D.A., Marks, D.S., Hayes, M.T. and Baquis, G.D. (2011) Acute Brachial Diplegia Due to Lyme Disease. Neurologist, 17, 24-27.
http://dx.doi.org/10.1097/NRL.0b013e31820038cd
[101] Elamin, M., Alderazi, Y., Mullins, G., Farrell, M.A., O’Connell, S. and Counihan, T.J. (2009) Perineuritis in Acute Lyme Neuroborreliosis. Muscle & Nerve, 39, 851-854.
http://dx.doi.org/10.1002/mus.21289
[102] Logigian, E.L., Kaplan, R.F. and Steere, A.C. (1990) Chronic Neurologic Manifestations of Lyme Disease. The New England Journal of Medicine, 323, 1438-1444.
http://dx.doi.org/10.1056/NEJM199011223232102
[103] Lelovas, P., Dontas, I., Bassiakou, E. and Xanthos, T. (2008) Cardiac Implications of Lyme Disease, Diagnosis and Therapeutic Approach. International Journal of Cardiology, 129, 15-21.
http://dx.doi.org/10.1016/j.ijcard.2008.01.044
[104] Vegsundvag, J., Nordeide, J., Reikvam, A. and Jenum, P. (1993) Late Cardiac Manifestation of Infection with Borrelia burgdorferi (Lyme Disease). BMJ, 307, 173.
http://dx.doi.org/10.1136/bmj.307.6897.173
[105] Stanek, G., Klein, J., Bittner, R. and Glogar, D. (1991) Borrelia burgdorferi as an Etiologic Agent in Chronic Heart Failure? Scandinavian Journal of Infectious Diseases. Supplementum, 77, 85-87.
[106] Kindstrand, E., Nilsson, B.Y., Hovmark, A., Pirskanen, R. and Asbrink, E. (2002) Peripheral Neuropathy in Acrodermatitis Chronica Atrophicans—Effect of Treatment. Acta Neurologica Scandinavica, 106, 253-257.
http://dx.doi.org/10.1034/j.1600-0404.2002.01336.x
[107] Dicaudo, D.J., Su, W.P., Marshall, W.F., Malawista, S.E., Barthold, S. and Persing, D.H. (1994) Acrodermatitis Chronica Atrophicans in the United States: Clinical and Histopathologic Features of Six Cases. Cutis, 54, 81-84.
[108] Jaffe, E.S., Harris, N.L., Stein, H. and Vardiman, J. (2001) World Health Organization Classification of Tumours. In: Jaffe, E.S., Harris, N.L., Stein, H. and Vardiman, J., Eds., Pathology and Genetics of Tumours of Haematopoietic and Lymphoid Tissues, IARC Press, Lyon, 10-302.
[109] Suarez, F., Lortholary, O., Hermine, O., et al. (2006) Infection-Associated Lymphomas Derived from Marginal Zone B Cells: A Model of Antigen-Driven Lymphoproliferation. Blood, 107, 3034-3044.
http://dx.doi.org/10.1182/blood-2005-09-3679
[110] Goos, M. (1971) Acrodermatitis Chronica Atrophicans and Malignant Lymphoma. Acta Dermato-Venereologica (Stockholm), 51, 457-459.
[111] Garbe, C., Stein, H., Dienemann, D. and Orfanos, C.E. (1991) Borrelia burgdorferi Associated Cutaneous B Cell Lymphoma: Clinical and Immunologic Characterization of Four Cases. Journal of the American Academy of Dermatology, 24, 584-590.
http://dx.doi.org/10.1016/0190-9622(91)70088-J
[112] Rijlaarsdam, J.U., Van der Putte, S.C.J., Berti, E., et al. (1993) Cutaneous Immunocytomas: A Clinicopathological Study of 26 Cases. Histopathology, 23, 117-125.
http://dx.doi.org/10.1111/j.1365-2559.1993.tb00469.x
[113] Munksgaard, L., Obitz, E.R., Goodlad, J.R., et al. (2004) Demonstration of B. burgdorferi-DNA in Two Cases of Nodal Lymphoma. Leukemia & Lymphoma, 45, 1721-1723.
http://dx.doi.org/10.1080/10428190410001683723
[114] Schollkopf, C., Melbye, M., Munksgaard, L., Smedby, K.E., Rostgaard, K., Glimelius, B., Chang, E.T., Roos, G., Hansen, M., Adami, H. and Hjalgrim, H. (2008) Borrelia Infection and Risk of Non-Hodgkin Lymphoma. Blood, 111, 5524-5529.
http://dx.doi.org/10.1182/blood-2007-08-109611
[115] Shapiro, E.D. and Gerber, M.A. (2006) Chapter 5. Lyme Disease. In: Baker, C.J., Klein, J. and Remington, J., Eds., Infectious Diseases of the Fetus and Newborn Infant, Elsevier, Philadelphia, 485-497.
http://dx.doi.org/10.1016/B0-72-160537-0/50017-7
[116] Silver, R.M., Yang, L., Daynes, R.A., Branch, D.W., et al. (1995) Fetal Out Comein Murine Lyme Disease. Infection and Immunity, 63, 66-72.
[117] Schlesinger, P.A., Duray, P.H., Burke, B.A., Steere, A.C. and Stillman, M.T. (1985) Maternal-Fetal Transmission of Lyme Disease Spirochete, Borrelia burgdorferi. Annals of Internal Medicine, 103, 67-68.
http://dx.doi.org/10.7326/0003-4819-103-1-67
[118] Weber, K., Bratzke, H.J., Neubert, U., Wilske, B. and Duray, P.H. (1988) Borrelia burgdorferi in a Newborn Despite Oral Penicillin for Lyme borreliosis during Pregnancy. The Pediatric Infectious Disease Journal, 7, 286-289.
http://dx.doi.org/10.1097/00006454-198804000-00010
[119] Mylonas, I. (2011) Borreliosis during Pregnancy: A Risk for the Unborn Child. Vector-Borne and Zoonotic Diseases, 11, 891-898.
http://dx.doi.org/10.1089/vbz.2010.0102
[120] Evans, J. (1999) Lyme Disease. Current Opinion in Rheumatology, 11, 281-288.
http://dx.doi.org/10.1097/00002281-199907000-00010
[121] Nadelman, R.B. and Wormser, G.P. (1998) Lyme borreliosis. The Lancet, 352, 557-565.
http://dx.doi.org/10.1016/S0140-6736(98)01146-5
[122] Pfister, H.W., Wilske, B. and Weber, K. (1994) Lyme borreliosis: Basic Science and Clinical Aspects. The Lancet, 343, 1013-1016.
http://dx.doi.org/10.1016/S0140-6736(94)90130-9
[123] Striker, R.B. and Winger, E.E. (2001) Decreased CD57 Lymphocyte Subset in Patients with Chronic Lyme Disease. Immunology Letters, 76, 43-48.
http://dx.doi.org/10.1016/S0165-2478(00)00316-3
[124] Sansoni, P., Cossarizza, A., Brianti, V., Fagnoni, F., Snelli, G., Monti, D., Marcato, A., Passeri, G., Ortolani, C. and Forti, E. (1993) Lymphocyte Subsets and Natural Killer Cell Activity in Healthy Old People and Centenarians. Blood, 82, 2767-2773.
[125] Dinges, D.F., Douglas, S.D., Zaugg, L., Campbell, D.E., McMann, J.M., Whitehouse, W.G., Orne, E.C., Kapoor, S.C., Icaza, E. and Orne, M.T. (1994) Leukocytosis and Natural Killer Cell Function Parallel Neurobehavioral Fatigue Induced by 64 Hours of Sleep Deprivation. Journal of Clinical Investigation, 93, 1930-1939.
http://dx.doi.org/10.1172/JCI117184
[126] Wang, E.C. and Borysiewicz, L.K. (1995) The Role of CD8, CD57 Cells in Human Cytomegalovirus and Other Viral Infections. Scandinavian Journal of Infectious Diseases, 99, 69-77.
[127] Yssel, H., Shanafelt, M.C., Soderberg, C., Schneider, P.V., Anzola, J. and Peltz, G. (1991) Borrelia burgdorferi Activates a T Helper Type 1-Like T Cell Subset in Lyme Arthritis. The Journal of Experimental Medicine, 174, 593-601.
http://dx.doi.org/10.1084/jem.174.3.593
[128] Kreuzfelder, E., Shen, G., Bittorf, M., Scheiermann, N., Thraenhart, O., Seidel, D. and Grosse-Wilde, H. (1992) Enumeration of T, B and Natural Killer Peripheral Blood Cells of Patients with Multiple Sclerosis and Controls. European Neurology, 32, 190-194.
http://dx.doi.org/10.1159/000116820
[129] Eoli, M., Ferrarini, M., Dufour, A., Heltaj, S., Bevilacqua, L., Comi, G., Cosi, V., Filippini, G., Martinelli, V. and Milanese, C. (1993) Presence of T-Cell Subset Abnormalities in Newly Diagnosed Cases of Multiple Sclerosis and Relationship with Short-Term Clinical Activity. Journal of Neurology, 240, 79-82.
http://dx.doi.org/10.1007/BF00858721
[130] Arai, K., Yamamura, S., Seki, S., Hanyu, T., Takahashi, H.E. and Abo, T. (1998) Increase of CD57 T Cells in Knee Joints and Adjacent Bone Marrow of Rheumatoid Arthritis Patients: Implication for an Anti-Inflammatory Role. Clinical Experimental Immunology, 111, 345-352.
http://dx.doi.org/10.1046/j.1365-2249.1998.00511.x
[131] Imberti, L., Sottini, A., Signorini, S., Gorla, R. and Primi, D. (1997) Oligoclonal CD4 CD57 T-Cell Expansions Contribute to the Imbalanced T-Cell Receptor Repertoire of Rheumatoid Arthritis Patients. Blood, 89, 2822-2832.
[132] Gallo, P., Chiusole, M., Sanzari, M., Sivieri, S., Piccinno, M.G., Argentiero, V., Rizzotti, P. and Tavolato, B. (1994) Effect of High-Dose Steroid Therapy on T-Cell Populations. A Longitudinal Study in MS Patients. Acta Neurologica Scandinavica, 89, 95-101.
http://dx.doi.org/10.1111/j.1600-0404.1994.tb01642.x
[133] Shoemaker, R.C., Giclas, P.C., Crowder, C., House, D. and Glovsky, M.M. (2008) Complement Split Products C3a and C4a Are Early Markers of Acute Lyme Disease in Tick Bite Patients in the United States. International Archives of Allergy and Immunology, 146, 255-261.
http://dx.doi.org/10.1159/000116362
[134] Stricker, R.B., Savely, V.R., Montanya, N.C. and Giclas, P.C. (2008) Complement Split Products C3a and C4a in Chronic Lyme Disease. Scandinavian Journal of Immunology, 69, 64-69.
http://dx.doi.org/10.1111/j.1365-3083.2008.02191.x
[135] Mocco, J., Wilson, D.A., Komotar, R.J., et al. (2006) Alterations in Plasma Complement Levels after Human Ischemic Stroke. Neurosurgery, 59, 28-33.
http://dx.doi.org/10.1227/01.NEU.0000219221.14280.65
[136] Mack, W.J., Ducruet, A.F., Hickman, Z.L., et al. (2007) Early Plasma Complement C3a Levels Correlate with Functional Outcome after Aneurysmal Subarachnoid Hemorrhage. Neurosurgery, 61, 255-260.
http://dx.doi.org/10.1227/01.NEU.0000255518.96837.8E
[137] Sorensen, B., Streib, J.E., Strand, M., et al. (2003) Complement Activation in a Model of Chronic Fatigue Syndrome. Journal of Allergy and Clinical Immunology, 112, 397-403.
http://dx.doi.org/10.1067/mai.2003.1615
[138] Panelius, J., Lahdenne, P., Saxen, H., et al. (2003) Diagnosis of Lyme Neuroborreliosis with Antibodies to Recombinant Proteins DbpA, BBK32, and OspC, and VlsE IR6 Peptide. Journal of Neurology, 250, 1318-1327.
http://dx.doi.org/10.1007/s00415-003-0205-2
[139] Skarpaas, T., Liostad, U., Sobye, M. and Mygland, A. (2007) Sensitivity and Specificity of a Commercial C6 Peptide Enzyme Immuno Assay in Diagnosis of Acute Lyme Neuroborreliosis. European Journal of Clinical Microbiology Infectious Diseases, 26, 675-677.
http://dx.doi.org/10.1007/s10096-007-0336-y
[140] Tjernberg, I., Schon, T., Ernerudh, J., Wistedt, A.C., Forsberg, P. and Eliasson, I. (2008) C6-Peptide Serology as Diagnostic Tool in Neuroborreliosis. APMIS, 116, 393-399.
http://dx.doi.org/10.1111/j.1600-0463.2008.00842.x
[141] Vermeersch, P., Resseler, S., Nackers, E. and Lagrou, K. (2009) The C6 Lyme Antibody Test Has Low Sensitivity for Antibody Detection in Cerebrospinal Fluid. Diagnostic Microbiology and Infectious Disease, 64, 347-349.
http://dx.doi.org/10.1016/j.diagmicrobio.2009.03.013
[142] Wilske, B., Fingerle, V. and Schulte-Spechtel, U. (2007) Microbiological and Serological Diagnosis of Lyme borreliosis. FEMS Immunology and Medical Microbiology, 49, 13-21.
http://dx.doi.org/10.1111/j.1574-695X.2006.00139.x
[143] Brouqui, P., Bacellar, F., Baranton, G., et al. (2004) Guidelines for the Diagnosis of Tick-Borne Bacterial Diseases in Europe. Clinical Microbiology and Infection, 10, 1108-1132.
http://dx.doi.org/10.1111/j.1469-0691.2004.01019.x
[144] Johnson, B.J., Robbins, K.E., Bailey, R.E., et al. (1996) Serodiagnosis of Lyme Disease: Accuracy of a Two-Step Approach Using a Flagella-Based ELISA and Immunoblotting. The Journal of Infectious Diseases, 174, 346-353.
http://dx.doi.org/10.1093/infdis/174.2.346
[145] Ulvestad, E. and Kristoffersen, E.K. (2002) False Positive Serological Test in Suspected Borreliosis. Tidsskrift For Den Norske Laegeforening, 122, 88-90.
[146] Mygland, A., Skarpaas, T. and Ljostad, U. (2006) Chronic Polyneuropathy and Lyme Disease. European Journal of Neurology, 13, 1213-1215.
http://dx.doi.org/10.1111/j.1468-1331.2006.01395.x
[147] Van Dam, A.P., Kuiper, H., Vos, K., et al. (1993) Different Genospecies of Borrelia burgdorferi Are Associated with Distinct Clinical Manifestations of Lyme borreliosis. Clinical Infectious Diseases, 17, 708-717.
http://dx.doi.org/10.1093/clinids/17.4.708
[148] Von Stedingk, L.V., Olsson, I., Hanson, H.S., Asbrink, E. and Hovmark, A. (1995) Polymerase Chain Reaction for Detection of Borrelia burgdorferi DNA in Skin Lesions of Early and Late Lyme borreliosis. European Journal of Clinical Microbiology Infectious Diseases, 14, 1-5.
http://dx.doi.org/10.1007/BF02112610
[149] Jaulhac, B., Heller, R., Limbach, F.X., et al. (2000) Direct Molecular Typing of Borrelia burgdorferi Sensu Lato Species in Synovial Samples from Patients with Lyme Arthritis. Journal of Clinical Microbiology, 38, 1895-1900.
[150] Eiffert, H., Karsten, A., Thomssen, R. and Christen, H.J. (1998) Characterization of Borrelia burgdorferi Strains in Lyme Arthritis. Scandinavian Journal of Infectious Diseases, 30, 265-268.
http://dx.doi.org/10.1080/00365549850160918
[151] Cerar, T., Ogrinc, K., Cimperman, J., Lotric-Furlan, S., Strle, F. and Ruzic-Sabljic, E. (2008) Validation of Cultivation and PCR Methods for Diagnosis of Lyme Neuroborreliosis. Journal of Clinical Microbiology, 46, 3375-3379.
http://dx.doi.org/10.1128/JCM.00410-08
[152] Lebech, A.M. (2002) Polymerase Chain Reaction in Diagnosis of Borrelia burgdorferi Infections and Studies on Taxonomic Classification. APMIS Supplement, 105, 1-40.
[153] Molloy, P.J., Persing, D.H. and Berardi, V.P. (2001) False-Positive Results of PCR Testing for Lyme Disease. Clinical Infectious Diseases, 33, 412-413.
http://dx.doi.org/10.1086/321911
[154] Cameron, D., Gaito, A., Harris, N., et al. (2004) Evidence-Based Guidelines for the Management of Lyme Disease. Expert Review of Anti-infective Therapy, 2, S1-S13.
http://dx.doi.org/10.1586/14789072.2.1.S1
[155] Wormser, G.P., Dattwyler, R.J., Shapiro, E.D., et al. (2006) The Clinical Assessment, Treatment, and Prevention of Lyme Disease, Human Granulocytic Anaplasmosis, and Babesiosis: Clinical Practice Guidelines by the Infectious Diseases Society of America. Clinical Infectious Diseases, 43, 1089-1134.
http://dx.doi.org/10.1086/508667
[156] Stanek, G., O’Connell, S., Cimmino, M., et al. (1996) European Union Concerted Action on Risk Assessment in Lyme borreliosis: Clinical Case Definitions for Lyme borreliosis. Wiener Klinische Wochenschrift, 108, 741-747.
[157] Mygland, A., Ljostad, U., Fingerle, V., Rupprecht, T., Schmutzhard, E. and Steiner, I. (2010) EFNS Guidelines on the Diagnosis and Management of European Lyme Neuroborreliosis. European Journal of Neurology, 17, 8-16.
http://dx.doi.org/10.1111/j.1468-1331.2009.02862.x

  
comments powered by Disqus

Copyright © 2017 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.