Development of a multiantigen panel for improved detection of borrelia burgdorferi infection in early lyme disease

Journal of Clinical Microbiology

Volumn 53, Issue 12, 2015, Pages 3834-3841

  Lahey, Lauren J ^a,b   Panas, Michael W ^b   Mao, Rong ^a,b   Delanoy, Michelle ^c   Flanagan, John J ^c   Binder, Steven R ^c   Rebman, Alison W ^d   Montoya, Jose G ^b   Soloski, Mark J ^d   Steere, Allen C ^e   Dattwyler, Raymond J ^f,g   Arnaboldi, Paul M ^f,g   Aucott, John N ^d   Robinson, William H ^a,b  

^a VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BIO RAD LABORATORIES   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

^f Biopeptides Corp   (United States)

^g NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; PROTEIN DBPB; PROTEIN OSPC; PROTEIN P100; PROTEIN PERP59 MV; PROTEIN PFLAB MV; PROTEIN PLA 7; PROTEIN POSPC TYPE K; PROTEIN POSPF MV; PROTEIN PP35 MV; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; BACTERIUM ANTIBODY; MEMBRANE PROTEIN;

ALGORITHM; ANTIBODY TITER; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DIAGNOSTIC ACCURACY; DISEASE DURATION; EARLY LYME DISEASE; ENZYME IMMUNOASSAY; ERYTHEMA CHRONICUM MIGRANS; HUMAN; INTERMETHOD COMPARISON; LABORATORY DEVICE; LABORATORY DIAGNOSIS; LYME DISEASE; MAJOR CLINICAL STUDY; MOLECULAR DYNAMICS; MULTIPLEX BEAD ARRAY; NONHUMAN; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SENSITIVITY AND SPECIFICITY; SEROLOGY; TWO TIERED TESTING ALGORITHM; VALIDATION PROCESS; ADULT; AGED; BLOOD; BORRELIA BURGDORFERI; COHORT ANALYSIS; COMPARATIVE STUDY; DIAGNOSTIC TEST; EARLY DIAGNOSIS; EVALUATION STUDY; FEMALE; IMMUNOASSAY; IMMUNOLOGY; MALE; MIDDLE AGED; PROCEDURES; UNITED STATES; YOUNG ADULT;

ADULT; AGED; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BORRELIA BURGDORFERI; COHORT STUDIES; DIAGNOSTIC TESTS, ROUTINE; EARLY DIAGNOSIS; FEMALE; HUMANS; IMMUNOASSAY; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; LYME DISEASE; MALE; MEMBRANE PROTEINS; MIDDLE AGED; SENSITIVITY AND SPECIFICITY; UNITED STATES; YOUNG ADULT;

EID: 84947796364     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.02111-15     Document Type: Article

References (44)

1. Stanek G, Wormser GP, Gray J, Strle F. (2012). Lyme borreliosis. Lancet 379: 461-473. http://dx.doi.org/10.1016/S0140-6736(11)60103-7
2. Centers for Disease Control and Prevention. (1997). Case definitions for infectious conditions under public health surveillance. MMWR Recomm Rep 46: 1-55
3. Steere AC. (1989). Lyme disease. N Engl J Med 321: 586-596. http://dx.doi.org/10.1056/NEJM198908313210906
4. Steere AC. (2001). Lyme disease. N Engl J Med 345: 115-125. http://dx.doi.org/10.1056/NEJM200107123450207
5. Shapiro ED. (2014). Clinical practice. Lyme disease. N Engl J Med 370: 1724-1731. http://dx.doi.org/10.1056/NEJMcp1314325
6. Wormser GP. (2006). Clinical practice. Early Lyme disease. N Engl J Med 354: 2794-2801
7. Kowalski TJ, Tata S, Berth W, Mathiason MA, Agger WA. (2010). Antibiotic treatment duration and long-term outcomes of patients with early Lyme disease from a Lyme disease-hyperendemic area. Clin Infect Dis 50: 512-520. http://dx.doi.org/10.1086/649920
8. Wormser GP, Ramanathan R, Nowakowski J, McKenna D, Holmgren D, Visintainer P, Dornbush R, Singh B, Nadelman RB. (2003). Duration of antibiotic therapy for early Lyme disease. A randomized, double-blind, placebo-controlled trial. Ann Intern Med 138: 697-704
9. Wormser GP, Dattwyler RJ, Shapiro ED, Halperin JJ, Steere AC, Klempner MS, Krause PJ, Bakken JS, Strle F, Stanek G, Bockenstedt L, Fish D, Dumler JS, Nadelman RB. (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. Clin Infect Dis 43: 1089-1134. http://dx.doi.org/10.1086/508667
10. Aguero-Rosenfeld ME, Wang G, Schwartz I, Wormser GP. (2005). Diagnosis of Lyme borreliosis. Clin Microbiol Rev 18: 484-509. http://dx.doi.org/10.1128/CMR.18.3.484-509.2005
11. Marques AR. (2015). Laboratory diagnosis of Lyme disease: advances and challenges. Infect Dis Clin North Am 29: 295-307. http://dx.doi.org/10.1016/j.idc.2015.02.005
12. Centers for Disease Control and Prevention. (1995). Recommendations for test performance and interpretation from the Second National Conference on Serologic Diagnosis of Lyme Disease. MMWR Morb Mortal Wkly Rep 44: 590-591
13. Branda JA, Linskey K, Kim YA, Steere AC, Ferraro MJ. (2011). Twotiered antibody testing for Lyme disease with use of 2 enzyme immunoassays, a whole-cell sonicate enzyme immunoassay followed by a VlsE C6 peptide enzyme immunoassay. Clin Infect Dis 53: 541-547. http://dx.doi.org/10.1093/cid/cir464
14. Wormser GP, Schriefer M, Aguero-Rosenfeld ME, Levin A, Steere AC, Nadelman RB, Nowakowski J, Marques A, Johnson BJ, Dumler JS. (2013). Single-tier testing with the C6 peptide ELISA kit compared with two-tier testing for Lyme disease. Diagn Microbiol Infect Dis 75: 9-15. http://dx.doi.org/10.1016/j.diagmicrobio.2012.09.003
15. Fallon BA, Pavlicova M, Coffino SW, Brenner C. (2014). A comparison of Lyme disease serologic test results from 4 laboratories in patients with persistent symptoms after antibiotic treatment. Clin Infect Dis 59: 1705-1710. http://dx.doi.org/10.1093/cid/ciu703
16. Ang CW, Notermans DW, Hommes M, Simoons-Smit AM, Herremans T. (2011). Large differences between test strategies for the detection of anti-Borrelia antibodies are revealed by comparing eight ELISAs and five immunoblots. Eur J Clin Microbiol Infect Dis 30: 1027-1032. http://dx.doi.org/10.1007/s10096-011-1157-6
17. Muller I, Freitag MH, Poggensee G, Scharnetzky E, Straube E, Schoerner C, Hlobil H, Hagedorn HJ, Stanek G, Schubert-Unkmeir A, Norris DE, Gensichen J, Hunfeld KP. (2012). Evaluating frequency, diagnostic quality, and cost of Lyme borreliosis testing in Germany: a retrospective model analysis. Clin Dev Immunol 2012: 595427. http://dx.doi.org/10.1155/2012/595427
18. Arnaboldi PM, Seedarnee R, Sambir M, Callister SM, Imparato JA, Dattwyler RJ. (2013). Outer surface protein C peptide derived from Borrelia burgdorferi sensu stricto as a target for serodiagnosis of early Lyme disease. Clin Vaccine Immunol 20: 474-481. http://dx.doi.org/10.1128/CVI.00608-12
19. Signorino G, Arnaboldi PM, Petzke MM, Dattwyler RJ. (2014). Identification of OppA2 linear epitopes as serodiagnostic markers for Lyme disease. Clin Vaccine Immunol 21: 704-711. http://dx.doi.org/10.1128/CVI.00792-13
20. Arnaboldi PM, Sambir M, Dattwyler RJ. (2014). Decorin binding proteins A and B in the serodiagnosis of Lyme disease in North America. Clin Vaccine Immunol 21: 1426-1436. http://dx.doi.org/10.1128/CVI.00383-14
21. Chandra PE, Sokolove J, Hipp BG, Lindstrom TM, Elder JT, Reveille JD, Eberl H, Klause U, Robinson WH. (2011). Novel multiplex technology for diagnostic characterization of rheumatoid arthritis. Arthritis Res Ther 13: R102. http://dx.doi.org/10.1186/ar3383
22. Sokolove J, Bromberg R, Deane KD, Lahey LJ, Derber LA, Chandra PE, Edison JD, Gilliland WR, Tibshirani RJ, Norris JM, Holers VM, Robinson WH. (2012). Autoantibody epitope spreading in the pre-clinical phase predicts progression to rheumatoid arthritis. PLoS One 7: e35296. http://dx.doi.org/10.1371/journal.pone.0035296
23. Wagner CA, Sokolove J, Lahey LJ, Bengtsson C, Saevarsdottir S, Alfredsson L, Delanoy M, Lindstrom TM, Walker RP, Bromberg R, Chandra PE, Binder SR, Klareskog L, Robinson WH. (2015). Identification of anticitrullinated protein antibody reactivities in a subset of anti-CCP-negative rheumatoid arthritis: association with cigarette smoking and HLA-DRB1 shared epitope alleles. Ann Rheum Dis 74: 579-586. http://dx.doi.org/10.1136/annrheumdis-2013-203915
24. Dessau RB, Moller JK, Kolmos B, Henningsson AJ. (2015). Multiplex assay (Mikrogen recomBead) for detection of serum IgG and IgM antibodies to 13 recombinant antigens of Borrelia burgdorferi sensu lato in patients with neuroborreliosis: the more the better? J Med Microbiol 64: 224-231. http://dx.doi.org/10.1099/jmm.0.000009
25. Porwancher RB, Hagerty CG, Fan J, Landsberg L, Johnson BJ, Kopnitsky M, Steere AC, Kulas K, Wong SJ. (2011). Multiplex immunoassay for Lyme disease using VlsE1-IgG and pepC10-IgM antibodies: improving test performance through bioinformatics. Clin Vaccine Immunol 18: 851-859. http://dx.doi.org/10.1128/CVI.00409-10
26. Embers ME, Hasenkampf NR, Jacobs MB, Philipp MT. (2012). Dynamic longitudinal antibody responses during Borrelia burgdorferi infection and antibiotic treatment of rhesus macaques. Clin Vaccine Immunol 19: 1218-1226. http://dx.doi.org/10.1128/CVI.00228-12
27. Soloski MJ, Crowder LA, Lahey LJ, Wagner CA, Robinson WH, Aucott JN. (2014). Serum inflammatory mediators as markers of human Lyme disease activity. PLoS One 9: e93243. http://dx.doi.org/10.1371/journal.pone.0093243
28. Rebman AW, Crowder LA, Kirkpatrick A, Aucott JN. (2015). Characteristics of seroconversion and implications for diagnosis of post-treatment Lyme disease syndrome: acute and convalescent serology among a prospective cohort of early Lyme disease patients. Clin Rheumatol 34: 585-589. http://dx.doi.org/10.1007/s10067-014-2706-z
29. Steere AC, McHugh G, Damle N, Sikand VK. (2008). Prospective study of serologic tests for Lyme disease. Clin Infect Dis 47: 188-195. http://dx.doi.org/10.1086/589242
30. Kannian P, McHugh G, Johnson BJ, Bacon RM, Glickstein LJ, Steere AC. (2007). Antibody responses to Borrelia burgdorferi in patients with antibiotic-refractory, antibiotic-responsive, or non-antibiotic-treated Lyme arthritis. Arthritis Rheum 56: 4216-4225. http://dx.doi.org/10.1002/art.23135
31. Barbour AG, Jasinskas A, Kayala MA, Davies DH, Steere AC, Baldi P, Felgner PL. (2008). A genome-wide proteome array reveals a limited set of immunogens in natural infections of humans and white-footed mice with Borrelia burgdorferi. Infect Immun 76: 3374-3389. http://dx.doi.org/10.1128/IAI.00048-08
32. Stringer EA, Baker KS, Carroll IR, Montoya JG, Chu L, Maecker HT, Younger JW. (2013). Daily cytokine fluctuations, driven by leptin, are associated with fatigue severity in chronic fatigue syndrome: evidence of inflammatory pathology. J Transl Med 11: 93. http://dx.doi.org/10.1186/1479-5876-11-93
33. Watt T, Oberfoell S, Balise R, Lunn MR, Kar AK, Merrihew L, Bhangoo MS, Montoya JG. (2012). Response to valganciclovir in chronic fatigue syndrome patients with human herpesvirus 6 and Epstein-Barr virus IgG antibody titers. J Med Virol 84: 1967-1974. http://dx.doi.org/10.1002/jmv.23411
34. Arnaboldi PM, Dattwyler RJ. (2015). Cross-reactive epitopes in Borrelia burgdorferi p66. Clin Vaccine Immunol 22: 840-843. http://dx.doi.org/10.1128/CVI.00217-15
35. Chandra A, Latov N, Wormser GP, Marques AR, Alaedini A. (2011). Epitope mapping of antibodies to VlsE protein of Borrelia burgdorferi in post-Lyme disease syndrome. Clin Immunol 141: 103-110. http://dx.doi.org/10.1016/j.clim.2011.06.005
36. Alere. 13 October 2014. ZEUS ELISA Borrelia VlsE1/pepC10 IgG/IgM test system package insert. http://www.alere.com/us/en/product-details/zeus-borrelia-test-system.html. Accessed 2 July 2015
37. Aguero-Rosenfeld ME, Nowakowski J, Bittker S, Cooper D, Nadelman RB, Wormser GP. (1996). Evolution of the serologic response to Borrelia burgdorferi in treated patients with culture-confirmed erythema migrans. J Clin Microbiol 34: 1-9
38. Fikrig E, Barthold SW, Sun W, Feng W, Telford SR, III, Flavell RA. (1997). Borrelia burgdorferi P35 and P37 proteins, expressed in vivo, elicit protective immunity. Immunity 6: 531-539. http://dx.doi.org/10.1016/S1074-7613(00)80341-6
39. Fikrig E, Feng W, Barthold SW, Telford SR, III, Flavell RA. (2000). Arthropod-and host-specific Borrelia burgdorferi bbk32 expression and the inhibition of spirochete transmission. J Immunol 164: 5344-5351. http://dx.doi.org/10.4049/jimmunol.164.10.5344
40. Stevenson B, Bono JL, Schwan TG, Rosa P. (1998). Borrelia burgdorferi erp proteins are immunogenic in mammals infected by tick bite, and their synthesis is inducible in cultured bacteria. Infect Immun 66: 2648-2654
41. Brissette CA, Haupt K, Barthel D, Cooley AE, Bowman A, Skerka C, Wallich R, Zipfel PF, Kraiczy P, Stevenson B. (2009). Borrelia burgdorferi infection-associated surface proteins ErpP, ErpA, and ErpC bind human plasminogen. Infect Immun 77: 300-306. http://dx.doi.org/10.1128/IAI.01133-08
42. Probert WS, Johnson BJ. (1998). Identification of a 47 kDa fibronectinbinding protein expressed by Borrelia burgdorferi isolate B31. Mol Microbiol 30: 1003-1015. http://dx.doi.org/10.1046/j.1365-2958.1998.01127.x
43. Wormser GP, Masters E, Nowakowski J, McKenna D, Holmgren D, Ma K, Ihde L, Cavaliere LF, Nadelman RB. (2005). Prospective clinical evaluation of patients from Missouri and New York with erythema migranslike skin lesions. Clin Infect Dis 41: 958-965. http://dx.doi.org/10.1086/432935
44. Aucott J, Morrison C, Munoz B, Rowe PC, Schwarzwalder A, West SK. (2009). Diagnostic challenges of early Lyme disease: lessons from a community case series. BMC Infect Dis 9: 79. http://dx.doi.org/10.1186/1471-2334-9-79