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Chen HW, Zhang Z, Halsey ES, Guevara C, Canal E, Hall E, Maves R, Tilley DH, Kochel TJ, Ching WM, 2013. Detection of Leptospira-specific antibodies using a recombinant antigen-based enzyme-linked immunosorbent assay. Am J Trop Med Hyg 89: 1088–1094.
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An Improved Enzyme-Linked Immunoassay for the Detection of Leptospira-Specific Antibodies
Hua-Wei Chen
Hua-Wei Chen
Naval Medical Research Center, Silver Spring, Maryland;
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Heather Lukas
Heather Lukas
Naval Medical Research Center, Silver Spring, Maryland;
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Kira Becker
Kira Becker
Naval Medical Research Center, Silver Spring, Maryland;
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Giulia Weissenberger
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Naval Medical Research Center, Silver Spring, Maryland;
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Eric S. Halsey
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Naval Medical Research Unit No. 6, Lima, Peru;
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Carolina Guevara
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Naval Medical Research Unit No. 6, Lima, Peru;
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Enrique Canal
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Naval Medical Research Unit No. 6, Lima, Peru;
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Eric Hall
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Naval Medical Research Center, Silver Spring, Maryland;
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Ryan C. Maves
Ryan C. Maves
Naval Medical Research Unit No. 6, Lima, Peru;
Naval Medical Center San Diego, San Diego, California;
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Naval Medical Center San Diego, San Diego, California;
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Drake H. Tilley
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Naval Medical Center San Diego, San Diego, California;
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Lynn Kuo
Lynn Kuo
Department of Statistics, University of Connecticut, Storrs, Connecticut
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Tadeusz J. Kochel
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Naval Medical Research Center, Silver Spring, Maryland;
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Wei-Mei Ching
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Leptospirosis is a neglected zoonotic disease with worldwide endemicity and continues to be a significant public health burden on resource-limited populations. Previously, we produced three highly purified recombinant antigens (rLipL32, rLipL41, and rLigA-Rep) and evaluated their performance of detecting Leptospira-specific antibodies in enzyme-linked immunosorbent assay (ELISA) as compared with the microscopic agglutination test (MAT). The overall sensitivity of this assay approached 90%. Recently, another recombinant antigen (rLigB-Rep) was prepared. We tested each individual antigen and a 1:1:1:1 mixture of these four antigens for the detection of Leptospira-specific antibodies in ELISA. The performance of these recombinant antigens was evaluated with a much larger febrile patient panel (337 MAT-confirmed positive sera and 92 MAT-negative sera from febrile patients). Combining the detection results of immunoglobulin M and immunoglobulin G from these four individual antigens, the overall sensitivity was close to 90% but the specificity was only 66%, based on the MAT reference method. The overall sensitivity and specificity of the four-antigen mixture were 82% and 86%, respectively. The mixture of four antigens also exhibited a broader reactivity with MAT-positive samples of 18 serovars from six major pathogenic Leptospira species. Given the limitations of MAT, the data were further analyzed by Bayesian latent class model, showing that ELISA using a 1:1:1:1 mixture still maintained high sensitivity (79%) and specificity (88%) as compared with the sensitivity (90%) and specificity (83%) of MAT. Therefore, ELISA using a mixture of these four antigens could be a very useful test for seroprevalence studies.
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Author Notes
Financial support: This research was supported by Naval Medical Research Center, research work unit 6000.RAD1.J.A0310 and the United States Department of Defense Global Emerging Infections Systems Research Program, work unit number 847705.82000.25GB.B0016.
Copyright statement: The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense, or the U.S. government. E. S. H, C. G., E. C., E. H., R. C. M., D. H. T., T. J. K., and W-M. C. are employees of the U.S. government. This work was prepared as part of their official duties. Title 17 U.S.C. §105 provides that “Copyright protection under this title is not available for any work of the United States Government.” Title 17 U.S.C. §101 defines a U.S. government work as a work prepared by a military service member or employee of the U.S. government as part of that person’s official duties.
Authors’ addresses: Hua-Wei Chen, Heather Lukas, Kira Becker, Giulia Weissenberger, Eric Hall, Tadeusz J. Kochel, and Wei-Mei Ching, Naval Medical Research Center, Silver Spring, MD, E-mails: huawei.chen2.ctr@mail.mil, lukas.heather@gmail.com, kbecker2015@yahoo.com, gweis990@gmail.com, eric.r.hall2.mil@mail.mil, tadeusz.kochel@nbacc.dhs.gov, and wei-mei.m.ching.civ@mail.mil. Eric S. Halsey, Carolina Guevara, and Enrique Canal, Naval Medical Research Unit No. 6, Lima, Peru, E-mails: ycw8@cdc.gov, carolina.guevara.fn@mail.mil, and enrique.a.canal.fn@mail.mil. Ryan C. Maves, Naval Medical Research Unit No. 6, Lima, Peru, and Naval Medical Center San Diego, San Diego, CA, E-mail: ryan.c.maves.mil@mail.mil. Drake H. Tilley, Naval Medical Center San Diego, San Diego, CA, E-mail: drake.h.tilley.mil@mail.mil. Lynn Kuo, Department of Statistics, University of Connecticut, Storrs, CT, E-mail: lynn.kuo@uconn.edu.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Pappas G, Papadimitriou P, Siozopoulou V, Christou L, Akritidis N, 2008. The globalization of leptospirosis: worldwide incidence trends. Int J Infect Dis 12: 351–357.
-
2.
Levett PN, 2001. Leptospirosis. Clin Microbiol Rev 14: 296–326.
-
3.
Costa F, Hagan JE, Calcagno J, Kane M, Torgerson P, Martinez-Silveira MS, Stein C, Abela-Ridder B, Ko AI, 2015. Global morbidity and mortality of leptospirosis: a systematic review. PLoS Negl Trop Dis 9: e0003898.
-
4.
Cruz LS, Vargas R, Lopes AA, 2009. Leptospirosis: a worldwide resurgent zoonosis and important cause of acute renal failure and death in developing nations. Ethn Dis 19: 37–41.
-
5.
Sethi S, Sharma N, Kakkar N, Taneja J, Chatterjee SS, Banga SS, Sharma M, 2010. Increasing trends of leptospirosis in northern India: a clinico-epidemiological study. PLoS Negl Trop Dis 4: 579.
-
6.
Victoriano AF et al. 2009. Leptospirosis in the Asia Pacific region. BMC Infect Dis 9: 147.
-
7.
Lim VK, 2011. Leptospirosis: a re-emerging infection. Malays J Pathol 33: 1–5.
-
8.
Reller ME, Bodinayake C, Nagahawatte A, Devasiri V, Kodikara-Arachichi W, Strouse JJ, Flom JE, Dumler JS, Woods CW, 2011. Leptospirosis as frequent cause of acute febrile illness in southern Sri Lanka. Emerg Infect Dis 17: 1678–1684.
-
9.
Bourhy P et al. 2012. Human Leptospira isolates circulating in Mayotte (Indian Ocean) have unique serological and molecular features. J Clin Microbiol 50: 307–311.
-
10.
Fonzar UJ, Langoni H, 2012. Geographic analysis on the occurrence of human and canine leptospirosis in the city of Maringá, state of Paraná, Brazil. Rev Soc Bras Med Trop 45: 100–105.
-
11.
Lau CL, Dobson AJ, Smythe LD, Fearnley EJ, Skelly C, Clements AC, Craig SB, Fuimaono SD, Weinstein P, 2012. Leptospirosis in American Samoa 2010: epidemiology, environmental drivers, and the management of emergence. Am J Trop Med Hyg 86: 309–319.
-
12.
Zhang C, Wang H, Yan J, 2012. Leptospirosis prevalence in Chinese populations in the last two decades. Microbes Infect 14: 317–323.
-
13.
McBride AJ, Athanazio DA, Reis MG, Ko AI, 2005. Leptospirosis. Curr Opin Infect Dis 18: 376–386.
-
14.
Ko AI, Goarant C, Picardeau M, 2009. Leptospira: the dawn of the molecular genetics era for an emerging zoonotic pathogen. Nat Rev Microbiol 7: 736–747.
-
15.
Zaki SR, Shieh WJ, 1996. Leptospirosis associated with outbreak of acute febrile illness and pulmonary haemorrhage, Nicaragua, 1995. The epidemic working group at ministry of health in Nicaragua. Lancet 347: 535–536.
-
16.
Gouveia EL, Metcalfe J, de Carvalho AL, Aires TS, Villasboas-Bisneto JC, Queirroz A, Santos AC, Salgado K, Reis MG, Ko AI, 2008. Leptospirosis-associated severe pulmonary hemorrhagic syndrome, Salvador, Brazil. Emerg Infect Dis 14: 505–508.
-
17.
Papa A, Theoharidou D, Antoniadis A, 2009. Pulmonary involvement and leptospirosis, Greece. Emerg Infect Dis 15: 834–835.
-
18.
Crump JA et al. 2013. Etiology of severe non-malaria febrile illness in northern Tanzania: a prospective cohort study. PLoS Negl Trop Dis 7: e2324.
-
19.
LaRocque RC, Breiman RF, Ari MD, Morey RE, Janan FA, Hayes JM, Hossain MA, Brooks WA, Levett PN, 2005. Leptospirosis during dengue outbreak, Bangladesh. Emerg Infect Dis 11: 766–769.
-
20.
Abela-Ridder B, Sikkema R, Hartskeerl RA, 2010. Estimating the burden of human leptospirosis. Int J Antimicrob Agents 36 (Suppl 1): S5–S7.
-
21.
Biggs HM, Hertz JT, Munishi OM, Galloway RL, Marks F, Saganda W, Maro VP, Crump JA, 2013. Estimating leptospirosis incidence using hospital-based surveillance and a population-based health care utilization survey in Tanzania. PLoS Negl Trop Dis 7: e2589.
-
22.
Levett PN, 2007. Leptoapira. Manual of Clinical Microbiiology, 9th edition. Washington, DC: American Society for Microbiolgy Press, 963–970.
-
23.
Bharti AR et al. 2003. Leptospirosis: a zoonotic disease of global importance. Lancet Infect Dis 3: 757–771.
-
24.
Flannery B et al. 2001. Evaluation of recombinant Leptospira antigen-based enzyme-linked immunosorbent assays for the serodiagnosis of leptospirosis. J Clin Microbiol 39: 3303–3310.
-
25.
Srimanote P, Wongdeethai N, Jieanampunkul P, Samonkiert S, Leepiyasakulchai C, Kalambaheti T, Prachayasittikul V, 2008. Recombinant ligA for leptospirosis diagnosis and ligA among the Leptospira spp. clinical isolates. J Microbiol Methods 72: 73–81.
-
26.
Chalayon P, Chanket P, Boonchawalit T, Chattanadee S, Srimanote P, Kalambaheti T, 2011. Leptospirosis serodiagnosis by ELISA based on recombinant outer membrane protein. Trans R Soc Trop Med Hyg 105: 289–297.
-
27.
Chen HW, Zhang Z, Halsey ES, Guevara C, Canal E, Hall E, Maves R, Tilley DH, Kochel TJ, Ching WM, 2013. Detection of Leptospira-specific antibodies using a recombinant antigen-based enzyme-linked immunosorbent assay. Am J Trop Med Hyg 89: 1088–1094.
-
28.
Kitashoji E et al. 2015. Diagnostic accuracy of recombinant immunoglobulin-like protein a-based IgM ELISA for the early diagnosis of leptospirosis in the Philippines. PLoS Negl Trop Dis 9: e0003879.
-
29.
Studier FW, Moffatt BA, 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189: 113–130.
-
30.
Matsunaga J et al. 2003. Pathogenic Leptospira species express surface-exposed proteins belonging to the bacterial immunoglobulin superfamily. Mol Microbiol 49: 929–945.
-
31.
Frey A, Di Canzio J, Zurakowski D, 1998. A statistically defined endpoint titer determination method for immunoassays. J Immunol Methods 221: 35–41.
-
32.
Joseph L, Gyorkos TW, Coupal L, 1995. Bayesian estimation of disease prevalence and the parameters of diagnostic tests in the absence of a gold standard. Am J Epidemiol 141: 263–272.
-
33.
Dendukuri N, Joseph L, 2001. Bayesian approaches to modeling the conditional dependence between multiple diagnostic tests. Biometrics 57: 158–167.
-
34.
Vacek PM, 1985. The effect of conditional dependence on the evaluation of diagnostic tests. Biometrics 41: 959–968.
-
35.
Branscum AJ, Gardner IA, Johnson WO, 2005. Estimation of diagnostic-test sensitivity and specificity through Bayesian modeling. Prev Vet Med 68: 145–163.
-
36.
Palaniappan RU et al. 2002. Cloning and molecular characterization of an immunogenic LigA protein of Leptospira interrogans. Infect Immun 70: 5924–5930.
-
37.
Koizumi N, Watanabe H, 2004. Leptospiral immunoglobulin-like proteins elicit protective immunity. Vaccine 22: 1545–1552.
-
38.
Mcbride AJ, Cerqueira GM, Suchard MA, Moreira AN, Zuerner RL, Reis MG, Haake DA, Ko AI, Dellagostin OA, 2009. Genetic diversity of the leptospiral immunoglobulin-like (Lig) genes in pathogenic Leptospira spp. Infect Genet Evol 9: 196–205.
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