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Enzyme-Linked Immunosorbent Assay for Detection of Antibodies to the Venereal Disease Research Laboratory (VDRL) Antigen in Syphilis

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Enzyme-Linked Immunosorbent Assay for Detection of Antibodies to the Venereal Disease Research Laboratory (VDRL) Antigen in Syphilis JOURNAL OF CLINICAL MICROBIOLOGY, Sept. 1987, p. 1711-1716 Vol. 25, No. 9 0095-1137/87/091711-06$02.00/0 Copyright © 1987, American Society for Microbiology Enzyme-Linked Immunosorbent Assay for Detection of Antibodies to the Venereal Disease Research Laboratory (VDRL) Antigen in Syphilis NILS STRANDBERG PEDERSEN,1* OLE 0RUM,' AND S0REN MOURITSEN2 World Health Organization Collaborating Centre for Reference and Research on Treponematoses, Department of Treponematoses,' and Autoimmune Laboratory,2 Statens Seruminstitut, DK-2300 Copenhagen S, Denmark Received 9 March 1987/Accepted 27 May 1987 An enzyme-linked immunosorbent assay (ELISA) for detection of immunoglobulin G (IgG) and IgM to cardiolipin, lecithin, and cholesterol (VDRL [Venereal Disease Research Laboratory] ELISA) is described. The specificity of the VDRL ELISA for IgG and IgM was 99.6 and 99.5%, respectively, with sera from 1,008 persons without syphilis. For a group of patients with false-positive results in traditional nontreponemal tests and for patients with autoimmune diseases, the VDRL ELISA for IgG had a higher specificity than the VDRL ELISA for IgM. The sensitivity for IgG and IgM with 118 sera from patients with untreated syphilis was 96.6 and 94.9%, respectively, which was equivalent to the sensitivities of the traditional nontreponemal tests. The performance of the VDRL ELISA was compared with that of an ELISA that uses cardiolipin as the antigen (cardiolipin ELISA). The VDRL ELISA was significantly more sensitive (P s 0.01) than the cardiolipin ELISA with 25 sera from syphilis patients but was less sensitive (P - 0.01) with 53 sera from patients with autoimmune diseases. The antibody reactivity in the VDRL ELISA could not be absorbed out by lecithin and cholesterol, and the sera from patients with syphilis did not react in an ELISA that uses cholesterol and lecithin as the antigen. This indicates that cholesterol and lecithin, although not antigenic by themselves, may change the structural form of the epitope on cardiolipin so that it becomes more recognizable for antibodies in syphilis and less recognizable for antibodies in autoimmune diseases. The results of the VDRL ELISA were expressed in percentages of the absorbance value of a positive control. The VDRL ELISA gave, without titration of sera, quantitative results that correlated with the quantitative results of the traditional nontreponemal tests obtained by titration. The VDRL ELISA will be well suited for large-scale testing for syphilis and may replace other nontreponemal tests. Serological tests for syphilis can be divided in two major posttreatment monitoring and for the detection of reinfec- groups, the nontreponemal and the treponemal tests. The tions (10). nontreponemal tests or standard tests for syphilis detect The nontreponemal tests presently used are not ideal. antibodies against the phospholipid hapten cardiolipin, in None of the tests used today is able to distinguish between complex with lecithin and cholesterol. This antigen complex immunoglobulin G (IgG) and IgM without previous separa- is used either in a complement fixation test (Wassermann tion of serum. Detection of IgM is important for the diagno- test) or in agglutination tests such as the Venereal Disease sis of congenital syphilis, because IgM does not cross the Research Laboratory (VDRL) test, the automated reagin intact placenta, and IgM in newborns indicates active syph- test (ART), or the rapid plasma reagin test (19). The sero- ilis. The Wassermann test used in Europe requires fresh logical diagnosis of syphilis still depends to a large extent on complement, which makes the test troublesome. The VDRL the results of a nontreponemal test, supplemented when test requires fresh and accurate preparation of antigen and necessary by a confirmatory treponemal antibody test, i.e., microscopic visualization of agglutination. The ART and the the fluorescent treponemal antibody absorption (FTA-ABS) rapid plasma reagin test are easier to perform, but interpre- test (19) or the Treponema pallidum hemagglutination test tation of weak-positive results may often be difficult. False- (13). The nontreponemal tests are extremely valuable for negative results may occur in the VDRL test, the ART, and screening purposes and may have even higher specificities the rapid plasma reagin test when strongly positive sera are tests The for syphilis than the treponemal (10, 15). trepo- tested, because of prozone phenomena (18). Recently a nemal tests not be used as but as should screening tests, only radioimmunosorbent assay (7) and an enzyme-linked im- tests on selected serum from confirmatory highly samples munosorbent assay (ELISA) (11) have been described for patients who are suspected of a present or previous the detection of anti-cardiolipin antibodies. These tests have treponemal infection (3, 15). Furthermore, whereas a not been evaluated as syphilis diagnostic tests but have been test becomes within 6 to nontreponemal generally negative used to detect anti-cardiolipin antibodies in patients with 12 months after treatment of early syphilis, the treponemal autoimmune diseases, i.e., systemic lupus erythematosus tests may remain positive for many years (2, 16). Quantita- (SLE). tive nontreponemal tests are therefore useful both for In the present study, we have developed an ELISA for determination of IgG and IgM against the VDRL antigen. * Corresponding author. The sensitivity and specificity of this method were compared 1711 1712 PEDERSEN ET AL. J. CLIN. MICROBIOL. with those of a cardiolipin ELISA, a cardiolipin Wasser- filtered through a 0.22-,um-pore-size filter (Millex-GS; Milli- mann (CWRM) test, an ART, and an FTA-ABS test. pore, Molsheim, France). The absorbed serum was then tested as described above. MATERIALS AND METHODS Routine syphilis serological methods. All sera were tested by the ART (19) and, if positive, quantified by the rapid Lipid antigens. Cardiolipin was purified by the method of plasma reagin test (19). All sera were also tested by the Pangborn (12), and lecithin was purified by the method of CWRM test as modified by Môrch (17), and sera from Riis Nielsen (14). Cholesterol was obtained from Pfanstiehl syphilis patients were also analyzed by the FTA-ABS test. Lab, Waukegan, 111. The purity of all lipids was tested by The conjugate used in the FTA-ABS test was a rabbit anti- thin-layer chromatography. human IgG, IgA, IgM (code F1009; DAKO-Immunoglobulins). Conjugates. The conjugates used were horseradish perox- Diagnoses of syphilis. The diagnoses of syphilis were made idase-conjugated rabbit anti-human IgG (code P214, lot 091) on the basis of extensive centralized, serological, and clini- and anti-human IgM (code P215, lot 0.25A), both from cal data collected at the Department of Treponematoses, DAKO-Immunoglobulins, Copenhagen, Denmark. Statens Seruminstitut, Copenhagen. VDRL ELISA for IgG and IgM. Each well of flat-bottom Sera. Sera were chosen from specimens submitted for polyvinyl chloride microtiter plates (Titertek, catalog no. routine syphilis serological analysis during a 4-month period 77-173-05; Flow Laboratories, Irvine, Scotland) was coated in 1986, except for 25 samples from patients with secondary with 25 .1t of an ethanol solution containing 0.003% (wt/vol) syphilis (group 2), which were collected in 1980 and stored at cardiolipin, 0.09% (wt/vol) cholesterol, and 0.021% (wt/vol) -20°C, and 500 samples from blood donors, which were lecithin (the VDRL antigen diluted 10 times in absolute collected in 1982. None of the sera tested was heat inacti- ethanol). The solvent was evaporated at 4°C overnight. The vated. plates were washed three times with phosphate-buffered Group 1: patients with untreated primary syphilis. There saline (PBS), pH 7.4, and then coated with 100 iil of 10% were 46 patients with primary untreated syphilis. All patients (vol/vol) bovine serum in PBS (PBS-BS) at room tempera- had lesions suspected ofbeing chancres, and all had sera that ture for 1 h. Before use, the bovine serum was tested and were reactive in the FTA-ABS test. found negative by the CWRM test and the ART. The wells Group 2: patients with untreated secondary syphilis. There were aspirated and washed as described above, and 100 ,uI of were 32 patients with untreated secondary syphilis. All the serum to be tested was diluted 1:100 in PBS-BS and patients had exanthema, and all gave sera that were reactive added to each of two wells. A positive and a negative control in the CWRM, ART, and FTA-ABS tests. serum were included in every experiment. The positive Group 3: patients with untreated late syphilis. There were control was obtained from a syphilis patient and had optical five patients with untreated neurosyphilis. All patients had densities of 1.2 and 1.9 in the ELISAs for IgG and IgM, cerebrospinal fluid that gave reactive results in the CWRM respectively. The negative control serum was obtained from and FTA-ABS tests. a blood donor. The optical density values for this were 0.1 Group 4: patients with untreated serologically diagnosed and 0.15 in the ELISAs for IgG and IgM, respectively. After early syphilis. There were 35 patients with serologically incubation for 2 h at room temperature, the plates were diagnosed syphilis. All patients were positive in the CWRM, aspirated and washed, and 100 jil of conjugate diluted in ART, and FTA-ABS tests. None of the patients had clinical PBS-BS was added. Incubation took place for 2 h at room findings indicating syphilis, and because of a rapid serolog- temperature, the plates were then aspirated and washed, and ical response to treatment the diagnosis of early syphilis was 200 1tl of substrate (41 mg of o-phenylenediamine [Sigma made. Chemical Co., St. Louis, Mo.], 100 ml of citrate buffer [pH Group 5: patients with treated syphilis. There were 146 5], 25 Fd of 30% H202) was added to each well. After patients with treated syphilis. The stages at the time of incubation for 15 min at room temperature, the reaction was diagnosis differed, and both early and late syphilis cases stopped by the addition of 50 ,ul of 3 M H2SO4 to each well.
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