CHAPTER 1 INTRODUCTION
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1 CHAPTER 1 INTRODUCTION 42
2 1.0 Introduction Syphilis is a sexually transmitted disease (STD) caused by the spirochete bacterium Treponema pallidum subsp. pallidum. Over 11 million cases of adult syphilis are reported worldwide each year (2009). (1) In addition, the disease can be transmitted congenitally affecting 1,500,000 or more infants annually. (70) The course of untreated syphilis infection follows a relapsing course which may span many years. The disease exhibits a variety of clinical presentations, which have been classically divided into four stages. The primary stage of syphilis occurs after an incubation period of 9-90 days, and is usually characterized by the appearance of a single painless ulcer at the site of inoculation. If left untreated, this primary lesion resolves spontaneously with the majority of patients subsequently developing secondary syphilis. The secondary stage of infection is characterized by rash-like skin lesions that can cover part or all of the body including the soles of the feet and palms of the hands. The rash normally appears 1-6 months after the onset of the primary lesion. Thereafter, the rash will usually resolve spontaneously without treatment and the patient has no apparent signs or symptoms of infection. This period of latency can last many years before development of the late, destructive stage of infection, namely tertiary syphilis. Tertiary syphilis is the final phase of untreated infection. It is characterized by widespread lesions of the skin, bones, and internal organs. Ultimately, severe neurologic and/or cardiovascular lesions may cause possible dementia, insanity, blindness, and sudden death from cardiovascular complications. (2) The mainstay of syphilis screening and diagnosis is serological testing The immune response to the disease involves the production of two distinct antibodies, namely nontreponemal antibodies which recognize lipoidal material released from damaged host cells and treponemal antibodies which are specific for T. pallidum antigens. At the present time, the detection of both nontreponemal and treponemal antibodies require the use of specialized equipment, with testing being performed in a laboratory by trained technicians. In most settings, the test results may not be available on the same day that the specimen has been collected 1 42
3 Currently-available laboratory based nontreponemal (cardiolipin) tests include the Venereal Disease Research Laboratory (VDRL), unheated serum reagin (USR), toluidine red unheated serum (TRUST) and the rapid plasma reagin (RPR) card tests. (3 ) The VDRL and USR tests require the use of a microscope to visualize a flocculation reaction that occurs when reactive sera are mixed with cardiolipin-containing antigen, while the TRUST, and RPR are macroscopic flocculation tests. (4 6) The antigen used in the RPR test is prepared from a modified VDRL antigen suspension containing choline chloride, EDTA and fine charcoal particles as the visualizing agent. All these nontreponemal tests are labor intensive and could be considered subjective. The treponemal tests include the fluorescent treponemal antibody-absorption (FTA-ABS) test, the Treponema pallidum hemagglutination assay (TPHA), the Treponema pallidum passive particle agglutination test (TP-PA), (7,8) enzyme immunoassays (EIAs), chemiluminescence assays (CIA) and immunochromatographic point of care (POC) assays for specific antibodies to Treponema pallidum ). (3) Serum samples from suspected patients are often sent to laboratories for analysis where they are initially screened with a nontreponemal test such as the RPR or VDRL. The reactivity of the sera are then confirmed using a treponemal test such as an FTA-ABS test, TPHA, TP-PA or EIA. If both the nontreponemal and treponemal tests show reactivity, then the patient is counseled and treatment provided. However, since there is often a considerable time lag in obtaining the results, the patient may not return to the clinical site for treatment. In such cases, not only does the patient remain untreated, but there are opportunities for further spread of the disease. Because syphilis is a disease of worldwide distribution and of public health significance, a rapid point-of-care test that can be used to screen and confirm the serological status of an individual attending an STD or antenatal clinic in resource-poor settings, would allow them to be counseled by the physician as to whether they have active infection that would require immediate treatment before leaving the premises. At present, there is no dual point-of-care test available which is capable of screening and confirming the results on the same device. The goal of the studies reported in this thesis has been to develop and optimize two rapid point-of-care tests for syphilis, capable of detecting both nontreponemal and treponemal antibodies, thus serving as both a screening and confirmatory test for the disease. This is an 2
4 approach long advocated by the World Health Organization (WHO), (Treponemal Infections, Technical Report Series 674, Geneva: 1982). The tests developed during the course of these studies have proved simple to perform, require no expertise in interpretation of results and are capable of being read within 2 to 15 minutes. These tests are ideal for use in field epidemiological studies where laboratory facilities are not available and where a rapid serological diagnosis is important. Two formats of the rapid point-of-care test have been designed, namely an immunofiltration (flow-through) and immunochromatographic (lateral flow) device to be used with whole blood or serum/plasma samples. This thesis also describes the development and optimization of two new laboratory-based tests, an enzyme linked immunosorbent assay (ELISA) and a multiplex chemiluminescence assay which have also been designed for the simultaneous detection of nontreponemal and treponemal antibodies. These tests have the advantage that they can be fully automated and would be ideal for use in high volume laboratories. At the present time, there is no point-ofcare or ELISA/chemiluminescence tests capable of detecting nontreponemal antibody anywhere in the world. Viable tests such as those described in this thesis are urgently needed to alleviate both the scourge of adult syphilis and to aid the congenital syphilis elimination efforts of the World Health Organization. Efforts to develop immunochromatographic tests that include cardiolipin antigen have been frustrated by the difficulty of attaching cardiolipin to a porous support, such as nitrocellulose. The nonpolar nature of the fatty acid side chains of cardiolipin imparts a high degree of hydrophobicity to the molecule that also makes it difficult to bind cardiolipin to polar surfaces, such as nitrocellulose, latex beads or polystyrene ELISA plates. An attempt has previously been made to develop a single rapid dot-immunogold filtration assay as a screening test for syphilis using a cardiolipin-based antigen for the detection of anti-cardiolipin antibodies. (9) Design flaws prevented this method from being useful in the diagnosis of the disease. In this assay the nitrocellulose (NC) membrane was treated with 80% alcohol for 10 minutes which dissolved the membrane and exposed the plastic backing. The antigen, one µl of a mixture of 2 mg cardiolipin and 2 mg of cholesterol in 50% alcohol, was applied to the exposed plastic backing resulting in poor adherence and resulting considerable sample to sample variability. The detector signal used was Protein A 3
5 conjugated to colloidal gold which detects IgG but not IgM. (10) In contrast, the studies described in this thesis employ reagents conjugated to colloidal gold that can detect both classes of immunoglobulin in early or late stages of infection. The studies described here employ two of the author's patents in the lateral flow and flow-through devices namely, a non treponemal antigen that is prepared from synthetic VDRL antigen (U.S. Patent Application No. 10/009,698), (11) while this antigen is bound to nitrocellulose by utilizing the technique described in the U.S. Patent Application Publication US 2009/ A1. (12) The method of attaching the antigen to the nitrocellulose membrane is based on the fractionation and the chromatographic affinity purification of IgG from a hyperimmune syphilitic serum. The process is followed by papain enzymatic separation of the Fab fragments from the IgG. The Fab fragments of the hyperimmune sera are specific for the micelles prepared from the synthetic VDRL antigen and form a bridge between the micelle and the nitrocellulose membrane. An alternative method employed, is the isolation of small particle size micelles (< 5 µm) by differential centrifugation and membrane filtration. The small particle-sized micelle is able to attach directly to the membrane by electrostatic coupling of the negativelycharged head groups of cardiolipin, to the strong dipole of the nitrate ester of the nitrocellulose membrane The treponemal antigen used in all dual tests (both point-of-care and laboratory-based) described in this thesis is a recombinant Tp17 antigen, expressed by E. coli constructs which can be attached directly to the membrane of lateral flow or flow-through devices. The treponemal antigen also readily attaches to solid surfaces such as nitrocellulose membranes, latex beads or polystyrene ELISA plates. These surfaces bind proteins by hydrogen bonding, hydrophobic interactions and by electrostatic mechanisms. It should be noted that point-of-care tests for the detection of treponemal antibodies are already commercially-available; these include the Determine (Inverness Laboratories), Visitect (Omega Diagnostics), Espline TP, Visitect-Syphlis and SD Syphilis 3.0 (Standard Diagnostics). (13-16) However, a positive test with these products is indicative of life-time exposure to syphilis and does not necessarily denote an active infection. 4
6 In the commercially-available treponemal rapid lateral flow tests, the treponemal antigen employed in these tests are protein in nature. The chemistry involved in the preparation of the running or wash buffer for the lateral flow tests require the addition of surfactants and detergents which are necessary for the migration of the serum sample through the membrane, but the addition of these chemicals are detrimental to the nontreponemal antigen causing disruption of the cardiolipin micelles. This is one of the main reasons why commercial companies have not used nontreponemal antigens as in the Dot-Immuno Filtration Assay of the past. In contrast, the lateral flow format developed in the present work presented here has utilized a very low concentration of the mild detergent Tergitol, which has a minimal effect on micelle antigens. The lateral flow format is based on the principle of immunochromatography, (17) where nitrocellulose membranes are attached to a sample pad, conjugate pad and an absorbent pad in 5 mm x 60 mm strips on a plastic support. Prior to assembly, the nitrocellulose membrane is sprayed separately with the cardiolipin micelle antigen and recombinant treponemal antigen as capture reagents. A stripe of goat anti-human serum is used as procedural control. When the patient serum is added to the sampling pad, it migrates by capillary action wetting the conjugate pad which contains the detector agent comprised of goat anti-human IgG/IgM conjugated to colloidal gold. The complex formed by the serum and conjugate moves through the membrane over the zone to which the capture agents have been immobilized forming visible dark red purple lines. Negative sera show no lines except in the control region. A positive reaction is characterized by the appearance of visible lines in the cardiolipin antigen, treponemal antigen and control region. A previous attempt to produce and to commercialize a nontreponemal ELISA for the serodiagnosis of syphilis (18) also failed largely as result of flaws in design. The nontreponemal antigen used was an ethanolic solution of cardiolipin, lecithin and cholesterol which is the standard formulation for the VDRL antigen flocculation test. Microtiter plates were coated with the ethanolic antigen solution and allowed to evaporate. Since there is no direct mechanism of binding the antigen to the plates, the antigen eluted variably from the plates after the addition of serum samples and during subsequent washing steps of the ELISA test, resulting in a lack of well-to-well reproducibility. 5
7 To overcome these difficulties, the cardiolipin antigen was chemically modified according to the author's U.S. Patent No. 7,888,043 B2, (19) in which the double bonds of the fatty acids were oxidized to carboxyl groups and activated with 1-ethyl-3-(3-dimethylamino-propyl) carbodiimide, and attached covalently to the amine group of a microtiter amino ELISA plate or latex beads of a chemiluminescence system. The active component of the nontreponemal antigen is cardiolipin, which is a phospholipid comprising of three molecules of glycerol joined by two phosphodiester bridges. The two hydroxyl groups of the external glycerol molecules are esterified with four 18-carbon unsaturated fatty acids (linoleoyl), each of which has two double bonds. It is known that the binding site of cardiolipin is attributed to two phosphate groups and the β-hydroxyl group of the central glycerol moiety. (20-23) This configuration of the central glycerol moiety is essential for the serologic specificity of the cardiolipin antigen reacting with syphilitic sera. (24) Once the nontreponemal (cardiolipin) antigen was modified by micelle separation, then the antigen could be attached to solid surfaces such as nitrocellulose membranes, making it possible to develop a rapid dual point of care test applicable to both the lateral flow and flow-through formats. Also with the modification of the cardiolipin molecule by oxidation of the double bonds of the fatty acids, the resulting carboxyl groups were activated and were able to be attached to solid surfaces containing amine groups. This resulted in the development of two dual laboratory based tests, ideal for automated high volume testing with numerical value results that can be used for monitoring efficacy of syphilis treatment. 6
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