Evaluation of the new ARCHITECT CMV IgM, IgG and IgG avidity assays
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1 JCM Accepts, published online ahead of print on 1 April 0 J. Clin. Microbiol. doi:./jcm.01-0 Copyright 0, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved. 1 Evaluation of the new ARCHITECT CMV IgM, IgG and IgG avidity assays 1 K. Lagrou, M. Bodeus, 1 M. Van Ranst, P. Goubau Department of Medical Diagnostic Sciences, Katholieke Universiteit Leuven, Leuven, Belgium Department of Microbiology, Université Catholique de Louvain, Brussels, Belgium Running title: Architect CMV assays Corresponding author: Prof. K. Lagrou UZ Leuven Laboratoriumgeneeskunde Herestraat 000 Leuven Phone: + (0)1 0 Fax: + (0)1 1 katrien.lagrou@uz.kuleuven.be 1
2 Abstract Objectives: A panel of new CMV assays for the ARCHITECT instrument has been developed including a CMV avidity assay based on a new technology. The purpose of this study was to compare the performance of the fully automated CMV IgM, IgG and IgG avidity tests on ARCHITECT with other available assays. Methods: 0 consecutive fresh patient sera ( routine sera ) and sera from pregnant women with a recent CMV primary infection ( seroconversion sera ) were tested for CMV IgM and IgG on ARCHITECT (Abbott), VIDAS (BioMérieux) and with Enzygnost assays (Siemens). The seroconversion sera and 0 preselected AxSYM IgM negative, IgG positive sera were also tested with the IgG avidity tests on ARCHITECT and VIDAS. Results: The relative agreement for CMV IgM determination on routine sera between ARCHITECT and VIDAS, Enzygnost and AxSYM was respectively %, % and % for CMV IgM tests and %, % and % for CMV IgG tests. The specificity of the CMV IgG avidity test was % for ARCHITECT and % for VIDAS. No high CMV IgG avidity test results were found within the first months after seroconversion with both assays. Conclusion: The correlation between the newly developed CMV IgM and IgG tests on ARCHITECT with the VIDAS and Enzygnost assays was excellent ( %). The CMV IgG avidity test reliably excluded recent infections and showed an excellent specificity (%).
3 Introduction Human cytomegalovirus (CMV) is the most common cause of congenital infection. Primary infections occur in 0. to.0% of all pregnancies. In utero transmission of CMV can take place during primary maternal infection or during non primary infection (reactivation and reinfection) of seropositive mothers but the transmission rate to the fetus is much higher in non-immune mothers (up to 0%) compared to immune mothers (0-1%) (1). Fowler et al. showed that naturally acquired immunity results in a % reduction in the risk of congenital CMV infection in future pregnancies (). Screening for CMV antibodies in pregnant women is a controversial issue and is not supported by international guidelines. Opponents of CMV screening during pregnancy bring up that there is no clearly effective intervention available. In addition, no tests can reliably predict which infected fetuses will have serious sequelae. The prognostic value of viral load determination of amniotic fluid is still a matter of debate and has the disadvantage of its invasive character (,,,,,). On the other hand, many parents wish antenatal diagnosis of intrauterine infections and CMV screening is generally offered by gynecologists. Prenatal screening certainly has advantages such as the fact that precautionary hygienic measures can be suggested to CMV seronegative pregnant women. The knowledge of a primary CMV infection in a pregnant woman can lead to a closer follow-up of the fetus by ultrasound and nuclear magnetic resonance. For the diagnosis of a primary CMV infection in pregnancy it is of utmost importance that we have reliable, non-invasive tests available. CMV-specific immunoglobulin M (IgM) is produced during primary infection, but is also detectable during reactivation and reinfection (). A test that enables the discrimination between a primary infection and a non-primary infection is important for counseling the parents regarding the risk of congenital infection.
4 1 CMV IgG avidity testing has been shown to be useful for distinguishing primary and nonprimary infection (1,,,). It measures the binding affinity of IgG antibodies. At the onset of infection, IgG of low avidity are produced. Over time, maturation of the antibody occurs resulting in increased binding affinity and thus higher avidity. A diagnostic algorithm for CMV serology screening in pregnant women based on CMV IgM, IgG and IgG avidity testing was proposed by Munro et al. (1). Recently, a panel of new CMV assays for the ARCHITECT instrument has been developed including a CMV IgG avidity assay. It is the first platform that enables complete automation of avidity testing. While conventional avidity assays remove low avidity antibodies by a chaotropic agent, in the ARCHITECT test high avidity antibodies are removed by neutralization with liquid antigen and low avidity antibodies are detected directly. The purpose of this study was to evaluate the performance characteristics of the ARCHITECT CMV IgM, IgG and avidity assay and to compare the results with available CMV assays from biomérieux and Siemens.
5 Materials and methods Human serum samples were provided for routine diagnosis in the laboratories of the University Hospitals Leuven and the University Hospitals St Luc (Brussels). (i) Routine specimens. 0 consecutive fresh sera submitted for CMV serology testing on the AxSYM instrument (Abbott Laboratories, Abbott Park, Ill) were used to evaluate the correlation between the ARCHITECT (Abbott), AxSYM (Abbott), VIDAS (biomérieux) and Enzygnost assays (Siemens). 0 consecutively AxSYM CMV IgM negative, IgG positive specimens were selected to evaluate the specificity of the IgG avidity tests. (ii) Seroconversion sera. selected frozen sera from 1 pregnant women with a recent primary CMV infection were used to evaluate the IgG avidity tests. From of these 1 women, recent seroconversion was known to have occurred in a time period ranging from weeks to months. The number of sera per patient ranged from 1 to. Determination of CMV IgM, CMV IgG and CMV IgG avidity All routine specimens were tested using commercially available assays from three different manufacturers, namely AxSYM CMV IgM and IgG, ARCHITECT CMV IgM and IgG, VIDAS CMV IgM and IgG and Enzygnost anti-cmv IgM and IgG assays. All assays are fully automated with the exception of the Enzygnost assays that were performed on the BEPIII instrument (Siemens). The main characteristics of the assays used are summarized in Table 1 including interpretation of results. 0 consecutively selected AxSYM CMV IgM negative, IgG positive sera were additionally tested with ARCHITECT and VIDAS CMV IgG avidity tests.
6 Selected specimens from pregnant women with a recent primary CMV infection were tested with ARCHITECT CMV IgM, IgG and IgG avidity assays, VIDAS CMV IgM, IgG and IgG avidity assay as well as Enzygnost anti-cmv IgG and IgM assays. Frozen specimens were centrifuged prior to testing. All tests were performed and interpreted according the instructions of the manufacturer. On ARCHITECT CMV IgG with avidity < 0.0% are considered low avidity antibodies, IgG with avidity between 0.0% and.% gray zone results and IgG with avidity 0.0% are considered high avidity antibodies. On VIDAS CMV IgG with avidity.0% are low avidity antibodies, IgG with avidity between % and 0% are considered gray zone results and IgG with avidity 0.0% are high avidity antibodies. Performance evaluation The relative agreement between two assays was calculated as follows: [Number of concordant samples/number of all tested samples on both assays] 0%. Gray zone results were considered positive in this calculation. The correlation between positive sera was calculated as follows: [Number of concordant positive samples/number samples that tested positive with either one or both assays] 0%. Statistics: The differences in CMV IgG avidity in sera with a low and a high CMV IgG concentration were analysed with the t-test using Analyse-it software.
7 Results Of the 0 routine sera tested, sera (.%) were reactive in the ARCHITECT CMV IgM assay with gray zone results and positive results. Thirty (1.%) of the positive sera were positive in all assays tested. Only one serum sample (0.%) was reactive (gray zone result) exclusively on the ARCHITECT instrument whereas sera (.0%) where reactive only on the AxSYM instrument. The correlation between the different assays for CMV IgM determination is given in table. The relative agreement between ARCHITECT and VIDAS, Enzygnost and AxSYM CMV IgM tests was respectively %, % and %. Gray zone results were considered as positive results in these calculations. The correlation between positive sera between ARCHITECT and VIDAS, Enzygnost and AxSYM CMV IgM tests was respectively %, % and %. Gray zone results were not taken into account for this calculation. Of the 0 sera tested, 1 sera were reactive in the ARCHITECT CMV IgG assay (prevalence of CMV IgG antibodies = %). Twelve sera (.%) tested negative on AxSYM but positive on ARCHITECT. One serum was only positive on ARCHITECT. This sample was from a lung transplant recipient who tested positive with the AxSYM CMV IgG test in the past. One serum was only positive on the VIDAS. This serum was from a heart transplant recipient who tested negative on AxSYM in the past. All CMV cultures (from different body sites) taken from this patient were negative. The number of CMV IgG reactive sera with the different assays is given in table. The relative agreement between ARCHITECT and VIDAS, Enzygnost and AxSYM CMV IgG tests was respectively %, % and %. Gray zone results were considered as positive results in these calculations. The correlation between positive sera between ARCHITECT and VIDAS, Enzygnost and AxSYM CMV IgG tests was respectively %, % and %.
8 In figure 1 the avidity percentage is given for all seroconversion sera in relation to the timing of the sampling after the last CMV IgG negative serum. No high CMV IgG avidity test results were found within the first months after seroconversion with the ARCHITECT and VIDAS CMV IgG avidity assay. High avidity was attained earlier on ARCHITECT than on VIDAS in patients. In three patients no clear gradual increase in avidity was observed after seroconversion although at least four sera were drawn over a period of at least three months after seroconversion. On VIDAS a small increase in IgG avidity was seen in these patients whereas sometimes even a decrease in the avidity value was seen on ARCHITECT (data not shown). One hundred preselected AxSYM IgG positive, IgM negative sera were tested with the CMV IgG avidity test on ARCHITECT and VIDAS for evaluation of the specificity of the CMV IgG avidity tests. On ARCHITECT, the avidity was high ( 0%) in sera (specificity CMV IgG avidity = %). The two low avidity results (% and %) were found in sera from immunosuppressed patients after transplantation. On VIDAS, the avidity was high ( 0%) in % the sera (specificity CMV IgG avidity = %). A very low avidity (1 and %) was found in sera on VIDAS. The CMV IgG concentration was low in these two sera (1 and AU/mL). The avidity according to the CMV IgG concentration for the ARCHITECT and VIDAS instrument is given in figure. The avidity was statically lower (p<0.001) in sera with a low (< AU/mL) IgG concentration (mean avidity= 0.%) compared to sera with a higher (> AU/mL) concentration (mean avidity =.%) on VIDAS (t-test). This phenomenon was not observed on ARCHITECT (mean avidity =.1% versus.%, p = 0.01).
9 Discussion The performance of the new CMV assays developed for the ARCHITECT instrument, including a CMV IgG avidity test, was evaluated in this study on 0 routine sera and seroconversion sera. The correlation between the CMV IgM and IgG tests on ARCHITECT with the VIDAS and Enzygnost assays was excellent ( %). The CMV IgG avidity test reliably excluded recent infections and showed an excellent specificity (%). In the context of the diagnosis of a congenital CMV infection it is important to have a reliable CMV IgM assay. There is no gold standard available for the determination of CMV IgM antibodies. Therefore in several studies one of the tests is chosen as the standard or a majority agreement of test results in different methods is considered to be the true test result (,). Of course such an approach has important limitations. We evaluated the correlation between the ARCHITECT assay and the other comparator assays. The fact that only one serum of the routine sera was positive exclusively on ARCHITECT supports a good specificity of this test which is probably better than the specificity of the CMV IgM test on AxSYM ( sera were positive exclusively on the CMV IgM test on AxSYM) and seems to be similar to the VIDAS test The use of a more specific CMV IgM assay for the screening of pregnant woman decreases the need of additional avidity testing of the CMV IgG antibodies. The discrepancy of the CMV IgM reactive sera on the different systems may partly be due to the different capacity of the different systems to pick up only primary CMV IgM and not CMV IgM produced during reactivation of the virus. Before the widespread availability of molecular methods to monitor immunocompromised patients for CMV disease, serological methods were used in this indication. In this context, CMV IgM assays were designed for a sensitive detection of IgM in the context of reactivation. Nowadays, molecular methods have shown to be superior to serological tests for the diagnosis of CMV infection in the immunocompromised patient population and serological methods are mainly used for the
10 diagnosis of CMV infection in immunocompetent patients and pregnant woman. A positive point of the ARCHITECT CMV IgM assay is the less populated gray zone compared to the two other assays. With the Enzygnost assay.% of gray zone results were obtained when testing routine samples. Gray zone results are difficult to interpret by the clinicians and often result in the testing of follow-up sera. This additional testing may cause anxiety in the parents and results in additional costs. IgM are also produced during reactivation and reinfection or even due to polyclonal stimulation. CMV IgM can also persist at a low level up to weeks, depending upon the individual patient and the sensitivity of the IgM assay used (). All these factors complicate the interpretation of a positive CMV IgM test result tremendously. A test which enables the distinction between primary and non-primary CMV infection is highly needed. The CMV IgG avidity has been shown to have this capacity. The combination of a CMV IgM test with a low CMV IgG avidity improves the specificity of the diagnosis of a primary infection. Patients with a high avidity can be reassured to have a low risk for in utero transmission. From our results it is clear that there is a large variation in avidity of the IgG in relation to the timing of the sampling after the last CMV IgG negative serum in pregnant women. This is partly due to the fact that the exact timing of infection is not known and cannot be taken into account. But important inter-individual differences in maturation rates of IgG antibodies are also observed. In a minority of the patients no clear maturation was seen during the first three months after seroconversion. It is not clear if this phenomenon is more common in pregnant woman than in non-pregnant women and is an interesting point for further research. With the ARCHITECT assay a decrease in avidity results was sometimes even seen. This is possibly due to the fact that different dilution protocols are automatically used depending on the IgG concentration. Small differences in IgG concentration may sometimes result in the application of a different dilution protocol and this may possibly cause irregularities in the evolution of the IgG avidity
11 results for particular patients. The company does not position the avidity test as a quantitative test but as a qualitative test. Further studies are needed to evaluate the increase in the avidity values on ARCHITECT in patients after seroconversion. This is relevant, as in a woman with a low avidity results, a follow-up serum is often drawn and a significant increase in avidity is used to confirm a recent primary infection. An important part (%) of sera from past infection tested for CMV IgG avidity did not reach the cutoff for high avidity on VIDAS. The consequence is that about one quarter of pregnant woman with a past infection cannot be reassured when using the VIDAS. From our results it seems that lowering the cutoff level on VIDAS is not a solution, as some rather high avidity results were sometimes obtained early after seroconversion. To our surprise we noticed a correlation between the IgG concentration and the avidity on VIDAS. Low avidity results in sera from past infection were nearly exclusively seen in sera with a low IgG concentration. On VIDAS a statistically significant difference in avidity results was observed between sera with a low IgG concentration and sera with higher IgG concentration. Although avidity of the IgG antibodies can be determined in sera with an IgG concentration higher than or equal to AU/mL according to the guidelines of the manufacturer it seems that the test is not reliable on sera with IgG concentrations below - AU/mL. In conclusion, the correlation between the newly developed CMV IgM and IgG tests on ARCHITECT with several well established comparator assays was excellent and highest with the VIDAS test. The CMV IgG avidity test reliably excluded recent infections and showed an excellent specificity.
12 Acknowledgement The study was funded by Abbott Diagnostics. 1
13 Reference List Bodeus, M., S. Feyder, and P. Goubau. 1. Avidity of IgG antibodies distinguishes primary from non-primary cytomegalovirus infection in pregnant women. Clin.Diagn.Virol. :-1.. Fowler, K. B., S. Stagno, and R. F. Pass. 0. Interval between births and risk of congenital cytomegalovirus infection. Clin.Infect.Dis. :-.. Gouarin, S., E. Gault, A. Vabret, D. Cointe, F. Rozenberg, L. Grangeot-Keros, P. Barjot, A. Garbarg-Chenon, P. Lebon, and F. Freymuth. 0. Real-time PCR quantification of human cytomegalovirus DNA in amniotic fluid samples from mothers with primary infection. J.Clin.Microbiol. 0:1-1.. Grangeot-Keros, L., M. J. Mayaux, P. Lebon, F. Freymuth, G. Eugene, R. Stricker, and E. Dussaix. 1. Value of cytomegalovirus (CMV) IgG avidity index for the diagnosis of primary CMV infection in pregnant women. J.Infect.Dis. 1:-.. Guerra, B., T. Lazzarotto, S. Quarta, M. Lanari, L. Bovicelli, A. Nicolosi, and M. P. Landini. 00. Prenatal diagnosis of symptomatic congenital cytomegalovirus infection. Am.J.Obstet.Gynecol. :-.. Kanengisser-Pines, B., Y. Hazan, G. Pines, and Z. Appelman. 0. High cytomegalovirus IgG avidity is a reliable indicator of past infection in patients with positive IgM detected during the first trimester of pregnancy. J.Perinat.Med.[Epub ahead of print].
14 . Lazzarotto, T., L. Gabrielli, M. P. Foschini, M. Lanari, B. Guerra, V. Eusebi, and M. P. Landini. 0. Congenital cytomegalovirus infection in twin pregnancies: viral load in the amniotic fluid and pregnancy outcome. Pediatrics :e-e Lazzarotto, T., C. Galli, R. Pulvirenti, R. Rescaldani, R. Vezzo, G. A. La, C. Martinelli, R. S. La, G. Agresti, L. Grillner, M. Nordin, R. M. van, B. Combs, G. T. Maine, and M. P. Landini. 01. Evaluation of the Abbott AxSYM cytomegalovirus (CMV) immunoglobulin M (IgM) assay in conjunction with other CMV IgM tests and a CMV IgG avidity assay. Clin.Diagn.Lab Immunol. :1-1.. Lazzarotto, T., P. Spezzacatena, P. Pradelli, D. A. Abate, S. Varani, and M. P. Landini. 1. Avidity of immunoglobulin G directed against human cytomegalovirus during primary and secondary infections in immunocompetent and immunocompromised subjects. Clin.Diagn.Lab Immunol. :-.. Lazzarotto, T., S. Varani, B. Guerra, A. Nicolosi, M. Lanari, and M. P. Landini. 00. Prenatal indicators of congenital cytomegalovirus infection. J.Pediatr. :0-.. Maine, G. T., R. Stricker, M. Schuler, J. Spesard, S. Brojanac, B. Iriarte, K. Herwig, T. Gramins, B. Combs, J. Wise, H. Simmons, T. Gram, J. Lonze, D. Ruzicki, B. Byrne, J. D. Clifton, L. E. Chovan, D. Wachta, C. Holas, D. Wang, T. Wilson, S. Tomazic-Allen, M. A. Clements, G. L. Wright, Jr., T. Lazzarotto, A. Ripalti, and M. P. Landini. 00. Development and clinical evaluation of a recombinant-antigen-based cytomegalovirus immunoglobulin M automated immunoassay using the Abbott AxSYM analyzer. J.Clin.Microbiol. :-1.
15 1. Munro, S. C., B. Hall, L. R. Whybin, L. Leader, P. Robertson, G. T. Maine, and W. D. Rawlinson. 0. Diagnosis of and screening for cytomegalovirus infection in pregnant women. J.Clin.Microbiol. : Picone, O., J. M. Costa, M. Leruez-Ville, P. Ernault, M. Olivi, and Y. Ville. 0. Cytomegalovirus (CMV) glycoprotein B genotype and CMV DNA load in the amniotic fluid of infected fetuses. Prenat.Diagn. : Revello, M. G. and G. Gerna. 0. Diagnosis and management of human cytomegalovirus infection in the mother, fetus, and newborn infant. Clin.Microbiol.Rev. :0-.. Revello, M. G., M. Zavattoni, M. Furione, F. Baldanti, and G. Gerna. 1. Quantification of human cytomegalovirus DNA in amniotic fluid of mothers of congenitally infected fetuses. J.Clin.Microbiol. : Stagno, S. and R. J. Whitley. 1. Herpesvirus infections of pregnancy. Part I: Cytomegalovirus and Epstein-Barr virus infections. N.Engl.J.Med :10-1.
16 s Table 1. Characteristics of CMV assays Assay Manufacturer Antigen Test type/procedure Unit Interpretation of results ARCHITECT CMV IgG Abbott viral lysate CMIA - step, indirect anti-igg detection arbitrary units (AU/mL) <.0 nonreactive.0 reactive AxSYM CMV IgG Abbott viral lysate MEIA - step, indirect anti-igg detection < negative arbitrary units (AU/mL) positive < 0.0 negative > 0.0 positive Enzygnost CMV IgG Siemens purified antigen EIA - step, indirect anti-igg detection adsorbance value (A) equivocal VIDAS CMV IgG BioMérieux viral lysate ELFA - step, indirect anti-igg detection arbitrary units (au/ml) ARCHITECT CMV IgM Abbott viral lysate and rag CMIA - step, indirect anti-igm detection Index AxSYM CMV IgM Abbott recomb. Antigen MEIA - step, indirect anti-igm detection Index Enzygnost CMV IgM Siemens purified anigen EIA - step, indirect anti-igm detection adsorbance value (A) VIDAS CMV IgM BioMérieux viral lysate ELFA - step, indirect anti-igm detection Index (i) ARCHITECT CMV IgG Avidity Abbott viral lysate CMIA - two assays with and without liquid CMV antigen to neutralise high avidity CMV antibodies % Avidity < negative > positive - equivocal < 0. nonreactive 1.00 reactive equivocal < 0.00 negative 0.00 positive equivocal < 0.0 negative > 0.0 positive equivocal < 0.0 negative 0.0 positive < 0. equivocal < 0.0 % low avidity > 0.0 % high avidity equivocal < 0. low avidity VIDAS CMV IgG Avidity BioMérieux viral lysate ELFA - two assays with and without molar urea to dissociate low avidity antibodies Avidity Index (AI) > 0. high avidity 0. - < 0. equivocal CMIA Chemiluminescent microparticle immunoassay, MEIA Microparticle enzyme immunoassay, ELISA Enzyme immunoassay, ELFA Enzyme-linked fluorescent assay 1
17 Table. Correlation between ARCHITECT and VIDAS, Enzygnost and AxSYM CMV IgM assays on 0 routine samples VIDAS Enzygnost AxSYM neg gray zone pos neg gray zone pos neg gray zone pos negative 0 1 ARCHITECT gray zone positive 1 1 Table Correlation between Architect and VIDAS, Enzygnost and AxSYM CMV IgG assays on 0 routine samples VIDAS Enzygnost AxSYM neg gray zone pos neg gray zone pos neg pos negative ARCHITECT positive 1 1 1
18 Figure legends Figure 1. CMV IgG avidity results in relation to the timing of the sampling after the last CMV IgG negative serum in pregnant woman (CO: cutoff value for high avidity). Figure CMV IgG avidity according to the CMV IgG concentration for the ARCHITECT and VIDAS instrument tested on 0 preselected AxSYM IgG positive, IgM negative samples. Downloaded from on January 1, 1 by guest 1
19 Figure Avidity % Avidity % Weeks after the last IgG negative serum Architect CO Architect Vidas CO Vidas Downloaded from Weeks after the last IgG negative serum on January 1, 1 by guest 1
20 Figure ARCHITECT Avidity (%) Avidity (%) CMV IgG (AU/mL) VIDAS CMV IgG (AU/mL) AU/mL: Arbitrary Units per milliliter
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