MULTICENTRIC EVALUATION OF NEW COMMERCIAL ENZYME IMMUNOASSAYS FOR THE DETECTION OF IGM AND TOTAL ANTIBODIES AGAINST HEPATITIS A
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1 CVI Accepts, published online ahead of print on June 0 Clin. Vaccine Immunol. doi:./cvi.000- Copyright 0, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved. 1 MULTICENTRIC EVALUATION OF NEW COMMERCIAL ENZYME IMMUNOASSAYS FOR THE DETECTION OF IGM AND TOTAL ANTIBODIES AGAINST HEPATITIS A VIRUS M.C. Arcangeletti 1, E. Dussaix, F. Ferraglia 1, A.M. Roque-Afonso, A. Graube, C. Chezzi Department of Pathology and Laboratory Medicine, University of Parma, Parma, Italy. National Reference Center for Hepatitis A, Paul Brousse Hospital, Villejuif, France Running title: New enzyme immunoassays for HAV antibody detection Corresponding Author: Microbiology Section, Department of Pathology and Laboratory Medicine, University of Parma, Viale Antonio Gramsci 1, 1 Parma, Italy. Tel Fax address: mariacristina.arcangeletti@unipr.it Downloaded from on July, 01 by guest 1
2 A multicentric clinical study was conducted on representative sera from 1 European and American subjects for the evaluation of new anti-hav enzyme immunoassays from Bio-Rad Laboratories. Comparison with reference DiaSorin S.p.A. tests confirmed the good performance of Bio-Rad assays (.% and.% overall agreement for total antibodies and IgM, respectively). Downloaded from on July, 01 by guest
3 The etiological agent of hepatitis A is a non-enveloped, positive stranded RNA virus (HAV) that is typically transmitted via the fecal-oral route (). HAV infection is still the most common cause of acute viral hepatitis worldwide and remains a serious health problem not only in the developing world, but also in industrialized countries (, ). It can lead to a multiplicity of clinical features, ranging from asymptomatic infection to fulminant fatal disease (1). Over the last decades, improvement in the living conditions of several world populations has prevented young people from acquiring asymptomatic infection (which provides a lifelong protection), leaving them susceptible to hepatitis A infection (, ). With regard to adults, certain categories of people are exposed to a higher risk of infection and therefore subjected to cyclic outbreaks of hepatitis A, such as men who have sexual intercourse with men, both injection and non-injection drug users and travelers returning from developing countries (1,,,, 1, 1, 1, 1). It is also worth mentioning that HAV infected persons with chronic liver disease are likely to develop fulminant hepatitis A (1, 1). This global scenario of hepatitis A epidemiology calls for an increase in research to be carried out in the coming years and measures taken to control and prevent the spread of this infectious disease. In particular, vaccination against hepatitis A is recommended for all the aforementioned high risk categories of people and represents an important tool in the prevention of virus spread and epidemic outbreaks (). Laboratory diagnosis of hepatitis A is mainly based on the detection of antibodies associated with acute and past infection (IgM and IgG, respectively); complementary tests can be used in some cases for the diagnosis of recent infection (, 1). In pre-vaccination programs, however, the detection of total anti-hav antibodies is also critical for establishing whether individuals have acquired immunity and for identifying those susceptible to HAV infection. Downloaded from on July, 01 by guest
4 This study aimed to evaluate the performance of two novel anti-hav enzyme immunoassays developed by Bio-Rad Laboratories (MONOLISA TM Anti-HAV IgM EIA and MONOLISA TM Anti-HAV EIA) and to compare their results to those obtained using the FDA-approved ETI-AB-HAV-IgMK PLUS and ETI-AB-HAVK PLUS assays from DiaSorin S.p.A.. The tests were performed and the results interpreted according to the manufacturers instructions. Relative sensitivity and specificity, as well as agreement between the Bio-Rad and DiaSorin assay results, were calculated excluding unresolved equivocal (concordant and discordant borderline) data; % binomial confidence intervals (CI) were applied to the results. The study was conducted on representative serum samples from 1 European and US subjects from Parma University-Medical School in Italy (), Paul Brousse Hospital in France (), and in the United States (US) of America (). A retrospective study (total antibodies and IgM) was performed on sera (stored at - 0 C) that had been collected from a population with known hepatitis A status: acute (HAV IgM-positive) and past-infected/recovered (HAV IgG-positive) hepatitis A patients. A prospective study (total antibodies and IgM) was conducted on sera from subjects with unknown hepatitis A status. This population consisted of the following categories: General hospitalized ( European); Symptoms of hepatitis (: European and 1 US); High risk for hepatitis A (: European and 0 US); Healthcare workers ( European). A prevalence study (total antibodies) was performed on subjects (the above mentioned European groups of General hospitalized and Healthcare, and a further General hospitalized US individuals), not related to hepatitis infections and representative of the healthy population. Downloaded from on July, 01 by guest
5 Total HAV antibody response was also evaluated in 0 subjects who had received one of the three vaccines licensed in the US (VAQTA : Merck & Co; HAVRIX or TWINRIX vaccines: GlaxoSmithKline). Samples from individuals with unknown hepatitis A status were collected after obtaining their written informed consent and upon protocol approval by the Ethics Committee of the public organizations involved in the study. The results obtained in the retrospective and prospective studies by comparing Bio-Rad and DiaSorin (reference) total antibodies and IgM immunoassays are presented in Table 1. All equivocal (concordant and discordant borderline) results displayed in Table 1 were confirmed by repeating the tests on the same samples, in order to avoid any possible technical problem. Only one sample, belonging to the Past-infected/recovered category, gave different results: initially positive for IgM with Bio-Rad and borderline with DiaSorin test, then positive with both the assays (thus, considered in the statistical analysis). With regard to total antibodies, discrepant results (i.e. reactive with MONOLISA Anti- HAV EIA vs. non-reactive with ETI-AB-HAVK PLUS) were found in the High risk for hepatitis A category and confirmed upon repetition of the tests. Concerning IgM, discrepant results (i.e. reactive with MONOLISA Anti-HAV IgM EIA vs. non-reactive with ETI-AB-HAV-IgMK PLUS) were observed in the Past-infected/recovered, General hospitalized and High risk for hepatitis A categories. The tests were repeated on the same samples and, when possible, complementary assays, such as anti-hav IgG avidity and HAV RNA detection (, 1), were also performed in order to ascertain acute infection (Table ). The relative sensitivity of MONOLISA Anti-HAV EIA (vs. ETI-AB-HAVK PLUS) and MONOLISA TM Anti-HAV IgM EIA (vs. ETI-HA-IgMK PLUS), determined on the samples included in the retrospective and prospective studies, was 0% in both cases (total antibodies: / - CI:.1%-0%; IgM: / - CI:.%-0%). Relative Downloaded from on July, 01 by guest
6 specificity was.% (/0 - CI:.1%-.%) for total antibodies and.% (1/1 - CI:.%-.%) for IgM antibodies. The overall agreement was.% (/1 CI:.%-.%) for total antibodies and.% (1/1 CI:.%-.%) for IgM. HAV antibody prevalence in subjects representative of the healthy population (patients hospitalized with conditions unrelated to hepatitis virus infection and healthcare workers) was estimated with MONOLISA TM Anti-HAV EIA for Europe (N= ) and for the US (N= ) (Figure 1). The results obtained from the above populations show that prevalence is higher in Europe than in the US and that, mostly in the former case, it is related to subject age range, being progressively higher in older individuals, in accordance with data obtained by other Authors (). HAV total antibody response using MONOLISA TM Anti-HAV EIA and ETI-AB-HAVK PLUS was also evaluated in subjects who had received one of the three vaccines licensed in the US (VAQTA, HAVRIX, or TWINRIX vaccines). It is important to note that only a limited number of vaccinated subjects develops a transient IgM anti-hav response (1), while immunized people always produce IgG anti-hav. This is why only total antibodies were assayed in the evaluation of samples from vaccinated populations. Post-vaccination samples from subjects who had received the VAQTA vaccine were assayed and both tests found all samples to be reactive (data not shown). With regard to HAVRIX vaccination, HAV total antibody response was evaluated in pre- and postvaccination samples (two-dose schedule). Once again, coincident results were found with both tests, showing a correct improvement of the HAV antibody response in postvaccination samples (not shown). For the evaluation of TWINRIX ( injections at 0, 1 and months), 1 subjects were enrolled; a pre-vaccination sample was collected the day of the first vaccination dose. A second sample was obtained before the second dose was injected (one month after the first one), while the second and third vaccination-dose Downloaded from on July, 01 by guest
7 samples were not available. With regard to MONOLISA TM Anti-HAV EIA (Figure ), the results show a slight increase in the HAV antibody response after the first injection in the majority of the subjects enrolled in the study (subject 1 was already immunized against HAV before the first vaccination dose); cases (subjects,,, 1) that were found negative after the first dose. The ETI-AB-HAVK PLUS assay gave identical results, except for the borderline values of post-vaccination samples and 1 (data not shown). In summary, data derived from this multicentric study indicate that the MONOLISA Anti- HAV IgM and Anti-HAV (total Ig) EIA (Bio-Rad Laboratories) are specific and sensitive assays which may be used effectively in the laboratory diagnosis of acute or past HAV infection and for the identification of HAV susceptible individuals to be enrolled in vaccination programs. Their performance is comparable with that of ETI-AB-HAVK and IgMK PLUS tests from DiaSorin S.p.A.. Bio-Rad MONOLISA Anti-HAV IgM and Anti- HAV (total Ig) EIA thus represent a valid alternative choice, with the additional advantage of the shorter times required to perform the Bio-Rad tests. At the present time, also the latter assays have been cleared by FDA. The few discrepant results (positive with Bio-Rad vs. negative with DiaSorin tests), mostly related to IgM detection, could be due to a slightly higher sensitivity of the Bio-Rad assays, permitting the detection of low amounts of IgM, that in some cases could persist after the acute stage; however, the possibility of false positive results cannot be ruled out. This work was supported by Bio-Rad Laboratories, Marnes La Coquette, France. The results and conclusions in this report are of the Authors and do not necessarily represent the views of the funding manufacturer. Downloaded from on July, 01 by guest
8 REFERENCES 1. Bouvet, E. 00. Sexual practices and transmission of HAV and HCV. Euro Surveill. :.. Centers for Disease Control and Prevention. 00. Prevention of hepatitis A through active or passive immunization. Recommandation of Advisory Committee on Immunization Practices. MMWR Morb. Mortal. Wkly. Rep. (RR-):1-0.. Chodick, G., S. Ashkenazi, and Y. Lerman. 00. The risk of hepatitis A infection among healthcare workers: a review of reported outbreaks and sero-epidemiologic studies. J. Hosp. Infect. :1-0.. FitzSimons, D. Hendrickx, G., Vorsters, A., Van Damme, P., 0. Hepatitis A and E: Update on prevention and epidemiology. Vaccine. :-.. Hollinger, F. B., B. Bell, D. Levy-Bruhl, D. Shouval, S. Wiersma, and P. Van Damme. 00. Hepatitis A and B vaccination and public health. Journal of Viral Hepatitis. 1 (Suppl.1):1-.. Jacobsen, K. H., and J. S. Koopman. 00. The effects of socioeconomic development on worldwide hepatitis A virus seroprevalence patterns. Int. J. Epidemiol. : Jacobsen, K. H., and Wiersma, S. T. 0. Hepatitis A virus seroprevalence by age and world region, and 00. Vaccine. :-.. Latimer, W. W., A. G. Moleko, A. Melnikov, M. Mitchell, S. G. Severtson, S. von Thomsen, C. Graham, D. Alama, and L. Floyd. 00. Prevalence and correlates of hepatitis A among adult drug users: the significance of incarceration and race/ethnicity. Vaccine. :1-.. Nainan, O. V., G. Xia, G. Vaughan, and H. S. Margolis. 00. Diagnosis of Hepatitis A Virus Infection: a Molecular Approach. Clin. Microbiol. Rev. 1 (1): -. Downloaded from on July, 01 by guest
9 Nelson, K. E. 00. Global Changes in the Epidemiology of Hepatitis A Virus Infections. Clin. Infect. Dis. :1-.. Nothdurft, H. D., A. L. Dahlgren, E. A. Gallagher, H. Kollaritsch, D. Overbosch, M. L. Rummukainen, P. Rendi-Wagner, R. Steffen, and P. Van Damme; ad hoc Travel Medicine Expert Panel for ESENEM. 00. The risk of acquiring hepatitis A and B among travelers in selected Eastern and Southern Europe and non-european Mediterranean countries: review and consensus statement on hepatitis A and B vaccination. J. Travel. Med. 1:-1 1. Reimer, J., J. Lorenzen, B. Baetz, B. Fischer, J. Rehm, C. Haasen, and M. Backmund. 00. Multiple viral hepatitis in injection drug users and associated risk factors. J. Gastroenterol. Hepatol. : Roque-Alfonso, A. M., V. Mackiewicz, and E. Dussaix. 00. Detection of immunoglobulin M antibody to hepatitis A virus in patients without acute hepatitis A: the usefulness of specific immunoglobulin G avidity. Clin. Infect. Dis. :- 1. Shim, M., I. Khaykis, J. Park, and E. J. Bini. 00. Susceptibility to hepatitis A in patients with chronic liver disease due to hepatitis C virus infection: missed opportunities for vaccination. Hepatology. :-. 1. Stene-Johansen, K., G. Tjon, E. Schreier, V. Bremer, S. Bruisten, S. L. Ngui, M. King, R. M. Pinto, L. Aragonès, A. Mazick, S. Corbet, L. Sundqvist, H. Blystad, H. Norder, and K. Skaug. 00. Molecular epidemiological studies show that hepatitis A virus is endemic among active homosexual men in Europe. J Med Virol. :-. 1. Taylor, R. M., T. Davern, S. Munoz, S. H. Han, B. McGuire, A. M. Larson, L. Hynan, W. M. Lee, R. J. Fontana, and US Acute Liver Failure Study Group. 00. Fulminant hepatitis A virus infection in the United States: Incidence, prognosis, and outcomes. Hepatology. :1-1. Downloaded from on July, 01 by guest
10 1. Toovey, S. 00. Travelling to Africa: health risks reviewed. Travel Med Infect Dis. : Victor, J. C., T. Y. Surdina, S. Z. Suleimenova, M. O. Favorov, B. P. Bell, and A. S. Monto. 00. Person-to-person transmission of hepatitis A virus in an urban area of intermediate endemicity: implications for vaccination strategies. Am J Epidemiol. 1:0-. Downloaded from on July, 01 by guest
11 TABLE 1. Anti-HAV total antibodies and IgM in sera from subjects with known (retrospective study) and unknown (prospective study) hepatitis A status SPECIMEN CATEGORY RETROSPECTIVE STUDY Past-infected/ recovered HAV No. of samples ETI-AB-HAVK PLUS TOTAL ANTIBODIES MONOLISA Anti-HAV EIA R NR R NR No. of samples with equivocal ETI-AB-HAV IgMK PLUS IgM MONOLISA Anti-HAV IgM EIA results * R NR R NR No. of samples with equivocal results * Acute hepatitis A Total for study type PROSPECTIVE STUDY General hospitalized population Symptoms of hepatitis population High risk for hepatitis A population Healthcare workers Total for study type 0 01 Total for all study types R: Reactive, NR: Non-reactive *: Equivocal (concordant and discordant borderline) results were confirmed by repeating the tests on the same samples, except for 1 sample in the Pastinfected/recovered HAV category, initially positive for IgM with Bio-Rad and borderline with DiaSorin test, then positive with both the assays. Confirmed equivocal results were excluded from statistical analysis. Downloaded from on July, 01 by guest
12 TABLE. Analysis of discrepant IgM samples from subjects with known and unknown hepatitis A status SPECIMEN CATEGORY Past-infected/recovered population General hospitalized population Symptoms of hepatitis population Demographic (gender, age) F, F, M, M, F, 1 M, F, 1 MONOLISA Anti-HAV IgM EIA Ratio* Interpretation Sample OD ETI-AB-HAV-IgMK PLUS Cutoff OD Interpretation # 1.1 R NR 1.0 BRD NR 1. R NR 1.01 BRD NR 1. R NR 1.1 R NR 1.1 R NR 1.1 R NR.0 R NR. R NR 1. R NR 1. R NR. R NR n.e. - n.e. - - Anti- HAV IgG avidity Complementary Information HAV RNA Total HAV antibodies n.e. n.e. R n.e. n.e. R High Negative R High Negative R High Negative R n.e. n.e. R n.e. n.e. R F: female; M: male; R: Reactive, NR: Non-reactive, BRD: borderline, n.e.: not evaluated; OD: optical density. * Results are expressed as the ratio of the sample OD (S) to the cut-off OD (CO): (S/CO). The presence or absence of anti-hav IgM antibodies (MONOLISA Anti-HAV IgM EIA non-competitive test) was determined as follows: specimens with ratio values greater than or equal to 1.1 were considered as reactive (antibodies present) and those with ratios less than 0. as non-reactive (antibodies absent). Specimens with ratios greater than or equal to 0. times the CO value and less than 1.1 times the CO value (0. < ratio < 1.1) were considered to be equivocal (borderline). For each run, the CO was calculated as the mean of OD values (that must be greater than 0. and less than.) of the positive cut-off calibrator divided by. For each run, the CO was determined by adding 0.0 to the mean of the calibrator absorbance values (that must be greater than and less than 0.). # The presence or absence of anti-hav IgM antibodies (ETI-HA-IgMK PLUS non-competitive test) was determined by comparing the OD value of the patient serum with the CO value. Patient specimens with absorbance values less than the CO value (and not within -0% of the CO) were considered as non-reactive, and those with values greater than the CO as reactive. Absorbance values ranging between 0 and 0% below the CO were considered as equivocal (borderline). The presence of HAV RNA was evaluated using a One-Step RT-PCR kit (Qiagen) amplifying a 1-bp fragment that encompasses the VP1/A junction of the HAV genome. The sensitivity of the RT-PCR assay was IU/ml, as assessed on serial dilutions of the World Health Organization HAV RNA standard. The presence of HAV total antibodies was confirmed using the DiaSorin ETI-AB-HAVK PLUS (competitive format) reference immunoassay. In this case, the CO was calculated for each run as the mean absorbance of three calibration values (that must be greater than the positive control OD and less than 0% of the negative control OD). The presence or absence of anti-hav antibodies was determined by comparing the OD value of the patient serum with the CO value: absorbance values less than the CO were considered as reactive, and those with values greater than CO (and not within 0% above the CO) as non-reactive. Absorbance values ranging between 0 and 0% above the CO were considered as equivocal (borderline). Downloaded from on July, 01 by guest
13 0% / / % of total HAV Ab reactive 0% 0% 0% 0% 0% / / 1/ /1 / 1/ 0/ /1 1/ / > Age (years) % Reactive Europe (N= ); % Reactive US (N= ) Downloaded from on July, 01 by guest
14 1 1 subjects Ratio Monolisa Anti- HAV EIA 0 Month 1 Month Downloaded from on July, 01 by guest
15 FIGURE CAPTIONS Figure 1. HAV antibody prevalence in Europe (N= ) and in US (N= ) using MONOLISA TM Anti-HAV EIA. The study was performed on subjects representative of healthy population (patients hospitalized with conditions unrelated to hepatitis virus infection and healthcare workers). For each age range category, the number of reactive subjects (presence of total anti-hav antibodies) to the total subject number is displayed on each histogram. Figure. HAV antibody response following TWINRIX vaccination. HAV total antibody response to TWINRIX vaccination (Glaxo SmithKline; three-doses schedule) was evaluated on 1 subjects using MONOLISA anti-hav EIA. A pre-vaccination sample ( 0 Month ) was collected the day of the first vaccination dose. A second sample ( 1 Month ) was obtained before the second dose was injected (one month after the first dose). The second and third vaccination dose samples were not available. Downloaded from on July, 01 by guest
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