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JAIDS Journal of Acquired Immune Deficiency Syndromes:
Basic Science

Signal-Boosted Qualitative Ultrasensitive p24 Antigen Assay for Diagnosis of Subtype C HIV-1 Infection in Infants Under the Age of 2 Years

Zijenah, Lynn S PhD*; Tobaiwa, Ocean BSc*; Rusakaniko, Simbarashe PhD†; Nathoo, Kusum J MD‡; Nhembe, Margaret SRN‡; Matibe, Petronella SRN‡; Katzenstein, David A MD§

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Author Information

From the Departments of *Immunology, †Community Medicine, and ‡Paediatrics, Division of Infectious Diseases, College of Health Sciences, University of Zimbabwe, Harare, Zimbabwe; and §AIDS Research, Stanford University Medical School, Stanford, CA.

Received for publication December 29, 2004; accepted January 25, 2005.

Supported in part by a grant from the Doris Duke Charitable Foundation.

The Medical Research Council of Zimbabwe approved this study. None of the authors have a financial conflict of interest.

Reprints: Lynn S. Zijenah, Department of Immunology, College of Health Sciences, University of Zimbabwe, Mazoe Street, PO Box A 178, Avondale, Harare, Zimbabwe (e-mail: LZIJENAH@HEALTHNET.ZW).

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Abstract

The gold standard for diagnosis of HIV-1 infection in infants under the age of 2 years is DNA or reverse transcriptase polymerase chain reaction. However, these tests are expensive and therefore not available in resource-limited countries. With the increasing availability of antiretroviral drugs for prevention of mother-to-child transmission of HIV and treatment of AIDS in resource-poor countries, there is an urgent need to develop cheaper, alternative, and cost-effective laboratory methods for early diagnosis of infant HIV-1 infection that will be useful in identifying infected infants who may benefit from early cotrimoxazole prophylaxis or commencement of antiretroviral therapy. We evaluated an alternative method, the enzyme-linked immunosorbent assay-based qualitative ultrasensitive p24 antigen assay for diagnosis of subtype C HIV-1 infection in infants under the age of 2 years using DNA polymerase chain reaction as the reference method. The assay showed a sensitivity of 96.7% (95% CI: 93.0-100) for detection of HIV-1 infection among infants 0-18 months of age with a specificity of 96.1% (95% CI: 91.7-100). These evaluated parameters were not statistically different between infants aged 0-6 and 7-18 months. The ultrasensitive p24 antigen assay is a useful diagnostic test for detection of HIV-1 infection among infants aged 0-18 months.

The gold standard for diagnosis of HIV-1 infection in infants under the age of 2 years is DNA polymerase chain reaction (PCR) or reverse transcriptase (RT)-PCR.1-3 These molecular diagnostic assays are not only expensive but require specialized laboratory personnel training and equipment, making them unavailable in developing countries, mainly because of cost. With the increasing availability of single-dose nevirapine for prevention of mother-to-child transmission (MTCT)4 of HIV and antiretroviral drugs for treatment of AIDS in resource-poor countries, there is an urgent need to develop cheaper, alternative, and cost-effective laboratory methods for early diagnosis of infant HIV-1 infection that can be used in identifying infected infants who may benefit from early cotrimoxazole prophylaxis or initiation of highly active antiretroviral therapy (HAART).

Prior to the development of DNA PCR and RT-PCR, HIV-1 p24 antigen tests were employed as a means for detection of HIV-1. Nevertheless, the variations of this assay revealed varying degrees of sensitivity and specificity. HIV-1 p24 antigen is mainly bound to the antibody as an immune complex, resulting in underdetection of the antigen by conventional methods.5-8 Acid treatment of serum or plasma to disrupt the immune complex improved the sensitivity of the p24 antigen assay; however, the assay is considered insufficient for detection of infant HIV-1 infection.9-13

Steps to enhance sensitivity of the assay include the development of an ultrasensitive p24 antigen assay, which involves heat-mediated immune complex dissociation and signal amplification-boosted enzyme-linked immunosorbent assay (ELISA), produced by Perkin Elmer Life Sciences (Boston, MA) as a research reagent with a potential value for diagnosis of perinatal HIV infection.14 This assay, which was developed based mainly on HIV-1 subtype B virus, has been validated in countries where subtypes A, B, D, and C predominate.15-18 A similarly modified immune complex dissociated p24 antigen assay using Vironostika HIV-1 p24 antigen ELISA kit was also validated in Thailand, where HIV-1 subtype E predominates.19 The main objective of this study was to evaluate the qualitative ultrasensitive p24 antigen assay for diagnosis of HIV-1 infection in infants under the age of 2 years in Zimbabwe using DNA PCR as the reference method.

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MATERIALS AND METHODS

Study Cohort

The infant specimens used in this study were obtained from 2 independent prospective studies; the short-course zidovudine (AZT) study and the Pediatric AIDS Clinical Definition study (PACD). The infants included in the study were under the age of 2 years. All the infants were breast-feeding at the time of specimen collection. The short-course AZT study was aimed at preventing MTCT of HIV and was conducted between 1999-2002. In the AZT study, mothers received short-course AZT starting at 36 weeks' gestation and continuing throughout labor. Their infants received AZT for 7 days.

In the PACD study, hospitalized children aged between 2 and 18 months were prospectively enrolled into the study, between 2002 and 2003, following informed consent from their mothers. The mothers of these children did not receive antiretroviral therapy for prevention of MTCT or for HIV disease. The PACD study is a hospital-based cross-sectional survey employing case-control analysis. Children presenting in the moribund state, requiring immediate resuscitation, or those with known HIV status or those whose mothers/guardians refused to sign the informed consent were excluded from the study. The main objective of the PACD study is to identify clinical symptoms associated with HIV-1 infection in infants under the age of 18 months, which may be used in the absence of laboratory tests, for HIV-1 diagnosis.

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Blood Collection and Processing

Two aliquots of whole blood were collected in EDTA from each of the 164 infants in the combined short-course AZT and PACD studies. One aliquot of infant whole blood was centrifuged at 200 g for 10 minutes to obtain plasma that was then stored at −80°C until used for the p24 antigen assay. The 2nd whole blood aliquot was used for DNA PCR.

The laboratory tests described below were conducted in a blind fashion.

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DNA PCR Analysis

DNA PCR Roche amplification assay version 1.5 (Roche Diagnostics, Branchburg, NJ) was employed as the reference standard for diagnosis of infant HIV-1 infection status. DNA extraction, amplification, and detection were performed and results interpreted following the manufacturer's instructions as we have previously described.20,21

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Ultrasensitive p24 Antigen Assay

The p24 antigen ultrasensitive assay was carried out in accordance with the manufacturer's instructions (Perkin Elmer Life Sciences, Boston, MA). Briefly, 50-μL plasma test samples, kit controls, and kit reference standards were each diluted with 250 μL Triton X-100 0.5% (included in the kit) and the specimens boiled for 5 min at 100°C in a dry heat block. Samples were then cooled for 5 min and 250 μL transferred to microplate wells coated with a highly specific mouse monoclonal antibody to HIV-1 p24 antigen. After incubation at room temperature for 2 hours, the microplate was then washed using an automated microplate washer (Bio-Tech Instruments, Montreal, Quebec, Canada) and reincubated with 100 μL of biotinylated detector antibody added to all wells except the substrate blank well. Following further washing to remove unbound antibody, 100 μL of streptavidin-horse peroxidase conjugate was added to each well, and the microplate was incubated for 15 min at room temperature. The microplate was then washed, and 100 μL of orthophenylenediamine-HCl was added to each well. The microplate was then inserted into the plate reader for kinetic reading using the Quanti-kin detection software for HIV-1 p 24 ELISA kit (Perkin Elmer Life Sciences). After 30 min of incubation, the reaction was stopped by adding 100 μL of stop solution (included in the kit) to each well and endpoint reading was performed using the Quanti-kin software. The software allows automatic computer-driven data collection from plate reader and quantitation of sample measurements. The results are both quantitative, expressed as concentration of p24 antigen, and qualitative, expressed as HIV-1 positive or negative. For the comparative evaluation study, we were mainly interested in the qualitative results.

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Infant Grouping

In the current study, in addition to overall evaluation of samples obtained from all the infants aged 0-18 months, the evaluated parameters were also compared based on infant age groups 0-6 and 7-18 months.

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Statistical Analysis

Specificity was defined as the percentage of reference standard HIV-negative samples that were negative by the assay under evaluation. Sensitivity was defined as the percentage of reference standard HIV-positive samples found reactive by assay under evaluation. Test efficiency (TE) refers to the overall ability of a test to correctly identify all positives and negatives (the absence of false positives and false negatives). It is a combination of the sensitivity and the specificity of an assay and gives an idea of the total effectiveness of the assay. Positive predictive value (PPV) was defined as the probability that a specimen contains p24 antigen ratio <1 when the test was DNA positive. Negative predictive value (NPV) was defined as the probability that a specimen does not have detectable p24 antigen when the test was DNA PCR negative.

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RESULTS

Of the 164 infant specimens tested using DNA PCR, 91 were HIV-1 positive and 73 were HIV-1 negative. The 91 PCR-positive infants included 9 infants who had evidence of in utero transmission as determined by serial DNA PCR of birth and subsequent samples tested in longitudinal short-course AZT MTCT studies (Zijenah et al, unpublished data). The median age of these infants at specimen collection was 7.0 months (interquartile range [IQR]: 4-12) and 5.0 months (IQR: 3-13) for HIV infected and uninfected, respectively (P = 0.20).

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DNA PCR Versus Ultrasensitive p24 Antigen Assay

The detection range of the p24 antigen assay is 1500-625,000 fg/mL. Eighty-eight of the 91 PCR-positive samples contained sufficient signal in the p24 ultrasensitive assay to be considered positive for evidence of infection. Seventy-six samples were p24 antigen negative. The 3 false-negative samples by p24 antigen assay were repeat-tested with reproducible negative results. These 3 specimens also had undetectable virus load (<400 copies/mL) using Roche Amplicor Monitor version 1.5 (Roche Diagnostics, Branchburg, NJ) as we have previously described.22 The overall (infants aged 0-18 months) specificity and sensitivity of the p24 antigen assay were 96.1% (95% CI: 91.7-100) and 96.7% (95% CI: 93.0-100), respectively, with PPV and NPV of 91.6 and 98.5%, respectively, and a TE of 96.4% (95% CI: 93.6-99.2). These evaluated parameters for the p24 antigen assay were also compared based on infant age group (Table 1). The specificity and sensitivity among the infants aged 0-6 months were 96.9% (95% CI: 90.8-100) and 98.1% (95% CI: 94.6-100), respectively, with a PPV and NVP of 93.3 and 99.2%, respectively, and a TE of 97.7% (95% CI: 94.5-100). For the infants aged 7-18 months, the specificity and sensitivity were 91.1% (95% CI: 82.8-99.4) and 89.5% (95% CI: 79.9-99.2), respectively, with a PPV and NVP of 81.7 and 95.1%, respectively, and a TE of 90.4% (95% CI: 84.0-96.6). Comparison of the sensitivity, specificity, and TE between the infants aged 0-6 months and those aged 7-18 months showed that the 95% CIs overlap between the groups, which imply no statistically significant difference in these 2 age groups.

Table 1
Table 1
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DISCUSSION

In resource-poor countries, the major constraint in the use of DNA PCR for diagnosis of HIV-1 infection in infants under the age of 18 months is the cost of the equipment and the reagents. In addition, highly trained laboratory personnel and stringent quality assurance measures are needed to run this assay for routine diagnosis of HIV infection in infants.

In Zimbabwe, ELISA is routinely performed in both public and private laboratories for diagnosis of various infections including HIV-1. However, because of the transplacental transfer of maternal IgG antibodies, which may persist in infants for up to 18 months, ELISA is not suitable for diagnosis of HIV-1 infection in these infants. Thus a virus-specific test is needed to differentiate HIV-1 seropositivity based on maternal antibodies vs. actual infant infection.

The ultrasensitive p24 antigen assay is an ELISA-based method; laboratories that routinely use ELISA for diagnosis of other infections can easily adopt it. This method is relatively simple, easy to follow, and cheaper than DNA PCR when considering the initial cost of equipment, reagents, and training of laboratory personnel for the latter. Indeed, currently the cost of DNA PCR per test sample in Zimbabwe is US $50 compared with US $10 for the ultrasensitive p24 assay.

The 3 studies that have validated the Perkin Elmer HIV-1 Ultra antigen assay for diagnosis of HIV infection in infants have reported a sensitivity ranging from 97%-99% and a specificity of 98%-100%.16-18 In 2 of these studies, the evaluated parameters were for infants aged 0 to >52 weeks.16,18 In the South African study, the infants were aged 6-28 weeks.17 The overall sensitivity (98%) and specificity (97%) for the infants aged 0-72 weeks in the current study are comparable to those reported in the 3 above-mentioned studies. In the current study, when these parameters were evaluated based on 2 infant age groups, the sensitivity, specificity, and TE for those aged 0-6 months were not significantly different from those of those aged 7-18 months. The majority of infant HIV infection occurs in utero and intrapartum.23 However, several studies conducted in Africa have reported that transmission through breast-feeding is quite substantial.24-28 The 0- to 6-month period would identify infants with in utero, intrapartum, and early postpartum HIV infection. In the current study, all the 9 infants with in utero HIV-1 infection were positive by the p24 antigen assay. However, although we detected HIV-1 infection among infants 7-18 months of age, we do not know the precise timing of infection in these infants, as we did not have specimens collected at earlier ages.

In summary, the ultrasensitive p24 antigen assay is a useful diagnostic test for detection of HIV-1 subtype C infection among infants aged 0-18 months. Clearly, this relatively affordable test will be useful in identifying infected infants who may benefit from early cotrimoxazole prophylaxis or commencement of HAART and for management of HIV-infected infants in developing countries in general.

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Keywords:

infant HIV diagnosis; DNA polymerase chain reaction; p24 antigen; Zimbabwe

© 2005 Lippincott Williams & Wilkins, Inc.

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