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Virology

Diagnostic Accuracy of Rapid Antigen Detection Tests for Respiratory Syncytial Virus Infection: Systematic Review and Meta-analysis

Caroline Chartrand, Nicolas Tremblay, Christian Renaud, Jesse Papenburg
Y.-W. Tang, Editor
Caroline Chartrand
aDepartment of Pediatrics, Centre Hospitalier Universitaire Sainte-Justine, Université de Montréal, Montreal, QC, Canada
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Nicolas Tremblay
bUnité d'immunovirologie moléculaire, Centre de recherche du Centre hospitalier de l'Université de Montréal, Montreal, QC, Canada
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Christian Renaud
aDepartment of Pediatrics, Centre Hospitalier Universitaire Sainte-Justine, Université de Montréal, Montreal, QC, Canada
cDepartment of Microbiology, Centre Hospitalier Universitaire Sainte-Justine, Université de Montréal, Montreal, QC, Canada
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Jesse Papenburg
dDepartments of Pediatrics and Microbiology, Montreal Children's Hospital, Montreal, QC, Canada
eDepartment of Epidemiology, Biostatistics and Occupational Health, McGill University, Montreal, QC, Canada
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Y.-W. Tang
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DOI: 10.1128/JCM.01816-15
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ABSTRACT

Respiratory syncytial virus (RSV) rapid antigen detection tests (RADT) are extensively used in clinical laboratories. We performed a systematic review and meta-analysis to evaluate the accuracy of RADTs for diagnosis of RSV infection and to determine factors associated with accuracy estimates. We searched EMBASE and PubMed for diagnostic-accuracy studies of commercialized RSV RADTs. Studies reporting sensitivity and specificity data compared to a reference standard (reverse transcriptase PCR [RT-PCR], immunofluorescence, or viral culture) were considered. Two reviewers independently extracted data on study characteristics, diagnostic-accuracy estimates, and study quality. Accuracy estimates were pooled using bivariate random-effects regression models. Heterogeneity was investigated with prespecified subgroup analyses. Seventy-one articles met inclusion criteria. Overall, RSV RADT pooled sensitivity and specificity were 80% (95% confidence interval [CI], 76% to 83%) and 97% (95% CI, 96% to 98%), respectively. Positive- and negative-likelihood ratios were 25.5 (95% CI, 18.3 to 35.5) and 0.21 (95% CI, 0.18 to 0.24), respectively. Sensitivity was higher in children (81% [95% CI, 78%, 84%]) than in adults (29% [95% CI, 11% to 48%]). Because of this disparity, further subgroup analyses were restricted to pediatric data (63 studies). Test sensitivity was poorest using RT-PCR as a reference standard and highest using immunofluorescence (74% versus 88%; P < 0.001). Industry-sponsored studies reported significantly higher sensitivity (87% versus 78%; P = 0.01). Our results suggest that the poor sensitivity of RSV RADTs in adults may preclude their use in this population. Furthermore, industry-sponsored studies and those that did not use RT-PCR as a reference standard likely overestimated test sensitivity.

INTRODUCTION

Acute respiratory infection (ARI) due to respiratory syncytial virus (RSV) is a leading cause of emergency department (ED) visits and hospitalizations in infants and children (1–3). RSV also produces substantial morbidity and mortality among the elderly and adults with underlying medical conditions (4, 5).

Accurate and prompt diagnosis of RSV ARI can have important benefits for patient care. Because concurrent serious bacterial infection with RSV is uncommon, especially in children (6), a timely diagnosis of RSV ARI should diminish unnecessary antibiotic use (7–9). It may also minimize ancillary testing (10), decrease hospital stay durations (11), and permit prompt implementation of cohort assignment for the purpose of limiting nosocomial transmission within hospitals and long-term-care facilities (13–16, 57). Laboratory testing of respiratory secretions is required for confirmation of RSV infection because its seasonality and nonspecific clinical manifestations may overlap those of other viral and bacterial causes of ARI (17, 18).

There are currently four RSV diagnostic modalities in clinical use. Viral culture was long considered the gold standard for RSV diagnosis, but it has a turnaround time of 3 to 7 days (1 to 2 days for shell vial culture) (19). Reverse transcriptase PCR (RT-PCR) has a much shorter turnaround time (hours) than and analytic and clinical sensitivities superior to those of culture; it is now the reference diagnostic method for respiratory virus detection (17, 20). However, only ∼15% of clinical laboratories participating in the United States National Respiratory and Enteric Virus Surveillance System (NREVSS) presently identify RSV by RT-PCR because of its associated costs and because of the specialized equipment and expertise required (21). Immunofluorescence (IF) testing for RSV detection is potentially faster than RT-PCR but is less sensitive and requires considerable technical skill (19). Finally, a number of commercially developed rapid antigen detection tests (RADTs) are currently available for the diagnosis of RSV ARI. These assays are easy to perform and provide results in less than 30 min, and several of them have the potential for point-of-care use (22). Although they are less sensitive than culture, their speed and ease of use have made them an integral part of the diagnostic algorithm of many clinical laboratories (21, 22). It is thus crucial for clinicians and for public health surveillance systems that rely on such tests for decision-making to understand their performance characteristics and the factors that might influence them.

To date, the literature evaluating the performance characteristics of RSV RADTs has not yet been systematically reviewed. Therefore, the primary objective of this systematic review and meta-analysis was to summarize the available evidence on the diagnostic accuracy of commercialized RADTs for detecting RSV infection in patients with ARI. We also aimed to determine if patient, test, and methodological factors (e.g., patient age, type of specimen, commercial brand, clinical presentation, duration of symptoms, point-of-care testing, industry study sponsorship, and genotype of infecting RSV strain) might influence RADT accuracy estimates.

MATERIALS AND METHODS

Prior to conducting this study, a protocol was prepared according to standard guidelines for the systematic review of diagnostic studies (23, 24). The PRISMA statement was used for preparing this report (25).

Information sources and searches.PubMed and EMBASE were searched for data added from their inception through November 2013. An update of the search, performed through April 2015, was conducted in PubMed. Studies published in either English or French were considered. The search strategy was designed with the help of an experienced librarian and contained search terms for RSV infection and search terms for rapid diagnostic immunoassays, including the most common brand names (see Table S1 in the supplemental material). Additionally, the reference list of all included studies and relevant recent narrative reviews was manually searched for additional studies.

Eligibility criteria and study selection.Studies were considered for inclusion if they assessed the diagnostic accuracy of a commercial rapid immunoassay for RSV in patients with suspected ARI. RADT was defined as any commercialized immunoassay that identifies RSV antigen in respiratory specimens in 30 min or less. In-house tests and precommercial versions were excluded since they are not widely available and may not be standardized. Acceptable reference standards included viral culture, RT-PCR, and IF. Studies were excluded if the rapid test was itself part of a composite reference standard (incorporation bias) or if only rapid-test-negative samples were tested with the reference standard (partial verification bias). Studies were also excluded if they pertained to patients without respiratory illness.

Only original studies that described their methods and reported enough data for the construction of the standard two-by-two table were included. Editorials, letters to the editors, and conference abstracts were excluded since they usually contained insufficient information on many important data items relevant to the investigation of sources of heterogeneity (such as patient characteristics, type of specimen, point-of-care use, etc.) and the ascertainment of methodological quality (blind procedures, patient selection, etc.). Attempts were made to contact the authors if there was insufficient information to construct the two-by-two table. Of the 3 authors contacted, 2 provided additional data.

Following the electronic database search, the title and abstract were screened by one reviewer (C. Chartrand). Full-text articles of relevant citations were obtained and independently assessed for eligibility by two reviewers (C. Chartrand and N. Tremblay). Disagreements were solved by consensus or by involvement of a third reviewer (J. Papenburg).

Data extraction and assessment of the risk of bias.A data extraction form was created and initially used for pilot purposes with a subset of 5 studies by two reviewers (C. Chartrand and J. Papenburg) before being finalized. Two reviewers (C. Chartrand and N. Tremblay) independently extracted data from all included studies and assessed risk of bias. Disagreements were solved by consensus or by involvement of a third reviewer (J. Papenburg).

In the data collection process, the following assumptions or simplifications were applied. In determining the reference standard, traditional viral culture and shell vial culture were considered together, regardless of the cell line used. Similarly, RT-PCR and immunofluorescence were each considered as a whole, independently of the kit or protocol used. If separate information was available for two or more reference standards, RT-PCR was chosen in priority, because of its superior sensitivity and specificity, followed by immunofluorescence and then viral culture. The study population was considered to be pediatric if most (>85%) of the study subjects were younger than 21 of age or if the investigation was carried out in a pediatric hospital. Point-of-care testing was defined as a test done outside a formal laboratory setting by personnel other than trained laboratory personnel. Specimens were considered to have been collected during the epidemic season for RSV if they were collected during winter or early spring. A study was considered to have been industry sponsored if the industry funded the study or provided index tests to be used in the study.

The risk of bias of included studies was assessed using the Quality Assessment of Diagnostic-accuracy studies (QUADAS) 2 tool (26). Risk of bias assessment was used to present an overall picture of the quality of the included studies.

Data synthesis and analysis.Data were extracted to construct two-by-two tables, which were used to calculate the sensitivity and specificity of the rapid tests in each study. The sensitivity and specificity estimates were pooled across studies using a bivariate random-effects regression model (27). The bivariate model takes into consideration the potential tradeoff between sensitivity and specificity by incorporating this negative correlation into the analysis. Since heterogeneity is usually expected in meta-analysis of accuracy diagnostic studies, a random-effects model is generally preferred (27). The model was also used to draw a summary receiver operating curve plot to graphically depict each study's sensitivity and specificity, along with the summary point. Analyses were conducted using the user-written command midas in STATA (Stata Corp., TX, USA).

Some articles (16 of 71) compared two to four rapid tests using the same specimens. Since inclusion of these in our meta-analysis would have resulted in (at least) doubled counting results from certain studies, one rapid test comparison was selected per study. After we carried out a sensitivity analysis to assess the impact on the overall accuracy of systematically selecting the most (and then the least) accurate test, the most common test was selected, favoring those still commercially available.

Substantial heterogeneity in levels of test accuracy was expected, and subgroup analyses were planned to attempt to explain the heterogeneity. The following variables were selected a priori as potential sources of heterogeneity: population age (children versus adults), genotype of circulating RSV strain (type A versus type B), brand of rapid test, type of respiratory specimen, duration of symptoms before testing, reference standard used, point-of-care testing, setting and season during which the test was carried out, blind procedures, and industry sponsoring. These variables were added as covariates to the bivariate model, providing enough studies were available in each subgroup. Summary sensitivity and specificity estimates were calculated for each level of a particular covariate, along with their 95% confidence intervals. A P value below 0.05 was used to decide whether there were statistically significant differences in accuracy (joint sensitivity and specificity) across the levels of a particular covariate.

RESULTS

Study selection.After we screened titles and abstracts, 192 articles were eligible for full text review. Of these, 62 articles (28–89) were included in the study (Fig. 1). The update of the search in April 2015 yielded 9 new articles (90–98). The full list of excluded studies, with reasons for exclusion, is available from us upon request.

FIG 1
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FIG 1

Study selection. A flow chart summarizing evidence search and study selection is shown. (Flow diagram template from reference 25; for more information, see http://www.prisma-statement.org/.)

Study characteristics.Table 1 presents the main characteristics and results of the 71 included studies, while Table 2 summarizes the distributions of the main variables of interest. Most (83%) studies were conducted in children, and very few (3%) looked specifically at the adult population. Less than half (44%) of the studies gave any information about the clinical presentation of the included patients, and very few (8%) provided information on the duration of symptoms before testing. Fifteen different rapid tests were evaluated by the included studies. The most frequently studied were the Abbott TestPack RSV (Abbott Laboratories, North Chicago, IL) (23 studies), the Directigen tests (Directigen RSV [20 studies] and the newer Directigen EZ RSV [8 studies] [Becton Dickinson, Franklin Lakes, NJ]), and the Binax NOW RSV (Binax, Inverness Medical, Portland ME) (16 studies). RT-PCR was the reference standard in 41% of the studies, while immunofluorescence and culture were each used in half of the remaining studies.

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TABLE 1

Characteristics of 71 individual studies included in the reviewa

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TABLE 2

Characteristics of 71 included studies

Risk of bias of included studies.Figure 2 presents an overview of the risk of bias of included studies, using the QUADAS-2 criteria. Because of our inclusion criteria, all included studies used an appropriate reference standard. Since culture, immunofluorescence, and RT-PCR were considered to be objective tests, whether or not they were interpreted without knowledge of the results of the index test was deemed not to impact the risk of bias assessment. However, only 61% of the included studies reported that index test results were interpreted without knowledge of the results of the reference standard, an important potential source of bias with the use of the nonautomated colorimetric tests (99). Patient selection (consecutive or random) and their applicability for the research question were difficult to ascertain for many studies, but very few (3 studies) used a clear case control design, which, by creating an extreme contrast, can overestimate a test's accuracy.

FIG 2
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FIG 2

Risk of bias of included studies. Data represent the risk of bias of included studies as assessed by reviewers using the Quality Assessment of Diagnostic Accuracy Studies (QUADAS) 2 tool.

Synthesis of results.Overall, rapid immunoassays for RSV demonstrated pooled sensitivity of 80% (95% CI, 76 to 83) and pooled specificity of 97% (95% CI, 96 to 98). This corresponds to a positive likelihood ratio of 25.5 (95% CI, 18.3 to 35.5) and a negative likelihood ratio of 0.21 (95% CI, 0.18 to 0.24). Systematically choosing the most accurate test or the least accurate test in cases in which a study evaluated two or more rapid tests did not significantly change the overall accuracy (for the best tests, pooled sensitivity was 80% [95% CI, 77 to 83] and pooled specificity was 97% [95% CI, 95 to 98]; for the worst tests, pooled sensitivity was 79% [95% CI, 75 to 82] and pooled specificity was 96% [95% CI, 95 to 98]). As shown in the summary receiver operating characteristic (SROC) plot in Fig. 3, there was a greater variation in sensitivity (from 12.2% to 98.3%) than specificity (from 67.1% to 100%) across studies, with only 13% of the reports indicating specificity estimates below 85%. Forest plots of individual studies and pooled sensitivity and specificity estimates are presented in Fig. S1 in the supplemental material.

FIG 3
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FIG 3

Hierarchical summary receiver operating characteristic curve plot of RSV rapid antigen detection test diagnostic-accuracy studies. Individual studies (n = 71) are shown as open circles. The summary operating point is shown as a closed diamond (with surrounding 95% confidence and prediction contours), representing sensitivity (SENS) and specificity (SPEC) estimates pooled by using a bivariate random-effects regression model. The hierarchical summary receiver operating characteristic curve (SROC) is shown as a solid line. AUC, area under the curve.

Investigation of heterogeneity.In an attempt to explain the observed heterogeneity in test accuracy (mainly in terms of sensitivity), subgroup analyses were conducted. Table 3 presents the accuracy estimates for the different subgroups.

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TABLE 3

RSV RADT accuracy estimates from subgroup analysesa

Rapid tests for RSV were significantly more sensitive in children than in adults, with pooled sensitivity of 81% (95% CI, 78 to 84) in children and pooled sensitivity of only 29% (95% CI, 11 to 48) in adults. Because of this important disparity in terms of sensitivity and the relatively small number of studies in adults, the rest of the subgroup analyses were conducted exclusively in children (pediatric studies and pediatric subgroup data from mixed-population studies) to alleviate the confounding that would result from an unbalanced distribution of adults and children between levels of another variable. Eight studies were thus excluded from the other subgroup analyses.

As expected, rapid tests for RSV performed worst in assessments against RT-PCR (pooled sensitivity, 74% [95% CI, 71 to 78]) and better in assessments against immunofluorescence (pooled sensitivity, 88% [95% CI, 86 to 91]) or culture (pooled sensitivity, 83% [95% CI, 79 to 88]) owing to the higher accuracy of RT-PCR.

Test accuracy results were fairly similar between the different rapid tests and the different types of specimens used (Table 3). Two immunoassays recently cleared by the FDA that employ an instrument-based digital scan of the test strip to improve accuracy, the BD Veritor RSV (Becton, Dickinson and Company, Franklin Lakes, NJ) and the Quidel Sofia RSV (Quidel Corporation, San Diego, CA), were evaluated in 4 and 5 studies, respectively. However, when two or more index tests were evaluated in a study, our prespecified selection criterion employed to determine which results should be included in our pooled analyses was the use of the most commonly evaluated method. Consequently, too few studies of these two automated immunoassays were available to be included in our pooled subgroup analyses for bivariate random-effect models to converge. Nevertheless, analyzed separately, the pooled accuracy estimates from the 4 BD Veritor RSV studies (sensitivity, 76% [95% CI, 72 to 80]; specificity, 99% [95% CI, 98 to 99]) and the 5 Quidel Sofia RSV studies (sensitivity, 77% [95% CI, 71 to 82]; specificity, 97% [95% CI, 93 to 98]) were similar to those of our overall results of RADTs compared to a reference standard of RT-PCR.

Neither the clinical setting in which the test was performed nor whether or not it was done at the point of care had a significant impact on RADT accuracy. As well, methodological issues, such as whether the samples were collected during the epidemic season for RSV or whether the rapid tests were interpreted without knowledge of the result of the reference standard, did not have a statistically significant effect on the pooled accuracy estimates, although studies that reported blind procedures of the rapid test tended to have lower pooled sensitivity (79% versus 84%, P = 0.11). Industry-sponsored studies reported significantly higher sensitivity for rapid tests for RSV (pooled sensitivity of 87% [95% CI, 83 to 90] compared to 78% [95% CI, 75 to 82] for studies not sponsored by the industry). Since the year 2000, the proportions of studies that included RT-PCR as the reference standard were not significantly different between those sponsored by industry and those not sponsored by industry (50% and 72%, respectively; P = 0.25). We did not analyze studies published before 2000 for this last comparison because RT-PCR was not widely available prior to that time and because only one pre-2000 publication reported RT-PCR results (88).

Too few studies gave information on symptom duration before testing to allow us to do pooled analyses. Similarly, only 5 studies compared the sensitivities of the rapid test for detecting RSV type A and RSV type B (specificity could not be calculated since the rapid tests do not discriminate between the different genotypes). Results of analyses of the effect of RSV genotype on RADT accuracy are presented in Table S2 in the supplemental material.

DISCUSSION

This systematic review and meta-analysis is the first to synthesize the available evidence on the diagnostic accuracy of RSV RADTs. Overall, we observed that these simple and rapid assays displayed consistently high specificity (97%) and positive likelihood ratio (25.5) results. Therefore, physicians can diagnose RSV ARI with confidence on the basis of a positive RSV RADT result. Timely and accurate diagnosis of RSV has the potential to improve patient care and decrease health care costs by permitting prompt hospital infection control measures (13–15, 57) and by decreasing unnecessary antibiotic use (7–9) and unneeded ancillary investigations (e.g., chest radiography, blood cultures, and urine cultures) (10, 11).

A key finding of our study is that RSV RADTs demonstrated a sensitivity of only 29% in adults. It should be noted that this pooled estimate of sensitivity is based on relatively limited data: 4 studies that evaluated RSV RADTs in 738 adults, including elderly and immunocompromised subjects (33, 34, 38, 60). However, poorer sensitivity with advancing age is expected, because prior immunity, although insufficient to protect against reinfection, diminishes viral titers in respiratory secretions as well as the duration of viral shedding (22, 100, 101). Given the observed lack of sensitivity of RSV RADTs in adults, their utility in this population, especially among the elderly and the immunocompromised, is probably very limited. In children, we observed an overall pooled sensitivity of 81%. This level of accuracy is likely to be considered acceptable by many users. However, among pediatric studies, in comparisons of RADTs to RT-PCR, pooled sensitivity decreased to 74%. Therefore, clinicians need to be aware of the possibility of false-negative RADT results in children and should consider retesting a negative sample by a more sensitive method, e.g., RT-PCR, if the result could influence patient management. From a public health perspective, because clinical laboratories that provide data to RSV surveillance systems frequently use RADTs (21, 102), test sensitivity must be taken into account to avoid underestimating the burden of RSV-associated disease.

We found that choice of reference standard by the investigators significantly affected RADT sensitivity estimates. Studies that employed only viral culture or immunofluorescence as a comparator exhibited pooled sensitivities that were 9% or 14% higher, respectively, than those that used RT-PCR. RSV diagnostic research that does not use RT-PCR as a reference standard is therefore likely to overestimate RADT accuracy. However, using RT-PCR in the clinical setting, it has been observed that this method may detect asymptomatic or very low levels of viral shedding, which could sometimes be of questionable significance (103).

Among the 63 pediatric studies included in our subgroup analyses, approximately one-third declared industry sponsorship in the form of funding or in kind provision of study materials. These industry-sponsored studies produced significantly higher sensitivity estimates (87% versus 78%; P = 0.01). There is considerable evidence that industry-sponsored biomedical research tends to produce proindustry results (104). Our finding might be partially explained by industry preferentially supporting study designs that favor the performance of their product (105), e.g., the index test, by the systematic use of a less accurate comparator. While the proportion of industry-sponsored studies published since the year 2000 that used RT-PCR was smaller than that of nonsponsored studies, this difference was not statistically significant (50% versus 72%; P = 0.25). Publication bias, the phenomenon of favorable results being published more frequently than negative results, has also been hypothesized to contribute to associations between industry sponsorship and study outcomes (104). We could not formally assess publication bias because the methods typically employed for its detection are not reliable when used with diagnostic-accuracy data (27).

Two novel RADT platforms use automated instruments, the BD Veritor System and the Quidel Sofia Analyser, to read the signal produced by the test strip. These newer-generation RADTs eliminate the potential subjectivity of an operator visualizing and interpreting test results, which can lead to improved assay performance (106). However, the pooled estimates of the sensitivities of these novel RSV RADTs (76% and 77% compared to RT-PCR) were not substantially different from those of other assays in our review. This is in keeping with our overall finding that the levels of accuracy did not differ significantly across commercial brands.

The evidence base for this review has potential limitations. We highlight a nearly uniform lack of important contextual information among included studies. Data that are not readily available to laboratory practitioners, such as clinical manifestations, presence of comorbidities, and duration of symptoms, are relevant because they could affect RADT accuracy. Also, patient age clearly influences test performance. Although we were able to broadly stratify data into pediatric and adult age groups, we could not perform finer analyses on the effect of age, as further age subcategories were not uniformly reported, if at all. Finally, we were unable to draw any conclusions about the effect of RSV genotype on RADT sensitivity because too few studies used a comparator that could distinguish RSV-A from RSV-B.

Because of their simplicity and speed, RSV RADTs are considered by many clinical laboratories to be valuable diagnostic tools, despite their modest sensitivity compared to more-complex diagnostic methods such as RT-PCR. Novel, highly accurate rapid molecular assays for RSV that may be just as fast and easy to operate as RADTs are currently in development (20, 107). Nevertheless, the relatively low cost of commercial RSV RADTs and the advent of newer assays with automated readers are likely to ensure their continued widespread use in the near future, particularly in children. Therefore, understanding their performance characteristics is important to inform diagnostic laboratory researchers who must decide upon their implementation, clinicians who rely on RSV RADTs to guide patient management, and public health authorities who must interpret RSV surveillance data that utilize RADT results. Our systematic review and meta-analysis suggest that the very poor pooled sensitivity of RSV RADTs in adults may preclude their use in this population. We also found that studies published to date that were sponsored by industry produced higher index test sensitivity estimates. Finally, diagnostic-accuracy studies that did not use RT-PCR as a reference standard likely produced overestimates of RSV RADT sensitivity.

ACKNOWLEDGMENTS

We thank Nandini Dendukuri for helpful discussions regarding data analysis and Patricia S. Fontela for her thoughtful review of the manuscript.

FOOTNOTES

    • Received 15 July 2015.
    • Returned for modification 10 August 2015.
    • Accepted 1 September 2015.
    • Accepted manuscript posted online 9 September 2015.
  • Supplemental material for this article may be found at http://dx.doi.org/10.1128/JCM.01816-15.

  • Copyright © 2015, American Society for Microbiology. All Rights Reserved.

REFERENCES

  1. 1.↵
    1. Nair H,
    2. Nokes DJ,
    3. Gessner BD,
    4. Dherani M,
    5. Madhi SA,
    6. Singleton RJ,
    7. O'Brien KL,
    8. Roca A,
    9. Wright PF,
    10. Bruce N,
    11. Chandran A,
    12. Theodoratou E,
    13. Sutanto A,
    14. Sedyaningsih ER,
    15. Ngama M,
    16. Munywoki PK,
    17. Kartasasmita C,
    18. Simoes EA,
    19. Rudan I,
    20. Weber MW,
    21. Campbell H
    . 2010. Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. Lancet 375:1545–1555. doi:10.1016/S0140-6736(10)60206-1.
    OpenUrlCrossRefPubMedWeb of Science
  2. 2.↵
    1. Papenburg J,
    2. Hamelin ME,
    3. Ouhoummane N,
    4. Carbonneau J,
    5. Ouakki M,
    6. Raymond F,
    7. Robitaille L,
    8. Corbeil J,
    9. Caouette G,
    10. Frenette L,
    11. De Serres G,
    12. Boivin G
    . 2012. Comparison of risk factors for human metapneumovirus and respiratory syncytial virus disease severity in young children. J Infect Dis 206:178–189. doi:10.1093/infdis/jis333.
    OpenUrlCrossRefPubMed
  3. 3.↵
    1. Hall CB,
    2. Weinberg GA,
    3. Iwane MK,
    4. Blumkin AK,
    5. Edwards KM,
    6. Staat MA,
    7. Auinger P,
    8. Griffin MR,
    9. Poehling KA,
    10. Erdman D,
    11. Grijalva CG,
    12. Zhu Y,
    13. Szilagyi P
    . 2009. The burden of respiratory syncytial virus infection in young children. N Engl J Med 360:588–598. doi:10.1056/NEJMoa0804877.
    OpenUrlCrossRefPubMedWeb of Science
  4. 4.↵
    1. Falsey AR,
    2. Hennessey PA,
    3. Formica MA,
    4. Cox C,
    5. Walsh EE
    . 2005. Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 352:1749–1759. doi:10.1056/NEJMoa043951.
    OpenUrlCrossRefPubMedWeb of Science
  5. 5.↵
    1. Papenburg J,
    2. Boivin G
    . 2010. The distinguishing features of human metapneumovirus and respiratory syncytial virus. Rev Med Virol 20:245–260. doi:10.1002/rmv.651.
    OpenUrlCrossRefPubMed
  6. 6.↵
    1. Purcell K,
    2. Fergie J
    . 2002. Concurrent serious bacterial infections in 2396 infants and children hospitalized with respiratory syncytial virus lower respiratory tract infections. Arch Pediatr Adolesc Med 156:322–324. doi:10.1001/archpedi.156.4.322.
    OpenUrlCrossRefPubMedWeb of Science
  7. 7.↵
    1. Byington CL,
    2. Castillo H,
    3. Gerber K,
    4. Daly JA,
    5. Brimley LA,
    6. Adams S,
    7. Christenson JC,
    8. Pavia AT
    . 2002. The effect of rapid respiratory viral diagnostic testing on antibiotic use in a children's hospital. Arch Pediatr Adolesc Med 156:1230–1234. doi:10.1001/archpedi.156.12.1230.
    OpenUrlCrossRefPubMedWeb of Science
  8. 8.↵
    1. Adcock PM,
    2. Stout GG,
    3. Hauck MA,
    4. Marshall GS
    . 1997. Effect of rapid viral diagnosis on the management of children hospitalized with lower respiratory tract infection. Pediatr Infect Dis J 16:842–846. doi:10.1097/00006454-199709000-00005.
    OpenUrlCrossRefPubMedWeb of Science
  9. 9.↵
    1. Ferronato ÂE,
    2. Gilio AE,
    3. Ferraro AA,
    4. de Paulis M,
    5. Vieira SE
    . 2012. Etiological diagnosis reduces the use of antibiotics in infants with bronchiolitis. Clinics (Sao Paulo) 67:1001–1006. doi:10.6061/clinics/2012(09)03.
    OpenUrlCrossRefPubMed
  10. 10.↵
    1. Woo PC,
    2. Chiu SS,
    3. Seto WH,
    4. Peiris M
    . 1997. Cost-effectiveness of rapid diagnosis of viral respiratory tract infections in pediatric patients. J Clin Microbiol 35:1579–1581.
    OpenUrlAbstract/FREE Full Text
  11. 11.↵
    1. Barenfanger J,
    2. Drake C,
    3. Leon N,
    4. Mueller T,
    5. Troutt T
    . 2000. Clinical and financial benefits of rapid detection of respiratory viruses: an outcomes study. J Clin Microbiol 38:2824–2828.
    OpenUrlAbstract/FREE Full Text
  12. 12.
    Reference deleted.
  13. 13.↵
    1. Krasinski K,
    2. LaCouture R,
    3. Holzman RS,
    4. Waithe E,
    5. Bonk S,
    6. Hanna B
    . 1990. Screening for respiratory syncytial virus and assignment to a cohort at admission to reduce nosocomial transmission. J Pediatr 116:894–898. doi:10.1016/S0022-3476(05)80646-8.
    OpenUrlCrossRefPubMedWeb of Science
  14. 14.↵
    1. Madge P,
    2. Paton JY,
    3. McColl JH,
    4. Mackie PL
    . 1992. Prospective controlled study of four infection-control procedures to prevent nosocomial infection with respiratory syncytial virus. Lancet 340:1079–1083. doi:10.1016/0140-6736(92)93088-5.
    OpenUrlCrossRefPubMedWeb of Science
  15. 15.↵
    RSV Outbreak Investigation Team. 2014. Contributing and terminating factors of a large RSV outbreak in an adult hematology and transplant unit. PLoS Curr 6:pii:ecurrents.outbreaks.3bc85b2a508d205ecc4a5534ecb1f9be. doi:10.1371/currents.outbreaks.3bc85b2a508d205ecc4a5534ecb1f9be.
    OpenUrlCrossRef
  16. 16.↵
    1. Caram LB,
    2. Chen J,
    3. Taggart EW,
    4. Hillyard DR,
    5. She R,
    6. Polage CR,
    7. Twersky J,
    8. Schmader K,
    9. Petti CA,
    10. Woods CW
    . 2009. Respiratory syncytial virus outbreak in a long-term care facility detected using reverse transcriptase polymerase chain reaction: an argument for real-time detection methods. J Am Geriatr Soc 57:482–485. doi:10.1111/j.1532-5415.2008.02153.x.
    OpenUrlCrossRefPubMedWeb of Science
  17. 17.↵
    1. Vallières E,
    2. Renaud C
    . 2013. Clinical and economical impact of multiplex respiratory virus assays. Diagn Microbiol Infect Dis 76:255–261. doi:10.1016/j.diagmicrobio.2013.03.008.
    OpenUrlCrossRefPubMed
  18. 18.↵
    1. Thornton HV,
    2. Blair PS,
    3. Lovering AM,
    4. Muir P,
    5. Hay AD
    . 2015. Clinical presentation and microbiological diagnosis in paediatric respiratory tract infection: a systematic review. Br J Gen Pract 65:e69–81. doi:10.3399/bjgp15X683497.
    OpenUrlAbstract/FREE Full Text
  19. 19.↵
    1. Robinson CC
    . 2009. Respiratory viruses, p 203–248. In Specter S, Hodinka R, Young S, Wiedbrauk D (ed), Clinical virology manual. ASM Press, Washington, DC.
  20. 20.↵
    1. Somerville LK,
    2. Ratnamohan VM,
    3. Dwyer DE,
    4. Kok J
    . 2015. Molecular diagnosis of respiratory viruses. Pathology 47:243–249. doi:10.1097/PAT.0000000000000240.
    OpenUrlCrossRefPubMed
  21. 21.↵
    1. Haynes AK,
    2. Prill MM,
    3. Iwane MK,
    4. Gerber SI
    . 2014. Respiratory syncytial virus—United States, July 2012–June 2014. MMWR Morb Mortal Wkly Rep 63:1133–1136.
    OpenUrlPubMed
  22. 22.↵
    1. Prendergast C,
    2. Papenburg J
    . 2013. Rapid antigen-based testing for respiratory syncytial virus: moving diagnostics from bench to bedside? Future Microbiol 8:435–444. doi:10.2217/fmb.13.9.
    OpenUrlCrossRefPubMed
  23. 23.↵
    1. Leeflang MM,
    2. Deeks JJ,
    3. Gatsonis C,
    4. Bossuyt PM
    . 2008. Systematic reviews of diagnostic test accuracy. Ann Intern Med 149:889–897. doi:10.7326/0003-4819-149-12-200812160-00008.
    OpenUrlCrossRefPubMedWeb of Science
  24. 24.↵
    1. Pai M,
    2. McCulloch M,
    3. Gorman JD,
    4. Pai N,
    5. Enanoria W,
    6. Kennedy G,
    7. Tharyan P,
    8. Colford JM, Jr
    . 2004. Systematic reviews and meta-analyses: an illustrated, step-by-step guide. Natl Med J India 17:86–95.
    OpenUrlPubMed
  25. 25.↵
    1. Moher D,
    2. Liberati A,
    3. Tetzlaff J,
    4. Altman DG
    . 2009. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 62:1006–1012. doi:10.1016/j.jclinepi.2009.06.005.
    OpenUrlCrossRefPubMedWeb of Science
  26. 26.↵
    1. Whiting PF,
    2. Rutjes AW,
    3. Westwood ME,
    4. Mallett S,
    5. Deeks JJ,
    6. Reitsma JB,
    7. Leeflang MM,
    8. Sterne JA,
    9. Bossuyt PM
    . 2011. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536. doi:10.7326/0003-4819-155-8-201110180-00009.
    OpenUrlCrossRefPubMedWeb of Science
  27. 27.↵
    1. Leeflang MM
    . 2014. Systematic reviews and meta-analyses of diagnostic test accuracy. Clin Microbiol Infect 20:105–113. doi:10.1111/1469-0691.12474.
    OpenUrlCrossRefPubMed
  28. 28.↵
    1. Aldous WK,
    2. Gerber K,
    3. Taggart EW,
    4. Rupp J,
    5. Wintch J,
    6. Daly JA
    . 2005. A comparison of Thermo Electron RSV OIA to viral culture and direct fluorescent assay testing for respiratory syncytial virus. J Clin Virol 32:224–228. doi:10.1016/j.jcv.2004.07.010.
    OpenUrlCrossRefPubMed
  29. 29.↵
    1. Aldous WK,
    2. Gerber K,
    3. Taggart EW,
    4. Thomas J,
    5. Tidwell D,
    6. Daly JA
    . 2004. A comparison of Binax NOW to viral culture and direct fluorescent assay testing for respiratory syncytial virus. Diagn Microbiol Infect Dis 49:265–268. doi:10.1016/j.diagmicrobio.2004.04.005.
    OpenUrlCrossRefPubMed
  30. 30.↵
    1. Aslanzadeh J,
    2. Zheng X,
    3. Li H,
    4. Tetreault J,
    5. Ratkiewicz I,
    6. Meng S,
    7. Hamilton P,
    8. Tang Y-W
    . 2008. Prospective evaluation of rapid antigen tests for diagnosis of respiratory syncytial virus and human metapneumovirus infections. J Clin Microbiol 46:1682–1685. doi:10.1128/JCM.00008-08.
    OpenUrlAbstract/FREE Full Text
  31. 31.↵
    1. Boivin G,
    2. Cote S,
    3. Dery P,
    4. De Serres G,
    5. Bergeron MG
    . 2004. Multiplex real-time PCR assay for detection of influenza and human respiratory syncytial viruses. J Clin Microbiol 42:45–51. doi:10.1128/JCM.42.1.45-51.2004.
    OpenUrlAbstract/FREE Full Text
  32. 32.↵
    1. Bonroy C,
    2. Vankeerberghen A,
    3. Boel A,
    4. De Beenhouwer H
    . 2007. Use of a multiplex real-time PCR to study the incidence of human metapneumovirus and human respiratory syncytial virus infections during two winter seasons in a Belgian paediatric hospital. Clin Microbiol Infect 13:504–509. doi:10.1111/j.1469-0691.2007.01682.x.
    OpenUrlCrossRefPubMed
  33. 33.↵
    1. Borek AP,
    2. Clemens SH,
    3. Gaskins VK,
    4. Aird DZ,
    5. Valsamakis A
    . 2006. Respiratory syncytial virus detection by remel Xpect, Binax Now RSV, direct immunofluorescent staining, and tissue culture. J Clin Microbiol 44:1105–1107. doi:10.1128/JCM.44.3.1105-1107.2006.
    OpenUrlAbstract/FREE Full Text
  34. 34.↵
    1. Casiano-Colon AE,
    2. Hulbert BB,
    3. Mayer TK,
    4. Walsh EE,
    5. Falsey AR
    . 2003. Lack of sensitivity of rapid antigen tests for the diagnosis of respiratory syncytial virus infection in adults. J Clin Virol 28:169–174. doi:10.1016/S1386-6532(03)00002-7.
    OpenUrlCrossRefPubMedWeb of Science
  35. 35.↵
    1. Cruz AT,
    2. Cazacu AC,
    3. Greer JM,
    4. Demmler GJ
    . 2007. Performance of a rapid assay (Binax NOW) for detection of respiratory syncytial virus at a children's hospital over a 3-year period. J Clin Microbiol 45:1993–1995. doi:10.1128/JCM.00279-07.
    OpenUrlAbstract/FREE Full Text
  36. 36.↵
    1. Dayan P,
    2. Ahmad F,
    3. Urtecho J,
    4. Novick M,
    5. Dixon P,
    6. Levine D,
    7. Miller S
    . 2002. Test characteristics of the respiratory syncytial virus enzyme-linked immunoabsorbent assay in febrile infants < or = 60 days of age. Clinical Pediatrics 41:415–418. doi:10.1177/000992280204100606.
    OpenUrlCrossRefPubMed
  37. 37.↵
    1. Dominguez EA,
    2. Taber LH,
    3. Couch RB
    . 1993. Comparison of rapid diagnostic techniques for respiratory syncytial and influenza A virus respiratory infections in young children. J Clin Microbiol 31:2286–2290.
    OpenUrlAbstract/FREE Full Text
  38. 38.↵
    1. Englund JA,
    2. Piedra PA,
    3. Jewell A,
    4. Patel K,
    5. Baxter BB,
    6. Whimbey E
    . 1996. Rapid diagnosis of respiratory syncytial virus infections in immunocompromised adults. J Clin Microbiol 34:1649–1653.
    OpenUrlAbstract/FREE Full Text
  39. 39.↵
    1. Freymuth F,
    2. Brooks W,
    3. Petitjean J,
    4. Daon F,
    5. Constantini S
    . 1991. Evaluation of an enzyme membrane immunoassay (Directigen RSV) for the rapid diagnosis of respiratory syncytial virus infections. Pathol Biol (Paris) 39:283–286.
    OpenUrlPubMed
  40. 40.↵
    1. Garea MT,
    2. Lopez JM,
    3. Perez Del Molino ML,
    4. Coira A,
    5. Pardo F
    . 1992. Comparison of a new commercial enzyme immunoassay for rapid detection of respiratory syncytial virus. Eur J Clin Microbiol Infect Dis 11:175–177. doi:10.1007/BF01967073.
    OpenUrlCrossRefPubMedWeb of Science
  41. 41.↵
    1. Ginocchio CC,
    2. Swierkosz E,
    3. McAdam AJ,
    4. Marcon M,
    5. Storch GA,
    6. Valsamakis A,
    7. Juretschko S,
    8. Romero J,
    9. Yen-Lieberman B
    . 2010. Multicenter study of clinical performance of the 3M rapid detection RSV test. J Clin Microbiol 48:2337–2343. doi:10.1128/JCM.00130-10.
    OpenUrlAbstract/FREE Full Text
  42. 42.↵
    1. Goodrich JS,
    2. Miller MB
    . 2007. Comparison of Cepheid's analyte-specific reagents with BD directigen for detection of respiratory syncytial virus. J Clin Microbiol 45:604–606. doi:10.1128/JCM.01325-06.
    OpenUrlAbstract/FREE Full Text
  43. 43.↵
    1. Gregson D,
    2. Lloyd T,
    3. Buchan S,
    4. Church D
    . 2005. Comparison of the RSV Respi-Strip with direct fluorescent-antigen detection for diagnosis of respiratory syncytial virus infection in pediatric patients. J Clin Microbiol 43:5782–5783. doi:10.1128/JCM.43.11.5782-5783.2005.
    OpenUrlAbstract/FREE Full Text
  44. 44.↵
    1. Gröndahl B,
    2. Puppe W,
    3. Weigl J,
    4. Schmitt HJ
    . 2005. Comparison of the BD Directigen Flu A+B kit and the Abbott TestPack RSV with a multiplex RT-PCR ELISA for rapid detection of influenza viruses and respiratory syncytial virus. Clin Microbiol Infect 11:848–850. doi:10.1111/j.1469-0691.2005.01223.x.
    OpenUrlCrossRefPubMed
  45. 45.↵
    1. Halstead DC,
    2. Todd S,
    3. Fritch G
    . 1990. Evaluation of five methods for respiratory syncytial virus detection. J Clin Microbiol 28:1021–1025.
    OpenUrlAbstract/FREE Full Text
  46. 46.↵
    1. Holter E,
    2. Abrahamsen TG,
    3. Rod G,
    4. Holten E
    . 1998. Discrepancy between results of a commercial enzyme immunoassay kit and immunofluorescence staining for detection of respiratory syncytial virus antigen. Eur J Clin Microbiol Infect Dis 17:595–596. doi:10.1007/BF01708629.
    OpenUrlCrossRefPubMed
  47. 47.↵
    1. Khanom AB,
    2. Velvin C,
    3. Hawrami K,
    4. Schutten M,
    5. Patel M,
    6. Holmes MV,
    7. Atkinson C,
    8. Breuer J,
    9. FitzSimons J,
    10. Geretti AM
    . 2011. Performance of a nurse-led paediatric point of care service for respiratory syncytial virus testing in secondary care. J Infect 62:52–58. doi:10.1016/j.jinf.2010.11.002.
    OpenUrlCrossRefPubMedWeb of Science
  48. 48.↵
    1. Kok T,
    2. Barancek K,
    3. Burrell CJ
    . 1990. Evaluation of the Becton Dickinson Directigen test for respiratory syncytial virus in nasopharyngeal aspirates. J Clin Microbiol 28:1458–1459.
    OpenUrlAbstract/FREE Full Text
  49. 49.↵
    1. Krilov LR,
    2. Lipson SM,
    3. Barone SR,
    4. Kaplan MH,
    5. Ciamician Z,
    6. Harkness SH
    . 1994. Evaluation of a rapid diagnostic test for respiratory syncytial virus (RSV): potential for bedside diagnosis. Pediatrics 93(Pt 1):903–906.
    OpenUrlAbstract/FREE Full Text
  50. 50.↵
    1. Kuroiwa Y,
    2. Nagai K,
    3. Okita L,
    4. Ukae S,
    5. Mori T,
    6. Hotsubo T,
    7. Tsutsumi H
    . 2004. Comparison of an immunochromatography test with multiplex reverse transcription-PCR for rapid diagnosis of respiratory syncytial virus infections. J Clin Microbiol 42:4812–4814. doi:10.1128/JCM.42.10.4812-4814.2004.
    OpenUrlAbstract/FREE Full Text
  51. 51.↵
    1. Liao RS,
    2. Tomalty LL,
    3. Majury A,
    4. Zoutman DE
    . 2009. Comparison of viral isolation and multiplex real-time reverse transcription-PCR for confirmation of respiratory syncytial virus and influenza virus detection by antigen immunoassays. J Clin Microbiol 47:527–532. doi:10.1128/JCM.01213-08.
    OpenUrlAbstract/FREE Full Text
  52. 52.↵
    1. Lipson SM,
    2. Krilov LR
    . 1994. Comparison of the rapid second generation directigen EIA with cell culture and immunofluorescence for the detection of respiratory syncytial virus in nasopharyngeal aspirates. Clin Diagn Virol 2:105–112. doi:10.1016/0928-0197(94)90043-4.
    OpenUrlCrossRefPubMed
  53. 53.↵
    1. Mackenzie A,
    2. Hallam N,
    3. Mitchell E,
    4. Beattie T
    . 1999. Near patient testing for respiratory syncytial virus in paediatric accident and emergency: prospective pilot study. Br Med J 319:289–290. doi:10.1136/bmj.319.7205.289.
    OpenUrlFREE Full Text
  54. 54.↵
    1. Mendoza J,
    2. Rojas A,
    3. Navarro JM,
    4. Plata C,
    5. de la Rosa M
    . 1992. Evaluation of three rapid enzyme immunoassays and cell culture for detection of respiratory syncytial virus. Eur J Clin Microbiol Infect Dis 11:452–454. doi:10.1007/BF01961862.
    OpenUrlCrossRefPubMed
  55. 55.↵
    1. Miernyk K,
    2. Bulkow L,
    3. DeByle C,
    4. Chikoyak L,
    5. Hummel KB,
    6. Hennessy T,
    7. Singleton R
    . 2011. Performance of a rapid antigen test (Binax NOW RSV) for diagnosis of respiratory syncytial virus compared with real-time polymerase chain reaction in a pediatric population. J Clin Virol 50:240–243. doi:10.1016/j.jcv.2010.11.011.
    OpenUrlCrossRefPubMed
  56. 56.↵
    1. Miller H,
    2. Milk R,
    3. Diaz-Mitoma F
    . 1993. Comparison of the VIDAS RSV assay and the Abbott Testpack RSV with direct immunofluorescence for detection of respiratory syncytial virus in nasopharyngeal aspirates. J Clin Microbiol 31:1336–1338.
    OpenUrlAbstract/FREE Full Text
  57. 57.↵
    1. Mills JM,
    2. Harper J,
    3. Broomfield D,
    4. Templeton KE
    . 2011. Rapid testing for respiratory syncytial virus in a paediatric emergency department: benefits for infection control and bed management. J Hosp Infect 77:248–251. doi:10.1016/j.jhin.2010.11.019.
    OpenUrlCrossRefPubMed
  58. 58.↵
    1. Mokkapati VK,
    2. Sam Niedbala R,
    3. Kardos K,
    4. Perez RJ,
    5. Guo M,
    6. Tanke HJ,
    7. Corstjens PLAM
    . 2007. Evaluation of UPlink-RSV: prototype rapid antigen test for detection of respiratory syncytial virus infection. Ann N Y Acad Sci 1098:476–485. doi:10.1196/annals.1384.021.
    OpenUrlCrossRefPubMed
  59. 59.↵
    1. Munjal I,
    2. Gialanella P,
    3. Goss C,
    4. McKitrick JC,
    5. Avner JR,
    6. Pan Q,
    7. Litman N,
    8. Levi MH
    . 2011. Evaluation of the 3M rapid detection test for respiratory syncytial virus (RSV) in children during the early stages of the 2009 RSV season. J Clin Microbiol 49:1151–1153. doi:10.1128/JCM.02038-10.
    OpenUrlAbstract/FREE Full Text
  60. 60.↵
    1. Ohm-Smith MJ,
    2. Nassos PS,
    3. Haller BL
    . 2004. Evaluation of the Binax NOW, BD Directigen, and BD Directigen EZ assays for detection of respiratory syncytial virus. J Clin Microbiol 42:2996–2999. doi:10.1128/JCM.42.7.2996-2999.2004.
    OpenUrlAbstract/FREE Full Text
  61. 61.↵
    1. Olsen MA,
    2. Shuck KM,
    3. Sambol AR
    . 1993. Evaluation of Abbott TestPack RSV for the diagnosis of respiratory syncytial virus infections. Diagn Microbiol Infect Dis 16:105–109. doi:10.1016/0732-8893(93)90003-P.
    OpenUrlCrossRefPubMed
  62. 62.↵
    1. Papenburg J,
    2. Buckeridge DL,
    3. De Serres G,
    4. Boivin G
    . 2013. Host and viral factors affecting clinical performance of a rapid diagnostic test for respiratory syncytial virus in hospitalized children. J Pediatrics 163:911–913. doi:10.1016/j.jpeds.2013.03.067.
    OpenUrlCrossRefPubMed
  63. 63.↵
    1. Rath B,
    2. Tief F,
    3. Obermeier P,
    4. Tuerk E,
    5. Karsch K,
    6. Muehlhans S,
    7. Adamou E,
    8. Duwe S,
    9. Schweiger B
    . 2012. Early detection of influenza A and B infection in infants and children using conventional and fluorescence-based rapid testing. J Clin Virol 55:329–333. doi:10.1016/j.jcv.2012.08.002.
    OpenUrlCrossRefPubMed
  64. 64.↵
    1. Reijans M,
    2. Dingemans G,
    3. Klaassen CH,
    4. Meis JF,
    5. Keijdener J,
    6. Mulders B,
    7. Eadie K,
    8. van Leeuwen W,
    9. van Belkum A,
    10. Horrevorts AM,
    11. Simons G
    . 2008. RespiFinder: a new multiparameter test to differentially identify fifteen respiratory viruses. J Clin Microbiol 46:1232–1240. doi:10.1128/JCM.02294-07.
    OpenUrlAbstract/FREE Full Text
  65. 65.↵
    1. Reina J,
    2. Gonzalez Gardenas M,
    3. Ruiz de Gopegui E,
    4. Padilla E,
    5. Ballesteros F,
    6. Mari M,
    7. Munar M
    . 2004. Prospective evaluation of a dot-blot enzyme immunoassay (Directigen RSV) for the antigenic detection of respiratory syncytial virus from nasopharyngeal aspirates of paediatric patients. Clin Microbiol Infect 10:967–971. doi:10.1111/j.1469-0691.2004.00986.x.
    OpenUrlCrossRefPubMed
  66. 66.↵
    1. Ribes JA,
    2. Seabolt JP,
    3. Overman SB
    . 2002. Performance characteristics of VIDAS and Directigen respiratory syncytial virus (RSV) antigen detection assays and culture for the identification of RSV in respiratory specimens. J Clin Microbiol 40:1818–1820. doi:10.1128/JCM.40.5.1818-1820.2002.
    OpenUrlAbstract/FREE Full Text
  67. 67.↵
    1. Rothbarth PH,
    2. Hermus MC,
    3. Schrijnemakers P
    . 1991. Reliability of two new test kits for rapid diagnosis of respiratory syncytial virus infection. J Clin Microbiol 29:824–826.
    OpenUrlAbstract/FREE Full Text
  68. 68.↵
    1. Sánchez-Yebra W,
    2. Ávila-Carrillo JA,
    3. Giménez-Sánchez F,
    4. Reyes-Bertos A,
    5. Sánchez-Forte M,
    6. Morales-Torres M,
    7. Rojas A,
    8. Mendoza J
    ; LRTI Research Group. 2012. Viral agents causing lower respiratory tract infections in hospitalized children: evaluation of the Speed-Oligo RSV assay for the detection of respiratory syncytial virus. Eur J Clin Microbiol Infect Dis 31:243–250. doi:10.1007/s10096-011-1300-4.
    OpenUrlCrossRefPubMed
  69. 69.↵
    1. Schauer U,
    2. Ihorst G,
    3. Rohwedder A,
    4. Petersen G,
    5. Berner R,
    6. Frank HD,
    7. Forster J,
    8. Stephan V
    . 2007. Evaluation of respiratory syncytial virus detection by rapid antigen tests in childhood. Klin Padiatr 219:212–216. doi:10.1055/s-2006-933530.
    OpenUrlCrossRefPubMed
  70. 70.↵
    1. Selvarangan R,
    2. Abel D,
    3. Hamilton M
    . 2008. Comparison of BD Directigen EZ RSV and Binax NOW RSV tests for rapid detection of respiratory syncytial virus from nasopharyngeal aspirates in a pediatric population. Diagn Microbiol Infect Dis 62:157–161. doi:10.1016/j.diagmicrobio.2008.05.005.
    OpenUrlCrossRefPubMed
  71. 71.↵
    1. Shirato K,
    2. Nishimura H,
    3. Saijo M,
    4. Okamoto M,
    5. Noda M,
    6. Tashiro M,
    7. Taguchi F
    . 2007. Diagnosis of human respiratory syncytial virus infection using reverse transcription loop-mediated isothermal amplification. J Virol Methods 139:78–84. doi:10.1016/j.jviromet.2006.09.014.
    OpenUrlCrossRefPubMed
  72. 72.↵
    1. Slinger R,
    2. Milk R,
    3. Gaboury I,
    4. Diaz-Mitoma F
    . 2004. Evaluation of the QuickLab RSV test, a new rapid lateral-flow immunoassay for detection of respiratory syncytial virus antigen. J Clin Microbiol 42:3731–3733. doi:10.1128/JCM.42.8.3731-3733.2004.
    OpenUrlAbstract/FREE Full Text
  73. 73.↵
    1. Smith MC,
    2. Creutz C,
    3. Huang YT
    . 1991. Detection of respiratory syncytial virus in nasopharyngeal secretions by shell vial technique. J Clin Microbiol 29:463–465.
    OpenUrlAbstract/FREE Full Text
  74. 74.↵
    1. Subbarao EK,
    2. Dietrich MC,
    3. De Sierra TM,
    4. Black CJ,
    5. Super DM,
    6. Thomas F,
    7. Kumar ML
    . 1989. Rapid detection of respiratory syncytial virus by a biotin-enhanced immunoassay: test performance by laboratory technologists and housestaff. Pediatr Infect Dis J 8:865–869. doi:10.1097/00006454-198912000-00008.
    OpenUrlCrossRefPubMed
  75. 75.↵
    1. Swierkosz EM,
    2. Flanders R,
    3. Melvin L,
    4. Miller JD,
    5. Kline MW
    . 1989. Evaluation of the Abbott TESTPACK RSV enzyme immunoassay for detection of respiratory syncytial virus in nasopharyngeal swab specimens. J Clin Microbiol 27:1151–1154.
    OpenUrlAbstract/FREE Full Text
  76. 76.↵
    1. Thomas EE,
    2. Book LE
    . 1991. Comparison of two rapid methods for detection of respiratory syncytial virus (RSV) (Testpack RSV and ortho RSV ELISA) with direct immunofluorescence and virus isolation for the diagnosis of pediatric RSV infection. J Clin Microbiol 29:632–635.
    OpenUrlAbstract/FREE Full Text
  77. 77.↵
    1. Tillmann RL,
    2. Simon A,
    3. Muller A,
    4. Schildgen O
    . 2007. Sensitive commercial NASBA assay for the detection of respiratory syncytial virus in clinical specimen. PLoS One 2:e1357. doi:10.1371/journal.pone.0001357.
    OpenUrlCrossRefPubMed
  78. 78.↵
    1. Todd SJ,
    2. Minnich L,
    3. Waner JL
    . 1995. Comparison of rapid immunofluorescence procedure with TestPack RSV and Directigen FLU-A for diagnosis of respiratory syncytial virus and influenza A virus. J Clin Microbiol 33:1650–1651.
    OpenUrlAbstract/FREE Full Text
  79. 79.↵
    1. Ushio M,
    2. Yui I,
    3. Yoshida N,
    4. Fujino M,
    5. Yonekawa T,
    6. Ota Y,
    7. Notomi T,
    8. Nakayama T
    . 2005. Detection of respiratory syncytial virus genome by subgroups-A, B specific reverse transcription loop-mediated isothermal amplification (RT-LAMP). J Med Virol 77:121–127. doi:10.1002/jmv.20424.
    OpenUrlCrossRefPubMed
  80. 80.↵
    1. Van Beers D,
    2. De Foor M,
    3. Di Cesare L,
    4. Vandenvelde C
    . 1991. Evaluation of a commercial enzyme immunomembrane filter assay for detection of respiratory syncytial virus in clinical specimens. Eur J Clin Microbiol Infect Dis 10:1073–1076. doi:10.1007/BF01984934.
    OpenUrlCrossRefPubMed
  81. 81.↵
    1. Vaz-de-Lima LR,
    2. Souza MC,
    3. Matsumoto T,
    4. Hong MA,
    5. Salgado MM,
    6. Barbosa ML,
    7. Sato NS,
    8. Requejo HI,
    9. Oliveira CA,
    10. Pecchini R,
    11. Berezin E,
    12. Passos SD,
    13. Schvartsman C,
    14. Pasmanick A,
    15. Durigon EL,
    16. Ueda M
    . 2008. Performance of indirect immunofluorescence assay, immunochromatography assay and reverse transcription-polymerase chain reaction for detecting human respiratory syncytial virus in nasopharyngeal aspirate samples. Mem Inst Oswaldo Cruz 103:463–467.
    OpenUrlPubMed
  82. 82.↵
    1. Waecker NJ, Jr,
    2. Shope TR,
    3. Weber PA,
    4. Buck ML,
    5. Domingo RC,
    6. Hooper DG
    . 1993. The Rhino-Probe nasal curette for detecting respiratory syncytial virus in children. Pediatr Infect Dis J 12:326–329. doi:10.1097/00006454-199304000-00012.
    OpenUrlCrossRefPubMed
  83. 83.↵
    1. Walsh P,
    2. Overmyer C,
    3. Hancock C,
    4. Heffner J,
    5. Walker N,
    6. Nguyen T,
    7. Shanholtzer L,
    8. Caldera E,
    9. Pusavat J,
    10. Mordechai E,
    11. Adelson ME,
    12. Iacono KT
    . 2014. Is the interpretation of rapid antigen testing for respiratory syncytial virus as simple as positive or negative? Emerg Med J 31:153–159. doi:10.1136/emermed-2013-202729.
    OpenUrlAbstract/FREE Full Text
  84. 84.↵
    1. Waner JL,
    2. Whitehurst NJ,
    3. Todd SJ,
    4. Shalaby H,
    5. Wall LV
    . 1990. Comparison of directigen RSV with viral isolation and direct immunofluorescence for the identification of respiratory syncytial virus. J Clin Microbiol 28:480–483.
    OpenUrlAbstract/FREE Full Text
  85. 85.↵
    1. Wren CG,
    2. Bate BJ,
    3. Masters HB,
    4. Lauer BA
    . 1990. Detection of respiratory syncytial virus antigen in nasal washings by Abbott TestPack enzyme immunoassay. J Clin Microbiol 28:1395–1397.
    OpenUrlAbstract/FREE Full Text
  86. 86.↵
    1. Wyder-Westh C,
    2. Duppenthaler A,
    3. Gorgievski-Hrisoho M,
    4. Aebi C
    . 2003. Evaluation of two rapid detection assays for identification of respiratory syncytial virus in nasopharyngeal secretions of young children. Eur J Clin Microbiol Infect Dis 22:774–775. doi:10.1007/s10096-003-1045-9.
    OpenUrlCrossRefPubMed
  87. 87.↵
    1. Yen AB,
    2. Demmler-Harrison GJ
    . 2011. Rapid antigen testing to detect respiratory syncytial virus performs well in neonates. Pediatr Infect Dis J 30:234–237. doi:10.1097/INF.0b013e3181fa44e3.
    OpenUrlCrossRef
  88. 88.↵
    1. Yoshio H,
    2. Yamada M,
    3. Nii S
    . 1996. Reverse transcription-polymerase chain reaction amplification of respiratory syncytial virus genome from neonatal nasal swab samples. Acta Paediatr Jpn 38:429–433. doi:10.1111/j.1442-200X.1996.tb03521.x.
    OpenUrlCrossRefPubMed
  89. 89.↵
    1. Zheng X,
    2. Quianzon S,
    3. Mu Y,
    4. Katz BZ
    . 2004. Comparison of two new rapid antigen detection assays for respiratory syncytial virus with another assay and shell vial culture. J Clin Virol 31:130–133. doi:10.1016/j.jcv.2004.03.017.
    OpenUrlCrossRefPubMedWeb of Science
  90. 90.↵
    1. Bell JJ,
    2. Anderson EJ,
    3. Greene WH,
    4. Romero JR,
    5. Merchant M,
    6. Selvarangan R
    . 2014. Multicenter clinical performance evaluation of BD Veritor system for rapid detection of respiratory syncytial virus. J Clin Virol 61:113–117. doi:10.1016/j.jcv.2014.05.020.
    OpenUrlCrossRefPubMed
  91. 91.↵
    1. Bruning AH,
    2. van Dijk K,
    3. van Eijk HW,
    4. Koen G,
    5. van Woensel JB,
    6. Kruisinga FH,
    7. Pajkrt D,
    8. Wolthers KC
    . 2014. Evaluation of a rapid antigen detection point-of-care test for respiratory syncytial virus and influenza in a pediatric hospitalized population in the Netherlands. Diagn Microbiol Infect Dis 80:292–293. doi:10.1016/j.diagmicrobio.2014.08.010.
    OpenUrlCrossRefPubMed
  92. 92.↵
    1. Nakao A,
    2. Hisata K,
    3. Matsunaga N,
    4. Fujimori M,
    5. Yoshikawa N,
    6. Komatsu M,
    7. Kikuchi K,
    8. Takahashi H,
    9. Shimizu T
    . 2014. The clinical utility of a near patient care rapid microarray-based diagnostic test for influenza and respiratory syncytial virus infections in the pediatric setting. Diagn Microbiol Infect Dis 78:363–367. doi:10.1016/j.diagmicrobio.2013.11.005.
    OpenUrlCrossRefPubMed
  93. 93.↵
    1. Pfeil J,
    2. Tabatabai J,
    3. Sander A,
    4. Ries M,
    5. Grulich-Henn J,
    6. Schnitzler P
    . 2014. Screening for respiratory syncytial virus and isolation strategies in children hospitalized with acute respiratory tract infection. Medicine 93:e144. doi:10.1097/MD.0000000000000144.
    OpenUrlCrossRefPubMed
  94. 94.↵
    1. Jang JW,
    2. Cho CH,
    3. Nam MH,
    4. Yoon SY,
    5. Lee CK,
    6. Lim CS,
    7. Kim WJ
    . 2015. Clinical performance evaluation of the Sofia RSV FIA rapid antigen test for diagnosis of respiratory syncytial virus infection. J Clin Microbiol 53:684–686. doi:10.1128/JCM.03324-14.
    OpenUrlAbstract/FREE Full Text
  95. 95.↵
    1. Kanwar N,
    2. Hassan F,
    3. Nguyen A,
    4. Selvarangan R
    . 2015. Head-to-head comparison of the diagnostic accuracies of BD Veritor System RSV and Quidel(R) Sofia(R) RSV FIA systems for respiratory syncytial virus (RSV) diagnosis. J Clin Virol 65:83–86. doi:10.1016/j.jcv.2015.02.008.
    OpenUrlCrossRefPubMed
  96. 96.↵
    1. Leonardi GP,
    2. Wilson AM,
    3. Dauz M,
    4. Zuretti AR
    . 2015. Evaluation of respiratory syncytial virus (RSV) direct antigen detection assays for use in point-of-care testing. J Virol Methods 213:131–134. doi:10.1016/j.jviromet.2014.11.016.
    OpenUrlCrossRefPubMed
  97. 97.↵
    1. Schwartz RH,
    2. Selvarangan R,
    3. Zissman EN
    . 1 April 2015, posting date. BD Veritor system respiratory syncytial virus rapid antigen detection test: point-of-care results in primary care pediatric offices compared with reverse transcriptase polymerase chain reaction and viral culture methods. Pediatr Emerg Care doi:10.1097/PEC.0000000000000371.
    OpenUrlCrossRef
  98. 98.↵
    1. Tuttle R,
    2. Weick A,
    3. Schwarz WS,
    4. Chen X,
    5. Obermeier P,
    6. Seeber L,
    7. Tief F,
    8. Muehlhans S,
    9. Karsch K,
    10. Peiser C,
    11. Duwe S,
    12. Schweiger B,
    13. Rath B
    . 2015. Evaluation of novel second-generation RSV and influenza rapid tests at the point of care. Diagn Microbiol Infect Dis 81:171–176. doi:10.1016/j.diagmicrobio.2014.11.013.
    OpenUrlCrossRefPubMed
  99. 99.↵
    1. Whiting PF,
    2. Rutjes AW,
    3. Westwood ME,
    4. Mallett S
    . 2013. A systematic review classifies sources of bias and variation in diagnostic test accuracy studies. J Clin Epidemiol 66:1093–1104. doi:10.1016/j.jclinepi.2013.05.014.
    OpenUrlCrossRefPubMed
  100. 100.↵
    1. Falsey AR
    . 2007. Respiratory syncytial virus infection in adults. Semin Respir Crit Care Med 28:171–181. doi:10.1055/s-2007-976489.
    OpenUrlCrossRefPubMedWeb of Science
  101. 101.↵
    1. Hall CB,
    2. Douglas RG, Jr,
    3. Geiman JM
    . 1976. Respiratory syncytial virus infections in infants: quantitation and duration of shedding. J Pediatr 89:11–15. doi:10.1016/S0022-3476(76)80918-3.
    OpenUrlCrossRefPubMedWeb of Science
  102. 102.↵
    1. Turner R,
    2. Saunders B,
    3. Edelman L
    . 2012. Did the 2009 influenza pandemic affect future laboratory testing methods for respiratory viruses? Abstr 28th Clin Virol Symp, Daytona Beach, FL, USA, 20 to 21 April 2012, poster S8.
  103. 103.↵
    1. Byington CL,
    2. Ampofo K,
    3. Stockmann C,
    4. Adler FR,
    5. Herbener A,
    6. Miller T,
    7. Sheng X,
    8. Blaschke AJ,
    9. Crisp R,
    10. Pavia AT
    . 2015. Community surveillance of respiratory viruses among families in the Utah Better Identification of Germs-Longitudinal Viral Epidemiology (BIG-LoVE) Study. Clin Infect Dis 61:1217–1224. doi:10.1093/cid/civ486.
    OpenUrlCrossRefPubMed
  104. 104.↵
    1. Bekelman JE,
    2. Li Y,
    3. Gross CP
    . 2003. Scope and impact of financial conflicts of interest in biomedical research: a systematic review. JAMA 289:454–465. doi:10.1001/jama.289.4.454.
    OpenUrlCrossRefPubMedWeb of Science
  105. 105.↵
    1. Djulbegovic B,
    2. Lacevic M,
    3. Cantor A,
    4. Fields KK,
    5. Bennett CL,
    6. Adams JR,
    7. Kuderer NM,
    8. Lyman GH
    . 2000. The uncertainty principle and industry-sponsored research. Lancet 356:635–638. doi:10.1016/S0140-6736(00)02605-2.
    OpenUrlCrossRefPubMedWeb of Science
  106. 106.↵
    1. Dunn JJ,
    2. Ginocchio CC
    . 1 October 2014. Can newly developed, rapid immunochromatographic antigen detection tests be reliably used for the laboratory diagnosis of influenza virus infections? J Clin Microbiol doi:10.1128/jcm.02739-14.
    OpenUrlCrossRef
  107. 107.↵
    1. Mahony J,
    2. Chong S,
    3. Bulir D,
    4. Ruyter A,
    5. Mwawasi K,
    6. Waltho D
    . 2013. Development of a sensitive loop-mediated isothermal amplification assay that provides specimen-to-result diagnosis of respiratory syncytial virus infection in 30 minutes. J Clin Microbiol 51:2696–2701. doi:10.1128/JCM.00662-13.
    OpenUrlAbstract/FREE Full Text
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Diagnostic Accuracy of Rapid Antigen Detection Tests for Respiratory Syncytial Virus Infection: Systematic Review and Meta-analysis
Caroline Chartrand, Nicolas Tremblay, Christian Renaud, Jesse Papenburg
Journal of Clinical Microbiology Nov 2015, 53 (12) 3738-3749; DOI: 10.1128/JCM.01816-15

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Diagnostic Accuracy of Rapid Antigen Detection Tests for Respiratory Syncytial Virus Infection: Systematic Review and Meta-analysis
Caroline Chartrand, Nicolas Tremblay, Christian Renaud, Jesse Papenburg
Journal of Clinical Microbiology Nov 2015, 53 (12) 3738-3749; DOI: 10.1128/JCM.01816-15
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