Accurate and rapid diagnosis is needed for timely intervention and clinical management of acute respiratory infections. This study evaluated performance characteristics of the Panther Fusion assay for the detection of influenza A virus (Flu A), influenza B virus (Flu B), respiratory syncytial virus (RSV), parainfluenza viruses 1 to 3 (Para 1 to 3), human metapneumovirus (hMPV), rhinovirus (RV), and adenovirus (Adeno) targets in comparison to those of the eSensor and Lyra assays using 395 nasopharyngeal (NP) and 104 lower respiratory tract (LRT) specimens.
KEYWORDS: Panther Fusion, respiratory virus, performance evaluation, automation, nasopharyngeal swabs, lower respiratory tract specimens
ABSTRACT
Accurate and rapid diagnosis is needed for timely intervention and clinical management of acute respiratory infections. This study evaluated performance characteristics of the Panther Fusion assay for the detection of influenza A virus (Flu A), influenza B virus (Flu B), respiratory syncytial virus (RSV), parainfluenza viruses 1 to 3 (Para 1 to 3), human metapneumovirus (hMPV), rhinovirus (RV), and adenovirus (Adeno) targets in comparison to those of the eSensor and Lyra assays using 395 nasopharyngeal (NP) and 104 lower respiratory tract (LRT) specimens. Based on the consensus positive result established (positive result in 2 of the 3 assays), the NP specimens for the Fusion and eSensor assays had 100% positive percent agreement (PPA) for all the analytes and the Lyra assays had 100% PPA for Flu A and Adeno analytes. A 100% negative percent agreement (NPA) was observed for all the Lyra analytes, whereas those for the Fusion targets ranged from 98.4 to 100% and those for the eSensor ranged from 99.4 to 100% for all the analytes except RV. For the LRT specimens, Fusion had 100% PPA and 100% NPA for all the targets except hMPV. There was a 100% PPA for eSensor analytes; the NPA ranged from 98 to 100%, except for RV. For the Lyra assays, the PPA ranged between 50 and 100%, while the NPA was 100% for all the targets except Adeno. The Fusion assay performed similarly to the eSensor assay for majority of the targets tested and provides laboratories with a fully automated random-access system to test for a broad array of viral respiratory pathogens.
INTRODUCTION
Acute respiratory infections (ARIs) are a leading cause of significant morbidity and mortality worldwide, particularly in immunocompromised patients. Seasonal respiratory illnesses caused by influenza virus and respiratory syncytial virus (RSV) substantially contribute to additional hospitalizations and mortality in the elderly, children, and patients with comorbidity (1, 2). The majority of acute upper respiratory infections (URIs) and lower respiratory infections (LRIs) are caused by viruses (3). Several studies have reported viruses that are associated with ARIs, such as influenza viruses A and B (Flu A and B), RSV A and B, parainfluenza viruses 1 to 4 (Para 1 to 4), coronaviruses, human metapneumovirus (hMPV), rhinovirus (RV), adenovirus (Adeno), and bocavirus (4–6). RSV and hMPV are believed to be the most important viral pathogens causing LRI in young children (7, 8). Most ARIs appear with overlapping clinical presentations, and therefore, physicians usually cannot differentiate the causative pathogen without laboratory testing. Accurate and timely identification of respiratory pathogens is thus critical for administering appropriate antiviral therapy, for adopting public health measures, and for controlling possible outbreaks.
ARIs have historically been diagnosed using several laboratory procedures, such as virus isolation in culture, rapid antigen detection by direct fluorescent antibody assay, and rapid enzyme immunoassays. In the past decade, owing to advancements in molecular diagnostics, many clinical virology laboratories adopted molecular assays, as they provide greater sensitivity than culture and other diagnostic methods. Utilization of these rapid molecular tests has been shown to significantly reduce antibiotic use and length of hospital stay (9–11). A variety of molecular assays have been reported for the identification and detection of respiratory pathogens. With the advent of multiplex real-time respiratory panels, diagnosis of multiple respiratory pathogens is achieved with rapid turnaround time for patient management decisions. The Panther Fusion (Hologic Inc., San Diego, CA) respiratory assays consist of three multiplex real-time PCR panels (Flu A/Flu B/RSV, Paraflu, and AdV/hMPV/RV) designed to detect an array of respiratory viruses. The objective of this study was to evaluate performance characteristics of Fusion assay in comparison to two FDA-cleared assays using both nasopharyngeal swab (NP) and lower respiratory tract (LRT) specimens.
MATERIALS AND METHODS
Clinical specimens.
A total of 500 specimens were collected for the study, including 395 nasopharyngeal (NP) swabs and 105 lower respiratory tract (LRT) specimens (bronchoalveolar lavage samples [BALs], n = 102, and bronchial washes [BW], n = 3). Among the samples, three were pediatric samples and remaining were from adult patients. These samples were submitted between January 2016 and January 2017 to Emory Medical Laboratories, Atlanta, GA, for routine testing. NP swabs were collected in Starswab Multitrans System tubes (Starplex Scientific Corp., TN). The residual NP and LRT samples were refrigerated for up to a week, and then samples were kept frozen at −80°C until testing.
Molecular assays for respiratory virus testing.
The multicenter study compared qualitative detection of Flu A, Flu B, RSV, Para 1 to 3, hMPV, RV, and Adeno targets using Panther Fusion (Fusion), eSensor RVP (eSensor; Genmark Dx, Carlsbad, CA) and Lyra (Quidel, San Diego, CA) respiratory assays. The Fusion, eSensor, and Lyra assays are FDA cleared for upper respiratory tract (URT) specimen types.
The three Fusion assays are multiplex real-time PCR assays that detect Flu A/Flu B/RSV, Para 1 to 4, and Adeno/hMPV/RV on the fully automated Panther Fusion system. The Fusion assays were performed according to the manufacturer's recommendations. The eSensor RVP detects 14 respiratory virus types and subtypes using the eSensor technology in a single assay. The samples were extracted using Roche MagNA Pure 96 system, which was not FDA cleared but was validated for use with the eSensor assay. A Para 4 assay was not available on the eSensor. The assay was performed as per the manufacturer's protocol. The four Lyra assays detect Flu A and B, RSV and hMPV, Para 1 to 3, and Adeno. The samples were extracted using Qiagen EZ1 advanced XL, and amplification and detection of targets were carried out on an Abbott m2000 real-time instrument. The EZ1 and m2000 real-time platforms are not FDA cleared for use with the Lyra assay. Para 4 and RV targets were not available on the Lyra assays. The assays were performed following the manufacturer's protocol.
Study design.
All the specimens were tested in a blinded fashion; the eSensor was performed at Emory, while the Fusion and Lyra assays were performed at Miriam Hospital Research Laboratory. The eSensor assay was used for clinical testing and therefore was performed in real time using prospective/fresh specimens, while the Fusion and Lyra assays were performed on frozen aliquots of those specimens. The study was approved by the Institutional Review Boards of Emory University and Miriam Hospital.
Consensus result and discordant resolution.
To evaluate the clinical performance of the Fusion assay compared to those of the other molecular assays tested, a consensus result was established if at least two of three tests were positive for the same analyte. Discordant specimens were further evaluated at the Hologic R&D laboratory at San Diego, CA, with laboratory-developed validated PCR-based assays using different primer/probe sets than used in the Fusion respiratory assays for Flu A, Flu B, RSV, Para 1 to 3, and hMPV. Discrepant analysis for Adeno was performed using the FDA-cleared Prodesse ProAdeno+ assay, and Para 4 and RV were evaluated using laboratory-developed PCR assays followed by bidirectional sequencing assays.
Statistical analysis.
Data analysis was performed using the proc frequency procedure in SAS version 9.4. Discordant results were analyzed using the chi-square likelihood ratio test. A P value of <0.05 was considered significant. The 95% confidence interval (CI) was calculated for positive percent agreement (PPA) and negative percent agreement (NPA) using the Wilson score method.
RESULTS
Method comparison for NP samples.
Among the 395 NP samples tested, 241 (61%) were identified as consensus positive, including 33 (13.7%) for Flu A, 18 (7.4%) for Flu B, 24 (10%) for hMPV, 22 (9.1%) for Para 1 to 3, 5 (2.1%) for Adeno, 91 (37.8%) for RV, and 48 (20%) for RSV. Due to the low number of positive results for Para 1, 2, and 3, the analysis was performed after combining these analytes. The Fusion assay detected one Para 4-positive sample among the NP samples tested. Results comparing each target/assay against the established consensus positive are shown in Table 1. The Fusion and eSensor assays had 100% PPA for all the targets, whereas Lyra had 100% PPA for Flu A and Adeno analytes. A 100% NPA was observed for all the Lyra analytes tested, while that for the Fusion assay ranged from 98.4 to 100%. The NPAs for eSensor ranged from 99.4 to 100% for all the analytes except RV, for which the NPA was 93.5%. The Lyra assay had relatively high number (67) of invalid results for Flu A (13), Flu B (16), Para 1 to 3 (8), RSV (14), hMPV (14), and Adeno (2) when testing NP samples. The Lyra assay is designed such that there can be invalid results for each individual target in the multiplex assay.
TABLE 1.
Detection of respiratory viruses from NP samples compared to consensus positive
| Analyte | Panther Fusion |
eSensor |
Lyrac |
|||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| PPAa |
NPAb |
PPAa |
NPAb |
PPAa |
NPAb |
|||||||
| No. positive/no. consensus positive | % (95% CI) | No. positive/no. consensus positive | % (95% CI) | No. positive/no. consensus positive | % (95% CI) | No. positive/no. consensus positive | % (95% CI) | No. positive/no. consensus positive | % (95% CI) | No. positive/no. consensus positive | % (95% CI) | |
| Flu A | 33/33 | 100 (89.6–100) | 362/362 | 100 (98.9–100) | 33/33 | 100 (89.6–100) | 362/363 | 99.7 (98.4–100) | 33/33 | 100 (89.6–100) | 362/362 | 100 (98.9–100) |
| Flu B | 18/18 | 100 (82.4–100) | 377/377 | 100 (98.9–100) | 18/18 | 100 (82.4–100) | 377/377 | 100 (98.9–100) | 15/18 | 83.3 (60.8–94.2) | 377/377 | 100 (98.9–100) |
| RSV | 48/48 | 100 (92.6–100) | 347/347 | 100 (98.9–100) | 48/48 | 100 (92.6–100) | 347/349 | 99.4 (97.9–99.8) | 36/48 | 75 (61.2–85.1) | 347/347 | 100 (98.9–100) |
| Para 1–3 | 22/22 | 100 (85.1–100) | 373/374 | 99.7 (98.5–100) | 22/22 | 100 (85.1–100) | 373/375 | 99.5 (98.1–99.9) | 15/22 | 68.2 (47.3–83.6) | 373/373 | 100 (98.9–100) |
| hMPV | 24/24 | 100 (86.2–100) | 371/375 | 98.9 (97.3–99.6) | 24/24 | 100 (86.2–100) | 371/372 | 99.7 (98.5–100) | 19/24 | 79.2 (59.5–90.8) | 371/371 | 100 (98.9–100) |
| Adeno | 5/5 | 100 (56.6–100) | 390/390 | 100 (99–100) | 5/5 | 100 (56.6–100) | 390/391 | 99.7 (98.6–100) | 5/5 | 100 (56.6–100) | 390/390 | 100 (99–100) |
| RV | 91/91 | 100 (96–100) | 304/309 | 98.4 (96.2–99.3) | 91/91 | 100 (96–100) | 304/325 | 93.5 (89.7–95.4) | ||||
PPA, positive percent agreement.
NPA, negative percent agreement.
The Lyra assay does not test for the RV target.
Five coinfections were detected from NP samples with the Fusion and eSensor assays, including RSV/hMPV, Flu A/RV, Adeno/RV, Para 3/Adeno, and RSV/RV. The Lyra assay detected the coinfections except for those with RV, as the assay does not include this target.
Method comparison for LRT samples.
A total of 70 (67.3%) consensus positive samples were identified for LRT specimens among the 104 samples analyzed. There was one invalid LRT sample for all targets on the Lyra assay that was not included in the analysis. The LRT consensus positive samples include 15 (21.4%) for Flu A, 2 (2.9%) for Flu B, 6 (8.6%) for hMPV, 4 (5.7%) for Para 1 to 3, 5 (7.1%) for Adeno, 27 (38.6%) for RV, and 11 (15.7%) for RSV. Results comparing each target/assay against the established consensus positive are shown in Table 2. The Fusion had 100% PPA for all targets and 100% NPA for all the targets except hMPV (96.1%). There was 100% PPA for eSensor analytes, whereas the NPA ranged from 98 to 100%, except for RV (79.4%). For the Lyra assays the PPA ranged between 50% and 100%, while the NPA was 100% for all the targets except Adeno (98.9%).
TABLE 2.
Detection of respiratory viruses from LRT samples compared to consensus positive
| Analyte | Panther Fusion |
eSensor |
Lyraa |
|||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| PPA |
NPA |
PPA |
NPA |
PPA |
NPA |
|||||||
| No. positive/no. consensus positive | % (95% CI) | No. positive/no. consensus positive | % (95% CI) | No. positive/no. consensus positive | % (95% CI) | No. positive/no. consensus positive | % (95% CI) | No. positive/no. consensus positive | % (95% CI) | No. positive/no. consensus positive | % (95% CI) | |
| Flu A | 15/15 | 100 (79.6 −100) | 89/89 | 100 (95.9–100) | 15/15 | 100 (79.6–100) | 89/90 | 98.9 (94–99.8) | 15/15 | 100 (79.6–100) | 89/89 | 100 (95.9–100) |
| Flu B | 2/2 | 100 (34.2–100) | 102/102 | 100 (96.4–100) | 2/2 | 100 (34.2–100) | 102/102 | 100 (96.4–100) | 1/2 | 50 (9.5–90.6) | 102/102 | 100 (96.4–100) |
| RSV | 11/11 | 100 (74.1–100) | 93/93 | 100 (96–100) | 11/11 | 100 (74.1–100) | 93/94 | 98.9 (94.2–99.8) | 8/11 | 72.7 (43.4–90.3) | 93/93 | 100 (96–100) |
| Para 1–3 | 4/4 | 100 (51–100) | 100/100 | 100 (96.3–100) | 4/4 | 100 (51–100) | 100/102 | 98 (93–99.4) | 2/4 | 50 (15–85) | 100/100 | 100 (96.3–100) |
| hMPV | 6/6 | 100 (61–100) | 98/102 | 96.1 (90–98.4) | 6/6 | 100 (61–100) | 98/99 | 98.9 (94.4–99.8) | 4/6 | 66.7 (30–90.3) | 98/98 | 100 (96.2–100) |
| Adeno | 5/5 | 100 (56.6–100) | 99/99 | 100 (96.3–100) | 5/5 | 100 (56.6–100) | 99/99 | 100 (96.3–100) | 5/5 | 100 (56.6–100) | 99/100 | 98.9 (94.5–99.8) |
| RV | 27/27 | 100 (87.5–100) | 77/77 | 100 (95.3–100) | 27/27 | 100 (87.5–100) | 77/97 | 79.4 (63.3–82.5) | ||||
The Lyra assay does not test for the RV target.
Discordant resolution.
Samples with discrepant results (54 NP and 36 LRT samples) were evaluated further; the results are given in Tables 3 and 4 for NP and LRT specimens, respectively. Each analyte was analyzed separately for false-negative and false-positive results. With NP samples, the Lyra assay had significantly high rates of false-negative results for RSV (P = 0.007), hMPV (P = 0.009), and Para 1 to 3 (0.036) compared to results for Fusion and eSensor assays. The eSensor had higher rates of false-positive RV results (P < 0.0001) than did the Fusion assay. With LRT specimens, the Lyra assay had RSV false-negative results (P = 0.027), the eSensor had a greater number of false-positive results with Para 1 to 3 (P = 0.036) and RV (P < 0.0001), and the Fusion assay had false-positive hMPV results (P = 0.048).
TABLE 3.
Discordant analysis for NP samples
| Analyte | No. of false-negative results |
P valuea | No. of false-positive results |
P valuea | ||||
|---|---|---|---|---|---|---|---|---|
| Fusion | eSensor | Lyra | Fusion | eSensor | Lyra | |||
| Flu A | 0 | 0 | 0 | 0 | 1 | 0 | 0.333 | |
| Flu B | 0 | 1 | 3 | 0.102 | 0 | 1 | 0 | 0.333 |
| RSV | 1 | 2 | 9 | 0.007 | 0 | 3 | 3 | 0.087 |
| Para 1–3 | 0 | 1 | 4 | 0.036 | 0 | 2 | 0 | 0.111 |
| Adeno | 0 | 0 | 0 | 0 | 1 | 0 | 0.333 | |
| hMPV | 0 | 0 | 4 | 0.009 | 3 | 1 | 0 | 0.115 |
| RV | 7 | 2 | 0.079 | 0 | 11 | <0.0001 | ||
| Total | 8 | 6 | 20 | 3 | 20 | 3 | ||
P values of <0.05 were considered significant.
TABLE 4.
Discordant analysis for LRT samples
| Analyte | No. of false-negative results |
P valuea | No. of false-positive results |
P valuea | ||||
|---|---|---|---|---|---|---|---|---|
| Fusion | eSensor | Lyra | Fusion | eSensor | Lyra | |||
| Flu A | 0 | 0 | 0 | 0 | 1 | 0 | 0.332 | |
| Flu B | 0 | 0 | 1 | 0.268 | 0 | 0 | 0 | |
| RSV | 0 | 0 | 3 | 0.027 | 0 | 1 | 0 | 0.332 |
| Para 1–3 | 0 | 0 | 2 | 0.072 | 0 | 3 | 0 | 0.036 |
| Adeno | 1 | 2 | 0 | 0.194 | 0 | 1 | 0 | 0.332 |
| hMPV | 0 | 0 | 1 | 0.314 | 4 | 1 | 0 | 0.048 |
| RV | 2 | 0 | 0.091 | 0 | 17 | <0.0001 | ||
| Total | 3 | 2 | 7 | 4 | 24 | 0 | ||
P values of <0.05 were considered significant.
DISCUSSION
In this study, we assessed the performance characteristics of the Fusion assays in comparison to two FDA-cleared assays for detection of respiratory viruses using both NP and LRT specimens. Currently, there are no published studies evaluating the performance of Fusion respiratory panel with any comparator assays. When testing NP specimens, the Fusion assays had performance characteristics (PPA and NPA) comparable to those of the eSensor assay; the one notable exception is fewer false-positive RV results with the Fusion assay. The eSensor assay has cross-reactivity between RV and enterovirus D68 (12), while the Fusion assay is designed for RV specificity and does not cross-react with enterovirus D68 or D70 (13). Unfortunately, these samples could not be further investigated for the presence or absence of enterovirus(es) using another method due to limited sample volume. Overall, the Lyra assays showed lower PPA for several analytes (RSV, Para 1 to 3, and hMPV) than both the eSensor and Fusion assays. Comparable results were seen with all three assays when testing LRT specimens. Currently, none of these assays are FDA cleared for LRT specimens. FDA clearance for LRT specimens would be very helpful for clinical laboratories, as it would eliminate the need for each laboratory to perform a validation.
There were 5 coinfections detected by the Fusion and eSensor assays; the coinfections not detected by the Lyra assays were due to the assays not targeting RV. Given the low number of coinfections in this study, it is not possible to draw any meaningful conclusions, and further study of coinfections with the Fusion assays is needed.
There are several FDA-cleared multiplexed respiratory assays currently available for the detection of respiratory viruses, such as Biofire Filmarray (BioFire Diagnostics, LLC, Salt Lake City, UT), Luminex NxTAG (Luminex Corporation, Austin, TX), eSensor and ePlex (GenMark Diagnostics, Inc., Carlsbad, CA), Lyra (Quidel, San Diego, CA) Simplexa Flu A/B & RSV (Focus Diagnostics, Inc.), and Verigene Respiratory Pathogens Flex nucleic acid test (Nanosphere, Inc.). The Fusion system is a fully automated random-access testing system which can also be used to test different assays on a single patient sample in the same run. The eSensor has the advantage of testing all analytes in a single assay, while Fusion and Lyra require three and four assays, respectively, to cover the range of analytes. However, the small panel format of the Fusion and Lyra assays offers laboratories the flexibility to test samples to meet their specific needs.
There are several limitations to this study. As mentioned above, the comparator tests were not FDA cleared for LRT specimens; however, there are no other tests currently available that are cleared for LRT specimens that could have been used in this study. The storage of the specimens could have contributed to the high number of false-positive results seen with the eSensor test, as this testing was done on fresh samples, while the Lyra and Fusion tests were performed on frozen aliquots of these samples. The storage or freeze/thaw cycle could have led to nucleic acid degradation causing false-negative results with the Lyra and Fusion assays, which appear to be false-positive results with the eSensor test. There were very few samples collected from pediatric patients, so additional studies are needed for this patient population.
In conclusion, the Fusion assay performed with similar positive and negative predictive agreements to the eSensor assay for majority of the targets tested and provides laboratories a system to test for a broad array of viral respiratory pathogens.
ACKNOWLEDGMENTS
This work was supported by Hologic Inc. (San Diego, CA) and in part by the Lifespan/Tufts/Brown Center for AIDS Research (P30AI042853) and Emory Center for AIDS Research (P30AI050409).
Angela M. Caliendo is a member of the Quidel and Luminex Scientific Advisory Boards. Colleen S. Kraft is a member of the Luminex Scientific Advisory Board and is a consultant for Biomed-Valley Discoveries.
The remaining authors do not have any competing interests to disclose.
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