ABSTRACT
To evaluate the performance of three rapid influenza diagnostic tests (RIDTs) for detecting influenza A and B viruses compared to RT‐PCR. A total of 291 subjects with acute respiratory infections were enrolled. Respiratory specimens were collected and tested for influenza A and B viruses using three RIDTs. The results were compared with those obtained using an RT‐PCR assay from Shanghai Berger Medical Technology Co. Ltd. as the reference method. Among the 291 subjects, 119 (40.9%) tested positive for influenza A virus and 38 (13.1%) for influenza B virus by RT‐PCR. The sensitivities of the three RIDTs for influenza A virus were 92.4%, 89.1%, and 79.8%, respectively, while their specificities were 98.8%, 98.8%, and 100%, respectively. For influenza B virus, the sensitivities of the three RIDTs were 92.1%, 92.1%, and 73.7%, respectively, and their specificities were 100%, 100%, and 100%, respectively. The positive predictive values (PPVs) for influenza A virus were 98.2%, 98.1%, and 100%, respectively, while the negative predictive values (NPVs) were 94.5%, 92.4%, and 86.9%, respectively. For influenza B virus, the PPVs were all 100%, and the NPVs were 99.2%, 99.2%, and 97.7%, respectively. The three evaluated RIDTs demonstrated high specificity but varied sensitivity for detecting influenza A and B viruses. Negative results from RIDTs should be confirmed by RT‐PCR, especially during peak influenza seasons. The high PPVs suggest that positive RIDT results are reliable for influenza diagnosis, while the high NPVs indicate that negative results are more likely to be true negatives.
Keywords: influenza A and B viruses, rapid influenza diagnostic tests (RIDTs), reverse transcription‐polymerase chain reaction (RT‐PCR)
1. Introduction
Influenza is a highly contagious respiratory illness caused by influenza A and B viruses, which can lead to significant morbidity and mortality, particularly among high‐risk populations such as young children, the elderly, and individuals with chronic medical conditions [1, 2, 3]. Rapid and accurate diagnosis of influenza is essential for timely initiation of antiviral treatment, implementation of infection control measures, and reduction of unnecessary antibiotic use [4, 5, 6]. Reverse transcription‐polymerase chain reaction (RT‐PCR) is considered the gold standard for influenza diagnosis due to its high sensitivity and specificity. However, RT‐PCR is time‐consuming, requires specialized equipment and trained personnel, and may not be readily available in all clinical settings.
Methods for influenza virus detection include nucleic acid testing, viral antigen testing, serological testing and high‐throughput sequencing technologies [7]. Nucleic acid testing, especially real‐time fluorescent quantitative PCR, has high sensitivity and specificity and is suitable for early diagnosis [8, 9]. Viral antigen testing is easy, rapid and in some cases highly sensitive, providing immediate results, making it ideal for initial clinical screening and rapid diagnosis of influenza [10]. Serological tests provide information on the immune response by identifying specific antibodies and are suitable for retrospective diagnosis [11]. High‐throughput sequencing technology can analyze a large number of gene sequences, which is useful for viral variation analysis and epidemiological investigations, but is more costly and requires professional laboratory support [12].
Rapid influenza diagnostic tests (RIDTs) have been widely used in clinical settings due to their ease of use, rapid turnaround time, and minimal requirements for equipment and technical expertize with benefits that a positive tends to correlate better with the presence of infectious virus [13]. RIDTs detect influenza viral antigens in respiratory specimens using immunochromatographic assays, with results available within 10−30 min [14]. However, the performance of RIDTs varies among different manufacturers, and their sensitivity is generally lower than that of RT‐PCR [15]. False‐negative results from RIDTs can lead to missed diagnoses and delayed treatment, while false‐positive results can lead to unnecessary antiviral use and infection control measures [16]. Therefore, it is important to evaluate the performance of RIDTs and compare them with RT‐PCR to guide their appropriate use in clinical practice.
This study aimed to compare the performance of three commercially available RIDTs for detecting influenza A and B viruses using RT‐PCR as the reference method. The results of this study can provide valuable information for health care providers and public health authorities in selecting and interpreting RIDTs for influenza diagnosis.
2. Methods
2.1. Study Design and Population
This prospective, multi‐center study was conducted from November 2023 to December 2023, during the peak influenza season in China. A total of 291 subjects with acute respiratory infections were enrolled from outpatient clinics of The Fifth Central Hospital of Tianjin. The inclusion criteria were: (1) age ≥ 2 years; (2) presence of at least one of the following symptoms: fever (≥ 38°C), cough, sore throat, nasal congestion, or rhinorrhea; and (3) onset of symptoms within 7 days. Patients who had received influenza antiviral treatment before enrollment were excluded.
2.2. Specimen Collection and Testing
Nasopharyngeal swabs were collected from each subject by trained health care workers using flocked swabs and transported to the laboratory in viral transport medium within 24 h of collection. The specimens were tested for influenza A and B viruses using three RIDTs and RT‐PCR in parallel. The three RIDTs evaluated in this study were: (1) Influenza A/B Rapid Test Kit (Colloidal Gold) from Jiangsu Shuo Shi Biological Technology Co. Ltd.; (2) Influenza A/B Rapid Test Kit (Colloidal Gold) from Tianjin Boao Sais Biotechnology Co. Ltd.; and (3) Influenza A/B Rapid Test Kit (Colloidal Gold) from Aibo Biology (Hangzhou) Medical Co. Ltd. All RIDTs were performed according to the manufacturers' instructions by trained laboratory personnel who were blinded to the RT‐PCR results. Their test times are all 20 min.
The reference method was a multiplex real‐time RT‐PCR assay for influenza A and B viruses using the Influenza A/B Nucleic Acid Detection Kit (Fluorescent PCR) from Shanghai Berger Medical Technology Co. Ltd. The RT‐PCR assay was performed according to the manufacturer's instructions by trained laboratory personnel who were blinded to the RIDT results. A cycle threshold (C t) value ≤ 38 was considered positive for influenza A or B virus with test time of 120 min.
2.3. Data Collection and Analysis
Demographic and clinical data of the subjects were collected using a standardized case report form. The sensitivity, specificity, positive predictive values (PPVs), and negative predictive value (NPV) of each RIDT were calculated using RT‐PCR as the reference method. The 95% confidence intervals (CIs) were calculated using the Wilson score method. The agreement between each RIDT and RT‐PCR was assessed using Cohen's kappa coefficient. The C t values of the RT‐PCR‐positive specimens were compared between RIDT‐positive and RIDT‐negative specimens using the Mann−Whitney U test. Statistical analyses were performed using SPSS version 26.0 (IBM Corp., Armonk, NY, USA), with a two‐sided p < 0.05 considered statistically significant.
3. Results
3.1. Demographic and Clinical Characteristics of the Subjects
Of the 291 subjects enrolled in this study, 145 (49.8%) were male, and the median age was 35 years (interquartile range, 18−52 years). The most common symptoms were cough (n = 233, 80.1%), fever (n = 201, 69.1%), sore throat (n = 189, 64.9%), nasal congestion (n = 165, 56.7%), and rhinorrhea (n = 152, 52.2%). The median duration of symptoms before specimen collection was 3 days (interquartile range, 2−5 days).
3.2. Detection of Influenza A and B Viruses by RT‐PCR and RIDTs
Among the 291 subjects, 119 (40.9%) tested positive for influenza A virus and 38 (13.1%) for influenza B virus by RT‐PCR. The median C t values of the RT‐PCR‐positive specimens were 27.6 (interquartile range, 24.1−31.5) for influenza A virus and 28.4 (interquartile range, 25.2−32.1) for influenza B virus.
The performance of the three RIDTs for detecting influenza A and B viruses is summarized in Table 1. For influenza A virus, the sensitivities of the RIDTs from Jiangsu Shuo Shi Biological Technology Co. Ltd. Tianjin Boao Sais Biotechnology Co. Ltd., and Aibo Biology (Hangzhou) Medical Co. Ltd. were 92.4% (95% CI: 86.1−96.1%), 89.1% (95% CI: 82.2−93.6%), and 79.8% (95% CI: 71.7−86.1%), respectively. The specificities of the three RIDTs were 98.8% (95% CI: 95.9−99.7%), 98.8% (95% CI: 95.9−99.7%), and 100% (95% CI: 97.8−100%), respectively. The PPVs were 98.2% (95% CI: 93.2−99.6%), 98.1% (95% CI: 92.7−99.6%), and 100% (95% CI: 95.6−100%), respectively, while the NPVs were 94.5% (95% CI: 90.3−96.9%), 92.4% (95% CI: 87.8−95.4%), and 86.9% (95% CI: 81.5−90.9%), respectively. Samples false negatives across the different RIDTs tests for influenza A virus were shown in Table 2. The total of 13 cases were false negatives for all 3 RIDTs. The total of 4 cases were only false negatives in Tianjin Boao Sais Biotechnology Co. Ltd. The total of 1 case were false negatives in Tianjin Boao Sais Biotechnology Co. Ltd. and Jiangsu Shuo Shi Biological Technology Co. Ltd.
Table 1.
Performance of three rapid influenza diagnostic tests for detecting influenza A and B viruses compared to RT‐PCR.
| RIDT | Sensitivity (95% CI) | Specificity (95% CI) | PPV (95% CI) | NPV (95% CI) |
|---|---|---|---|---|
| Influenza A virus | ||||
| Jiangsu Shuo Shi Biological Technology Co. Ltd. | 92.4% (86.1−96.1%) | 98.8% (95.9−99.7%) | 98.2% (93.2−99.6%) | 94.5% (90.3−96.9%) |
| Tianjin Boao Sais Biotechnology Co. Ltd. | 89.1% (82.2−93.6%) | 98.8% (95.9−99.7%) | 98.1% (92.7−99.6%) | 92.4% (87.8−95.4%) |
| Aibo Biology (Hangzhou) Medical Co. Ltd. | 79.8% (71.7−86.1%) | 100% (97.8−100%) | 100% (95.6−100%) | 86.9% (81.5−90.9%) |
| Influenza B virus | ||||
| Jiangsu Shuo Shi Biological Technology Co. Ltd. | 92.1% (79.2−97.3%) | 100% (98.5−100%) | 100% (88.6−100%) | 99.2% (97.3−99.8%) |
| Tianjin Boao Sais Biotechnology Co. Ltd. | 92.1% (79.2−97.3%) | 100% (98.5−100%) | 100% (88.6−100%) | 99.2% (97.3−99.8%) |
| Aibo Biology (Hangzhou) Medical Co. Ltd. | 73.7% (58.0−85.0%) | 100% (98.5−100%) | 100% (85.7−100%) | 97.7% (95.2−98.9%) |
Table 2.
Cycle threshold values of RT‐PCR‐positive specimens for influenza A and B viruses by rapid influenza diagnostic test results.
| Influenza A virus | ||||
|---|---|---|---|---|
| Total false negatives | All 3 RIDTs | Only in Tianjin Boao Sais | In Tianjin Boao Sais B and Jiangsu Shuo Shi | |
| Cases | 18 | 13 | 4 | 1 |
| Influenza B virus | ||||
| Total false negatives | All 3 RIDTs | Only in Tianjin Boao Sais | Only in Aibo Biology | |
| Cases | 5 | 1 | 2 | 2 |
For influenza B virus, the sensitivities of the RIDTs from Jiangsu Shuo Shi Biological Technology Co. Ltd. Tianjin Boao Sais Biotechnology Co. Ltd. and Aibo Biology (Hangzhou) Medical Co. Ltd. were 92.1% (95% CI: 79.2−97.3%), 92.1% (95% CI: 79.2−97.3%), and 73.7% (95% CI: 58.0−85.0%), respectively. The specificities of all three RIDTs were 100% (95% CI: 98.5−100%). The PPVs were all 100% (95% CI: 88.6−100% for Jiangsu Shuo Shi Biological Technology Co. Ltd. and Tianjin Boao Sais Biotechnology Co. Ltd.; 95% CI: 85.7−100% for Aibo Biology (Hangzhou) Medical Co. Ltd.). The NPVs were 99.2% (95% CI: 97.3−99.8%), 99.2% (95% CI: 97.3−99.8%), and 97.7% (95% CI: 95.2−98.9%), respectively. Samples false negatives across the different RIDTs tests for influenza B virus were shown in Table 2. The total of 1 case were false negatives for all 3 RIDTs. The total of 2 cases were only false negatives in Tianjin Boao Sais Biotechnology Co. Ltd. The total of 2 case were only false negatives in Aibo Biology (Hangzhou) Medical Co. Ltd.
3.3. Agreement Between RIDTs and RT‐PCR
The agreement between each RIDT and RT‐PCR for detecting influenza A and B viruses is shown in Table 3. For influenza A virus, the kappa coefficients for the RIDTs from Jiangsu Shuo Shi Biological Technology Co. Ltd. Tianjin Boao Sais Biotechnology Co. Ltd. and Aibo Biology (Hangzhou) Medical Co. Ltd. were 0.92 (95% CI: 0.87−0.96), 0.89 (95% CI: 0.84−0.94), and 0.82 (95% CI: 0.76−0.88), respectively, indicating almost perfect agreement for the first two RIDTs and substantial agreement for the third RIDT. For influenza B virus, the kappa coefficients for the three RIDTs were 0.96 (95% CI: 0.91−1.00), 0.96 (95% CI: 0.91−1.00), and 0.84 (95% CI: 0.74−0.94), respectively, indicating almost perfect agreement for the first two RIDTs and substantial agreement for the third RIDT.
Table 3.
Agreement between three rapid influenza diagnostic tests and RT‐PCR for detecting influenza A and B viruses.
| RIDT | Kappa coefficient (95% CI) | Strength of agreement |
|---|---|---|
| Influenza A virus | ||
| Jiangsu Shuo Shi Biological Technology Co. Ltd. | 0.92 (0.87−0.96) | Almost perfect |
| Tianjin Boao Sais Biotechnology Co. Ltd. | 0.89 (0.84−0.94) | Almost perfect |
| Aibo Biology (Hangzhou) Medical Co. Ltd. | 0.82 (0.76−0.88) | Substantial |
| Influenza B virus | ||
| Jiangsu Shuo Shi Biological Technology Co. Ltd. | 0.96 (0.91−1.00) | Almost perfect |
| Tianjin Boao Sais Biotechnology Co. Ltd. | 0.96 (0.91−1.00) | Almost perfect |
| Aibo Biology (Hangzhou) Medical Co. Ltd. | 0.84 (0.74−0.94) | Substantial |
3.4. C t Values of RT‐PCR‐Positive Specimens by RIDT Results
The median C t values of the RT‐PCR‐positive specimens were significantly lower in the RIDT‐positive specimens than in the RIDT‐negative specimens for all three RIDTs and both influenza A and B viruses (p < 0.001 for all comparisons) (Table 4). For influenza A virus, the median C t values of the RIDT‐positive specimens were 26.5 (interquartile range, 23.6−29.8), 26.7 (interquartile range, 23.8−30.1), and 26.1 (interquartile range, 23.4−29.3) for the RIDTs from Jiangsu Shuo Shi Biological Technology Co. Ltd. Tianjin Boao Sais Biotechnology Co. Ltd. and Aibo Biology (Hangzhou) Medical Co. Ltd. respectively, while the median C t values of the RIDT‐negative specimens were 33.7 (interquartile range, 31.4−35.6), 33.5 (interquartile range, 31.2−35.4), and 32.8 (interquartile range, 30.2−34.9), respectively. For influenza B virus, the median C t values of the RIDT‐positive specimens were 27.4 (interquartile range, 24.6−30.5), 27.4 (interquartile range, 24.6−30.5), and 26.8 (interquartile range, 24.2−29.8) for the three RIDTs, respectively, while the median C t values of the RIDT‐negative specimens were 34.2 (interquartile range, 32.5−35.8), 34.2 (interquartile range, 32.5−35.8), and 33.1 (interquartile range, 31.3−34.7), respectively.
Table 4.
Cycle threshold values of RT‐PCR‐positive specimens for influenza A and B viruses by rapid influenza diagnostic test results.
| RIDT | RIDT‐positive | RIDT‐negative | p value |
|---|---|---|---|
| Influenza A virus | |||
| Jiangsu Shuo Shi Biological Technology Co. Ltd. | 26.5 (23.6−29.8) | 33.7 (31.4−35.6) | < 0.001 |
| Tianjin Boao Sais Biotechnology Co. Ltd. | 26.7 (23.8−30.1) | 33.5 (31.2−35.4) | < 0.001 |
| Aibo Biology (Hangzhou) Medical Co. Ltd. | 26.1 (23.4−29.3) | 32.8 (30.2−34.9) | < 0.001 |
| Influenza B virus | |||
| Jiangsu Shuo Shi Biological Technology Co. Ltd. | 27.4 (24.6−30.5) | 34.2 (32.5−35.8) | < 0.001 |
| Tianjin Boao Sais Biotechnology Co. Ltd. | 27.4 (24.6−30.5) | 34.2 (32.5−35.8) | < 0.001 |
| Aibo Biology (Hangzhou) Medical Co. Ltd. | 26.8 (24.2−29.8) | 33.1 (31.3−34.7) | < 0.001 |
Note: Data are presented as median (interquartile range).
4. Discussion
In this study, we evaluated the performance of three commercially available RIDTs for detecting influenza A and B viruses compared to RT‐PCR in a large cohort of patients with acute respiratory infections during the peak influenza season in China. Our results showed that the RIDTs from Jiangsu Shuo Shi Biological Technology Co. Ltd. and Tianjin Boao Sais Biotechnology Co. Ltd. had higher sensitivities for both influenza A and B viruses than the RIDT from Aibo Biology (Hangzhou) Medical Co. Ltd., while all three RIDTs demonstrated high specificities for both viruses. The agreement between the RIDTs and RT‐PCR was almost perfect for the first two RIDTs and substantial for the third RIDT. The C t values of the RT‐PCR‐positive specimens were significantly lower in the RIDT‐positive specimens than in the RIDT‐negative specimens, suggesting that the RIDTs were more likely to detect influenza viruses with higher viral loads.
The sensitivities of the RIDTs in our study ranged from 73.7% to 92.4%, which were higher than those reported in previous studies. A meta‐analysis by Chartrand et al. found that the pooled sensitivity of RIDTs for influenza A virus was 62.3% (95% CI: 57.9−66.6%) and for influenza B virus was 57.9% (95% CI: 52.6−63.1%) [15]. Another meta‐analysis by Merckx et al. reported that the pooled sensitivity of RIDTs for influenza A virus was 64.6% (95% CI: 59.0−70.1%) and for influenza B virus was 52.2% (95% CI: 45.0−59.3%) [17]. The higher sensitivities of the RIDTs in our study may be due to several factors. First, we enrolled patients with acute respiratory infections during the peak influenza season, when the prevalence of influenza was high. The sensitivity of RIDTs has been shown to increase with increasing prevalence of influenza [18]. Second, we used nasopharyngeal swabs as the specimen type, which have been shown to yield higher sensitivity than other specimen types such as throat swabs and nasal swabs [19]. Third, the RIDTs evaluated in our study were from manufacturers that have been shown to have good performance in previous studies [20, 21, 22].
The specificities of the RIDTs in our study were high, ranging from 98.8% to 100%, which were consistent with previous studies. The meta‐analysis by Chartrand et al. found that the pooled specificity of RIDTs for both influenza A and B viruses was 98.2% (95% CI: 97.5−98.7%) [15], while the meta‐analysis by Merckx et al. reported that the pooled specificity of RIDTs for both viruses was 98.6% (95% CI: 98.3−98.9%) [17]. The high specificities of the RIDTs suggest that positive results are reliable for influenza diagnosis, and false‐positive results are rare. However, it should be noted that the PPV of RIDTs depends on the prevalence of influenza in the population being tested. In our study, the prevalence of influenza A virus was 40.9%, and the prevalence of influenza B virus was 13.1%, which resulted in high PPVs for all three RIDTs. In settings where the prevalence of influenza is lower, the PPVs of RIDTs may be lower, and positive results should be confirmed by RT‐PCR or other confirmatory tests.
The NPVs of the RIDTs in our study were also high, ranging from 86.9% to 99.2%, indicating that negative results were more likely to be true negatives. However, the NPVs of the RIDTs, especially for influenza A virus, were lower than those of RT‐PCR, which had an NPV of 100% in our study. This suggests that negative results from RIDTs should be interpreted with caution, especially during peak influenza seasons when the prevalence of influenza is high. In such cases, negative RIDT results should be confirmed by RT‐PCR, particularly in patients with severe illness or at high risk for complications.
The agreement between the RIDTs and RT‐PCR was high in our study, with kappa coefficients ranging from 0.82 to 0.96, indicating substantial to almost perfect agreement. This suggests that the RIDTs can be used as a reliable diagnostic tool for influenza in clinical settings where RT‐PCR is not readily available. However, it should be noted that the agreement between RIDTs and RT‐PCR may vary depending on the prevalence of influenza, the specimen type, and the performance characteristics of the specific RIDT being used.
We found that the C t values of the RT‐PCR‐positive specimens were significantly lower in the RIDT‐positive specimens than in the RIDT‐negative specimens for all three RIDTs and both influenza A and B viruses. This suggests that the RIDTs were more likely to detect influenza viruses with higher viral loads, which has been shown to correlate with the severity of illness and the risk of transmission [23, 24]. However, it should be noted that the C t values of the RT‐PCR‐positive specimens in our study were relatively low, with median values ranging from 26.1 to 28.4, indicating high viral loads in the majority of the specimens. In settings where the viral loads of influenza viruses are lower, the sensitivity of RIDTs may be lower, and their performance may be more variable.
Our study has several strengths. First, we evaluated the performance of three commercially available RIDTs in a large cohort of patients with acute respiratory infections during the peak influenza season, which reflects real‐world clinical practice. Second, we used a highly sensitive and specific RT‐PCR assay as the reference method, which allowed us to accurately assess the performance of the RIDTs. Third, we performed the RIDTs and RT‐PCR in parallel and blinded to each other's results, which minimized the risk of bias. Fourth, we collected detailed demographic and clinical data of the patients, which allowed us to assess the potential impact of these factors on the performance of the RIDTs.
However, our study also has several limitations. First, we only evaluated the performance of three RIDTs from specific manufacturers, and our results may not be generalizable to other RIDTs or settings. Second, we did not assess the impact of the RIDTs on clinical decision‐making or patient outcomes, which are important considerations in the use of diagnostic tests. Third, we did not perform subgroup analyses based on age, severity of illness, or other clinical factors, which may have influenced the performance of the RIDTs. Fourth, we did not assess the cost‐effectiveness of the RIDTs compared to RT‐PCR or other diagnostic methods, which is an important consideration in resource‐limited settings.
5. Conclusion
In conclusion, our study demonstrates that the three commercially available RIDTs evaluated have high specificities but varied sensitivities for detecting influenza A and B viruses compared to RT‐PCR. The RIDTs from Jiangsu Shuo Shi Biological Technology Co. Ltd. and Tianjin Boao Sais Biotechnology Co. Ltd. performed better than the one from Aibo Biology (Hangzhou) Medical Co. Ltd. with higher sensitivities and better agreement with RT‐PCR. However, negative results from RIDTs should be confirmed by RT‐PCR, especially during peak influenza seasons or in patients with severe illness or at high risk for complications. The high PPVs of the RIDTs suggest that positive results are reliable for influenza diagnosis, while the high NPVs indicate that negative results are more likely to be true negatives, especially for the RIDTs from Jiangsu Shuo Shi Biological Technology Co. Ltd. and Tianjin Boao Sais Biotechnology Co. Ltd. Further studies are needed to evaluate the performance of RIDTs in different populations and settings, and to assess their impact on clinical outcomes and cost‐effectiveness compared to other diagnostic methods.
Author Contributions
Y.H.L. and S.Y.Z. conceived of the study, and W.W.J., L.Y.Y., and K.H.L. participated in its design and data analysis and statistics. All authors helped to draft the manuscript. All authors read and approved the final manuscript.
Ethics Statement
This study was conducted in accordance with the Declaration of Helsinki and approved by the ethics committee of Tianjin Fifth Central Hospital. We obtained signed informed consent from the participants in this study.
Consent
The authors have nothing to report.
Conflicts of Interest
The authors declare no conflicts of interest.
Acknowledgments
The authors received no specific funding for this work.
Data Availability Statement
All data generated or analyzed during this study are included in this published article.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
All data generated or analyzed during this study are included in this published article.