Impact of Nonpharmaceutical Interventions during the COVID-19 Pandemic on the Prevalence of Respiratory Syncytial Virus in Hospitalized Children with Lower Respiratory Tract Infections: A Systematic Review and Meta-Analysis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Search Strategy and Selection Criteria
2.2. Data Analysis
3. Results
3.1. Search Results
3.2. Characteristics of the Included Articles
3.3. Subgroup Analysis
3.4. Sensitivity Analysis
3.5. Stratified Analysis by World Health Organizations Regions, Countries, and Age Stratum
3.6. Meta-Regression Model Analysis
3.7. Analysis of Intensive Care Unit Admissions and Mortality
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Characteristics | N = 112 | % |
---|---|---|
Age range | ||
| 35 | 31.3 |
| 22 | 19.6 |
| 4 | 3.6 |
| 20 | 17.9 |
| 27 | 24.1 |
| 4 | 3.6 |
Male range (%) | 39.1–73.8% | |
Period of inclusion of participants; range | January 2015–December 2022 | |
Year of publication; range | 2017–2023 | |
Study design | ||
| 75 | 67 |
| 37 | 33 |
Sampling method | ||
| 110 | 98.2 |
| 2 | 1.8 |
Timing of data collection | ||
| 4 | 3.6 |
| 58 | 51.8 |
| 50 | 44.6 |
Study bias | ||
| 71 | 63.4 |
| 41 | 36.6 |
WHO region | ||
| 7 | 6.3 |
| 13 | 11.6 |
| 3 | 2.7 |
| 47 | 42 |
| 8 | 7.1 |
| 34 | 30.4 |
Type of assay | ||
| 22 | 19.6 |
| 85 | 75.9 |
| 5 | 4.5 |
Diagnostic technique $ | ||
| 6 | 5.4 |
| 16 | 14.3 |
| 5 | 4.5 |
| 14 | 12.5 |
| 18 | 16.1 |
| 16 | 14.3 |
| 2 | 1.8 |
| 31 | 27.7 |
| 4 | 3.6 |
Sample type | ||
| 7 | 6.3 |
| 9 | 8 |
| 62 | 55.4 |
| 11 | 9.8 |
| 8 | 7.1 |
| 7 | 6.3 |
| 3 | 2.7 |
| 5 | 4.5 |
Groups | Studies (n) | RSV-Positive (n) | Total (n) | Pooled Prevalence (95% CI) | Q-Value | I2 (%) | p Value Heterogeneity | p Value Egger Test | p Value Subgroup Difference |
---|---|---|---|---|---|---|---|---|---|
Overall | 112 | 45,900 | 308,985 | 21.51 [18.42; 24.96] | 22,893.65 | 99.0 | <0.0001 | <0.0001 | NA |
Subgroup analyses | |||||||||
Period | <0.0001 | ||||||||
Pre-pandemic (2015/20) | 83 | 33,735 | 223,673 | 25.60 [22.57; 28.88] | 15,032.9 | 99.0 | <0.0001 | <0.0001 | |
Lockdown (2020/21) | 46 | 4556 | 50,298 | 5.03 [2.67; 9.28] | 2581.79 | 98.3 | <0.0001 | 0.5569 | |
Post-lockdown (2021/22) | 28 | 7609 | 35,014 | 42.02 [31.49; 53.33] | 3765.28 | 99.3 | <0.0001 | <0.0001 | |
Seasons | <0.0001 | ||||||||
2015/16 | 24 | 7043 | 33,225 | 24.19 [19.45; 29.66] | 1620.84 | 98.60 | <0.0001 | 0.2232 | |
2016/17 | 21 | 4153 | 24,024 | 24.10 [17.86; 31.68] | 1298.39 | 98.50 | <0.0001 | 0.035 | |
2017/18 | 26 | 5295 | 40,942 | 28.82 [20.40; 39.01] | 2855.18 | 99.10 | <0.0001 | 0.0003 | |
2018/19 | 34 | 7369 | 41,586 | 27.02 [21.41; 33.47] | 2139.94 | 98.50 | <0.0001 | 0.0011 | |
2019/20 | 42 | 9875 | 83,896 | 24.29 [18.23; 31.58] | 5676.49 | 99.30 | <0.0001 | 0.0003 | |
2020/21 | 46 | 4556 | 50,298 | 5.03 [2.67; 9.28] | 2581.79 | 98.30 | <0.0001 | 0.5569 | |
2021/22 | 28 | 7609 | 35,014 | 42.02 [31.49; 53.33] | 3765.28 | 99.30 | <0.0001 | <0.0001 | |
WHO Region | 0.0004 | ||||||||
African | 7 | 837 | 3602 | 19.42 [14.19; 25.98] | 224.25 | 96.0 | <0.0001 | 0.0276 | |
Americas | 13 | 2029 | 6370 | 11.17 [2.19; 41.42] | 194.76 | 93.3 | <0.0001 | 0.7522 | |
Eastern Mediterranean | 3 | 151 | 568 | 26.53 [15.66; 41.25] | 33.53 | 94.0 | <0.0001 | NA | |
European | 47 | 14,877 | 70,357 | 28.90 [22.73; 35.98] | 7570.45 | 98.7 | <0.0001 | 0.0004 | |
South–East Asia | 8 | 1283 | 5987 | 24.85 [14.25; 39.67] | 758.49 | 98.7 | <0.0001 | 0.6948 | |
Western Pacific | 34 | 26,723 | 222,101 | 14.71 [12.28; 17.52] | 8245.53 | 99.0 | <0.0001 | 0.1071 | |
Age | <0.0001 | ||||||||
<2 years | 35 | 6815 | 17,696 | 43.54 [35.56; 51.87] | 1972.43 | 96.7 | <0.0001 | 0.0017 | |
<5 years | 22 | 7223 | 36,599 | 25.59 [21.03; 30.76] | 2760.33 | 98.8 | <0.0001 | 0.0781 | |
<10 years | 4 | 7706 | 65,262 | 17.34 [11.89; 24.58] | 1267.48 | 99.0 | <0.0001 | 0.1347 | |
<15 years | 20 | 5745 | 40,646 | 17.58 [12.82; 23.64] | 4016.97 | 99.1 | <0.0001 | 0.7428 | |
<18 years | 27 | 17,408 | 139,980 | 10.17 [7.29; 14.02] | 5,380.77 | 99.0 | <0.0001 | 0.9850 | |
Not reported | 4 | 1003 | 8802 | 9.94 [5.19; 18.18] | 276.85 | 95.7 | <0.0001 | 0.3230 | |
Design | 0.0840 | ||||||||
Cross-sectional | 75 | 35,091 | 263,251 | 19.64 [16.55; 23.15] | 15,271.27 | 98.9 | <0.0001 | <0.0001 | |
Longitudinal | 37 | 10,809 | 45,734 | 27.34 [19.47; 36.94] | 4589.11 | 98.8 | <0.0001 | 0.0379 | |
Timing of data collection | 0.5983 | ||||||||
Ambispective | 4 | 1449 | 11,714 | 15.30 [4.70; 39.82] | 657.29 | 98.8 | <0.0001 | NA | |
Prospective | 58 | 12,676 | 66,479 | 23.44 [18.63; 29.05] | 7496.05 | 98.9 | <0.0001 | 0.1370 | |
Retrospective | 50 | 31,775 | 230,792 | 20.82 [16.90; 25.37] | 12,692.16 | 99.0 | <0.0001 | 0.0007 | |
Risk of bias | 0.1453 | ||||||||
Low risk | 71 | 31,179 | 222,366 | 23.29 [19.18; 27.98] | 17,585.49 | 99.2 | <0.0001 | <0.0001 | |
Moderate risk | 41 | 14,721 | 86,619 | 18.49 [14.32; 23.54] | 5058.52 | 98.5 | <0.0001 | 0.0752 | |
Type of assay | 0.0007 | ||||||||
Immune assays ¥ | 22 | 19,476 | 180,647 | 13.94 [10.65; 18.04] | 4163.17 | 98.9 | <0.0001 | 0.5255 | |
Molecular assays ¥¥ | 85 | 22,523 | 103,157 | 24.96 [20.77; 29.69] | 10,441.27 | 98.5 | <0.0001 | 0.0350 | |
Mixed assays ¥¥¥ | 5 | 3901 | 25,181 | 14.74 [8.27; 24.91] | 872.62 | 96.3 | <0.0001 | 0.3155 | |
Diagnostic technique $ | 0.0016 | ||||||||
Antigen testing | 6 | 8018 | 75,112 | 17.78 [10.71; 28.05] | 1187.05 | 98.9 | <0.0001 | 0.4242 | |
Direct immunofluorescence | 16 | 11,458 | 105,535 | 12.46 [9.14; 16.77] | 2892.56 | 99.0 | <0.0001 | 0.8831 | |
Mixed assays ¥¥¥ | 5 | 3901 | 25,181 | 14.74 [8.27; 24.91] | 1187.05 | 98.9 | <0.0001 | 0.3155 | |
Multiplex PCR | 14 | 2083 | 10,831 | 27.32 [14.57; 45.30] | 2965.49 | 99.0 | <0.0001 | 0.0439 | |
Multiplex RT–PCR | 18 | 2215 | 7385 | 30.89 [22.03; 41.42] | 872.62 | 98.3 | <0.0001 | 0.3490 | |
PCR | 16 | 7247 | 32,319 | 24.91 [16.89; 35.12] | 1756.55 | 98.7 | <0.0001 | 0.8591 | |
qPCR | 2 | 52 | 140 | 38.93 [21.17; 60.20] | 828.23 | 97.0 | 0.0008 | NA | |
RT–PCR | 31 | 9193 | 46,668 | 22.15 [16.57; 28.95] | 3648.00 | 99.1 | <0.0001 | 0.0936 | |
RT–qPCR | 4 | 1733 | 5814 | 17.82 [3.59; 55.79] | 11.32 | 91.2 | <0.0001 | NA | |
Sample type | 0.0023 | ||||||||
Mixed specimens * | 7 | 3091 | 14,765 | 18.35 [8.59; 34.98] | 1408.90 | 99.0 | <0.0001 | 0.7840 | |
Nasal secretions | 9 | 1209 | 3493 | 21.39 [6.94; 49.83] | 263.44 | 95.8 | <0.0001 | 0.5521 | |
Nasopharyngeal secretions | 62 | 21,542 | 114,495 | 26.25 [21.48; 31.66] | 9150.13 | 98.7 | <0.0001 | <0.0001 | |
Nasopharyngeal secretions or BLF | 11 | 4374 | 52,107 | 12.12 [8.34; 17.28] | 1848.89 | 98.6 | <0.0001 | 0.0770 | |
Not reported | 8 | 10,981 | 85,775 | 21.26 [10.99; 37.13] | 2581.81 | 99.3 | <0.0001 | 0.0036 | |
Oropharyngeal secretions | 7 | 2663 | 20,375 | 15.48 [12.23; 19.39] | 778.85 | 97.7 | <0.0001 | 0.2721 | |
Sputum | 3 | 549 | 2063 | 25.23 [18.38; 33.58] | 44.03 | 95.5 | <0.0001 | NA | |
Throat secretions | 5 | 1491 | 15,912 | 16.79 [7.88; 32.26] | 1097.90 | 99.3 | <0.0001 | NA |
Groups | Studies (n) | RSV-Positive (n) | Total (n) | Pooled Prevalence (95% CI) | Q-Value | I2 (%) | p Value Heterogeneity | p Value Egger Test | p Value Subgroup Difference |
---|---|---|---|---|---|---|---|---|---|
WHO Region ## | |||||||||
European | 47 | 14,877 | 70,357 | 28.90 [22.73; 35.98] | 7570.45 | 98.7 | <0.0001 | 0.0004 | |
Period | <0.0001 | ||||||||
Pre-pandemic (2015/20) | 28 | 10,348 | 48,140 | 34.81 [29.47; 40.56] | 3905.86 | 98.50 | <0.0001 | 0.0001 | |
Lockdown (2020/21) | 23 | 1028 | 12,898 | 4.89 [1.68; 13.39] | 853.67 | 97.40 | <0.0001 | 0.7463 | |
Post-lockdown (2021/22) | 18 | 3501 | 9319 | 55.18 [42.96; 66.80] | 1479.62 | 98.90 | <0.0001 | 0.0093 | |
Western Pacific | 34 | 26,723 | 222,101 | 14.71 [12.28; 17.52] | 8245.53 | 99.0 | <0.0001 | 0.1071 | |
Period | 0.0024 | ||||||||
Pre-pandemic (2015/20) | 29 | 19,728 | 162,313 | 16.12 [13.28; 19.43] | 6290.45 | 99.10 | <0.0001 | 0.0424 | |
Lockdown (2020/21) | 16 | 3215 | 34,966 | 8.03 [4.99; 12.68] | 1240.05 | 98.80 | <0.0001 | 0.5502 | |
Post-lockdown (2021/22) | 8 | 3780 | 24,822 | 22.83 [15.42; 32.42] | 356.45 | 98.00 | <0.0001 | NA | |
Countries && | |||||||||
Italy | 20 | 5437 | 14,928 | 47.14 [37.07; 57.45] | 1877.72 | 97.8 | <0.0001 | 0.0011 | |
Period | 0.0024 | ||||||||
Pre-pandemic (2015/20) | 10 | 2955 | 9600 | 51.87 [43.11; 60.51] | 815.15 | 97.40 | <0.0001 | <0.0001 | |
Lockdown (2020/21) | 8 | 43 | 801 | 5.93 [0.89; 30.68] | 110.71 | 93.70 | <0.0001 | NA | |
Post-lockdown (2021/22) | 13 | 2439 | 4527 | 63.59 [53.25; 72.81] | 381.83 | 96.90 | <0.0001 | 0.0136 | |
China | 27 | 23,416 | 211,831 | 11.33 [9.61; 13.30] | 4416.56 | 98.6 | <0.0001 | 0.6889 | |
Period | 0.0002 | ||||||||
Pre-pandemic (2015/20) | 23 | 16,898 | 153,351 | 12.04 [10.12; 14.26] | 3350.33 | 98.70 | <0.0001 | 0.79 | |
Lockdown (2020/21) | 12 | 2868 | 34,012 | 6.64 [4.83; 9.07] | 347.18 | 96.80 | <0.0001 | 0.0314 | |
Post-lockdown (2021/22) | 6 | 3650 | 24,468 | 19.89 [12.49; 30.15] | 237.17 | 97.90 | <0.0001 | NA |
Groups | Studies (n) | RSV-positive (n) | Total (n) | Pooled Prevalence (95%CI) | Q-Value | I2 (%) | p Value Heterogeneity | p Value Egger Test | p Value Subgroup Difference |
---|---|---|---|---|---|---|---|---|---|
Age stratum | |||||||||
Age < 2 years | 35 | 6815 | 17,696 | 43.54 [35.56; 51.87] | 1972.43 | 96.7 | <0.0001 | 0.0017 | NA |
Period | <0.0001 | ||||||||
Pre-pandemic (2015/20) | 23 | 4844 | 12,939 | 47.82 [42.06; 53.65] | 1019.71 | 96.10 | <0.0001 | <0.0001 | |
Lockdown (2020/21) | 14 | 261 | 1359 | 6.46 [1.19; 28.29] | 137.86 | 90.60 | <0.0001 | 0.1192 | |
Post-lockdown (2021/22) | 12 | 1710 | 3398 | 67.61 [57.01; 76.67] | 698.1 | 98.40 | <0.0001 | 0.0004 | |
Age < 5 years | 22 | 7223 | 36,599 | 25.59 [21.03; 30.76] | 2760.33 | 98.8 | <0.0001 | 0.0781 | NA |
Period | 0.1193 | ||||||||
Pre-pandemic (2015/20) | 19 | 5424 | 23,892 | 25.58 [20.94; 30.84] | 1464.93 | 98.10 | <0.0001 | 0.4885 | |
Lockdown (2020/21) | 3 | 1422 | 11,913 | 17.34 [7.61; 34.84] | 380.63 | 99.50 | <0.0001 | NA | |
Post-lockdown (2021/22) | 2 | 377 | 794 | 42.69 [24.30; 63.35] | 57.54 | 98.30 | <0.0001 | NA | |
Age < 10 years | 4 | 7706 | 65,262 | 17.34 [11.89; 24.58] | 1267.48 | 99.0 | <0.0001 | 0.1347 | NA |
Period | 0.0384 | ||||||||
Pre-pandemic (2015/20) | 4 | 5554 | 48,007 | 20.48 [13.90; 29.11] | 1249.79 | 99.20 | <0.0001 | 0.1212 | |
Lockdown (2020/21) | 2 | 795 | 6989 | 7.39 [2.93; 17.40] | 5.34 | 81.30 | 0.0208 | NA | |
Post-lockdown (2021/22) | 1 | 1357 | 10,266 | 13.22 [12.58; 13.89] | 0 | NA | NA | NA | |
Age < 15 years | 20 | 5745 | 40,646 | 17.58 [12.82; 23.64] | 4016.97 | 99.1 | <0.0001 | 0.7428 | NA |
Period | <0.0001 | ||||||||
Pre-pandemic (2015/20) | 15 | 3963 | 31,279 | 19.46 [14.11; 26.23] | 1939.82 | 98.70 | <0.0001 | 0.0083 | |
Lockdown (2020/21) | 7 | 304 | 5790 | 6.02 [2.38; 14.39] | 168.99 | 96.40 | <0.0001 | NA | |
Post-lockdown (2021/22) | 6 | 1478 | 3577 | 31.37 [17.22; 50.12] | 87.88 | 94.30 | <0.0001 | NA | |
Age < 18 years | 27 | 17,408 | 139,980 | 10.17 [7.29; 14.02] | 5380.77 | 99.0 | <0.0001 | 0.9850 | NA |
Period | <0.0001 | ||||||||
Pre-pandemic (2015/20) | 19 | 13,026 | 99,877 | 16.68 [13.29; 20.72] | 3843.26 | 99.20 | <0.0001 | 0.1671 | |
Lockdown (2020/21) | 17 | 1695 | 23,124 | 2.53 [1.07; 5.85] | 1230.46 | 98.70 | <0.0001 | 0.1565 | |
Post-lockdown (2021/22) | 7 | 2687 | 16,979 | 17.61 [14.30; 21.51] | 48.9 | 87.70 | <0.0001 | NA |
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Leija-Martínez, J.J.; Esparza-Miranda, L.A.; Rivera-Alfaro, G.; Noyola, D.E. Impact of Nonpharmaceutical Interventions during the COVID-19 Pandemic on the Prevalence of Respiratory Syncytial Virus in Hospitalized Children with Lower Respiratory Tract Infections: A Systematic Review and Meta-Analysis. Viruses 2024, 16, 429. https://doi.org/10.3390/v16030429
Leija-Martínez JJ, Esparza-Miranda LA, Rivera-Alfaro G, Noyola DE. Impact of Nonpharmaceutical Interventions during the COVID-19 Pandemic on the Prevalence of Respiratory Syncytial Virus in Hospitalized Children with Lower Respiratory Tract Infections: A Systematic Review and Meta-Analysis. Viruses. 2024; 16(3):429. https://doi.org/10.3390/v16030429
Chicago/Turabian StyleLeija-Martínez, José J., Luis A. Esparza-Miranda, Gerardo Rivera-Alfaro, and Daniel E. Noyola. 2024. "Impact of Nonpharmaceutical Interventions during the COVID-19 Pandemic on the Prevalence of Respiratory Syncytial Virus in Hospitalized Children with Lower Respiratory Tract Infections: A Systematic Review and Meta-Analysis" Viruses 16, no. 3: 429. https://doi.org/10.3390/v16030429
APA StyleLeija-Martínez, J. J., Esparza-Miranda, L. A., Rivera-Alfaro, G., & Noyola, D. E. (2024). Impact of Nonpharmaceutical Interventions during the COVID-19 Pandemic on the Prevalence of Respiratory Syncytial Virus in Hospitalized Children with Lower Respiratory Tract Infections: A Systematic Review and Meta-Analysis. Viruses, 16(3), 429. https://doi.org/10.3390/v16030429