Investigating the human rhinovirus co-infection in patients with asthma exacerbations and COVID-19
Main Article Content
Keywords
Asthma exacerbation, COVID-19, Rhinovirus, Co-infection
Abstract
Objective: To investigate the co-infections with human rhinovirus (HRV) among patients with asthma exacerbation and COVID-19 in Jordan. Also, to determine the frequency of acute asthma exacerbation before and during the COVID-19 pandemic on a matched basis. Methods: The data of this prospective cohort research consisted of clinical variables. During the first visit, and after 14-days, nasopharyngeal swabs were taken and the quantitative polymerase chain reaction was performed for HRV and SARS-CoV-2 detection. Results: Forty-seven out of 175 (26.9%) COVID-19 adult cases have been diagnosed with asthma. The number of asthma exacerbations among the study participants was higher during 2021 than in 2020 (p=0.035). Most of the included asthmatic participants (61.7%) were only positive for SARS-CoV-2 and 38.3% were co-infected with HRV. The SARS-CoV-2 cycle threshold value was lower in samples infected with both viruses compared to samples infected with SARS-CoV-2 alone, p<0.005. Conclusion: Our findings indicate that HRV and SARS-CoV-2 were significantly more prevalent in asthma exacerbations than stable asthma. Thus, HRV and/or SARS-CoV-2 infections were potentially cofactors or contributors to the asthma exacerbation in this cohort. This is the first study, in Jordan, to investigate the HRV co-infection in COVID-19 asthmatic patients and HRV could be related with a higher severity of COVID-19.
References
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21. Scott SJ, Pfotenhauer B, Weiner JJ, et al. Respiratory Pathogen Coinfections in SARS-CoV-2-Positive Patients in SoutheasternWisconsin: A Retrospective Analysis. Microbiol Spectr. 2021;9(2):e0083121. https://doi.org/10.1128/Spectrum.00831-21
22. Çelebi Ö, Çelebi D. Viral Respiratory Tract Pathogens During the COVID-19 Pandemic. Eurasian J Med. 2021;53(2):123-6.https://doi.org/10.5152/eurasianjmed.2021.20459
23. Eisen AKA, Gularte JS, Demoliner M, et al. Low circulation of Influenza A and coinfection with SARS-CoV-2 among other
respiratory viruses during the COVID-19 pandemic in a region of southern Brazil. J Med Virol. 2021;93(7):4392-4398. https://
doi.org/10.1002/jmv.26975
24. Altawalbeh SM, Manoon NA, Ababneh MA, et al. Respiratory tract infection-induced asthma exacerbations in adults with asthma: assessing predictors and outcomes. The Journal of asthma: official journal of the Association for the Care of Asthma.2020;57(3):231-240. https://doi.org/10.1080/02770903.2019.1568454
25. BTS/SIGN. British guideline on the management of asthma. Thorax. 2014;69 Suppl 1:1-192.26. NAEPP. 2020 Focused Updates to the Asthma Management Guidelines: A Report from the National Asthma Education and Prevention Program Coordinating Committee Expert Panel Working Group. 2020.
27. GINA. Global Initiative for Asthma. 2020
28. Alsayed A, Talib W, Al-Dulaimi A, et al. The first detection of Pneumocystis jirovecii in asthmatic patients post COVID-19 in Jordan. Bosn J of Basic Med Sci. 2022 May 17 [cited 2022 May 25]. https://doi.org/10.17305/bjbms.2022.7335
29. Alsayed A, Al-Doori A, Al-Dulaimi A, et al. Influences of bovine colostrum on nasal swab microbiome and viral upper respiratory tract infections–A case report. Respiratory medicine case reports. 2020;31:101189. https://doi.org/10.1016/j.rmcr.2020.101189
30. McNemar Q. Note on the sampling error of the difference between correlated proportions or percentages. Psychometrika.1947;12:153-157.
31. Edwards AL. Note on the “correction for continuity” in testing the significance of the difference between correlated proportions
32. Omar S, Bartz C, Becker S, et al. Duration of SARS-CoV-2 RNA detection in COVID-19 patients in home isolation, Rhineland-Palatinate, Germany, 2020 - an interval-censored survival analysis. Euro Surveill. 2020;25(30). https://doi.org/10.2807/1560-7917.ES.2020.25.30.2001292
33. Evans D, Cowen S, Kammel M, et al. The dangers of using Cq to quantify nucleic acid in biological samples; a lesson from COVID-19. Clin Chem. 2021;68(1):153-162. https://doi.org/10.1093/clinchem/hvab219
34. Engelmann I, Alidjinou EK, Ogiez J, et al. Preanalytical issues and cycle threshold values in SARS-CoV-2 real-time RT-PCR testing: should test results include these? 2021;6(10):6528-6536. https://doi.org/10.1021/acsomega.1c00166
35. Engelmann I, Alidjinou EK, Lazrek M, et al. Comparison of two commercial quantitative PCR assays and correlation with the first WHO International Standard for human CMV. Diagn Microbiol Infect Dis. 2018;91(1):27-33. https://doi.org/10.1016/j.diagmicrobio.2017.12.021
36. Kuitunen I, Artama M, Haapanen M, Renko M. Rhinovirus spread in children during the COVID-19 pandemic despite social restrictions-A nationwide register study in Finland. J Med Virol. 2021;93(10):6063-6067. https://doi.org/10.1002/jmv.27180
37. Kitanovski S, Horemheb-Rubio G, Adams O, et al. Rhinovirus prevalence as indicator for efficacy of measures against SARSCoV-2. BMC Public Health. 2021;21(1):1178. https://doi.org/10.1186/s12889-021-11178-w
38. Kim MC, Kweon OJ, Lim YK, et al. Impact of social distancing on the spread of common respiratory viruses during the coronavirus disease outbreak. PLoS One. 2021;16(6):e0252963. https://doi.org/10.1371/journal.pone.0252963
39. Kim HM, Lee EJ, Lee NJ, et al. Impact of coronavirus disease 2019 on respiratory surveillance and explanation of high detection
rate of human rhinovirus during the pandemic in the Republic of Korea. Influenza Other Respir Viruses. 2021;15(6):721-731.https://doi.org/10.1111/irv.12894
40. Roh KH, Kim YK, Kim SW, et al. Coinfections with Respiratory Pathogens among COVID-19 Patients in Korea. Can J Infect DisMed Microbiol. 2021;2021:6651045. https://doi.org/10.1155/2021/6651045
41. Kim D, Quinn J, Pinsky B, et al. Rates of Co-infection Between SARS-CoV-2 and Other Respiratory Pathogens. Jama.2020;323(20):2085-2086. https://doi.org/10.1001/jama.2020.6266
42. Brotons P, Jordan I, Bassat Q, et al. The Positive Rhinovirus/Enterovirus Detection and SARS-CoV-2 Persistence beyond the Acute Infection Phase: An Intra-Household Surveillance Study. Viruses. 2021;13(8):1598. https://doi.org/10.3390/v13081598
43. Calderaro A, De Conto F, Buttrini M, et al. Human respiratory viruses, including SARS-CoV-2, circulating in the winter season 2019-2020 in Parma, Northern Italy. Int J Infect Dis. 2021;102:79-84. https://doi.org/10.1016/j.ijid.2020.09.1473
44. Groves HE, Piché-Renaud PP, Peci A, et al. The impact of the COVID-19 pandemic on influenza, respiratory syncytial virus, and other seasonal respiratory virus circulation in Canada: A population-based study. Lancet Reg Health Am. 2021;1:100015.https://doi.org/10.1016/j.lana.2021.100015
45. Holt PG, Sly PD. Viral infections and atopy in asthma pathogenesis: new rationales for asthma prevention and treatment. Nat
Med. 2012;18(5):726-735. https://doi.org/10.1038/nm.2768
46. Lemanske RF, Jr., Jackson DJ, Gangnon RE, et al. Rhinovirus illnesses during infancy predict subsequent childhood wheezing. JAllergy Clin Immunol. 2005;116(3):571-577. https://doi.org/10.1016/j.jaci.2005.06.024
47. Gern JE. Viral respiratory infection and the link to asthma. Pediatr Infect Dis J. 2008;27:S97-103. https://doi.org/10.1097/01.inf.0000108196.46134.a6
48. Bousquet J, Jutel M, Akdis CA, et al. ARIA-EAACI statement on asthma and COVID-19 (June 2, 2020). Allergy. 2021;76(3):689-697. https://doi.org/10.1111/all.14471
49. Alsayed A, El Hajji FD, Al-Najjar MA, et al. Patterns of antibiotic use, knowledge, and perceptions among different population categories: A comprehensive study based in Arabic countries. Saudi Pharmaceutical Journal. 2022; 30(3):317-328. https://doi.org/10.1016/j.jsps.2022.01.013
50. Abrams EM, Szefler SJ. Managing Asthma during Coronavirus Disease-2019: An Example for Other Chronic Conditions in Children and Adolescents. J Pediatr. 2020;222:221-226. https://doi.org/10.1016/j.jpeds.2020.04.049
51. Rodgers L, Sheppard M, Smith A, et al. Changes in Seasonal Respiratory Illnesses in the United States During the Coronavirus Disease 2019 (COVID-19) Pandemic. Clin Infect Dis. 2021;73:S110-s117. https://doi.org/10.1093/cid/ciab311
52. Bochkov YA, Watters K, Ashraf S, et al. Cadherin-related family member 3, a childhood asthma susceptibility gene product,mediates rhinovirus C binding and replication. Proc Natl Acad Sci USA. 2015;112(17):5485-5490. https://doi.org/10.1073/pnas.1421178112
53. Lee WM, Lemanske RF, Evans MD, et al. Human rhinovirus species and season of infection determine illness severity. Am JRespir Crit Care Med. 2012;186(9):886-891. https://doi.org/10.1164/rccm.201202-0330OC
54. Cox DW, Bizzintino J, Ferrari G, et al. Human rhinovirus species C infection in young children with acute wheeze is associated with increased acute respiratory hospital admissions. Am J Respir Crit Care Med. 2013;188(11):1358-1364. https://doi.org/10.1164/rccm.201303-0498OC
2. Jackson DJ. The role of rhinovirus infections in the development of early childhood asthma. Curr Opin Allergy Clin Immunol.2010;10(2):133-138. https://doi.org/10.1097/ACI.0b013e3283352f7c
3. Jackson DJ, Gangnon RE, Evans MD, et al. Wheezing rhinovirus illnesses in early life predict asthma development in high-risk
children. Am J Respir Crit Care Med. 2008;178(7):667-672. https://doi.org/10.1164/rccm.200802-309OC
4. Johnston SL, Pattemore PK, Sanderson G, et al. Community study of role of viral infections in exacerbations of asthma in 9-11 year old children. Bmj. 1995;310(6989):1225-1229. https://doi.org/10.1136/bmj.310.6989.1225
5. Nicholson KG, Kent J, Ireland DC. Respiratory viruses and exacerbations of asthma in adults. Bmj. 1993;307(6910):982-986. https://doi.org/10.1136/bmj.307.6910.982
6. Kennedy JL, Pham S, Borish L. Rhinovirus and Asthma Exacerbations. Immunol Allergy Clin North Am. 2019;39(3):335-344.https://doi.org/10.1016/j.iac.2019.03.003
7. Self WH, Williams DJ, Zhu Y, et al. Respiratory Viral Detection in Children and Adults: Comparing Asymptomatic Controls and
Patients with Community-Acquired Pneumonia. J Infect Dis. 2016;213(4):584-591. https://doi.org/10.1093/infdis/jiv323
8. Charles CH, Yelmene M, Luo GX. Recent advances in rhinovirus therapeutics. Curr Drug Targets Infect Disord. 2004;4(4):331-
337. https://doi.org/10.2174/1568005043340551
9. Papadopoulos N, Johnston S. The rhinovirus--not such an innocent? Qjm. 2001;94(1):1-3. https://doi.org/10.1093/qjmed/94.1.1
10. Brzezińska-Pawłowska OE, Rydzewska AD, Łuczyńska M, et al. Environmental factors affecting seasonality of ambulanceemergency service visits for exacerbations of asthma and COPD. The Journal of asthma: official journal of the Association forthe Care of Asthma. 2016;53(2):139-145. https://doi.org/10.3109/02770903.2015.1075547
11. Jartti T, Gern JE. Role of viral infections in the development and exacerbation of asthma in children. J Allergy Clin Immunol.2017;140(4):895-906. https://doi.org/10.1016/j.jaci.2017.08.003
12. Mackenzie JS, Smith DW. COVID-19: a novel zoonotic disease caused by a coronavirus from China: what we know and what we don’t. Microbiol Aust. 2020:Ma20013. https://doi.org/10.1071/MA20013
13. Watanabe Y, Kamioka Y, Seki M. Rhinovirus-Infected Patients in the COVID-19 Pandemic Period. Infect Drug Resist. 2021;14:609-611. https://doi.org/10.2147/IDR.S300001
14. Wu C, Chen X, Cai Y, et al. Risk Factors Associated With Acute Respiratory Distress Syndrome and Death in Patients With Coronavirus Disease 2019 Pneumonia in Wuhan, China. JAMA Intern Med. 2020;180(7):934-943. https://doi.org/10.1001/jamainternmed.2020.0994
15. Bates DV, Baker-Anderson M, Sizto R. Asthma attack periodicity: a study of hospital emergency visits in Vancouver. Environ Res.1990;51(1):51-70. https://doi.org/10.1016/s0013-9351(05)80182-3
16. Weiss KB. Seasonal trends in US asthma hospitalizations and mortality. Jama. 1990;263(17):2323-2328.17. Kimes D, Levine E, Timmins S, et al. Temporal dynamics of emergency department and hospital admissions of pediatric
asthmatics. Environ Res. 2004;94(1):7-17. https://doi.org/10.1016/s0013-9351(03)00046-x
18. Dawood FS, Kamimoto L, D’Mello TA, et al. Children with asthma hospitalized with seasonal or pandemic influenza, 2003-2009.Pediatrics. 2011;128(1):e27-32. https://doi.org/10.1542/peds.2010-3343
19. Merckx J, Ducharme FM, Martineau C, et al. Respiratory Viruses and Treatment Failure in Children with Asthma Exacerbation.Pediatrics. 2018;142(1). https://doi.org/10.1542/peds.2017-4105
20. Marriott D, Beresford R, Mirdad F, et al. Concomitant Marked Decline in Prevalence of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) and Other Respiratory Viruses Among Symptomatic Patients Following Public Health Interventions in Australia: Data from St Vincent’s Hospital and Associated Screening Clinics, Sydney, NSW. Clin Infect Dis.2021;72(10):e649-e651. https://doi.org/10.1093/cid/ciaa1256
21. Scott SJ, Pfotenhauer B, Weiner JJ, et al. Respiratory Pathogen Coinfections in SARS-CoV-2-Positive Patients in SoutheasternWisconsin: A Retrospective Analysis. Microbiol Spectr. 2021;9(2):e0083121. https://doi.org/10.1128/Spectrum.00831-21
22. Çelebi Ö, Çelebi D. Viral Respiratory Tract Pathogens During the COVID-19 Pandemic. Eurasian J Med. 2021;53(2):123-6.https://doi.org/10.5152/eurasianjmed.2021.20459
23. Eisen AKA, Gularte JS, Demoliner M, et al. Low circulation of Influenza A and coinfection with SARS-CoV-2 among other
respiratory viruses during the COVID-19 pandemic in a region of southern Brazil. J Med Virol. 2021;93(7):4392-4398. https://
doi.org/10.1002/jmv.26975
24. Altawalbeh SM, Manoon NA, Ababneh MA, et al. Respiratory tract infection-induced asthma exacerbations in adults with asthma: assessing predictors and outcomes. The Journal of asthma: official journal of the Association for the Care of Asthma.2020;57(3):231-240. https://doi.org/10.1080/02770903.2019.1568454
25. BTS/SIGN. British guideline on the management of asthma. Thorax. 2014;69 Suppl 1:1-192.26. NAEPP. 2020 Focused Updates to the Asthma Management Guidelines: A Report from the National Asthma Education and Prevention Program Coordinating Committee Expert Panel Working Group. 2020.
27. GINA. Global Initiative for Asthma. 2020
28. Alsayed A, Talib W, Al-Dulaimi A, et al. The first detection of Pneumocystis jirovecii in asthmatic patients post COVID-19 in Jordan. Bosn J of Basic Med Sci. 2022 May 17 [cited 2022 May 25]. https://doi.org/10.17305/bjbms.2022.7335
29. Alsayed A, Al-Doori A, Al-Dulaimi A, et al. Influences of bovine colostrum on nasal swab microbiome and viral upper respiratory tract infections–A case report. Respiratory medicine case reports. 2020;31:101189. https://doi.org/10.1016/j.rmcr.2020.101189
30. McNemar Q. Note on the sampling error of the difference between correlated proportions or percentages. Psychometrika.1947;12:153-157.
31. Edwards AL. Note on the “correction for continuity” in testing the significance of the difference between correlated proportions
32. Omar S, Bartz C, Becker S, et al. Duration of SARS-CoV-2 RNA detection in COVID-19 patients in home isolation, Rhineland-Palatinate, Germany, 2020 - an interval-censored survival analysis. Euro Surveill. 2020;25(30). https://doi.org/10.2807/1560-7917.ES.2020.25.30.2001292
33. Evans D, Cowen S, Kammel M, et al. The dangers of using Cq to quantify nucleic acid in biological samples; a lesson from COVID-19. Clin Chem. 2021;68(1):153-162. https://doi.org/10.1093/clinchem/hvab219
34. Engelmann I, Alidjinou EK, Ogiez J, et al. Preanalytical issues and cycle threshold values in SARS-CoV-2 real-time RT-PCR testing: should test results include these? 2021;6(10):6528-6536. https://doi.org/10.1021/acsomega.1c00166
35. Engelmann I, Alidjinou EK, Lazrek M, et al. Comparison of two commercial quantitative PCR assays and correlation with the first WHO International Standard for human CMV. Diagn Microbiol Infect Dis. 2018;91(1):27-33. https://doi.org/10.1016/j.diagmicrobio.2017.12.021
36. Kuitunen I, Artama M, Haapanen M, Renko M. Rhinovirus spread in children during the COVID-19 pandemic despite social restrictions-A nationwide register study in Finland. J Med Virol. 2021;93(10):6063-6067. https://doi.org/10.1002/jmv.27180
37. Kitanovski S, Horemheb-Rubio G, Adams O, et al. Rhinovirus prevalence as indicator for efficacy of measures against SARSCoV-2. BMC Public Health. 2021;21(1):1178. https://doi.org/10.1186/s12889-021-11178-w
38. Kim MC, Kweon OJ, Lim YK, et al. Impact of social distancing on the spread of common respiratory viruses during the coronavirus disease outbreak. PLoS One. 2021;16(6):e0252963. https://doi.org/10.1371/journal.pone.0252963
39. Kim HM, Lee EJ, Lee NJ, et al. Impact of coronavirus disease 2019 on respiratory surveillance and explanation of high detection
rate of human rhinovirus during the pandemic in the Republic of Korea. Influenza Other Respir Viruses. 2021;15(6):721-731.https://doi.org/10.1111/irv.12894
40. Roh KH, Kim YK, Kim SW, et al. Coinfections with Respiratory Pathogens among COVID-19 Patients in Korea. Can J Infect DisMed Microbiol. 2021;2021:6651045. https://doi.org/10.1155/2021/6651045
41. Kim D, Quinn J, Pinsky B, et al. Rates of Co-infection Between SARS-CoV-2 and Other Respiratory Pathogens. Jama.2020;323(20):2085-2086. https://doi.org/10.1001/jama.2020.6266
42. Brotons P, Jordan I, Bassat Q, et al. The Positive Rhinovirus/Enterovirus Detection and SARS-CoV-2 Persistence beyond the Acute Infection Phase: An Intra-Household Surveillance Study. Viruses. 2021;13(8):1598. https://doi.org/10.3390/v13081598
43. Calderaro A, De Conto F, Buttrini M, et al. Human respiratory viruses, including SARS-CoV-2, circulating in the winter season 2019-2020 in Parma, Northern Italy. Int J Infect Dis. 2021;102:79-84. https://doi.org/10.1016/j.ijid.2020.09.1473
44. Groves HE, Piché-Renaud PP, Peci A, et al. The impact of the COVID-19 pandemic on influenza, respiratory syncytial virus, and other seasonal respiratory virus circulation in Canada: A population-based study. Lancet Reg Health Am. 2021;1:100015.https://doi.org/10.1016/j.lana.2021.100015
45. Holt PG, Sly PD. Viral infections and atopy in asthma pathogenesis: new rationales for asthma prevention and treatment. Nat
Med. 2012;18(5):726-735. https://doi.org/10.1038/nm.2768
46. Lemanske RF, Jr., Jackson DJ, Gangnon RE, et al. Rhinovirus illnesses during infancy predict subsequent childhood wheezing. JAllergy Clin Immunol. 2005;116(3):571-577. https://doi.org/10.1016/j.jaci.2005.06.024
47. Gern JE. Viral respiratory infection and the link to asthma. Pediatr Infect Dis J. 2008;27:S97-103. https://doi.org/10.1097/01.inf.0000108196.46134.a6
48. Bousquet J, Jutel M, Akdis CA, et al. ARIA-EAACI statement on asthma and COVID-19 (June 2, 2020). Allergy. 2021;76(3):689-697. https://doi.org/10.1111/all.14471
49. Alsayed A, El Hajji FD, Al-Najjar MA, et al. Patterns of antibiotic use, knowledge, and perceptions among different population categories: A comprehensive study based in Arabic countries. Saudi Pharmaceutical Journal. 2022; 30(3):317-328. https://doi.org/10.1016/j.jsps.2022.01.013
50. Abrams EM, Szefler SJ. Managing Asthma during Coronavirus Disease-2019: An Example for Other Chronic Conditions in Children and Adolescents. J Pediatr. 2020;222:221-226. https://doi.org/10.1016/j.jpeds.2020.04.049
51. Rodgers L, Sheppard M, Smith A, et al. Changes in Seasonal Respiratory Illnesses in the United States During the Coronavirus Disease 2019 (COVID-19) Pandemic. Clin Infect Dis. 2021;73:S110-s117. https://doi.org/10.1093/cid/ciab311
52. Bochkov YA, Watters K, Ashraf S, et al. Cadherin-related family member 3, a childhood asthma susceptibility gene product,mediates rhinovirus C binding and replication. Proc Natl Acad Sci USA. 2015;112(17):5485-5490. https://doi.org/10.1073/pnas.1421178112
53. Lee WM, Lemanske RF, Evans MD, et al. Human rhinovirus species and season of infection determine illness severity. Am JRespir Crit Care Med. 2012;186(9):886-891. https://doi.org/10.1164/rccm.201202-0330OC
54. Cox DW, Bizzintino J, Ferrari G, et al. Human rhinovirus species C infection in young children with acute wheeze is associated with increased acute respiratory hospital admissions. Am J Respir Crit Care Med. 2013;188(11):1358-1364. https://doi.org/10.1164/rccm.201303-0498OC
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Investigating the human rhinovirus co-infection in patients with asthma exacerbations and COVID-19. Pharm Pract (Granada) [Internet]. 2022 Jul. 4 [cited 2024 Dec. 2];20(2):2665. Available from: https://www.pharmacypractice.org/index.php/pp/article/view/2665
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Investigating the human rhinovirus co-infection in patients with asthma exacerbations and COVID-19. Pharm Pract (Granada) [Internet]. 2022 Jul. 4 [cited 2024 Dec. 2];20(2):2665. Available from: https://www.pharmacypractice.org/index.php/pp/article/view/2665