Molecular epidemiology of human respiratory syncytial virus (HRSV) in Iranian military trainees with acute respiratory symptoms in 2017
-
Mohammad Hadi Karbalaie Niya
,
Ali Salimi Jeda
,
Ahmad Tavakoli
,
Hesam Sohani
,
Fahimeh Safarnezhad Tameshkel
,
Mahshid Panahi
,
Morteza Izadi
,
Farhad Zamani
,
Hossein Keyvani
Abstract
Background and Objectives: Respiratory syncytial virus (RSV) is the leading cause of lower respiratory tract infection in many populations, including military recruits receiving basic training. Therefore, this study was set out to determine the molecular epidemiology, genotype and phylogenetic features of RSVs in patients with respiratory infection as a case study.
Materials and Methods: In this study, military barracks of Tehran, Iran, between January to March 2017 exposed to respiratory diseases were used for sampling. Throat swabs were taken, a reverse transcriptase-polymerase chain reaction (RT-PCR) assay was performed to identify RSV and then the genotyping and phylogenetic analyses of RSVs in patients with a respiratory infection.
Results: Among 400 Iranian military trainees with respiratory symptoms, RSV infection was identified in 2.75% (11/400) using RT-PCR. Sequencing showed the incidence of type A (2.5%, n=10) to be much higher than type B (0.25%, n=1); Sore throat was the most common symptom among RSV patients. Phylogenetic analysis revealed that the majority of strains from the studied samples were more consistent with those from the Philippines and the US strains.
Conclusion: This study is the first to document RSV as a major cause of acute respiratory illness among military trainees in Iran. The prevalence of RSV is substantial in the cold season and the prevalence of genotype A is dominant in the country, leading to take essential steps in preparing a preventive vaccine against this viral infection.
1. O'Shea MK, Ryan MAK, Hawksworth AW, Alsip BJ, Gray GC. Symptomatic respiratory syncytial virus infection in previously healthy young adults living in a crowded military environment. Clin Infect Dis 2005;41:311-317.
2. Gray GC, Callahan JD, Hawksworth AW, Fisher CA, Gaydos JC. Respiratory diseases among U.S. military personnel: countering emerging threats. Emerg Infect Dis 1999;5:379-385.
3. O'Shea MK, Pipkin C, Cane PA, Gray GC. Respiratory syncytial virus: an important cause of acute respiratory illness among young adults undergoing military training. Influenza Other Respir Viruses 2007;1:193-197.
4. Nam HH, Ison MG. Respiratory syncytial virus infection in adults. BMJ 2019;366:l5021.
5. Rima B, Collins P, Easton A, Fouchier R, Kurath G, Lamb RA, et al. ICTV virus taxonomy profile: pneumoviridae. J Gen Virol 2017;98:2912-2913.
6. Paes BA, Mitchell I, Banerji A, Lanctot KL, Langley JM. A decade of respiratory syncytial virus epidemiology and prophylaxis: translating evidence into everyday clinical practice. Can Respir J 2011;18(2):e10-9.
7. Volling C, Hassan K, Mazzulli T, Green K, Al-Den A, Hunter P, et al. Respiratory syncytial virus infection-associated hospitalization in adults: a retrospective cohort study. BMC Infect Dis 2014;14:665.
8. Guerra-Maupome M, Palmer MV, McGill JL, Sacco RE. Utility of the neonatal calf model for testing vaccines and intervention strategies for use against human RSV infection. Vaccines (Basel) 2019;7:7.
9. Gerretsen HE, Sande CJ. Development of respiratory syncytial virus (RSV) vaccines for infants. J Infect 2017;74 Suppl 1:S143-S146.
10. Paramore LC, Mahadevia PJ, Piedra PA. Outpatient RSV lower respiratory infections among high-risk infants and other pediatric populations. Pediatr Pulmonol 2010;45:578-584.
11. Branche AR, Falsey AR. Respiratory syncytial virus infection in older adults: an under-recognized problem. Drugs Aging 2015;32:261-269.
12. American Academy of Pediatrics Committee on Infectious Diseases; American Academy of Pediatrics Bronchiolitis Guidelines Committee. Updated guidance for palivizumab prophylaxis among infants and young children at increased risk of hospitalization for respiratory syncytial virus infection. Pediatrics 2014;134:415-420.
13. Robinson JL, Saux NL, Canadian Paediatric Society, Infectious Diseases and Immunization Committee. Preventing hospitalizations for respiratory syncytial virus infection. Paediatr Child Health 2015;20:321-326.
14. Haynes AK, Prill MM, Iwane MK, Gerber SI, Centers for Disease Control and Prevention (CDC). Respiratory syncytial virus--United States, July 2012-June 2014. MMWR Morb Mortal Wkly Rep 2014;63:1133-1136.
15. Kim JK, Jeon JS, Kim JW, Rheem I. Epidemiology of respiratory viral infection using multiplex rt-PCR in Cheonan, Korea (2006-2010). J Microbiol Biotechnol 2013;23:267-273.
16. Tognarelli EI, Bueno SM, Gonzalez PA. Immune-modulation by the human respiratory syncytial virus: focus on dendritic cells. Front Immunol 2019;10:810.
17. Hall CB, Walsh EE, Long CE, Schnabel KC. Immunity to and frequency of reinfection with respiratory syncytial virus. J Infect Dis 1991;163:693-698.
18. Russell CD, Unger SA, Walton M, Schwarze J. The human immune response to respiratory syncytial virus infection. Clin Microbiol Rev 2017;30:481-502.
19. Villafana T, Falloon J, Griffin MP, Zhu Q, Esser MT. Passive and active immunization against respiratory syncytial virus for the young and old. Expert Rev Vaccines 2017;16:1-13.
20. Kim D, Saleem M, Paes B, Mitchell I, Lanctot KL. Respiratory syncytial virus prophylaxis in infants with congenital diaphragmatic hernia in the Canadian respiratory syncytial virus evaluation study of palivizumab, 2005-2017. Clin Infect Dis 2019;69:980-986.
21. Shahabi A, Peneva D, Incerti D, McLaurin K, Stevens W. Assessing variation in the cost of palivizumab for respiratory syncytial virus prevention in preterm infants. Pharmacoecon Open 2018;2:53-61.
22. Gonik B. The burden of respiratory syncytial virus infection in adults and reproductive-aged women. Glob Health Sci Pract 2019;7:515-520.
23. Walsh EE, Falsey AR. Respiratory syncytial virus infection in adult populations. Infect Disord Drug
Targets 2012;12:98-102.
24. Mehta J, Walsh EE, Mahadevia PJ, Falsey AR. Risk factors for respiratory syncytial virus illness among patients with chronic obstructive pulmonary disease. COPD 2013;10:293-299.
25. Lennette EH, Stallones RA, Holguin AH. Pattern of respiratory virus infections in army recruits. Am J Hyg 1961;74:225-233.
26. Hers JF, Masurel N, Gans JC. Acute respiratory disease associated with pulmonary involvement in military servicement in The Netherlands. A serologic and bacteriologic survey, January 1967 to January 1968. Am Rev Respir Dis 1969;100:499-506.
27. Sanford JP. Acute respiratory disease in the United States Army in the Republic of Vietnam, 1965-1970. Yale J Biol Med 1975;48:179-184.
28. Radin JM, Hawksworth AW, Kammerer PE, Balansay M, Raman R, Lindsay SP, et al. Epidemiology of pathogen-specific respiratory infections among three US populations. PLoS One 2014;9(12):e114871.
29. Eick AA, Faix DJ, Tobler SK, Nevin RL, Lindler LE, Hu Z, et al. Serosurvey of bacterial and viral respiratory pathogens among deployed U.S. service members. Am J Prev Med 2011;41:573-580.
30. Park WJ. Seroprevalence of respiratory syncytial virus IgG among healthy young adults in basic training for the Republic of Korea Air Force. J Korean Med Sci 2014;29:1325-1327.
31. Lessler J, Reich NG, Brookmeyer R, Perl TM, Nelson KE, Cummings DA. Incubation periods of acute respiratory viral infections: a systematic review. Lancet Infect Dis 2009;9:291-300.
32. Sanchez JL, Cooper MJ, Myers CA, Cummings JF, Vest KG, Russell KL, et al. Respiratory infections in the U.S. military: recent experience and control. Clin Microbiol Rev 2015;28:743-800.
33. Kim CK, Choi J, Callaway Z, Kim HB, Chung JY, Koh YY, et al. Clinical and epidemiological comparison of human metapneumovirus and respiratory syncytial virus in seoul, Korea, 2003-2008. J Korean Med Sci 2010;25:342-347.
34. Li Y, Reeves RM, Wang X, Bassat Q, Brooks WA, Cohen C, et al. Global patterns in monthly activity of influenza virus, respiratory syncytial virus, parainfluenza virus, and metapneumovirus: a systematic analysis. Lancet Glob Health 2019;7(8):e1031-e1045.
35. Gamba-Sanchez N, Rodriguez-Martinez C, Sossa-Briceño M. Epidemic activity of respiratory syncytial virus is related to temperature and rainfall in equatorial tropical countries. Epidemiol Infect 2016;144:2057-2063.
36. Rodriguez-Martinez CE, Sossa-Briceno MP, Acuna-Cordero R. Relationship between meteorological conditions and respiratory syncytial virus in a tropical country. Epidemiol Infect 2015;143:2679-2686.
37. Sloan C, Heaton M, Kang S, Berrett C, Wu P, Gebretsadik T, et al. The impact of temperature and relative humidity on spatiotemporal patterns of infant bronchiolitis epidemics in the contiguous United States. Health Place 2017;45:46-54.
38. Wentz LM, Ward MD, Potter C, Oliver SJ, Jackson S, Izard RM, et al. Increased risk of upper respiratory infection in military recruits who report sleeping less than 6 h per night. Mil Med 2018;183(11-12):e699-e704.
39. Korzeniewski K, Nitsch-Osuch A, Konarski M, Guzek A, Prokop E, Bieniuk K. Prevalence of acute respiratory tract diseases among soldiers deployed for military operations in Iraq and Afghanistan. Adv Exp Med Biol 2013;788:117-124.
40. Soltis BW, Sanders JW, Putnam SD, Tribble DR, Riddle MS. Self reported incidence and morbidity of acute respiratory illness among deployed U.S. military in Iraq and Afghanistan. PLoS One 2009;4(7): e6177.
41. Zlateva KT, Vijgen L, Dekeersmaeker N, Naranjo C, Van Ranst M. Subgroup prevalence and genotype circulation patterns of human respiratory syncytial virus in Belgium during ten successive epidemic seasons. J Clin Microbiol 2007;45:3022-3030.
42. Venter M, van Niekerk S, Rakgantso A, Bent N. Identification of deletion mutant respiratory syncytial virus strains lacking most of the G protein in immunocompromised children with pneumonia in South Africa. J Virol 2011;85:8453-8457.
43. Tabatabai J, Thielen A, Lehners N, Daeumer M, Schnitzler P. Respiratory syncytial virus A in haematological patients with prolonged shedding: Premature stop codons and deletion of the genotype ON1 72-nucleotide-duplication in the attachment G gene. J Clin Virol 2018;98:10-17.
44. Venter M, Madhi SA, Tiemessen CT, Schoub BD. Genetic diversity and molecular epidemiology of respiratory syncytial virus over four consecutive seasons in South Africa: identification of new subgroup A and B genotypes. J Gen Virol 2001;82:2117-2124.
45. Parveen S, Sullender WM, Fowler K, Lefkowitz EJ, Kapoor SK, Broor S. Genetic variability in the G protein gene of group A and B respiratory syncytial viruses from India. J Clin Microbiol 2006;44:3055-3064.
46. Law B, Carbonell-Estrany X, Simoes E. An update on respiratory syncytial virus epidemiology: a developed country perspective. Respir Med 2002;96 Suppl B:S1-7.
47. Faghihloo E, Salimi V, Rezaei F, Naseri M, Mamishi S, Mahmoodi M, et al. Genetic diversity in the G protein gene of human respiratory syncytial virus among Iranian children with acute respiratory symptoms. Iran J Pediatr 2011;21:58-64.
48. Salimi V, Tavakoli-Yaraki M, Yavarian J, Bont L, Mokhtari-Azad T. Prevalence of human respiratory syncytial virus circulating in Iran. J Infect Public Health 2016;9:125-135.
49. Hall CB, Walsh EE, Long CE, Schnabel KC. Immunity to and frequency of reinfection with respiratory syncytial virus. J Infect Dis 1991;163:693-698.
50. Östlund MR, Lindell AT, Stenler S, Riedel HM, Wirgart BZ, Grillner L. Molecular epidemiology and genetic variability of respiratory syncytial virus (RSV) in Stockholm, 2002–2003. J Med Virol 2008;80:159-167.
2. Gray GC, Callahan JD, Hawksworth AW, Fisher CA, Gaydos JC. Respiratory diseases among U.S. military personnel: countering emerging threats. Emerg Infect Dis 1999;5:379-385.
3. O'Shea MK, Pipkin C, Cane PA, Gray GC. Respiratory syncytial virus: an important cause of acute respiratory illness among young adults undergoing military training. Influenza Other Respir Viruses 2007;1:193-197.
4. Nam HH, Ison MG. Respiratory syncytial virus infection in adults. BMJ 2019;366:l5021.
5. Rima B, Collins P, Easton A, Fouchier R, Kurath G, Lamb RA, et al. ICTV virus taxonomy profile: pneumoviridae. J Gen Virol 2017;98:2912-2913.
6. Paes BA, Mitchell I, Banerji A, Lanctot KL, Langley JM. A decade of respiratory syncytial virus epidemiology and prophylaxis: translating evidence into everyday clinical practice. Can Respir J 2011;18(2):e10-9.
7. Volling C, Hassan K, Mazzulli T, Green K, Al-Den A, Hunter P, et al. Respiratory syncytial virus infection-associated hospitalization in adults: a retrospective cohort study. BMC Infect Dis 2014;14:665.
8. Guerra-Maupome M, Palmer MV, McGill JL, Sacco RE. Utility of the neonatal calf model for testing vaccines and intervention strategies for use against human RSV infection. Vaccines (Basel) 2019;7:7.
9. Gerretsen HE, Sande CJ. Development of respiratory syncytial virus (RSV) vaccines for infants. J Infect 2017;74 Suppl 1:S143-S146.
10. Paramore LC, Mahadevia PJ, Piedra PA. Outpatient RSV lower respiratory infections among high-risk infants and other pediatric populations. Pediatr Pulmonol 2010;45:578-584.
11. Branche AR, Falsey AR. Respiratory syncytial virus infection in older adults: an under-recognized problem. Drugs Aging 2015;32:261-269.
12. American Academy of Pediatrics Committee on Infectious Diseases; American Academy of Pediatrics Bronchiolitis Guidelines Committee. Updated guidance for palivizumab prophylaxis among infants and young children at increased risk of hospitalization for respiratory syncytial virus infection. Pediatrics 2014;134:415-420.
13. Robinson JL, Saux NL, Canadian Paediatric Society, Infectious Diseases and Immunization Committee. Preventing hospitalizations for respiratory syncytial virus infection. Paediatr Child Health 2015;20:321-326.
14. Haynes AK, Prill MM, Iwane MK, Gerber SI, Centers for Disease Control and Prevention (CDC). Respiratory syncytial virus--United States, July 2012-June 2014. MMWR Morb Mortal Wkly Rep 2014;63:1133-1136.
15. Kim JK, Jeon JS, Kim JW, Rheem I. Epidemiology of respiratory viral infection using multiplex rt-PCR in Cheonan, Korea (2006-2010). J Microbiol Biotechnol 2013;23:267-273.
16. Tognarelli EI, Bueno SM, Gonzalez PA. Immune-modulation by the human respiratory syncytial virus: focus on dendritic cells. Front Immunol 2019;10:810.
17. Hall CB, Walsh EE, Long CE, Schnabel KC. Immunity to and frequency of reinfection with respiratory syncytial virus. J Infect Dis 1991;163:693-698.
18. Russell CD, Unger SA, Walton M, Schwarze J. The human immune response to respiratory syncytial virus infection. Clin Microbiol Rev 2017;30:481-502.
19. Villafana T, Falloon J, Griffin MP, Zhu Q, Esser MT. Passive and active immunization against respiratory syncytial virus for the young and old. Expert Rev Vaccines 2017;16:1-13.
20. Kim D, Saleem M, Paes B, Mitchell I, Lanctot KL. Respiratory syncytial virus prophylaxis in infants with congenital diaphragmatic hernia in the Canadian respiratory syncytial virus evaluation study of palivizumab, 2005-2017. Clin Infect Dis 2019;69:980-986.
21. Shahabi A, Peneva D, Incerti D, McLaurin K, Stevens W. Assessing variation in the cost of palivizumab for respiratory syncytial virus prevention in preterm infants. Pharmacoecon Open 2018;2:53-61.
22. Gonik B. The burden of respiratory syncytial virus infection in adults and reproductive-aged women. Glob Health Sci Pract 2019;7:515-520.
23. Walsh EE, Falsey AR. Respiratory syncytial virus infection in adult populations. Infect Disord Drug
Targets 2012;12:98-102.
24. Mehta J, Walsh EE, Mahadevia PJ, Falsey AR. Risk factors for respiratory syncytial virus illness among patients with chronic obstructive pulmonary disease. COPD 2013;10:293-299.
25. Lennette EH, Stallones RA, Holguin AH. Pattern of respiratory virus infections in army recruits. Am J Hyg 1961;74:225-233.
26. Hers JF, Masurel N, Gans JC. Acute respiratory disease associated with pulmonary involvement in military servicement in The Netherlands. A serologic and bacteriologic survey, January 1967 to January 1968. Am Rev Respir Dis 1969;100:499-506.
27. Sanford JP. Acute respiratory disease in the United States Army in the Republic of Vietnam, 1965-1970. Yale J Biol Med 1975;48:179-184.
28. Radin JM, Hawksworth AW, Kammerer PE, Balansay M, Raman R, Lindsay SP, et al. Epidemiology of pathogen-specific respiratory infections among three US populations. PLoS One 2014;9(12):e114871.
29. Eick AA, Faix DJ, Tobler SK, Nevin RL, Lindler LE, Hu Z, et al. Serosurvey of bacterial and viral respiratory pathogens among deployed U.S. service members. Am J Prev Med 2011;41:573-580.
30. Park WJ. Seroprevalence of respiratory syncytial virus IgG among healthy young adults in basic training for the Republic of Korea Air Force. J Korean Med Sci 2014;29:1325-1327.
31. Lessler J, Reich NG, Brookmeyer R, Perl TM, Nelson KE, Cummings DA. Incubation periods of acute respiratory viral infections: a systematic review. Lancet Infect Dis 2009;9:291-300.
32. Sanchez JL, Cooper MJ, Myers CA, Cummings JF, Vest KG, Russell KL, et al. Respiratory infections in the U.S. military: recent experience and control. Clin Microbiol Rev 2015;28:743-800.
33. Kim CK, Choi J, Callaway Z, Kim HB, Chung JY, Koh YY, et al. Clinical and epidemiological comparison of human metapneumovirus and respiratory syncytial virus in seoul, Korea, 2003-2008. J Korean Med Sci 2010;25:342-347.
34. Li Y, Reeves RM, Wang X, Bassat Q, Brooks WA, Cohen C, et al. Global patterns in monthly activity of influenza virus, respiratory syncytial virus, parainfluenza virus, and metapneumovirus: a systematic analysis. Lancet Glob Health 2019;7(8):e1031-e1045.
35. Gamba-Sanchez N, Rodriguez-Martinez C, Sossa-Briceño M. Epidemic activity of respiratory syncytial virus is related to temperature and rainfall in equatorial tropical countries. Epidemiol Infect 2016;144:2057-2063.
36. Rodriguez-Martinez CE, Sossa-Briceno MP, Acuna-Cordero R. Relationship between meteorological conditions and respiratory syncytial virus in a tropical country. Epidemiol Infect 2015;143:2679-2686.
37. Sloan C, Heaton M, Kang S, Berrett C, Wu P, Gebretsadik T, et al. The impact of temperature and relative humidity on spatiotemporal patterns of infant bronchiolitis epidemics in the contiguous United States. Health Place 2017;45:46-54.
38. Wentz LM, Ward MD, Potter C, Oliver SJ, Jackson S, Izard RM, et al. Increased risk of upper respiratory infection in military recruits who report sleeping less than 6 h per night. Mil Med 2018;183(11-12):e699-e704.
39. Korzeniewski K, Nitsch-Osuch A, Konarski M, Guzek A, Prokop E, Bieniuk K. Prevalence of acute respiratory tract diseases among soldiers deployed for military operations in Iraq and Afghanistan. Adv Exp Med Biol 2013;788:117-124.
40. Soltis BW, Sanders JW, Putnam SD, Tribble DR, Riddle MS. Self reported incidence and morbidity of acute respiratory illness among deployed U.S. military in Iraq and Afghanistan. PLoS One 2009;4(7): e6177.
41. Zlateva KT, Vijgen L, Dekeersmaeker N, Naranjo C, Van Ranst M. Subgroup prevalence and genotype circulation patterns of human respiratory syncytial virus in Belgium during ten successive epidemic seasons. J Clin Microbiol 2007;45:3022-3030.
42. Venter M, van Niekerk S, Rakgantso A, Bent N. Identification of deletion mutant respiratory syncytial virus strains lacking most of the G protein in immunocompromised children with pneumonia in South Africa. J Virol 2011;85:8453-8457.
43. Tabatabai J, Thielen A, Lehners N, Daeumer M, Schnitzler P. Respiratory syncytial virus A in haematological patients with prolonged shedding: Premature stop codons and deletion of the genotype ON1 72-nucleotide-duplication in the attachment G gene. J Clin Virol 2018;98:10-17.
44. Venter M, Madhi SA, Tiemessen CT, Schoub BD. Genetic diversity and molecular epidemiology of respiratory syncytial virus over four consecutive seasons in South Africa: identification of new subgroup A and B genotypes. J Gen Virol 2001;82:2117-2124.
45. Parveen S, Sullender WM, Fowler K, Lefkowitz EJ, Kapoor SK, Broor S. Genetic variability in the G protein gene of group A and B respiratory syncytial viruses from India. J Clin Microbiol 2006;44:3055-3064.
46. Law B, Carbonell-Estrany X, Simoes E. An update on respiratory syncytial virus epidemiology: a developed country perspective. Respir Med 2002;96 Suppl B:S1-7.
47. Faghihloo E, Salimi V, Rezaei F, Naseri M, Mamishi S, Mahmoodi M, et al. Genetic diversity in the G protein gene of human respiratory syncytial virus among Iranian children with acute respiratory symptoms. Iran J Pediatr 2011;21:58-64.
48. Salimi V, Tavakoli-Yaraki M, Yavarian J, Bont L, Mokhtari-Azad T. Prevalence of human respiratory syncytial virus circulating in Iran. J Infect Public Health 2016;9:125-135.
49. Hall CB, Walsh EE, Long CE, Schnabel KC. Immunity to and frequency of reinfection with respiratory syncytial virus. J Infect Dis 1991;163:693-698.
50. Östlund MR, Lindell AT, Stenler S, Riedel HM, Wirgart BZ, Grillner L. Molecular epidemiology and genetic variability of respiratory syncytial virus (RSV) in Stockholm, 2002–2003. J Med Virol 2008;80:159-167.
| Files | ||
| Issue | Vol 12 No 5 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v12i5.4612 | |
| Keywords | ||
| Respiratory tract infection; Human respiratory syncytial virus; Military trainees; Reverse transcription polymerase chain reaction; Genotyping | ||
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How to Cite
1.
Karbalaie Niya MH, Salimi Jeda A, Tavakoli A, Sohani H, Safarnezhad Tameshkel F, Panahi M, Izadi M, Zamani F, Keyvani H. Molecular epidemiology of human respiratory syncytial virus (HRSV) in Iranian military trainees with acute respiratory symptoms in 2017. Iran J Microbiol. 2020;12(5):495-502.
