Environmental Drivers of the Spatiotemporal Dynamics of Respiratory Syncytial Virus in the United States

English version České info

Respiratory syncytial virus (RSV) causes annual outbreaks of respiratory disease every winter in temperate climates, which can be severe particularly among infants. In the United States, RSV activity begins each autumn in Florida and appears to spread from the southeast to the northwest. Using data on hospitalizations and laboratory tests for RSV, we show that the timing of epidemics is associated with a variety of climatic factors, including temperature, vapor pressure, precipitation, and potential evapotranspiration (PET). Furthermore, using a dynamic model, we show that seasonal variation in the transmission rate of RSV can be correlated with the amplitude and timing of variation in PET, which is a measure of demand for water from the atmosphere. States with colder, drier weather and a large seasonal swing in PET tended to experience an alternating pattern of “early-big” RSV epidemics one year followed by a “late-small” epidemic the next year, which our model was able to reproduce based on the interaction between susceptible and infectious individuals. However, we cannot fully explain why epidemics begin in Florida. Being able to understand and predict the timing of RSV activity is important for optimizing the delivery of immunoprophylaxis to high-risk individuals.

Vyšlo v časopise: Environmental Drivers of the Spatiotemporal Dynamics of Respiratory Syncytial Virus in the United States. PLoS Pathog 11(1): e32767. doi:10.1371/journal.ppat.1004591
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004591

Souhrn

Zdroje

1. NairH, NokesDJ, GessnerBD, DheraniM, MadhiSA, et al. (2010) Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: A systematic review and meta-analysis. Lancet 375 : 1545–1555 doi:10.1016/S0140-6736(10)60206-1

2. ZhouH, ThompsonWW, ViboudCG, RingholzCM, ChengP-Y, et al. (2012) Hospitalizations associated with influenza and respiratory syncytial virus in the United States, 1993–2008. Clin Infect Dis 54 : 1427–1436 doi:10.1093/cid/cis211

3. GilchristS, TörökTJ, GaryHE, AlexanderJP, AndersonLJ (1994) National surveillance for respiratory syncytial virus, United States, 1985–1990. J Infect Dis 170 : 986–990.

4. MullinsJA, LamonteAC, BreseeJS, AndersonLJ (2003) Substantial variability in community respiratory syncytial virus season timing. Pediatr Infect Dis J 22 : 857–862 doi:10.1097/01.inf.0000090921.21313.d3

5. PanozzoCA, FowlkesAL, AndersonLJ (2007) Variation in timing of respiratory syncytial virus outbreaks: Lessons from national surveillance. Pediatr Infect Dis J 26: S41–5 doi:10.1097/INF.0b013e318157da82

6. StensballeLG, DevasundaramJK, SimõesEAF (2003) Respiratory syncytial virus epidemics: the ups and downs of a seasonal virus. Pediatr Infect Dis J 22: S21–32 doi:10.1097/01.inf.0000053882.70365.c9

7. WeberMW, MulhollandEK, GreenwoodBM (1998) Respiratory syncytial virus infection in tropical and developing countries. Trop Med Int Health 3 : 268–280.

8. Bloom-FeshbachK, AlonsoWJ, CharuV, TameriusJ, SimonsenL, et al. (2013) Latitudinal variations in seasonal activity of influenza and respiratory syncytial virus (RSV): a global comparative review. PLoS One 8: e54445 doi:10.1371/journal.pone.0054445

9. LightM, BaumanJ, MavundaK, MalinoskiF, EgglestonM (2008) Correlation between respiratory syncytial virus (RSV) test data and hospitalization of children for RSV lower respiratory tract illness in Florida. Pediatr Infect Dis J 27 : 512–518 doi:10.1097/INF.0b013e318168daf1

10. McGuinessCB, BoronML, SaundersB, EdelmanL, KumarVR, et al. (2014) Respiratory syncytial virus surveillance in the United States, 2007–2012: results from a national surveillance system. Pediatr Infect Dis J 33 : 589–594 doi:10.1097/INF.0000000000000257

11. Modified recommendations for use of palivizumab for prevention of respiratory syncytial virus infections. Pediatrics 124 : 1694–1701 doi:–10.1542/peds.2009–2345

12. LangleyGF, AndersonLJ (2011) Epidemiology and prevention of respiratory syncytial virus infections among infants and young children. Pediatr Infect Dis J 30 : 510–517 doi:10.1097/INF.0b013e3182184ae7

13. PaivaTM, IshidaMA, BenegaMA, SantosCO, OliveiraMI, et al. (2012) Shift in the timing of respiratory syncytial virus circulation in a subtropical megalopolis: Implications for immunoprophylaxis. J Med Virol 84 : 1825–1830 doi:10.1002/jmv

14. PanozzoCA, StockmanLJ, CurnsAT, AndersonLJ (2010) Use of respiratory syncytial virus surveillance data to optimize the timing of immunoprophylaxis. Pediatrics 126: e116–23 doi:–10.1542/peds.2009–3221

15. AlonsoWJ, LaranjeiraBJ, PereiraSAR, FlorencioCMGD, MorenoEC, et al. (2012) Comparative dynamics, morbidity and mortality burden of pediatric viral respiratory infections in an equatorial city. Pediatr Infect Dis J 31: e9–14 doi:10.1097/INF.0b013e31823883be

16. ChewFT, DoraisinghamS, LingAE, KumarasingheG, LeeBW (1998) Seasonal trends of viral respiratory tract infections in the tropics. Epidemiol Infect 121 : 121–128.

17. DonaldsonGC (2006) Climate change and the end of the respiratory syncytial virus season. Clin Infect Dis 42 : 677–679 doi:10.1086/500208

18. Du PrelJ-B, PuppeW, GröndahlB, KnufM, WeiglJAI, et al. (2009) Are meteorological parameters associated with acute respiratory tract infections? Clin Infect Dis 49 : 861–868 doi:10.1086/605435

19. FlormanA, McLarenL (1988) The effect of altitude and weather on the occurrence of outbreaks of respiratory syncytial virus infections. J Infect Dis 158 : 1401–1402.

20. LapeñaS, RoblesM, CastanonL (2005) Climatic factors and lower respiratory tract infection due to respiratory syncytial virus in hospitalised infants in northern Spain. Eur J Epidemiol 20 : 271–276 doi:10.1007/sl0654-004-4539-6

21. MartinAJ, GardnerP, McQuillinJ (1978) Epidemiology of respiratory viral infection among paediatric inpatients over a six-year period in north-east England. Lancet 11 : 1035–1038.

22. NoyolaDE, MandevillePB (2008) Effect of climatological factors on respiratory syncytial virus epidemics. Epidemiol Infect 136 : 1328–1332 doi:10.1017/S0950268807000143

23. SimõesEAF (2003) Environmental and demographic risk factors for respiratory syncytial virus lower respiratory tract disease. J Pediatr 143: S118–S126.

24. WaltonNA, PoyntonMR, GestelandPH, MaloneyC, StaesC, et al. (2010) Predicting the start week of respiratory syncytial virus outbreaks using real time weather variables. BMC Med Inform Decis Mak 10 : 68 doi:10.1186/1472-6947-10-68

25. YusufS, PiedimonteG, AuaisA, DemmlerG, KrishnanS, et al. (2007) The relationship of meteorological conditions to the epidemic activity of respiratory syncytial virus. Epidemiol Infect 135 : 1077–1090 doi:10.1017/S095026880600776X

26. WhiteLJ, WarisM, CanePA, NokesDJ, MedleyGF (2005) The transmission dynamics of groups A and B human respiratory syncytial virus (hRSV) in England & Wales and Finland: Seasonality and cross-protection. Epidemiol Infect 133 : 279–289.

27. WhiteLJ, MandlJN, GomesMGM, Bodley-TickellAT, CanePA, et al. (2007) Understanding the transmission dynamics of respiratory syncytial virus using multiple time series and nested models. Math Biosci 209 : 222–239 doi:10.1016/j.mbs.2006.08.018

28. LeecasterM, GestelandP, GreeneT, WaltonN, GundlapalliA, et al. (2011) Modeling the variations in pediatric respiratory syncytial virus seasonal epidemics. BMC Infect Dis 11 : 105 doi:10.1186/1471-2334-11-105

29. WeberA, WeberM, MilliganP (2001) Modeling epidemics caused by respiratory syncytial virus (RSV). Math Biosci 172 : 95–113.

30. PaynterS, YakobL, SimõesEAF, LuceroMG, TalloV, et al. (2014) Using mathematical transmission modelling to investigate drivers of respiratory syncytial virus seasonality in children in the Philippines. PLoS One 9: e90094 doi:10.1371/journal.pone.0090094

31. AltizerS, DobsonA, HosseiniP, HudsonP, PascualM, et al. (2006) Seasonality and the dynamics of infectious diseases. Ecol Lett 9 : 467–484 doi:10.1111/j.1461-0248.2005.00879.x

32. GrasslyNC, FraserC (2006) Seasonal infectious disease epidemiology. Proc Biol Sci 273 : 2541–2550 doi:10.1098/rspb.2006.3604

33. ShamanJ, PitzerVE, ViboudC, GrenfellBT, LipsitchM (2010) Absolute humidity and the seasonal onset of influenza in the continental United States. PLoS Biol 8: e1000316 doi:10.1371/journal.pbio.1000316

34. AcedoL, Díez-DomingoJ, MorañoJ, VillanuevaR-J (2010) Mathematical modelling of respiratory syncytial virus (RSV): Vaccination strategies and budget applications. Epidemiol Infect 138 : 853–860 doi:10.1017/S0950268809991373

35. ArenasAJ, González-ParraG, MorañoJ-A (2009) Stochastic modeling of the transmission of respiratory syncytial virus (RSV) in the region of Valencia, Spain. Biosystems 96 : 206–212 doi:10.1016/j.biosystems.2009.01.007

36. PitzerVE, ViboudC, SimonsenL, SteinerC, PanozzoCA, et al. (2009) Demographic variability, vaccination, and the spatiotemporal dynamics of rotavirus epidemics. Science (80-) 325 : 290–294 doi:10.1126/science.1172330

37. GlezenWP, TaberLH, FrankAL, KaselJA (1986) Risk of primary infection and reinfection with respiratory syncytial virus. Am J Dis Child 140 : 543–546.

38. NokesDJ, OkiroEA, NgamaM, WhiteLJ, OcholaR, et al. (2004) Respiratory syncytial virus epidemiology in a birth cohort from Kilifi district, Kenya: infection during the first year of life. J Infect Dis 190 : 1828–1832 doi:10.1086/425040

39. HallCB, WeinbergGA, IwaneMK, BlumkinAK, EdwardsKM, et al. (2009) The burden of respiratory syncytial virus infection in young children. N Engl J Med 360 : 588–598 doi:10.1056/NEJMoa0804877

40. ViboudC, BjørnstadON, SmithDL, SimonsenL, MillerMA, et al. (2006) Synchrony, waves, and spatial hierarchies in the spread of influenza. Science 312 : 447–451 doi:10.1126/science.1125237

41. HallCB, DouglasRG, GeimanJM (1980) Possible transmission by fomites of respiratory syncytial virus. J Infect Dis 141 : 98–102.

42. MeerhoffTJ, PagetJW, KimpenJL, SchellevisF (2009) Variation of respiratory syncytial virus and the relation with meteorological factors in different winter seasons. Pediatr Infect Dis J 28 : 860–866 doi:10.1097/INF.0b013e3181a3e949

43. De Mello FreitasFT (2013) Sentinel surveillance of influenza and other respiratory viruses, Brazil, 2000–2010. Brazilian J Infect Dis 17 : 62–68 doi:10.1016/j.bjid.2012.09.001

44. WelliverR (2009) The relationship of meteorological conditions to the epidemic activity of respiratory syncytial virus. Paediatr Respir Rev 10 Suppl 16–8 doi:10.1016/S1526-0542(09)70004-1

45. ZachariahP, ShahS, GaoD, SimõesEAF (2009) Predictors of the duration of the respiratory syncytial virus season. Pediatr Infect Dis J 28 : 772–776 doi:10.1097/INF.0b013e3181a3e5b6

46. WarisM, WhiteLJ (2006) Seasonality of respiratory syncytial virus infection. Clin Infect Dis 43 : 541 doi:10.1086/505986

47. SchenzleD (1984) An age-structured model of pre -⁠ and post-vaccination measles transmission. IMA J Math Appl Med Biol 1 : 169–191.

48. BolkerBM, GrenfellBT (1993) Chaos and biological complexity in measles dynamics. Proc R Soc Ser B Biol Sci 251 : 75–81.

49. ChaoDL, HalloranME, LonginiIM (2010) School opening dates predict pandemic influenza A(H1N1) outbreaks in the United States. J Infect Dis 202 : 877–880 doi:10.1086/655810

50. WarisM (1991) Pattern of respiratory syncytial virus epidemics in Finland: two-year cycles with alternating prevalence of groups A and B. J Infect Dis 163 : 464–469.

51. Mlinaric-GalinovicG, TabainI, KukovecT, VojnovicG, BozikovJ, et al. (2012) Analysis of biennial outbreak pattern of respiratory syncytial virus according to subtype (A and B) in the Zagreb region. Pediatr Int 54 : 331–335 doi:10.1111/j.1442-200X.2011.03557.x

52. MufsonMA, BelsheRB, OrvellC, NorrbyE (1988) Respiratory syncytial virus epidemics: variable dominance of subgroups A and B strains among children, 1981-1986. J Infect Dis 157 : 143–148.

53. HallCB, WalshEE, SchnabelKC, LongCE, McConnochieKM, et al. (1990) Occurrence of groups A and B of respiratory syncytial virus over 15 years: associated epidemiologic and clinical characteristics in hospitalized and ambulatory children. J Infect Dis 162 : 1283–1290.

54. WallingaJ, TeunisP, KretzschmarM (2006) Using data on social contacts to estimate age-specific transmission parameters for respiratory-spread infectious agents. Am J Epidemiol 164 : 936–944 doi:10.1093/aje/kwj317

55. MossongJ, HensN, JitM, BeutelsP, AuranenK, et al. (2008) Social contacts and mixing patterns relevant to the spread of infectious diseases. PLoS Med 5: e74 doi:10.1371/journal.pmed.0050074

56. EamesKTD, TilstonNL, Brooks-PollockE, EdmundsWJ (2012) Measured dynamic social contact patterns explain the spread of H1N1v influenza. PLoS Comput Biol 8: e1002425 doi:10.1371/journal.pcbi.1002425

57. GrenfellBT, PybusOG, GogJR, WoodJLN, DalyJM, et al. (2004) Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303 : 327–332 doi:10.1126/science.1090727

58. ViboudC, NelsonMI, TanY, HolmesEC (2013) Contrasting the epidemiological and evolutionary dynamics of influenza spatial transmission. Philos Trans R Soc Lond B Biol Sci 368 : 20120199.

59. (HCUP) HC and UP (n.d.) HCUP SID Database Documentation. Agency Healthc Res Qual Rockville, MD.

60. Population of States and Counties of the United States: 1790 to 1990 (n.d.). US Census Bur. Available: http://www.census.gov/population/www/censusdata/pop1790-1990.html. Accessed 4 April 2013.

61. CDC/NVSS (n.d.) Vital Statistics Online. Natl Vital Stat Syst. Available: http://www.cdc.gov/nchs/nvss.htm. Accessed 4 April 2013.

62. MitchellTD, JonesPD (2005) An improved method of constructing a database of monthly climate observations and associated high-resolution grids. Int J Climatol 25 : 693–712 doi:10.1002/joc.1181

63. GrenfellBT, BjørnstadON, KappeyJ (2001) Travelling waves and spatial hierarchies in measles epidemics. Nature 414 : 716–723 doi:10.1038/414716a

64. YuH, AlonsoWJ, FengL, TanY, ShuY, et al. (2013) Characterization of regional influenza seasonality patterns in china and implications for vaccination strategies: spatio-temporal modeling of surveillance data. PLoS Med 10: e1001552 doi:10.1371/journal.pmed.1001552

65. OcholaR, SandeC, FeganG, ScottPD, MedleyGF, et al. (2009) The level and duration of RSV-specific maternal IgG in infants in Kilifi Kenya. PLoS One 4: e8088 doi:10.1371/journal.pone.0008088

66. HendersonF, CollierA, ClydeWJ, DennyF (1979) Respiratory-Syncytial-Virus Infections, Reinfections and Immunity. N Engl J Med 300 : 530–534.

67. HallCB, GeimanJM, BiggarR (1976) Respiratory syncytial virus infections within families. N Engl J Med 294 : 414–419.

68. MontoA, BryanE, RhodesL (1974) The Tecumseh study of respiratory illness: VII. Further observations on the occurrence of respiratory syncytial virus and mycoplasma pneumoniae infections. Am J Epidemiol 100 : 458–468.

69. NokesDJ, OkiroEA, NgamaM, OcholaR, WhiteLJ, et al. (2008) Respiratory syncytial virus infection and disease in infants and young children observed from birth in Kilifi District, Kenya. Clin Infect Dis 46 : 50–57 doi:10.1086/524019

70. HallCB, WalshEE, LongCE, SchnabelKC (1991) Immunity to and frequency of reinfection with respiratory syncytial virus. J Infect Dis 163 : 693–698.

71. HallCB, DouglasRG, GeimanJM (1976) Respiratory syncytial virus infections in infants: quantitation and duration of shedding. J Pediatr 89 : 11–15.

72. OkiroEA, WhiteLJ, NgamaM, CanePA, MedleyGF, et al. (2010) Duration of shedding of respiratory syncytial virus in a community study of Kenyan children. BMC Infect Dis 10 : 15 doi:10.1186/1471-2334-10-15

73. BjørnstadON, FinkenstädtBF, GrenfellBT (2002) Dynamics of measles epidemics: Estimating scaling of transmission rates using a time series SIR model. Ecol Monogr 72 : 169–184.

74. GrenfellBT, BjørnstadON, FinkenstädtBF (2002) Dynamics of measles epidemics: Scaling noise, determinism, and predictability with the TSIR model. Ecol Monogr 72 : 185–202.