Przegląd Geograficzny T. 93 z. 1 (2021)
This study was designed to explore the impact of meteorological factors (air temperature, relative and absolute humidity, wind, cloudiness and precipitation) on influenza morbidity in four selected big cities in Poland – Cracow, Poznań, Warsaw and Wrocław. Atmospheric data obtained from four meteorological stations spread over six years (2013‑2018) were compared to influenza-like illnesses (ILI) reports, obtained from the Voivodship Units of the State Sanitary Inspection for the same locations and period. Data were analysed using Spearman correlation and negative binomial regressions to capture the nonlinear relationship between exposure to environmental conditions and influenza morbidity. Our study found a strong negative association of absolute air humidity with influenza infections (RR = 0.738) and positive relationship with minimal temperature (RR = 1.148). The effect of wind speed, cloudiness and precipitation on ILI was less evident. Proposed model is valid for all age groups in Polish cities, but suits the best to elderly citizens (65+). The model is also appropriate for different seasons, however only absolute humidity, minimal temperature and wind speed are considered significant variables all year round. Furthermore, we observed 6 to 9-days delay between particular adverse weather conditions and ILI morbidity increase, as 1-week lag model proved to have the highest predictive power (AIC = 8644.97). Although meteorological variables have statistically significant contribution to explain influenza morbidity, there are also other non-climatic factors, that can possibly influence the seasonality and complexity of influenza epidemiology in Polish cities.
Akaike, H. (1998). Information Theory and an Extension of the Maximum Likelihood Principle. W:E.Parzen, K. Tanabe, & G. Kitagawa (red.), Selected Papers of Hirotugu Akaike. Springer Series in Statis‑tics (Perspectives in Statistics). New York: Springer. https://doi.org/10.1007/978‑1-4612‑1694‑0_15
Babcock, H.M., Merz, L.R., & Fraser, V.J. (2006). Is Influenza an Influenza-Like Illness? Clinical Presentation of Influenza in Hospitalized Patients. Infection Control & Hospital Epidemiology, 27(3), 266‑270. https://doi.org/10.1086/501539
Bednarska, K., Hallmann-Szelińska, E. Kondratiuk, K., Rabczenko, D., & Brydak, L. (2016). Innowacje w nadzorze nad grypą w Polsce. Problemy Higieny i Epidemiologii, 97(2), 101‑105.
Błażejczyk, K., Baranowski, J., & Błażejczyk, A. (2015). Wpływ klimatu na stan zdrowia w Polsce: stan aktualny oraz prognoza do 2100 roku. Warszawa: Wydawnictwo Akademickie SEDNO. http://rcin.org.pl/igipz/Content/60110/WA51_79962_r2015_Wplyw-klimatu-na-sta.pdf
Bouvier, N.M., & Palese, P. (2008). The biology of influenza viruses. Vaccine, 26, D49-D53. https://doi.org/https://doi.org/10.1016/j.vaccine.2008.07.039
Brankston, G., Gitterman, L., Hirji, Z., Lemieux, C., & Gardam, M. (2007). Transmission of influenza A in human beings. The Lancet. Infectious Diseases, 7(4), 257‑265. https://doi.org/10.1016/S1473‑3099 (07)70029‑4
Brydak, L.B. (2012). Grypa - problem stary jak świat. Hygeia Public Health, 47(1), 1‑7.
Brydak, L.B. (2014). Grypa znana od stuleci - nadal groźna. Flu known for centuries - still dangerous Szczepionki i szczepienia przeciw grypie. Family Medicine & Primary Care Review, 16(2), 181‑184.
Buckingham-Jeffery, E., Morbey, R., House, T., Elliot, A. J., Harcourt, S., & Smith, G.E. (2017). Correcting for day of the week and public holiday effects: improving a national daily syndromic surveillance service for detecting public health threats. BMC Public Health, 17(1), 477. https://doi.org/10.1186/s12889‑017‑4372-y
Cannell, J.J., Vieth, R., Umhau, J.C., Holick, M.F., Grant, W.B., Madronich, S., Garland, C.F., & Giovannucci, E. (2006). Epidemic influenza and vitamin D. Epidemiology and Infection, 134, 1129‑1140. https://doi.org/10.1017/S0950268806007175
Chan, P K.S., Mok, H.Y., Lee, T.C., Chu, I.M.T., Lam, W.-Y., & Sung, J.J.Y. (2009). Seasonal influenza activity in Hong Kong and its association with meteorological variations. Journal of Medical Virology, 81(10), 1797‑1806. https://doi.org/10.1002/jmv.21551
Chen, G., Zhang, W., Li, S., Zhang, Y., Williams, G., Huxley, R., Ren, H., Cao, W., & Guo, Y. (2017). The impact of ambient fine particles on influenza transmission and the modification effects of temperature in China: A multi-city study. Environment International, 98, 82‑88. https://doi.org/10.1016/J.ENVINT.2016.10.004
Ciencewicki, J., & Jaspers, I. (2007). Air Pollution and Respiratory Viral Infection. Inhalation Toxicology, 19(14), 1135‑1146. https://doi.org/10.1080/08958370701665434
Cox, N.J., & Subbarao, K. (2000). Global Epidemiology of Influenza: Past and Present. Annual Review of Medicine, 51, 407‐421. https://doi.org/10.1146/annurev.med.51.1.407
Department of Infectious Disease Epidemiology and Surveillance NIZP-PZH. (2019). Definitions of infectious disease cases for the needs of epidemiological surveillance, 2018.
Dowell, S.F. (2001). Seasonal variation in host susceptibility and cycles of certain infectious diseases. Emerging Infectious Diseases, 7, 369‑374. https://doi.org/10.3201/eid0703.017301
du Prel, J., Puppe, W., Gröndahl, B., Knuf, M., Weigl, J.A.I., Schaaff, F., & Schmitt, H. (2009). Are Meteorological Parameters Associated with Acute Respiratory Tract Infections? Clinical Infectious Diseases, 49(6), 8618‑68. https://doi.org/10.1086/605435
Eccles, R. (2005). Understanding the symptoms of the common cold and influenza. The Lancet. Infectious Diseases, 5(11), 718‑725. https://doi.org/10.1016/S1473‑3099 (05)70270-X
Fdez-Arroyabe, P. (2012). Influenza epidemics and Spanish climatic domains. Health, 04(10), 941‑945. https://doi.org/10.4236/health.2012.430144
Feng, C., Li, J., Sun, W., Zhang, Y., & Wang, Q. (2016). Impact of ambient fine particulate matter (PM2.5) exposure on the risk of influenza-like-illness: A time-series analysis in Beijing, China. Environmental Health: A Global Access Science Source, 15(1), 1‑13. https://doi.org/10.1186/s12940‑016‑0115‑2
Finkelman, B.S., Viboud, C., Koelle, K., Ferrari, M.J., Bharti, N., & Grenfell, B.T. (2007). Global patterns in seasonal activity of influenza A/H3N2, A/H1N1, and B from 1997 to 2005: Viral coexistence and latitudinal gradients. PLoS ONE, 2(12), e1296. https://doi.org/10.1371/journal.pone.0001296
Fisman, D. (2012). Seasonality of viral infections: Mechanisms and unknowns. Clin
Gomez-Barroso, D., León-Gómez, I., Delgado-Sanz, C., & Larrauri, A. (2017). Climatic factors and influenza transmission, Spain, 2010‑2015. International Journal of Environmental Research and Public Health, 14(12), 1469. https://doi.org/10.3390/ijerph14121469
Heikkinen, T., & Järvinen, A. (2003). The common cold. The Lancet, 361(9351), 51‑59. https://doi.org/10.1016/S0140‑6736 (03)12162‑9
Huang, X., Mengersen, K., Milinovich, G., & Hu, W. (2017). Effect of weather variability on seasonal influenza among different age groups in Queensland, Australia: A Bayesian spatiotemporal analysis. Journal of Infectious Diseases, 215(11), 1695‑1701. https://doi.org/10.1093/infdis/jix181
Huppert, A., Barnea, O., Katriel, G., Yaari, R., Roll, U., & Stone, L. (2012). Modeling and Statistical Analysis of the Spatio-Temporal Patterns of Seasonal Influenza in Israel. PLoS ONE, 7(10), e45107. https://doi.org/10.1371/journal.pone.0045107
Hwang, J.-S., & Chan, C.-C. (2002). Effects of Air Pollution on Daily Clinic Visits for Lower Respiratory Tract Illness. American Journal of Epidemiology, 155(1), 1‑10. https://doi.org/10.1093/aje/155.1.1
Iha, Y., Kinjo, T., Parrott, G., Higa, F., Mori, H., & Fujita, J. (2016). Comparative epidemiology of influenza A and B viral infection in a subtropical region: a 7-year surveillance in Okinawa, Japan. BMC Infectious Diseases, 16(1), 650. https://doi.org/10.1186/s12879‑016‑1978‑0
Iwańczak, B. (2015). Zróżnicowanie przestrzenne zagrożenia grypą w Polsce. Prace i Studia Geograficzne, 57, 127‑144.
Jaakkola, K., Saukkoriipi, A., Jokelainen, J., Juvonen, R., Kauppila, J., Vainio, O., Ziegler, T., Rönkkö, E., Jaakkola, J.J.K., Ikäheimo, T.M., & the KIAS-Study Group (2014). Decline in temperature and humidity increases the occurrence of influenza in cold climate. Environmental Health, 13(1), 22. https://doi.org/10.1186/1476‑069X-13‑22
Jensen, M.M. (1964). Inactivation of Airborne Viruses by Ultraviolet Irradiation. Applied Microbiology, 12(5), 418‑420. https://doi.org/10.1128/aem.12.5.418‑420.1964
Johnson, J.B., & Omland, K.S. (2004). Model selection in ecology and evolution. Trends in Ecology and Evolution, 19(2), 101‑108. https://doi.org/10.1016/j.tree.2003.10.013
Korzeniecki, P. (2015). Warunki pogodowe sprzyjające zwiększonej zachorowalności na grypę w województwie mazowieckim (Weather conditions associated with increased occurrence of influenza in the Mazovia Voivodeship in Poland). W: P. Krąż, J. Liro, & M. Liro (red.), Współczesne problemy i kierunki badawcze w geografii, 3 (s. 109‑122). Kraków: Instytut Geografii i Gospodarki Przestrzennej UJ.
Lessler, J., Reich, N.G., Brookmeyer, R., Perl, T.M., Nelson, K.E., & Cummings, D.A.T. (2009). Incubation periods of acute respiratory viral infections: a systematic review. The Lancet. Infectious Diseases, 9(5), 291‑300. https://doi.org/10.1016/S1473‑3099 (09)70069‑6
Li, C.C., Wang, L., Eng, H.L., You, H.L., Chang, L.S., Tang, K.S., Lin, Y.J., Kuo, H.C., Lee, I.K., Liu, J.W., Huang, E.Y., & Yang, K.D. (2010). Correlation of pandemic (H1N1) 2009 viral load with diseas severity and prolonged viral shedding in children. Emerging Infectious Diseases, 16, 1266‑1272. https://doi.org/10.3201/eid1608.091918
Li, Y., Wang, X.L., & Zheng, X. (2018). Impact of weather factors on influenza hospitalization across different age groups in subtropical Hong Kong. International Journal of Biometeorology, 62(9), 1615‑1624. https://doi.org/10.1007/s00484‑018‑1561-z
Liu, X.X., Li, Y., Qin, G., Zhu, Y., Li, X., Zhang, J., Zhao, K., Hu, M., Wang, X.L., & Zheng, X. (2019). Effects of air pollutants on occurrences of influenza-like illness and laboratory-confirmed influenza in Hefei, China. International Journal of Biometeorology, 63(1), 51‑60. https://doi.org/10.1007/s00484‑018‑1633‑0
Lochmiller, R.L., & Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos, 88(1), 87‑98. https://doi.org/10.1034/j.1600‑0706.2000.880110.x
Lofgren, E., Fefferman, N.H., Naumov, Y.N., Gorski, J., & Naumova, E.N. (2007). Influenza Seasonality: Underlying Causes and Modeling Theories. Journal of Virology, 81(11), 5429‑5436. https://doi.org/10.1128/jvi.01680‑06
Lowen, A.C., Mubareka, S., Steel, J., & Palese, P. (2007). Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathogens, 3(10), 1470‑1476. https://doi.org/10.1371/journal.ppat.0030151
Mäkinen, T.M., Juvonen, R., Jokelainen, J., Harju, T.H., Peitso, A., Bloigu, A., Silvennoinen-Kassinen, S., Leinonen, M., & Hassi, J. (2009). Cold temperature and low humidity are associated with increased occurrence of respiratory tract infections. Respiratory Medicine, 103(3), 456‑462 https://doi.org/10.1016/j.rmed.2008.09.011
Martineau, A.R., Jolliffe, D.A., Hooper, R.L., Greenberg, L., Aloia, J.F., Bergman, P., Dubnov-Raz, G., Esposito, S., Ganmaa, D., Ginde, A.A., Goodall, E.C., Grant, C.C., Griffiths, C.J., Janssens, W., Laaksi, I., Manaseki-Holland, S., Mauger, D., Murdoch, D.R., Neale, R., & et al. (2017). Vitamin D supplementation to prevent acute respiratory tract infections: Systematic review and meta-analysis of individual participant data. BMJ (Online), 356. https://doi.org/10.1136/bmj.i6583
McDevitt, J., Rudnick, S., First, M., & Spengler, J. (2010). Role of absolute humidity in the inactivation of influenza viruses on stainless steel surfaces at elevated temperatures. Applied and Environmental Microbiology, 76(12), 3943‑3947. https://doi.org/10.1128/AEM.02674‑09
Meerhoff, T.J., Paget, W.J., Aguilera, J.F., & van der Velden, J. (2004). Harmonising the virological surveillance of influenza in Europe: results of an 18-country survey. Virus Research, 103(1‑2), 31‑33. https://doi.org/10.1016/j.virusres.2004.02.009
Moorthy, M., Castronovo, D., Abraham, A., Bhattacharyya, S., Gradus, S., Gorski, J., Naumov, Y.N., Fefferman, N.H., & Naumova, E.N. (2012). Deviations in influenza seasonality: Odd coincidence or obscure consequence? Clinical Microbiology and Infection, 18(10), 955‑962. https://doi.org/10.1111/j.1469‑0691.2012.03959.x
Mourtzoukou, E.G., & Falagas, M.E. (2007). Exposure to cold and respiratory tract infections. International Journal of Tuberculosis and Lung Disease, 11(9), 938‑943.
Narodowy Instytut Zdrowia Publicznego - PZH. (2019). Choroby zakaźne i zatrucia w Polsce. Biuletyn roczny. Pobrane z: http://wwwold.pzh.gov.pl/oldpage/epimeld/index_p.html (30.03.2020).
Nastos, P.T., & Matzarakis, A. (2006). Weather impacts on respiratory infections in Athens, Greece. International Journal of Biometeorology, 50(6), 358‑369. https://doi.org/10.1007/s00484‑006‑0031‑1
Nelson, M.I., & Holmes, E.C. (2007). The evolution of epidemic influenza. Nature Reviews Genetics, 8(3), 196‑205. https://doi.org/10.1038/nrg2053
Peci, A., Winter, A L., Li, Y., Gnaneshan, S., Liu, J., Mubareka, S., Gubbay, J.B., Humidity, A., & Humidity, R. (2019). Effects of Absolute Humidity, Relative Humidity, Temperature, and Wind Speed on Influenza Activity in Toronto, Ontario, Canada. Applied and Environmental Microbiology, 85(6), 1‑13. https://doi.org/10.1128/AEM.02426‑18
Pica, N., & Bouvier, N.M. (2012). Environmental factors affecting the transmission of respiratory viruses. Current Opinion in Virology, 2(1), 90‑95. https://doi.org/10.1016/j.coviro.2011.12.003
Polozov, I.V., Bezrukov, L., Gawrisch, K., & Zimmerberg, J. (2008). Progressive ordering with decreasing temperature of the phospholipids of influenza virus. Nature Chemical Biology, 4(4), 248‑255. https://doi.org/10.1038/nchembio.77
Price, R.H.M., Graham, C., & Ramalingam, S. (2019). Association between viral seasonality and meteorological factors. Scientific Reports, 9(1), 1‑11. https://doi.org/10.1038/s41598‑018‑37481-y
Romaszko, J., Skutecki, R., Bocheński, M., Cymes, I., Dragańska, E., Jastrzębski, P., Morocka-Tralle, I., Jalali, R., Jeznach-Steinhagen, A., & Glińska-Lewczuk, K. (2019). Applicability of the universal thermal climate index for predicting the outbreaks of respiratory tract infections: a mathematical modeling approach. International Journal of Biometeorology, 63(9), 1231‑1241. https://doi.org/10.1007/s00484‑019‑01740-y
Roussel, M., Pontier, D., Cohen, J.M., Lina, B., & Fouchet, D. (2016). Quantifying the role of weather on seasonal influenza. BMC Public Health, 16(1), 1‑14. https://doi.org/10.1186/s12889‑016‑3114-x
Ruf, B.R., & Knuf, M. (2014). The burden of seasonal and pandemic influenza in infants and children. European Journal of Pediatrics, 173, 265‑276. https://doi.org/10.1007/s00431‑013‑2023‑6
Sagripanti, J.-L., & Lytle, C.D. (2007). Inactivation of Influenza Virus by Solar Radiation. Photochemistry and Photobiology, 83(5), 1278‑1282. https://doi.org/10.1111/j.1751‑1097.2007.00177.x
Salah, B., Dinh Xuan, A.T., Fouilladieu, J.L., Lockhart, A., & Regnard, J. (1988). Nasal mucociliary transport in healthy subjects is slower when breathing dry air. European Respiratory Journal, 1(9), 846‑849.
Schulman, J.L., & Kilbourne, E.D. (1963). Experimental transmission of influenza virus infection in mice. II. some factors affecting the incidence of transmitted infection. The Journal of Experimental Medicine, 118(2), 267‑275. https://doi.org/10.1084/jem.118.2.267
Shaman, J., & Kohn, M. (2009). Absolute humidity modulates influenza survival, transmission, and seasonality. Proceedings of the National Academy of Sciences of the United States of America, 106(9), 3243‑3248. https://doi.org/10.1073/pnas.0806852106
Shaman, J., Pitzer, V.E., Viboud, C., Grenfell, B.T., & Lipsitch, M. (2010). Absolute humidity and the seasonal onset of influenza in the continental United States. PLoS Biology, 8(2), e1000316. https://doi.org/10.1371/journal.pbio.1000316
Shaw Stewart, P.D. (2016). Seasonality and selective trends in viral acute respiratory tract infections. Medical Hypotheses, 86, 104‑119. https://doi.org/10.1016/j.mehy.2015.11.005
Shoji, M., Katayama, K., & Sano, K. (2011). Absolute humidity as a deterministic factor affecting seasonal influenza epidemics in Japan. Tohoku Journal of Experimental Medicine, 224, 251‑256. https://doi.org/10.1620/tjem.224.251
Simonsen, L. (1999). The global impact of influenza on morbidity and mortality. Vaccine, 17 (Supplement 1), 3-10. https://doi.org/10.1016/S0264‑410X (99)00099‑7
Su, W., Wu, X., Geng, X., Zhao, X., Liu, Q., & Liu, T. (2019). The short-term effects of air pollutants on influenza-like illness in Jinan, China. BMC Public Health, 19(1), 1‑12. https://doi.org/10.1186/s12889‑019‑7607‑2
Sundell, N., Andersson, L.M., Brittain-Long, R., Lindh, M., & Westin, J. (2016). A four year seasonal survey of the relationship between outdoor climate and epidemiology of viral respiratory tract infections in a temperate climate. Journal of Clinical Virology, 84, 59‑63. https://doi.org/10.1016/j.jcv.2016.10.005
Tamerius, J., Nelson, M.I., Zhou, S.Z., Viboud, C., Miller, M.A., & Alonso, W.J. (2011). Global influenza seasonality: Reconciling patterns across temperate and tropical regions. Environmental Health Perspectives, 119(4), 439‑445. https://doi.org/10.1289/ehp.1002383
Tang, J.W., Lai, F.Y.L., Nymadawa, P., Deng, Y.-M., Ratnamohan, M., Petric, M., Loh, T.P., Tee, N.W.S., Dwyer, D.E., Barr, I.G., & Wong, F.Y.W. (2010). Comparison of the incidence of influenza in relation to climate factors during 2000‑2007 in five countries. Journal of Medical Virology, 82(11), 1958‑1965. https://doi.org/10.1002/jmv.21892
Tellier, R. (2006). Review of aerosol transmission of influenza A virus. Emerging Infectious Diseases, 12, 1657‑1662. https://doi.org/10.3201/eid1211.060426
Urashima, M., Segawa, T., Okazaki, M., Kurihara, M., Wada, Y., & Ida, H. (2010). Randomized trial of vitamin D supplementation to prevent seasonal influenza A in schoolchildren. American Journal of Clinical Nutrition, 91(5), 1255‑1260. https://doi.org/10.3945/ajcn.2009.29094
Valenciano, M., Kissling, E., & I-MOVE Case-Control Study Team. (2013). Early estimates of seasonal influenza vaccine effectiveness in Europe: results from the I-MOVE multicentre case-control study, 2012/13. Eurosurveillance, 18(7), 3. https://doi.org/https://doi.org/10.2807/ese.18.07.20400-en
Van Noort, S.P., Águas, R., Ballesteros, S., & Gomes, M.G.M. (2012). The role of weather on the relation between influenza and influenza-like illness. Journal of Theoretical Biology, 298, 131‑137. https://doi.org/10.1016/j.jtbi.2011.12.020
Wang, X.L., Yang, L., He, D.H., Chiu, A.P., Chan, K.H., Chan, K.P., Zhou, M., Wong, C.M., Guo, Q., & Hu, W. (2017). Different responses of influenza epidemic to weather factors among Shanghai, Hong Kong, and British Columbia. International Journal of Biometeorology, 61(6), 1043‑1053. https://doi.org/10.1007/s00484‑016‑1284-y
Weber, T.P., & Stilianakis, N.I. (2008). Inactivation of influenza A viruses in the environment and modes of transmission: A critical review. Journal of Infection, 57, 361‑373. https://doi.org/10.1016/j.jinf.2008.08.013
WHO. (2020). Virology of human influenza. Pobrane z: http://www.euro.who.int/en/health-top‑ics/communicable-diseases/influenza/data-and-statistics/virology-of-human-influenza (26.03.2020).
Wiemken, T.L., Mattingly, W.A., Furmanek, S.P., Guinn, B.E., English, C.L., Carrico, R.M., Peyrani, P., & Ramirez, J.A. (2017). Impact of Temperature Relative Humidity and Absolute Humidity on the incidence of hospitalizations for lower respiratory tract infections due to influenza, rjinovirus, and respiratory syncytial virus: results from community-axquired pneumonia organization. University of Louisville Journal of Respiratory Infections, 1(3), 27‑35. https://doi.org/10.18297/jri/vol1/iss3/7
Xiao, H., Tian, H., Lin, X., Gao, L., Dai, X., Zhang, X., Chen, B., Zhao, J., & Xu, J. (2013). Influence of extreme weather and meteorological anomalies on outbreaks of influenza A (H1N1). Chinese Science Bulletin, 58(7), 741‑749. https://doi.org/10.1007/s11434‑012‑5571‑7
Yaari, R., Katriel, G., Huppert, A., Axelsen, J.B., & Stone, L. (2013). Modelling seasonal influenza: The role of weather and punctuated antigenic drift. Journal of the Royal Society Interface, 10(84). https://doi.org/10.1098/rsif.2013.0298
Zambon, M., Stockton, J., Clewley, J., & Fleming, D. (2001). Contribution of influenza and respiratory syncytial virus to community cases of influenza-like illness: an observational study. The Lancet, 358(9291), 1410‑1416. https://doi.org/10.1016/S0140‑6736 (01)06528-X
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Institute of Geography and Spatial Organization of the Polish Academy of Sciences
Nov 6, 2023
Apr 12, 2021
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https://rcin.org.pl./publication/215378
Lindner-Cendrowska, Katarzyna
Mieszkowski, Łukasz
Symonides, Ewa
Koźmiński, Zygmunt (1902–1939)
Zając, Tadeusz
Leśniak, Andrzej