Assessment of climate change impact on the malaria vector Anopheles hyrcanus, West Nile disease, and incidence of melanoma in the Vojvodina Province (Serbia) using data from a regional climate model

Autoři: Dragutin T. Mihailović aff001;  Dušan Petrić aff002;  Tamaš Petrović aff003;  Ivana Hrnjaković-Cvjetković aff004;  Vladimir Djurdjevic aff006;  Emilija Nikolić-Đorić aff007;  Ilija Arsenić aff001;  Mina Petrić aff008;  Gordan Mimić aff011;  Aleksandra Ignjatović-Ćupina aff002
Působiště autorů: Department of Field and Vegetable Crops, Faculty of Agriculture, University of Novi Sad, Novi Sad, Serbia aff001;  Department of Plant and Environment Protection, Faculty of Agriculture, University of Novi Sad, Novi Sad, Serbia aff002;  Department for virology, Scientific Veterinary Institute “Novi Sad”, Novi Sad, Serbia aff003;  Institute of Public Health of Vojvodina, Novi Sad, Serbia aff004;  Faculty of Medicine, University of Novi Sad, Novi Sad, Serbia aff005;  Institute of Meteorology, Faculty of Physics, University of Belgrade, Belgrade, Serbia aff006;  Department of Agricultural Economics, Faculty of Agriculture, University of Novi Sad, Novi Sad, Serbia aff007;  Avia-GIS NV, Zoersel, Belgium aff008;  Department of Physics, Faculty of Sciences, University of Novi Sad, Novi Sad, Serbia aff009;  Department of Physics and Astronomy, Faculty of Sciences, University of Gent, Gent, Belgium aff010;  BioSense Institute, University of Novi Sad, Novi Sad, Serbia aff011
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article


Motivated by the One Health paradigm, we found the expected changes in temperature and UV radiation (UVR) to be a common trigger for enhancing the risk that viruses, vectors, and diseases pose to human and animal health. We compared data from the mosquito field collections and medical studies with regional climate model projections to examine the impact of climate change on the spreading of one malaria vector, the circulation of West Nile virus (WNV), and the incidence of melanoma. We analysed data obtained from ten selected years of standardised mosquito vector sampling with 219 unique location-year combinations, and 10 years of melanoma incidence. Trends in the observed data were compared to the climatic variables obtained by the coupled regional Eta Belgrade University and Princeton Ocean Model for the period 1961–2015 using the A1B scenario, and the expected changes up to 2030 were presented. Spreading and relative abundance of Anopheles hyrcanus was positively correlated with the trend of the mean annual temperature. We anticipated a nearly twofold increase in the number of invaded sites up to 2030. The frequency of WNV detections in Culex pipiens was significantly correlated to overwintering temperature averages and seasonal relative humidity at the sampling sites. Regression model projects a twofold increase in the incidence of WNV positive Cx. pipiens for a rise of 0.5°C in overwintering TOctober–April temperatures. The projected increase of 56% in the number of days with Tmax ≥ 30°C (Hot Days—HD) and UVR doses (up to 1.2%) corresponds to an increasing trend in melanoma incidence. Simulations of the Pannonian countries climate anticipate warmer and drier conditions with possible dominance of temperature and number of HD over other ecological factors. These signal the importance of monitoring the changes to the preparedness of mitigating the risk of vector-borne diseases and melanoma.

Klíčová slova:

Climate change – Climate modeling – Europe – Horses – Melanomas – Mosquitoes – Serbia – West Nile virus


1. Costello A, Abbas M, Allen A, Ball S, Bell S, Bellamy R, et al. Managing the health effects of climate change: lancet and University College London Institute for Global Health Commission. The Lancet. 2009;373: 1693–1733.

2. Mihailović DT, Lalić B, Drešković N, Mimić G, Djurdjević V, Jančić M. Climate change effects on crop yields in Serbia and related shifts of Köppen climate zones under the SRES-A1B and SRES-A2. Int J Climatol. 2015;35: 3320–3334. doi: 10.1002/joc.4209

3. King LJ, Anderson LR, Blackmore CG, Blackwell MJ, Lautner EA, Marcus LC, et al. Executive summary of the AVMA One Health Initiative Task Force report. J Am Vet Med Assoc. 2008;233: 259–261. doi: 10.2460/javma.233.2.259 18627228

4. Health—European External Action Service [Internet]. [cited 29 Mar 2019]. Available:

5. One World, One Health: OIE—World Organisation for Animal Health [Internet]. [cited 27 Mar 2019]. Available:

6. Kjellstrom T, McMichael AJ. Climate change threats to population health and well-being: the imperative of protective solutions that will last. Glob Health Action. 2013;6. doi: 10.3402/gha.v6i0.20816 23561024

7. Jovanović M, M Bogdanović G, Mijatović Jovanović V, Jeremić P, Ac Nikolić E. Analysis of cutaneous melanoma in the province of Vojvodina. J BUON Off J Balk Union Oncol. 2009;14: 441–6.

8. Petrović T, Šekler M, Petrić D, Lazić S, Debeljak Z, Vidanović D, et al. Methodology and results of integrated WNV surveillance programmes in Serbia. PLOS ONE. 2018;13: e0195439. doi: 10.1371/journal.pone.0195439 29624622

9. Petrić D, Petrović T, Hrnjaković Cvjetković I, Zgomba M, Milošević V, Lazić G, et al. West Nile virus “circulation” in Vojvodina, Serbia: Mosquito, bird, horse and human surveillance. Mol Cell Probes. 2017;31: 28–36. doi: 10.1016/j.mcp.2016.10.011 27777104

10. Zeller H, Lenglet A, Bortel WV. West Nile virus: the need to strengthen preparedness in Europe. Eurosurveillance. 2010;15: 19647. doi: 10.2807/ese.15.34.19647-en 20807490

11. World Health Organization, World Malaria Report 2018. Geneva: The Organization; 2018.

12. Vakali A, Patsoula E, Spanakos G, Danis K, Vassalou E, Tegos N, et al. Malaria in Greece, 1975 to 2010. Euro Surveill Bull Eur Sur Mal Transm Eur Commun Dis Bull. 2012;17.

13. Epidemiological update: West Nile virus transmission season in Europe, 2018 [Internet]. [cited 09Sep 2019]. Available from:

14. Wilson N, Lush D, Baker MG. Meteorological and climate change themes at the 2010 International Conference on Emerging Infectious Diseases. Euro Surveill Bull Eur Sur Mal Transm Eur Commun Dis Bull. 2010;15.

15. Calzolari M, Pautasso A, Montarsi F, Albieri A, Bellini R, Bonilauri P, et al. West Nile virus surveillance in 2013 via mosquito screening in northern Italy and the influence of weather on virus circulation. PLoS One. 2015;10: e0140915. doi: 10.1371/journal.pone.0140915 26488475

16. Apalla Z, Lallas A, Sotiriou E, Lazaridou E, Ioannides D. Epidemiological trends in skin cancer. Dermatol Pract Concept. 2017;7: 1.

17. Kerr JB, Seckmeyer G. Surface ultraviolet radiation: past and future Scientific Assessment of Ozone Depletion 2002. Geneva; 2003. Report No.: 47.

18. Summary for Policy makers. In: Nakićenović N, Swart R, editors. Special Report on Emissions Scenarios. Cambridge: Cambridge University Press—Published for the Intergovernmental Panel on Climate Change. 2000. pp. 1–21.

19. Moss R, Babiker M, Brinkman S, Calvo E, Carter T, Edmonds J et al. Towards new scenarios for analysis of emissions, climate change, impacts, and response strategies. IPCC Expert Meeting Report on New Scenarios. Intergovernmental Panel on Climate Change, Geneva. 2008. pp. 1–132.

20. Kottek M, Grieser J, Beck C, Rudolf B, Rubel F. World Map of the Köppen-Geiger climate classification updated. Meteorologische Zeitschrift. 2006;15(3):259–263.

21. Đurđević V, Rajković B. Development of the EBU-POM coupled regional climate model and results from climate change experiments. In: Mihailovic DT, Lalic B, editors. Advances in environmental modeling and measurements. New York, USA: Nova Science Publishers Inc; 2012. pp. 23–32.

22. Roeckner E, Bäuml G, Bonaventura L. The atmospheric general circulation model ECHAM5. Part I: Model description Report. Max Planck Institute for Meteorology; 2003 p. 127. Report No.: 349.

23. Jungclaus JH, Keenlyside N, Botzet M, Haak H, Luo J-J, Latif M, et al. Ocean Circulation and Tropical Variability in the Coupled Model ECHAM5/MPI-OM. J Clim. 2006;19: 3952–3972. doi: 10.1175/JCLI3827.1

24. Srdić Ž, Zgomba M, Petrić D. Les moustiques (Dip.Culicidae) et la demoustication en Vojvodina, Yugoslavia. IV Congrès sur la protection de la santé humaine et des cultures en milieu tropical. Marseille, France; 1986. pp. 489–495.

25. Petrić D. Seasonal and daily activity of adult mosquitoes (Diptera, Culicidae) in Vojvodina Province. Ph.D. Thesis, University of Novi Sad. 1989.

26. Petrić D, Hrnjaković-Cvjetković I, Radovanov J, Cvjetković D, Jerant-Patić V, Milošević V, et al. West Nile virus surveillance in humans and mosquitoes and detection of cell fusing agent virus in Vojvodina Province (Serbia). HealthMED 2012;6(2):462–68.

27. Becker N, Petrić D, Zgomba M, Boase C, Madon M, Dahl C, et al. Mosquitoes and their control. 2nd ed. Berlin Heidelberg: Springer-Verlag; 2010.

28. Vandenbroucke JP, Pearce N. Incidence rates in dynamic populations. Int J Epidemiol. 2012;41(5):1472–1479. doi: 10.1093/ije/dys142 23045207

29. Malinovic-Milicevic S, Mihailovic DT, Lalic B, Dreskovic N. Thermal environment and UV-B radiation indices in the Vojvodina region, Serbia. Clim Res. 2013;57: 111–121. doi: 10.3354/cr01163

30. Mihailović DT, Mimić G, Arsenić I. Climate Predictions: The Chaos and Complexity in Climate Models. In: Advances in Meteorology [Internet]. 2014 [cited 27 Mar 2019]. doi: 10.1155/2014/878249

31. Richman JS, Moorman JR. Physiological time-series analysis using approximate entropy and sample entropy. Am J Physiol Heart Circ Physiol. 2000;278: H2039–2049. doi: 10.1152/ajpheart.2000.278.6.H2039 10843903

32. Krzic A, Tosic I, Djurdjevic V, Veljovic K, Rajkovic B. Changes in some indices over Serbia according to the SRES A1B and A2 scenarios. Climate Research. 2011;49: 73–86.

33. Cavicchia L, Scoccimarro E, Gualdi S, Marson P, Ahrens B, Berthou S, et al. Mediterranean extreme precipitation: a multi-model assessment. Clim. Dyn. 2016. doi: 10.1007/s00382-016-3245-x

34. Dell’ Aquila A, Mariotti A, Bastin S, Calmanti S, Cavicchia L, Deque M, et al. Evaluation of simulated decadal variations over the Euro-Mediterranean region from ENSEMBLES to Med-CORDEX. Clim. Dyn. 2016. doi: 10.1007/s00382-016-3143-2

35. Mihailović DT, Nikolić-Đorić E, Malinović-Milićević S, Singh VP, Mihailović A, Stošić T et al. The Choice of an Appropriate Information Dissimilarity Measure for Hierarchical Clustering of River Streamflow Time Series, Based on Calculated Lyapunov Exponent and Kolmogorov Measures. Entropy. 2019; 21: 215.

36. Frison TW, Abarbanel HDI. Ocean gravity waves: A nonlinear analysis of observations. Geophys Res. 1997; 102(C1): 1051–1059. doi: 10.1029/96JC02993

37. Mihailovic DT, Mimic G, Arsenic I. Climate predictions: the chaos and complexity in climate models, Advances in Meteorology. 2014; doi: 10.1155/2014/878249

38. R Core Team. R: A Language and Environment for Statistical Computing [Internet]. Vienna: R Foundation for Statistical Computing; 2016. Available:

39. HS Global Inc. Eviews [Internet]. CA, USA: HS Global Inc.; 2016. Available:

40. TIBCO Software Inc. Statistica [Internet]. CA, USA: TIBCO Software Inc.; Available:

41. Hallmann CA, Sorg M, Jongejans E, Siepel H, Hofland N, Schwan H, et al. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PloS One. 2017;12: e0185809. doi: 10.1371/journal.pone.0185809 29045418

42. Moore CG. Interdisciplinary research in the ecology of vector-borne diseases: Opportunities and needs. Journal of Vector Ecology 2008;33(2):218–224. doi: 10.3376/1081-1710-33.2.218 19263839

43. Zimmerman B. Engaging with Complexity: Thrive! A Plan for a Healthier Nova Scotia. 2014; [e-print] Available from:

44. Lupulović D, Martin-Acebes MA, Lazić S, Alonso-Padilla J, Blazquez AB, Escribano-Romero E, et al. First serological evidence of West Nile virus activity in horses in Serbia. Vector Borne Zoonotic Dis. 2011;11(9):1303–5.40. doi: 10.1089/vbz.2010.0249 21438694

45. Petrović T, Blazquez AB, Lupulović D, Lazić G, Escribano-Romero E, Fabijan D, et al. Monitoring West Nile virus (WNV) infection in wild birds in Serbia during 2012: First isolation and characterisation of WNV strains from Serbia. Eurosurveillance. 2013;18(44):1–8.

46. Petrović V, Turkulov V, Ilić S, Milošević V, Petrović M, Petrić D, et al. First report of imported case of dengue fever in Republic of Serbia. Vol. 14, Travel Medicine and Infectious Disease. 2016. p. 60–1. doi: 10.1016/j.tmaid.2016.01.001 26822849

47. van der Linden P and Mitchell JFB, editors. ENSEMBLES Climate Change and its Impacts. Summary of research and results from the ENSEMBLES project. Exeter: Met Office Hadley Centre;. 2009.

48. Ministry of Environmental Protection of the Republic of Serbia. Second National Communication of the Republic of Serbia under the United Nations Framework Convention on Climate Change [Internet]. Belgrade: The Ministry; 2017 Aug. 162p [cited 2019 Sep 10]. Available from:

49. Hawkins E, Sutton R. The Potential to Narrow Uncertainty in Regional Climate Predictions. Bull Amer Meteor. 2009; 90(8): 1095–1108.

50. Adamović Ž. Distribution and abundance of anopheline mosquitoes (Diptera, Culicidae) in Vojvodina, Serbia. Acta Entomol Jugosl. 1979;15: 82.

51. Halgoš J, Benková I. First record of Anopheles hyrcanus (Diptera: Culicidae) from Slovakia. Biológia. 2004;59: 68.

52. Votýpka J, Šeblová V, Rádrová J. Spread of the West Nile virus vector Culex modestus and the potential malaria vector Anopheles hyrcanus in central Europe. J Vector Ecol. 2008;33: 269–277. doi: 10.3376/1081-1710-33.2.269 19263846

53. Lebl K, Brugger K, Rubel F. Predicting Culex pipiens/restuans population dynamics by interval lagged weather data. Parasit Vectors. 2013;6: 129. doi: 10.1186/1756-3305-6-129 23634763

54. Novikov YM, Vaulin OV. Expansion of Anopheles maculipennis s.s. (Diptera: Culicidae) to northeastern Europe and northwestern Asia: Causes and Consequences. Parasit Vectors. 2014;7: 389. doi: 10.1186/1756-3305-7-389 25148893

55. Seidel B, Nowotny N, Duh D, Indra A, Hufnagl P, Allerberger F. First records of the thermophilic mosquito Culiseta longiareolata (Macquart, 1838) in Austria, 2012, and in Slovenia, 2013. J Eur Mosq Control Assoc. 2013;31: 17–20.

56. Zittra C, Waringer J, Werblow A, Melaun C, Fuehrer H-P. Reconfirmation of Culiseta (Allotheobaldia) longiareolata (Macquart 1838) (Diptera: Culicidae) in Austria. The first sequence-confirmed findings in northeastern Austria. Acta ZooBot Austria. 2014;150: 17–24.

57. Tippelt L, Walther D, Kampen H. The thermophilic mosquito species Uranotaenia unguiculata Edwards, 1913 (Diptera: Culicidae) moves north in Germany. Parasitol Res. 2017;116: 3437–3440. doi: 10.1007/s00436-017-5652-2 29103095

58. Riordan DF. Effects of ultraviolet radiation on adults of Aedes aegypti (L.) (Diptera: Culicidae). Mosq News. 1969;29. Available:

59. Hori M, Shibuya K, Sato M, Saito Y. Lethal effects of short-wavelength visible light on insects. Sci Rep. 2014;4: 7383. doi: 10.1038/srep07383 25488603

60. Kramer L, Li J, Shi PY. West Nile virus. Lancet Neurol. 2007;6:171–181. doi: 10.1016/S1474-4422(07)70030-3 17239804

61. Blitvich BJ. Transmission dynamics and changing epidemiology of West Nile virus. Anim Health Res Rev. 2008;9:71–86. doi: 10.1017/S1466252307001430 18348742

62. Komar N. West Nile virus: epidemiology and ecology in North America. Adv Vir Res. 2003;6:185–234.

63. Calistri P, Giovannini A, Hubalek Z, Ionescu A, Monaco F, Savini G et al. Epidemiology of West Nile in Europe and in the Mediterranean basin. Open Virol J. 2010;4(1):29–37.

64. Medić S, Lazić S, Petrović T, Petrić D, Samojlović M, Lazić G et al. Evidence of the first clinical case of equine neuroinvasive West Nile Disease in Serbia, 2018. Acta veterinaria 2019;69(1):123–130.

65. Paz S, Malkinson D, Green MS, Tsioni G, Papa A, Danis K, et al. Permissive Summer Temperatures of the 2010 European West Nile Fever Upsurge. PLOS ONE. 2013;8: e56398. doi: 10.1371/journal.pone.0056398 23431374

66. Marcantonio M, Rizzoli A, Metz M, Rosà R, Marini G, Chadwick E, et al. Identifying the Environmental Conditions Favouring West Nile Virus Outbreaks in Europe. Gourbiere S, editor. PLOS ONE. 2015;10: e0121158. doi: 10.1371/journal.pone.0121158 25803814

67. Tran A, Sudre B, Paz S, Rossi M, Desbrosse A, Chevalier V, et al. Environmental predictors of West Nile fever risk in Europe. Int J Health Geogr. 2014;13: 26. doi: 10.1186/1476-072X-13-26 24986363

68. Paz S. Climate change impacts on West Nile virus transmission in a global context. Philos Trans R Soc B Biol Sci. 2015;370: 20130561–20130561. doi: 10.1098/rstb.2013.0561 25688020

69. Narayanan DL, Saladi RN, Fox JL. Ultraviolet radiation and skin cancer. Int J Dermatol. 2010;49: 978–986. doi: 10.1111/j.1365-4632.2010.04474.x 20883261

70. Lacy K, Alwan W. Skin cancer. Medicine (Baltimore). 2013;41: 402–405. doi: 10.1016/j.mpmed.2013.04.008

71. Leun JC van der. Uv-Carcinogenesis. Photochem Photobiol. 1984;39: 861–868. doi: 10.1111/j.1751-1097.1984.tb08872.x 6379697

72. Malinovic-Milicevic S, Mihailovic DT, Radovanovic MM. Reconstruction of the erythemal UV radiation data in Novi Sad (Serbia) using the NEOPLANTA parametric model. Theor Appl Climatol. 2015;121: 131–138. doi: 10.1007/s00704-014-1223-y

73. Malinović-Milićević S and Radovanović M 2016 UV radiation and heat wives in Vojvodina (Book 87) (Belgrade: Serbian Academy of Sciences and Arts, Institute of Geography „Jovan Cvijić”) p ISBN.

74. de Vries E, Tyczynski J, Parkin MD. Cutaneous malignant melanoma in Europe. Eur Netw Cancer Regist Int Agency Res Cancer. 2003;ENCR Cancer Fact Sheets no.4 1–4.

75. Demers AA, Nugent Z, Mihalcioiu C, Wiseman MC, Kliewer EV. Trends of nonmelanoma skin cancer from 1960 through 2000 in a Canadian population. J Am Acad Dermatol. 2005;53: 320–328. doi: 10.1016/j.jaad.2005.03.043 16021129

76. Wu S, Han J, Laden F, Qureshi AA. Long-term ultraviolet flux, other potential risk factors, and skin cancer risk: a cohort study. Cancer epidemiology, biomarkers and prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2014;23(6):1080–1089.

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