Potential Risk of Dengue and Chikungunya Outbreaks in Northern Italy Based on a Population Model of Aedes albopictus (Diptera: Culicidae)

PLoS Neglected Tropical Diseases

Volumn 10, Issue 6, 2016, Pages

  Guzzetta, Giorgio ^a   Montarsi, Fabrizio ^b   Baldacchino, Frédéric Alexandre ^c   Metz, Markus ^c   Capelli, Gioia ^b   Rizzoli, Annapaola ^c   Pugliese, Andrea ^d   Rosà, Roberto ^c   Poletti, Piero ^a,e   Merler, Stefano ^a  

^a FONDAZIONE BRUNO KESSLER   (Italy)

^b ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLE VENEZIE   (Italy)

^c RESEARCH AND INNOVATION CENTRE   (Italy)

^d UNIVERSITY OF TRENTO   (Italy)

^e BOCCONI UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AEDES ALBOPICTUS; ARBOVIRUS; ARTICLE; CHIKUNGUNYA; DENGUE; DISEASE SURVEILLANCE; DISEASE TRANSMISSION; ENVIRONMENTAL TEMPERATURE; GUILLAIN BARRE SYNDROME; HUMAN; INFECTION CONTROL; INFECTION RISK; ITALY; MATHEMATICAL MODEL; NONHUMAN; POLYMERASE CHAIN REACTION; PUBLIC HEALTH; VIRUS TRANSMISSION; AEDES; ANIMAL; ANIMAL DISPERSAL; BIOLOGICAL MODEL; CHIKUNGUNYA FEVER; EPIDEMIC; MOSQUITO VECTOR; PHYSIOLOGY; POPULATION DYNAMICS; RISK FACTOR; SEASON; STATISTICS AND NUMERICAL DATA; TIME FACTOR; VIROLOGY;

AEDES; ANIMAL DISTRIBUTION; ANIMALS; CHIKUNGUNYA FEVER; DENGUE; DISEASE OUTBREAKS; HUMANS; ITALY; MODELS, BIOLOGICAL; MOSQUITO VECTORS; POPULATION DYNAMICS; RISK FACTORS; SEASONS; TIME FACTORS;

EID: 84978064602     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0004762     Document Type: Article

References (61)

1. Knudsen AB, Romi R, Majori G, Occurrence and spread in Italy of Aedes albopictus, with implications for its introduction into other parts of Europe. J Am Mosq Control Assoc. 1996; 12(2 Pt 1):177–83. 8827590
2. Kraemer MU, Sinka ME, Duda KA, Mylne A, Shearer FM, Brady OJ, Messina JP, Barker CM, Moore CG, Carvalho RG, Coelho GE, Van Bortel W, Hendrickx G, Schaffner F, Wint GR, Elyazar IR, Teng HJ, Hay SI, The global compendium of Aedes aegypti and Ae. albopictus occurrence. Sci Data. 2015; 2:150035. doi: 10.1038/sdata.2015.3526175912
3. Vega-Rúa A, Zouache K, Caro V, Diancourt L, Delaunay P, Grandadam M, Failloux AB, High efficiency of temperate Aedes albopictus to transmit chikungunya and dengue viruses in the Southeast of France. PLoS One. 2013; 8(3):e59716. doi: 10.1371/journal.pone.005971623527259
4. Vega-Rúa A, Zouache K, Girod R, Failloux AB, Lourenço-de-Oliveira R, High level of vector competence of Aedes aegypti and Aedes albopictus from ten American countries as a crucial factor in the spread of chikungunya virus. J Virol. 2014; 88(11):6294–306. doi: 10.1128/JVI.00370-1424672026
5. Wong PS, Li MZ, Chong CS, Ng LC, Tan CH, Aedes (Stegomyia) albopictus (Skuse): a potential vector of Zika virus in Singapore. PLoS Negl Trop Dis. 2013; 7(8):e2348. doi: 10.1371/journal.pntd.000234823936579
6. Schaffner F, Medlock JM, Van Bortel W, Public health significance of invasive mosquitoes in Europe. Clin Microbiol Infect. 2013; 19(8):685–92. doi: 10.1111/1469-0691.1218923574618
7. Rezza G, Nicoletti L, Angelini R, Romi R, Finarelli AC, Panning M, Cordioli P, Fortuna C, Boros S, Magurano F, Silvi G, Angelini P, Dottori M, Ciufolini MG, Majori GC, Cassone A, CHIKV study groupInfection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet. 2007; 370(9602):1840–6. 18061059
8. Delisle E, Rousseau C, Broche B, Leparc-Goffart I, L'Ambert G, Cochet A, Prat C, Foulongne V, Ferre JB, Catelinois O, Flusin O, Tchernonog E, Moussion IE, Wiegandt A, Septfons A, Mendy A, Moyano MB, Laporte L, Maurel J, Jourdain F, Reynes J, Paty MC, Golliot F, chikungunya outbreak in Montpellier, France, September to October 2014. Euro Surveill. 2015; 20(17). pii: 21108. 25955774
9. Tomasello D, Schlagenhauf P, chikungunya and dengue autochthonous cases in Europe, 2007–2012. Travel Med Infect Dis. 2013; 11(5):274–84. doi: 10.1016/j.tmaid.2013.07.00623962447
10. Gjenero-Margan I, Aleraj B, Krajcar D, Lesnikar V, Klobučar A, Pem-Novosel I, Kurečić-Filipović S, Komparak S, Martić R, Duričić S, Betica-Radić L, Okmadžić J, Vilibić-Čavlek T, Babić-Erceg A, Turković B, Avsić-Županc T, Radić I, Ljubić M, Sarac K, Benić N, Mlinarić-Galinović G, Autochthonous dengue fever in Croatia, August-September 2010. Euro Surveill. 2011; 16(9). pii: 19805. 21392489
11. Wilder-Smith A, Quam M, Sessions O, Rocklov J, Liu-Helmersson J, Franco L, Khan K, The 2012 dengue outbreak in Madeira: exploring the origins. Euro Surveill. 2014; 19(8):20718. 24602277
12. Gould EA, Gallian P, De Lamballerie X, Charrel RN, First cases of autochthonous dengue fever and chikungunya fever in France: from bad dream to reality!Clin Microbiol Infect. 2010; 16(12):1702–4. doi: 10.1111/j.1469-0691.2010.03386.x21040155
13. Marchand E, Prat C, Jeannin C, Lafont E, Bergmann T, Flusin O, Rizzi J, Roux N, Busso V, Deniau J, Noel H, Vaillant V, Leparc-Goffart I, Six C, Paty MC, Autochthonous case of dengue in France, October 2013. Euro Surveill. 2013; 18(50):20661. 24342514
14. Ministero della Salute. Sorveglianza dei casi umani di chikungunya, Dengue, West Nile Disease ed altre arbovirosi e valutazione del rischio di trasmissione in Italia– 2015.
15. Delatte H, Gimonneau G, Triboire A, Fontenille D, Influence of temperature on immature development, survival, longevity, fecundity, and gonotrophic cycles of Aedes albopictus, vector of chikungunya and dengue in the Indian Ocean. J Med Entomol. 2009; 46(1):33–41. 19198515
16. Morin CW, Comrie AC, Ernst K, Climate and dengue transmission: evidence and implications. Environ Health Perspect. 2013;121(11–12):1264–72. doi: 10.1289/ehp.130655624058050
17. Alto BW, Juliano SA, Precipitation and Temperature Effects on Populations of Aedes albopictus (Diptera: Culicidae): Implications for Range Expansion. J Med Entomol. 2001;38(5):646–56. 11580037
18. Reiskind MH, Zarrabi AA, Water Surface Area and Depth Determine Oviposition Choice in Aedes albopictus (Diptera: Culicidae). J Med Entomol. 2012;49(1):71–6. 22308773
19. Trexler JD, Apperson CS, Schal C, Laboratory and Field Evaluations of Oviposition Responses of Aedes albopictus and Aedes triseriatus (Diptera: Culicidae) to Oak Leaf Infusions. J Med Entomol. 1998;35(6):967–76. 9835688
20. Delatte H, Dehecq JS, Thiria J, Domerg C, Paupy C, Fontenille D, Delatte 2008 Geographic Distribution and Developmental Sites of Aedes albopictus (Diptera: Culicidae) During a Chikungunya Epidemic Event. Vector Borne Zoonotic Dis. 2008;8(1):25–34.
21. Neteler M, David R, Rocchini D, Castellani C, Rizzoli A, Terra and Acqua satellites track tiger mosquito invasion: modelling the potential distribution of Aedes albopictus in northeastern Italy. International Journal of Health Geographics2011; 10, 49. doi: 10.1186/1476-072X-10-4921812983
22. Capelli G, Drago A, Martini S, Montarsi F, Soppelsa M, Delai N, Ravagnan S, Mazzon L, Schaffner F, Mathis A, Di Luca M, Romi R, Russo F, First report in Italy of the exotic mosquito species Aedes (Finlaya) koreicus, a potential vector of arboviruses and filariae. Parasite & Vectors2011, 4, 188.
23. Capelli G, Drago A, Martini S, Montarsi F, Soppelsa M, Delai N, Ravagnan S, Mazzon L, Schaffner F, Mathis A, Di Luca M, Romi R, Russo F, First report in Italy of the exotic mosquito species Aedes (Finlaya) koreicus, a potential vector of arboviruses and filariae. Parasit Vectors. 2011; 4:188. doi: 10.1186/1756-3305-4-18821951867
24. Montarsi F, Drago A, Martini S, Calzolari M, De Filippo F, Bianchi A, Mazzucato M, Ciocchetta S, Arnoldi D, Baldacchino F, Rizzoli A, Capelli G, Current distribution of the invasive mosquito species, Aedes koreicus [Hulecoeteomyia koreica] in northern Italy” Parasites and Vectors. 2015; 8:614. doi: 10.1186/s13071-015-1208-426626019
25. Becker N, Petric D, Zgomba M, Boase C, Madon M, Dahl C, Kaiser A, . (2010) Mosquitoes and Their Control. 2nd edition. Heidelberg, Springer.
26. Montarsi F, Martini S, Dal Pont M, Delai N, Milone NF, Mazzucato M, Soppelsa F, Cazzola L, Cazzin S, Ravagnan S, Ciocchetta S, Russo F, Capelli G, Distribution and habitat characterization of the recently introduced invasive mosquito Aedes koreicus (Hulecoeteomyia koreica), a new potential vector and pest in north-eastern Italy. Parasites & Vectors. 2013; 6, 292.
27. Metz M, Rocchini D, Neteler M, Surface temperatures at continental scale: tracking changes with remote sensing at unprecedented detail. Remote Sensing2014, 6, 3822–3840.
28. Poletti P, Messeri G, Ajelli M, Vallorani R, Rizzo C, Merler S, Transmission potential of chikungunya virus and control measures: the case of Italy. PLoS One. 2011May3;6(5):e18860. doi: 10.1371/journal.pone.001886021559329
29. Erickson RA, Presley SM, Allen LJ, Long KR, Cox SB, A stage-structured, Aedes albopictus population model. Ecological Modelling. 2010May10;221(9):1273–82.
30. Tran A, L'Ambert G, Lacour G, Benoît R, Demarchi M, Cros M, Cailly P, Aubry-Kientz M, Balenghien T, Ezanno P, A rainfall-and temperature-driven abundance model for Aedes albopictus populations. International journal of environmental research and public health. 2013Apr26;10(5):1698–719. doi: 10.3390/ijerph1005169823624579
31. Otero M, Solari HG, Schweigmann N, A stochastic population dynamics model for Aedes aegypti: formulation and application to a city with temperate climate. Bulletin of mathematical biology. 2006Nov1;68(8):1945–74. 16832731
32. Marini F, Caputo B, Pombi M, Tarsitani G, della Torre A, Study of Aedes albopictus dispersal in Rome, Italy, using sticky traps in mark-release-recapture experiments. Med Vet Entomol2010; 24(4):361–8. doi: 10.1111/j.1365-2915.2010.00898.x20666995
33. Smith DL, Battle KE, Hay SI, Barker CM, Scott TW, McKenzie FE, Ross, Macdonald, and a Theory for the Dynamics and Control of Mosquito-Transmitted Pathogens. PLoS Pathog. 2012;8(4):e1002588. doi: 10.1371/journal.ppat.100258822496640
34. Reiner RC, Perkins TA, Barker CM, Niu T, Chaves LF, Ellis AM, et al. A systematic review of mathematical models of mosquito-borne pathogen transmission: 1970–2010. J. R. Soc. Interface2013; 10.
35. Lloyd AL, Zhang J, Root AM, Stochasticity and heterogeneity in host–vector models. J R Soc Interface2007; 4: 851–86317580290
36. Lourenço J, Recker M, The 2012 Madeira dengue outbreak: epidemiological determinants and future epidemic potential. PLoS Negl Trop Dis. 2014; 8(8):e3083. doi: 10.1371/journal.pntd.000308325144749
37. Focks D, Daniels E, Haile DG, Keesling JE, (1995) A simulation model of the epidemiology of urban dengue fever: literature analysis, model development, preliminary validation, and samples of simulation results. The American journal of tropical medicine and hygiene53: 489–506. 7485707
38. Talbalaghi A, Moutailler S, Vazeille M, Failloux AB, Are Aedes albopictus or other mosquito species from northern Italy competent to sustain new arboviral outbreaks?Med Vet Entomol. 2010; 24(1):83–7. doi: 10.1111/j.1365-2915.2009.00853.x20377735
39. Dieng H, Rahman GM, Abu Hassan A, Che Salmah MR, Satho T, Miake F, Boots M, Sazaly A, The effects of simulated rainfall on immature population dynamics of Aedes albopictus and female oviposition. Int J Biometeorol2012; 56(1):113–20. doi: 10.1007/s00484-011-0402-021267602
40. Roiz D, Rosa R, Arnoldi D, Rizzoli A, Effects of temperature and rainfall on the activity and dynamics of host-seeking Aedes albopictus females in northern Italy. Vector Borne Zoonotic Dis. 2010; 10: 811–816. doi: 10.1089/vbz.2009.009820059318
41. Toma L, Severini F, Di Luca M, Bella A, Romi R, Seasonal patterns of oviposition and egg hatching rate of Aedes albopictus in Rome. J Am Mosq Control Assoc. 2003; 19: 19–22. 12674530
42. Napoli C, Salcuni P, Pompa MG, Declich S, Rizzo C, Estimated imported infections of chikungunya and Dengue in Italy, 2008 to 2011. J Travel Med2012; 19(5):294–7. doi: 10.1111/j.1708-8305.2012.00640.x22943269
43. Romi R, Severini F, Toma L, Cold acclimation and overwintering of female Aedes albopictus in Roma. Journal of the American Mosquito Control Association. 2006Mar;22(1):149–51. 16646341
44. Hanson SM, Craig GB, Jr1994. Cold acclimation, diapause, and geographic origin affect cold hardiness in eggs of Aedes albopictus (Diptera:Culicidae). J Med Entomol31:192–201. 8189409
45. Tsunoda T, Cuong TC, Dong TD, Yen NT, Le NH, Phong TV, Minakawa N, Winter refuge for Aedes aegypti and Ae. albopictus mosquitoes in Hanoi during Winter. PloS one. 2014Apr21;9(4):e95606. doi: 10.1371/journal.pone.009560624752230
46. Otero M, Schweigmann N, Solari HG, A stochastic spatial dynamical model for Aedes aegypti. Bulletin of mathematical biology. 2008Jul1;70(5):1297–325. doi: 10.1007/s11538-008-9300-y18293043
47. Yee DA, Juliano SA, Vamosi SM, Seasonal photoperiods alter developmental time and mass of an invasive mosquito, Aedes albopictus (Diptera: Culicidae), across its north-south range in the United States. J Med Entomol. 2012; 49(4):825–32. 22897042
48. Lacour G, Vernichon F, Cadilhac N, Boyer S, Lagneau C, Hance T, When mothers anticipate: effects of the prediapause stage on embryo development time and of maternal photoperiod on eggs of a temperate and a tropical strain of Aedes albopictus (Diptera: Culicidae). J Insect Physiol. 2014; 71:87–96. doi: 10.1016/j.jinsphys.2014.10.00825450563
49. Brady OJ, Johansson MA, Guerra CA, Bhatt S, Golding N, Pigott DM, Delatte H, Grech MG, Leisnham PT, Maciel-de-Freitas R, Styer LM, Smith DL, Scott TW, Gething PW, Hay SI, Modelling adult Aedes aegypti and Aedes albopictus survival at different temperatures in laboratory and field settings. Parasit Vectors. 2013; 6:351. doi: 10.1186/1756-3305-6-35124330720
50. Aznar VR, Otero M, De Majo MS, Fischer S, Solari HG, Modeling the complex hatching and development of Aedes aegypti in temperate climates. Ecological modelling. 2013Mar24;253:44–55.
51. Lambrechts L, Scott TW, Gubler DJ, Consequences of the Expanding Global Distribution of Aedes albopictus for Dengue Virus Transmission. PLoS Negl Trop Dis. 2010;4(5):e646. doi: 10.1371/journal.pntd.000064620520794
52. Medlock JM, Hansford KM, Schaffner F, Versteirt V, Hendrickx G, Zeller H, Van Bortel W, A review of the invasive mosquitoes in Europe: ecology, public health risks, and control options. Vector Borne Zoonotic Dis. 201212(6):435–47. doi: 10.1089/vbz.2011.081422448724
53. Schaffner F, Mathis A, Dengue and dengue vectors in the WHO European region: past, present, and scenarios for the future. Lancet Infect Dis. 2014;14(12):1271–80. doi: 10.1016/S1473-3099(14)70834-525172160
54. Kraemer MU, Sinka ME, Duda KA, Mylne AQ, Shearer FM, Barker CM, Moore CG, Carvalho RG, Coelho GE, Van Bortel W, Hendrickx G, Schaffner F, Elyazar IR, Teng HJ, Brady OJ, Messina JP, Pigott DM, Scott TW, Smith DL, Wint GR, Golding N, Hay SI, The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus. Elife. 2015;4:e08347. doi: 10.7554/eLife.0834726126267
55. Fortuna C, Remoli ME, Severini F, DI Luca M, Toma L, Fois F, Bucci P, Boccolini D, Romi R, Ciufolini MG, Evaluation of vector competence for West Nile virus in Italian Stegomyia albopicta (= Aedes albopictus) mosquitoes. Med Vet Entomol, 2015. doi: 10.1111/mve.12133 [Epub ahead of print]
56. Angelini P, Tamba M, Finarelli AC, Bellini R, Albieri A, Bonilauri P, Cavrini F, Dottori M, Gaibani P, Martini E, Mattivi A, Pierro AM, Rugna G, Sambri V, Squintani G, Macini P, West Nile virus circulation in Emilia-Romagna, Italy: the integrated surveillance system 2009. Euro Surveill. 2010; 15(16).
57. Tappe D, Rissland J, Gabriel M, Emmerich P, Gunther S, Held G, Smola S, Schmidt-Chanasit J, First case of laboratory-confirmed Zika virus infection imported into Europe, November 2013. Euro Surveill. 2014; 19(4). pii: 20685. 24507467
58. Oehler E, Watrin L, Larre P, Leparc-Goffart I, Lastere S, Valour F, Baudouin L, Mallet H, Musso D, Ghawche F, Zika virus infection complicated by Guillain-Barre syndrome—case report, French Polynesia, December 2013. Euro Surveill. 2014; 19(9). pii: 20720. 24626205
59. Fauci AS, Morens DM, Zika Virus in the Americas—Yet Another Arbovirus Threat. N Engl J Med. 2016; doi: 10.1056/NEJMp1600297
60. Duffy MR, Chen TH, Hancock WT, Powers AM, Kool JL, Lanciotti RS, Pretrick M, Marfel M, Holzbauer S, Dubray C, Guillaumot L, Griggs A, Bel M, Lambert AJ, Laven J, Kosoy O, Panella A, Biggerstaff BJ, Fischer M, Hayes EB, Zika virus outbreak on Yap Island, Federated States of Micronesia. N Engl J Med. 2009; 360(24):2536–43. doi: 10.1056/NEJMoa080571519516034
61. Ioos S, Mallet HP, Leparc Goffart I, Gauthier V, Cardoso T, Herida M, Current Zika virus epidemiology and recent epidemics. Med Mal Infect. 2014; 44(7):302–7. doi: 10.1016/j.medmal.2014.04.00825001879