Risk of canine and human exposure to Dirofilaria immitis infected mosquitoes in endemic areas of Italy

Particle and Fibre Toxicology

Mario Pietrobelli⁵  Domenico Otranto⁴  Gabriella Cancrini²  Stefania Cazzin¹  Rudi Cassini³  Giulia Simonato⁵  Antonio Frangipane di Regalbono⁵  Gioia Capelli¹ 

[1] Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro, Padua, Italy;Department of Public Health and Infectious Diseases-Parasitology Section, University of Rome “Sapienza”, Rome, Italy;Department of Comparative Biomedicine and Food Science, University of Padua, Legnaro, Padua, Italy;Department of Veterinary Medicine, University of Bari, Bari, Valenzano, Italy;Department of Animal Medicine, Production and Health, University of Padua, Legnaro, Padua, Italy

关键词: Risk of exposure;    Humans;    Dogs;    Mosquito vectors;    Dirofilaria immitis;   

Others  :  1228044
DOI  :  10.1186/1756-3305-6-60

 received in 2013-02-04, accepted in 2013-03-04,  发布年份 2013

【 摘 要 】

Background

The occurrence of infections by Dirofilaria immitis in canine and human populations depends on several factors linked to both the definitive and intermediate hosts. Little data are available on the risk of human and dog exposure to D. immitis in endemic areas. Data collected on dog- and human-bait traps in endemic areas of north-eastern Italy were used to estimate the likelihood of a receptive host coming into contact with an infected vector.

Methods

From 1997 to 1999, mosquitoes were collected from three sampling sites of north-eastern Italy on D. immitis microfilaraemic dogs and on human baits. The bite/night/host rates were determined based on the number of feeding and probing mosquitoes on dogs and humans, respectively. The survival/mortality rates of different species of mosquitoes following the blood meal, and the rate of natural Dirofilaria infection in unfed specimens were estimated. The risk of exposure of dogs and humans to infected mosquito species was determined by combining the bite/host/night and the mosquito infection rates.

Results

A total of 1,165 mosquitoes were collected on human (n = 815) and dog (n = 350) baits with varying species composition (i.e., Culex pipiens, 87.3% and Ochlerotatus caspius, 11.6%). Overall, dogs were more attractive to Cx pipiens than humans (feeding rate 70.2% vs probing rate 25.9%). The highest bite/night/host rate was 84.0 for dogs and 26.5 for humans. Cx pipiens displayed a mortality rate of 76.3% within 13 days and Oc. caspius of 100% within two days following the infective blood meal. In addition, D. immitis DNA was detected in unfed Cx pipiens (infection rate of 0.26%-2.07%). The infection rate adjusted for mosquito mortality was 0.38%. Based on data collected, the contact between an infected mosquito and a host can occur as often as every four nights for D. immitis infected-mosquitoes in dogs and within two weeks for humans.

Conclusions

Cx pipiens was confirmed as the most efficient natural vector of D. immitis in the studied area. In endemic areas, the risk of transmission can be very high for dogs and relevant for humans. Despite the increased awareness of veterinarians and owners on canine dirofilarioses, dogs from rural areas still maintain the natural life cycle of Dirofilaria spp., therefore acting as a source of infection to humans through vector bites.

【 授权许可】

   
2013 Capelli et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Kutz FW, Frederick W, Dobson RC: Effects of temperature on the development of Dirofilaria immitis (Leidy) in Anopheles quadrimaculatus say and on vector mortality resulting from this development. Ann Entomol Soc Am 1974, 67:325-331.
• [2]Cancrini G, Pietrobelli M, Frangipane di Regalbono A, Tampieri MP, della Torre A: Development of Dirofilaria and Setaria nematodes in Aedes albopictus. Parassitologia 1995, 37:141-145.
• [3]Cancrini G, Gabrielli S: Vectors of Dirofilaria nematods: biology behaviour and host/parasites relationships. In Proceeding of the First European Dirofilaria days: 22–25 February 2007; Zagreb, 2007. Edited by Genchi C, Rinaldi L, Cringoli G. Napoli: Rolando Editore; 2007:49-58.
• [4]Morchón R, Carretón E, González-Miguel J, Mellado-Hernández I: Heartworm disease (Dirofilaria immitis) and their vectors in Europe - New distribution trends. Front Physiol 2012, 3:196.
• [5]Genchi C, Kramer LH, Rivasi F: Dirofilarial infections in Europe. Vector Borne Zoonotic Dis 2011, 11:1307-1317.
• [6]Otranto D, Dantas-Torres F, Brianti E, Traversa D, Petrić D, Genchi C, Capelli G: Vector-borne helminths of dogs and humans in Europe. Parasit Vectors 2013, 6:16. BioMed Central Full Text
• [7]Rossi L, Pollono F, Meneguz PG, Cancrini G: Four species of mosquito as possible vectors for Dirofilaria immitis piedmont rice-fields. Parassitologia 1999, 41:537-542.
• [8]Muñnoz J, Eritja R, Alcaide M, Montalvo T, Soriguer RC, Figuerola J: Host-feeding patterns of native Culex pipiens and invasive Aedes albopictus mosquitoes (Diptera: Culicidae) in urban zones from Barcelona, Spain. J Med Entomol 2011, 48:956-960.
• [9]Cancrini G, Frangipane di Regalbono A, Ricci I, Tessarin C, Gabrielli S, Pietrobelli M: Aedes albopictus is a natural vector of Dirofilaria immitis in Italy. Vet Parasitol 2003, 118:195-202.
• [10]Otranto D, Capelli G, Genchi C: Changing distribution patterns of canine vector borne diseases in Italy: leishmaniosis vs. dirofilariosis. Parasit Vectors 2009, 2(Suppl 1):S2. BioMed Central Full Text
• [11]Latrofa MS, Montarsi F, Ciocchetta S, Annoscia G, Dantas-Torres F, Ravagnan S, Capelli G, Otranto D: Molecular xenomonitoring of Dirofilaria immitis and Dirofilaria repens in mosquitoes from north-eastern Italy by real-time PCR coupled with melting curve analysis. Parasit Vectors 2012, 5:76. BioMed Central Full Text
• [12]Service MW: Mosquito ecology: field sampling methods. 2nd edition. London and New York: Elsevier Applied Science; 1993.
• [13]Cancrini G, Magi M, Gabrielli S, Arispici M, Tolari F, Dell’Omodarme M, Prati MC: Natural vectors of dirofilariasis in rural and urban areas of the Tuscan region, central Italy. J Med Entomol 2006, 43:574-579.
• [14]Mattingly PF: The biology of mosquito-borne disease. In The Science of Biology (Series No I). Edited by Carthy JD, Sutcliffe JF. London, United Kingdom: George Allen and Unwin Ltd; 1969.
• [15]Coluzzi M, Petrarca V: Aspirator with paper cup for collecting mosquitoes and other insects. Mosq News 1973, 33:249-250.
• [16]Snow KR: Towards a checklist of British mosquitoes. Entomol Mon Mag 1987, 123:83-89.
• [17]Gerberg EJ, Ward RA, Barnard DR: Manual for Mosquito Rearing and Experimental Techniques. Bulletin No. 5 (revised). Lake Charles, Louisiana: Published by American Mosquito Control Association (AMCA), Inc; 1994:1-98.
• [18]Favia G, Dimopoulos G, Della Torre A, Touré YT, Coluzzi M, Louis C: Polymorphism detected by random PCR distinguish between chromosomal forms of Anopheles gambiae. Proc Natl Acad Sci 1994, 91(22):10315-10319.
• [19]Favia G, Lanfrancotti A, della Torre A, Cancrini G, Coluzzi M: Polymerase chain reaction-identification of Dirofilaria repens and Dirofilaria immitis. Parasitology 1996, 6:567-571.
• [20]Preacher KJ: Calculation for the chi-square test: An interactive calculation tool for chi-square tests of goodness of fit and independence. http://quantpsy.org webcite
• [21]Cowling DW, Gardner IA, Johnson WO: Comparison of methods for estimation of individual-level prevalence based on pooled samples. Prev Vet Med 1999, 39:211-225.
• [22]EpiTools epidemiological calculators. Available at: http://epitools.ausvet.com.au/content.php?page=home webcite
• [23]Capelli G, Poglayen G, Bertotti F, Giupponi S, Martini M: The host-parasite relationship in canine heartworm infection in a hyperendemic area of Italy. Vet Res Commun 1996, 20:320-330.
• [24]Lai CH, Tung KC, Ooi HK, Wang JS: Competence of Aedes albopictus and Culex quinquefasciatus as vector of Dirofilaria immitis after blood meal with different microfilarial density. Vet Parasitol 2000, 90:231-237.
• [25]Mulatti P, Bonfanti L, Capelli G, Capello K, Lorenzetto M, Terregino C, Monaco F, Ferri G, Marangon S: West Nile Virus in North-Eastern Italy, 2011: Entomological and Equine IgM-Based Surveillance to Detect Active Virus Circulation. Zoonoses Public Health 2011. Sep 13
• [26]European Center for Disease Control (ECDC), VIBORNET maps. available at: http://ecdc.europa.eu/en/activities/diseaseprogrammes/emerging_and_vector_borne_diseases/Pages/VBORNET_maps.aspx webcite
• [27]Cancrini G, Romi R, Gabrielli S, Toma L, DI Paolo M, Scaramozzino P: First finding of Dirofilaria repens in a natural population of Aedes albopictus. Med Vet Entomol 2003, 17:448-451.
• [28]Rebollar-Téllez EA: Human body odor, mosquito bites and the risk of disease transmission. Folia Entomol Mex 2005, 2:247-265.
• [29]Lacroix R, Mukabana WR, Gouagna LC, Koella JC: Malaria infection increases attractiveness of humans to mosquitoes. PLoS Biol 2005, 3:e298.
• [30]Cornet S, Nicot A, Rivero A, Gandon S: Malaria infection increases bird attractiveness to uninfected mosquitoes. Ecol Lett 2012. Dec 3