Heartworm disease in dogs is caused by Dirofilaria immitis, which is transmitted by mosquitoes.1,2 Cases of heartworm infection have been reported from every state in the United States since at least 2011, with high densities in the Mississippi Delta region and southeastern United States and > 136,000 new cases reported from across the United States in 2017.3 Although canids, particularly dogs and coyotes, are the primary, definitive hosts, D immitis can infect other animals, such as domestic cats, which can develop serious complications from heartworm-associated respiratory disease in response to as few as 1 to 3 adult D immitis worms.
Despite the wide availability of heartworm preventives, heartworm infection remains a major veterinary concern. In addition, evidence that some D immitis strains have become resistant to macrocyclic lactones has necessitated discontinuation of the so-called slow-kill method for treating micro-filaremia in dogs, which involved monthly administration of heartworm preventive.4–6
Other filarial diseases (eg, onchocerciasis and lymphatic filariasis) have been controlled well through integrated programs that use a combination of mitigation strategies (eg, mass treatment of at-risk human populations, vector management, and reduction of vector-host contact) to break the cycle of disease transmission.7,8 However, D immitis is transmitted by a broad range of mosquito species (≥ 17 species in Florida alone and ≥ 25 species in the United States as a whole) and can cycle between several species of definitive hosts. This broad diversity of potential vectors suggests that all mammal-biting mosquitoes could be candidate vectors.9–11 Because of differences in vector feeding patterns, breeding habitats, and geographic ranges,9 the key vectors of D immitis can vary from region to region along with local host and ecological conditions.
Various biological and sociobehavioral components of the risk that dogs will acquire heartworm infection have been proposed, including economic status of owners,6 proximity to vector habitat,12,13 emerging vector mosquito species combined with drug resistance among D immitis strains,9,14 and climatic factors.15,16 However, to the authors' knowledge, no comprehensive study of these relationships has been conducted in communities where heartworm infection is endemic. The purpose of the study reported here was to assess knowledge, attitudes, and practices regarding D immitis and mosquito vectors among residents (dog owners and non-dog owners) in 2 Florida communities—1 with a high prevalence of dogs with heartworm infection and 1 with a low prevalence—and to perform entomological surveys of mosquito species in these neighborhoods and identify mosquito species infected with D immitis.
This research was supported by NIH Training Grant T32RR018269 and by the USDA National Institute of Food and Agriculture, multistate project NYC-139835/NE-1443.
The authors declare that there were no conflicts of interest.
Presented in part as an oral presentation at the 6th International Congress of the Society for Vector Ecology, La Quinta, Calif, September 2013; as a poster at the 62nd Annual Meeting of the American Society of Tropical Medicine and Hygiene, Washington, DC, November 2013; and as a poster at the Cornell College of Veterinary Medicine 2nd Annual DVM Research Poster Session, Ithaca, NY, April 2014.
Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the view of the National Institute of Food and Agriculture or the USDA.
The authors thank Pam Davis from Columbia County Mosquito Control Program for her assistance and Sylvie Pitcher, who assisted with all aspects of mosquito collections and analysis.
Cornell large vegetation aspirator, Harrington Laboratory, Ithaca, NY.
BG-Sentinel trap, Biogents AG, Regensburg, Germany.
CDC Miniature Light Trap (light removed), model 512, John W. Hock Co, Gainesville, Fla.
Paint strainer bag, Master Craft Manufacturing Co, South El Monte, Calif.
Gentra PureGene Blood Kit, Gentra Systems, Minneapolis, Minn.
Multi Doc-It Digital Imaging System, UVP Inc, Upland, Calif.
ExoSAP-IT PCR Product Cleanup, USB Products, Affymetrix Inc, Cleveland, Ohio.
BLAST, National Center for Biotechnology Information, National Institutes of Health, Bethesda, Md. Available at: blast.ncbi.nlm.nih.gov/. Accessed May 16, 2016.
IBM SPSS Statistics for Windows, version 20.0, IBM Corp, Armonk, NY.
PooledInfRate software, version 4.0, Division of Vector-Borne Diseases, CDC, Fort Collins, Colo.
Coon BR. Field and laboratory studies of Culex erraticus (Diptera: Culicidae) ability to detect hosts, habitat identification and attempts at colonization. PhD dissertation, Entomology and Nematology Department, University of Florida, Gainesville, Fla, 2006.
2. Bowman DD, Atkins CE. Heartworm biology, treatment, and control. Vet Clin North Am Small Anim Pract 2009;39:1127–1158.
3. Companion Animal Parasite Council. Heartworm. Available at: www.capcvet.org/maps/#2017/all/heartworm-canine/dog/united-states/. Accessed Sep 30, 2018.
4. Geary TG, Bourguinat C, Prichard RK. Evidence for macrocyclic lactone anthelmintic resistance in Dirofilaria immitis. Top Companion Anim Med 2011;26:186–192.
5. Bourguinat C, Keller K, Bhan A, et al. Macrocyclic lactone resistance in Dirofilaria immitis. Vet Parasitol 2011;181:388–392.
6. Brown HE, Harrington LC, Kaufman PE, et al. Key factors influencing canine heartworm, Dirofilaria immitis, in the United States. Parasit Vectors 2012;5:245.
7. World Health Organization. Progress report 2000–2009 and strategic plan 2010–2020 of the global programme to eliminate lymphatic filariasis: halfway towards eliminating lymphatic filariasis. Geneva: World Health Organization, 2010.
8. Cupp EW, Sauerbrey M, Richards F. Elimination of human onchocerciasis: history of progress and current feasibility using ivermectin (Mectizan) monotherapy. Acta Trop 2011;120(suppl 1):S100–S108.
9. Ledesma N, Harrington L. Mosquito vectors of dog heartworm in the United States: vector status and factors influencing transmission efficiency. Top Companion Anim Med 2011;26:178–185.
10. Darsie RJ, Ward R. Identification and geographical distribution of the mosquitoes of North America, north of Mexico. Gainesville, Fla: University of Florida Press, 2005.
11. Kulasekera VL, Kramer L, Nasci RS, et al. West Nile virus infection in mosquitoes, birds, horses, and humans, Staten Island, New York, 2000. Emerg Infect Dis 2001;7:722–725.
12. Sacks BN, Chomel BB, Kasten RW. Modeling the distribution and abundance of the non-native parasite, canine heartworm, in California coyotes. Oikos 2004;105:415–425.
13. Sacks BN, Woodward DL, Colwell AE. A long-term study of non-native-heartworm transmission among coyotes in a Mediterranean ecosystem. Oikos 2003;102:478–490.
14. Tiawsirisup S. The potential for Aedes albopictus (skuse) (Diptera: Culicidae) to be a competent vector for canine heartworm, Dirofilaria immitis (leidy). Southeast Asian J Trop Med Public Health 2007;38(suppl 1):208–214.
15. Fortin JF, Slocombe JOD. Temperature requirements for the development of Dirofilaria immitis in Aedes triseriatus and Ae vexans. Mosq News 1981;41:623–633.
16. Knight DH, Lok JB. Seasonality of heartworm infection and implications for chemoprophylaxis. Clin Tech Small Anim Pract 1998;13:77–82.
17. Tuiten W, Koenraadt CJM, McComas K, et al. The effect of West Nile virus perceptions and knowledge on protective behavior and mosquito breeding in residential yards in upstate New York. EcoHealth 2009;6:42–51.
18. Edman JD, Evans FDS, Williams JA. Development of a diurnal resting box to collect Culiseta melanura (COQ). Am J Trop Med Hyg 1968;17:451–456.
19. Darsie RF, Morris CD. Keys to the adult females and fourth instar larvae of the mosquitoes of Florida (Diptera, Culicidae). Gainesville, Fla: Florida Mosquito Control Association, 2003;1:159.
20. Rishniw M, Barr SC, Simpson KW, et al. Discrimination between six species of canine microfilariae by a single polymerase chain reaction. Vet Parasitol 2006;135:303–314.
21. Biggerstaff BJ. PooledlnfRate, version 4.0: a Microsoft Office Excel Add-In to compute prevalence estimates from pooled samples. Fort Collins: Division of Vector-Borne Diseases, CDC, 2009.
22. Townzen JS, Brower AVZ, Judd DD. Identification of mosquito bloodmeals using mitochondrial cytochrome oxidase sub-unit I and cytochrome b gene sequences. Med Vet Entomol 2008;22:386–393.
23. CDC. Non-human disease cases. Reported to CDC ArboNET by county of residence. Available at: wwwn.cdc.gov/arbonet/maps/ADB_Diseases_Map/index.html. Accessed Sep 30, 2018.
24. Kartman L. Factors influencing infection of the mosquito with Dirofilaria immitis (leidy, 1856). Exp Parasitol 1953;2:27–78.
25. Scoles GA. Vectors of canine heartworm in the United States: a review of the literature including new data from Indiana, Florida, and Louisiana, in Proceedings. Heartworm Symp Am Heartworm Soc 1998;21–36.
26. Watts KJ, Reddy GR, Holmes RA, et al. Seasonal prevalence of third-stage larvae of Dirofilaria immitis in mosquitoes from Florida and Louisiana. J Parasitol 2001;87:322–329.
27. Sauerman DM Jr, Nayar JK. A survey for natural potential vectors of Dirofilaria immitis in Vero Beach, Florida. Mosq News 1983;43:222–225.
28. Day JF, Stark LM. Transmission patterns of St. Louis encephalitis and eastern equine encephalitis viruses in Florida: 1978–1993. J Med Entomol 1996;33:132–139.
29. Mendenhall IH, Tello SA, Neira LA, et al. Host preference of the arbovirus vector Culex erraticus (Diptera: Culicidae) at Sonso Lake, Cauca Valley department, Colombia. J Med Entomol 2012;49:1092–1102.
30. Mckay T, Bianco T, Rhodes L, et al. Prevalence of Dirofilaria immitis (Nematoda: Filarioidea) in mosquitoes from northeast Arkansas, the United States. J Med Entomol 2013;50:871–878.
31. Huang S, Smith DJ, Molaei G, et al. Prevalence of Dirofilaria immitis (Spirurida: Onchocercidae) infection in Aedes, Culex, and Culiseta mosquitoes from north San Joaquin Valley, CA. J Med Entomol 2013;50:1315–1323.
32. Frimeth JP, Arai HP. Some potential mosquito vectors of the canine heartworm, Dirofilaria immitis, in the Calgary region of southern Alberta. Can J Zool 1983;61:1156–1158.
33. Todaro WS, Morris CD, Heacock NA. Dirofilaria immitis and its potential mosquito vectors in central New York state. Am J Vet Res 1977;38:1197–1200.
34. Nasci RS, Mitchell CJ. Arbovirus titer variation in field-collected mosquitoes. J Am Mosq Control Assoc 1996;12:167–171.