Establishment of macrocyclic lactone resistant Dirofilaria immitis isolates in experimentally infected laboratory dogs

Parasites and Vectors

Volumn 7, Issue 1, 2014, Pages

  Pulaski, Cassan N ^a   Malone, John B ^a   Bourguinat, Catherine ^b   Prichard, Roger ^b   Geary, Timothy ^b   Ward, Danielle ^a   Klei, Thomas R ^a   Guidry, Tal ^e   Smith, George Bud ^f   Delcambre, Brooke ^a   Bova, Jonathan ^a   Pepping, Jenny ^a   Carmichael, James ^c   Schenker, Rudolf ^d   Pariaut, Romain ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c Novaitis Animal Health US Inc   (United States)

^d NOVARTIS PHARMA AG   (Switzerland)

^e Guidry Animal Hospital   (United States)

^f Bocage Animal Hospital   (United States)

Author keywords

Canine heartworms; Dirofilaria immitis; Drug resistance; Lack of efficacy; Macrocyclic lactone

Indexed keywords

IVERMECTIN; LACTONE DERIVATIVE; MACROCYCLIC LACTONE; UNCLASSIFIED DRUG; ANTHELMINTIC AGENT;

AEDES AEGYPTI; ANIMAL EXPERIMENT; ARTICLE; CHEMOPROPHYLAXIS; CONTROLLED STUDY; DIROFILARIA IMMITIS; DIROFILARIASIS; DRUG RESISTANCE; EXPERIMENTAL DOG; EXPERIMENTAL INFECTION; MALE; MICROFILARIA (NEMATODE LARVA); NONHUMAN; PARASITE ISOLATION; UNITED STATES; AEDES; ANIMAL; DISEASE MODEL; DOG; DOG DISEASE; DRUG EFFECTS; HUMAN; ISOLATION AND PURIFICATION; PARASITOLOGY; PROCEDURES;

AEDES; ANIMALS; ANTHELMINTICS; CHEMOPREVENTION; DIROFILARIA IMMITIS; DIROFILARIASIS; DISEASE MODELS, ANIMAL; DOG DISEASES; DOGS; DRUG RESISTANCE; HUMANS; IVERMECTIN; LOUISIANA; MALE; MISSISSIPPI;

EID: 84964697455     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/s13071-014-0494-6     Document Type: Article

References (34)

1. Hampshire VA: Evaluation of efficacy of heartworm preventive products at the FDA. Vet Parasitol 2005, 133:191-195.
2. Pulaski Cassan N, Malone John B, Lynch Sara A: Geospatial Patterns of Macrocyclic Lactone Preventive Drugs Lack of Efficacy Against Dirofilaria immitis in Louisiana. In Proc American Association of Veterinary Parasitologists 56th Annual Meeting: 16-19 July 2011. St. Louis, MO: American Association of Veterinary Parasitology; 2011:49.
3. Blagburn BL, Vaughn JL, Butler JM, Mount JD, Spencer JA, Carmichael J, Schenker R: Evaluation or Susceptibility of Heartworm (Dirofilaria immitis) Biotypes to Macrocyclic Lactones Using Microfilariae-based Single Dose and Dose-Mortality Regression Assays. In Proc American Association of Veterinary Parasitologists 56th Annual Meeting: 16-19 July 2011. St. Louis, MO: American Association of Veterinary Parasitology; 2011:98-99.
4. Evans CC, Moorhead AR, Storey BE, Wolstenholme AJ: Kaplan RM: Development of an in vitro bioassay for measuring susceptibility to macrocyclic lactone anthelmintics in Dirofilaria immitis. Int J Parasitol Drug Drug Resist 2013, 3:102-108.
5. Bourguinat C, Keller K, Bhan A, Peregrine A, Geary T, Prichard R: Macrocyclic lactone resistance in Dirofilaria immitis. Vet Parasitol 2011, 181:388-392.
6. Bourguinat C, Keller K, Blagburn B, Schenker R, Geary T, Prichard R: Correlation between loss of efficacy of macrocyclic lactone heartworm anthelmintics and P-glycoprotein genotype. Vet Parasitol 2011, 176:374-381.
7. Bourguinat C, Keller K, Prichard R, Geary T: Genetic polymorphism in Dirofilaria immitis. Vet Parasitol 2011, 176:368-373.
8. Geary T, Bourguinat C, Prichard R: Evidence for macrocyclic lactone anthelmintic resistance in Dirofilaria immitis. Top Companion Anim Med 2011, 26:185-192.
9. Bowman DD, Mannella C: Macrocyclic Lactones and Dirofilaria immitis microfilariae. Top Companion Anim Med 2011, 26:160-172.
10. Bowman DD: Heartworms, macrocyclic lactones, and the specter of resistance to prevention in the United States. Parasit Vectors 2012, 5:13.
11. Pulaski C, Malone J, Ward D, Klei T, Pariaut R, Bourguinat C, Prichard R, Carmichael J, Schenker R: 2013. In Proc 14th Triennial American Heartworm Symposium. LA: 8-10 September 2013. New Orleans, LA: American Heartworm Society; 2013:22.
12. Kaminsky R, Lizundia R, Blagburn B, Bowman D, Carmichael J, Schenker R, Epe C, Sager H: Efficacy studies in dogs demonstrate resistance of Dirofilaria against ivermectin and other macrocyclic lactones. In Proc American Association of Veterinary Parasitologists 58th Annual Meeting: 20-23 July 2013. Chicago, IL: American Association of Veterinary Parasitology; 2013:66.
13. NIAID/NIH Filariasis Research Reagent Repository Center (FR3): Standard Operating Procedure Protocol Manual, SOP Number 8.2-8.5. University of Georgia; 2011. www.Filariasiscenter.org/parasite-resources/Protocols.
14. Smith PH, Wiles SE, Malone JB, Monahan CM: Collection, Preservation and Diagnostic Methods. In Flynn's Parasites of Laboratory Animals. 2nd edition. Edited by Baker, David G. Ames IA: Blackwell Publishing; 2007:1-13.
15. McCall JW, Genchi C, Kramer LH, Guerrero J, Venco L: Heartworm Disease in Animals and Humans. Adv Parasitol 2008, 66:193-285.
16. McCall JW, Genchi C, Kramer L, Guerrero J, Dzimianski MT, Supakorndej P, Mansour AM, McCall SD, Supakorndej N, Grandi G, Carson B: Heartworm and Wolbachia: Therapeutic implications. Vet Parasitol 2008, 158:201-214.
17. McCall JW, Kramer L, Genchi C, Guerrero J, Dzimianski MT, Mansur A, McCall SD, Carson B: Doxycycline Treatment of Heartworm Microfilaremic Dogs Inhibit Embryogenesis, Blocks Further Transmission, Gradually Eliminates Circulating Microfilariae, and Kills Some Adult Heartworms. In Proc 14th Triennial American Heartworm Symposium. LA: 8-10 September 2013. New Orleans, LA: American Heartworm Society; 2013:25.
18. Kaplan R: Anthelmintic resistance in nematodes of horses. Vet Res 2002, 33:491-507.
19. Slocombe JO, Surgeoner D, GA S: Determination of the heartworm transmission period and its use in diagnosis and control. In Proc of the Heartworm Symposium. 17-19 March 1989; Charleston SC. Edited by Otto GF, Jackson RF, Knight DH, Campbell WC, Courtney CH, Dillon R, Hite SC Jackson RI, Levine BG, Lewis RE, Noyes JD. Washington DC: American Heartworm Society; 1989:19-26.
20. McKay T, Bianco T, Rhodes L, Barnett S: Prevalence of Dirofilaria immitis (Nematoda: Filarioidea) in mosquitoes from northeast Arkansas, the United States. J Mel Entomol 2013, 50:871-878.
21. 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(4):178-185.
22. Brown HE, Harrington LC, Kaufman PE, McKay T, Bowman DD, Nelson CT, Wan D, Lund R: Key factors influencing canine heartworm, Dirofilaria immitis, in the United States. Parasit Vectors 2012, 5:245.
23. Brady OL, Johansson MA, Guerra CA, Bhatt S, Golding N, Pigott DM, Delatte H, Grech MG, Leisnham PT, Freitas RM, Styler 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.
24. Dixon-Jimenez A, Rapaport G, Coleman AE, Creevy K, Roth I, Correa M, Moorhead A: Current Attitudes and Approaches to Canine Heartworm Disease Treatment Among Veterinarians in the Southeastern United States. In Triennial American Heartworm Symposium. LA: 8-10 September 2013. New Orleans, LA: American Heartworm Society; 2013:42.
25. Nana-Djeunga H, Bourguinat C, Pion SDS, Kamgno J, Gardon J, Njiokou F, Boussinesq M, Prichard RK: Single nucleotide polymorphism in B-tubulin selected on Onchocerca volvulus following repeated ivermectin treatment: Possible indication of resistance. Mol Biochem Parasitol 2012, 185:10-18.
26. Blair LS, Campbell WC: Efficacy of Ivermectin against Dirofilaria immitis larvae in dogs 31, 60, and 90 days after injection. Am J Vet Res 1980, 41(12):2108.
27. Campbell WC: Efficacy of the avermectins against filarial parasites: a short review. Vet Res Commun 1982, 5(3):251-262.
28. Godel C, Kumar S, Koutsovoulos G, Ludin P, Nilsson D, Commandatore F, Wrobel N, Thompson M, Schmid CD, Gota S, Bringaud F, Wolstenholme A, Bandi C, Epe C, Kaminsky R, Blaxger M, Maser P: The genome of the heartworm, Dirofilaria immitis, reveals drug and vaccine targets. FASEB J 2012, 26:4650-4661.
29. Gasser RB, Cantacessi C: Heartworm genomics: unprecedented opportunities for fundamental molecular insights and new intervention strategies. Top Companion Anim Med 2011, 26(4):193-199.
30. Geary J, Satti M, Moreno Y, Madrill N, Whitten D, Headley SA, Agnew D, Geary T, Mackenzie C: First analysis of the secretome of the canine heartworm. Dirofilaria Immitis Parasit Vectors 2012, 5:140.
31. Bell AS, Huijben S, Paaijmans KP, Sim DG, Chan BHK, Nelson WA, Read AF: Enhanced transmission of drug-resistant parasites to mosquitoes following drug treatment in rodent malaria. PLoS One 2013, 10:1371.
32. Belanger DH, Perkins SL, Rockwell RF: Inference of population structure and patterns of gene flow in canine heartworm (Dirofilaria immitis). J Parasitol 2011, 97(4):602-609.
33. Read AF, Day T, Huijben S: The evolution of drug resistance and the curious orthodoxy of aggressive chemotherapy. PNAS 2011, 108(suppl 2):10871.
34. Malone JB: Biology-based mapping of vector-borne parasites by geographic information systems and remote sensing. Parassitologia 2005, 47:27-50.