Topics in Companion Animal Medicine
Volume 26, Issue 4 , Pages 160-172 , November 2011

Macrocyclic Lactones and Dirofilaria immitis Microfilariae

  • Dwight D. Bowman, MS, PhD

      Affiliations

    • Department of Microbiology and Immunology, Veterinary Medical Center, Cornell University College of Veterinary Medicine, Ithaca, NY USA
    • Corresponding Author InformationAddress reprint requests to: Dwight D. Bowman, MS, PhD, Department of Microbiology and Immunology, Veterinary Medical Center, Cornell University College of Veterinary Medicine, C4-119, Ithaca, NY 14853-6401
    • ,
  • Claire Mannella, DVM, DACVIM

      Affiliations

    • Novartis Animal Health US, Inc. Greensboro, NC USA

References 

  1. Hampshire VA. Evaluation of efficacy of heartworm preventive products at the FDA. Vet Parasitol. 2005;133:191–195
  2. Blagburn B, Dillon R, Prichard R, et al. Characterization of Heartworm Prevention Failures in the Central United States [abstract], in Proceedings of the State of the Heartworm Symposium. In: Batavia, IL: American Heartworm Society; 2010;p. 27–28
  3. Anderson RC. Nematode Parasites of Vertebrates. Their Development and Transmission. ed 2. Wallingford, Oxon, UK: CABI Publishing; 2000;
  4. Beaver PC, Jung RC, Cupp EW. The filaria, in Clinical Parasitology. In: Philadelphia, PA: Lea & Febiger; 1984;p. 350–399
  5. Lok JB. Dirofilaria sp.: taxonomy and distribution. In:  Boreham PFL,  Atwell RB editor. Dirofilariasis. London: CRC Press; 1988;p. 1–28
  6. Georgi JR, Georgi ME. Canine Clinical Parasitology. In: Philadelphia, PA: Lea & Febiger; 1992;p. 193–200
  7. Megat Abd Rani PA, Irwin PJ, Gatne M, et al. A survey of canine filarial diseases of veterinary and public health significance in India. Parasit Vectors. 2010;3:30
  8. Foley H. Microfilaires du chien dans le Sud-Oranais. Ann Inst Pasteur (Paris). 1921;35:212–217
  9. Tarello W. Dermatitis associated with Dirofilaria repens microfilariae in a dog from Rome. Vet J. 2003;165(2):175–177
  10. Traversa D, Aste G, Milillo P, et al. Autochthonous foci of canine and feline infections by Dirofilaria immitis and Dirofilaria repens in central Italy. Vet Parasitol. 2010;169(1/2):128–132
  11. 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(3/4):303–314
  12. Mantovani A. Transplacental transmission of microfilariae of Dirofilaria immitis in the dog. J Parasitol. 1966;52:116
  13. Underwood PC, Harwood PD. Survival and location of the microfilariae of Dirofilaria immitis in the dog. J Parasitol. 1939;25:23–33
  14. Atwell RB. Clinical signs and diagnosis of canine dirofilariasis. In:  Boreham PFL,  Atwell RB editor. Boca Raton, FL: Dirofilariasis; 1988;p. 61–81
  15. Hoskins JD, Hagstad HV, Hribernik TN, et al. Heartworm disease in dogs from Louisiana: pretreatment clinical and laboratory evaluation. J Am Anim Hosp Assoc. 1984;20:205–210
  16. Allain DS, Kagan IG, Schlotthauer JC. Serologic studies on dogs experimentally infected with Dirofilaria immitis. In:  Bradley RE,  Pacheco G editor. Gainesville, FL: Canine Heartworm Disease, The Current Knowledge; 1972;p. 69–76
  17. Wong M. A comparison of ELISA and IFA titers in dirofilariasis in dogs. In:  Otto GF editors. Proceedings of the Heartworm Symposium '80. Batavia, IL: American Heartworm Society; 1981;p. 41–47
  18. Weil GJ. Dirofilaria immitis: identification and partial characterization of parasite antigens in the serum of infected dogs. Exp Parasitol. 1987;64:244–251
  19. McTier TL, McCall JW, Supakorndej N. Features of adult heartworm antigen test kits. In:  Soll MD,  Knight DH editor. Proceedings of the Heartworm Symposium '95. Batavia, IL: American Heartworm Society; 1995;p. 115–120
  20. Stenzenberger R, Gothe R. Studies on adulticide and microfilaricide therapy of naturally Dirofilaria immitis infected dogs with Immiticide and ivermectin, respectively (Tierarztliche Praxis). Ausgabe K, Kleintiere/Heimtiere. 1999;27:104–108
  21. Hewitt RI, White E, Wallace WS, et al. Experimental chemotherapy of filariasis. II. Effect of piperazine derivatives against naturally acquired filarial infections in cotton rats and dogs. J Lab Clin Med. 1947;33:1304–1313
  22. Grove DI. Onchocerciasis, in A History of Human Helminthology. In: Oxon, UK: CABI; 1990;p. 661–691
  23. Jackson RF. Microfilaricides. Semin Vet Med Surg (Small Anim). 1987;2:44–47
  24. Powers KG, Parbuoni EL, Furrow RD. Dirofilaria immitis: 1. Adverse reactions associated with diethylcarbamazine therapy in microfilaremic dogs. In:  Otto GF editors. Proceedings of the Heartworm Symposium '80. Batavia, IL: American Heartworm Society; 1981;p. 108–111
  25. Jackson RF, Seymour WG. Efficacy of avermectins against microfilariae of Dirofilaria immitis. In:  Otto GF editors. Proceedings of the Heartworm Symposium '80. Batavia, IL: American Heartworm Society; 1981;p. 131–136
  26. Schlotthauer JC, Stromberg BE, Paul AJ, et al. Safety and acceptability of ivermectin in dogs with naturally acquired patent infection of Dirofilaria immitis. In:  Otto GF editors. Proceedings of the Heartworm Symposium '86. Batavia, IL: American Heartworm Society; 1986;p. 29–32
  27. Bowman DD, Johnson RC, Ulrich ME, et al. Effects of long-term administration of ivermectin and milbemycin oxime on circulating microfilariae and parasite antigenemia in dogs with patent heartworm infections. In:  Soll MD editors. Proceedings of the Heartworm Symposium '92. Batavia, IL: American Heartworm Society; 1992;p. 151–158
  28. Courtney CH, Zeng QY, MalerMM . The effect of chronic administration of milbemycin oxime and ivermectin on microfilaremias in heartworm-infected. In:  Seward RL editors. Recent Advances in Heartworm Disease Symposium '98. Batavia, IL: American Heartworm Society; 1998;p. 193–199
  29. McCall JW, Ryan WG, Roberts RE, et al. Heartworm adulticide activity of prophylactic doses of ivermectin (6 μg/kg) plus pyrantel administered monthly to dogs. In:  Seward RL editors. Recent Advances in Heartworm Disease Symposium '98. Batavia, IL: American Heartworm Society; 1998;p. 209–215
  30. Blagburn BL, Paul AJ, Newton JC, et al. Safety of moxidectin canine SR (sustained release) injectable in ivermectin-sensitive collies and in naturally infected mongrel dogs. In:  Seward RL editors. Recent Advances in Heartworm Disease: Symposium '01. Batavia, IL: American Heartworm Society; 2001;p. 159–163
  31. Dzimianski MT, McCall JW, Steffens WL, et al. The safety of selamectin in heartworm infected dogs and its effect on adult worms and microfilariae. In:  Seward RL editors. Recent Advances in Heartworm Disease: Symposium '01. Batavia, IL: American Heartworm Society; 2001;p. 135–140
  32. Courtney CH, Jackson RF. Recurrence of microfilariae of Dirofilaria immitis after microfilaricidal therapy without an adulticide. In:  Morgan HC editors. Proceedings of the Heartworm Symposium 1974. Batavia, IL: American Heartworm Society; 1974;p. 87–88
  33. Bowman DD, Atkins CE. Heartworm biology, treatment, and control. Vet Clin North Am (Small Anim Pract). 2009;39(6):1127–1158
  34. Lok JB, Knight DH, Ramada EI. Effects of ivermectin on embryogenesis in Dirofilaria immitis: age structure and spatial distribution of intrauterine forms as a function of dosage and time post treatment. In:  Otto GF editors. Proceedings of the Heartworm Symposium '89. Washington DC: American Heartworm Society; 1989;p. 85–94
  35. Bowman DD, Neumann NR, Rawlings C, et al. Effect of avermectins on microfilariae in dogs with existing and developing heartworm infections. In:  Seward RL editors. Recent Advances in Heartworm Disease: Symposium '01. Batavia, IL: American Heartworm Society; 2001;p. 173–178
  36. McCall JW, Guerrero J, Roberts RE, et al. Further evidence of clinical prophylactic, retro-active (reach-back) and adulticidal activity of monthly administrations of ivermectin (Heartgard Plus™) in dogs experimentally infected with heartworms. In:  Seward RL editors. Recent Advances in Heartworm Disease: Symposium '01. Batavia, IL: American Heartworm Society; 2001;p. 189–200
  37. McCall JW, Supakorndej P, Dzimianski MT, et al. Evaluation of retroactive and adulticidal activity of moxidectin canine SR (sustained release) injectable formulation against Dirofilaria immitis in beagles. In:  Seward RL editors. Recent Advances in Heartworm Disease, Symposium '01. Batavia, IL: American Heartworm Society; 2001;p. 165–172
  38. Bowman DD. Why heartworm preventive dales should not go over the counter. http://www.veterinarypracticenews.comAccessed August 29, 2011
  39. American Heartworm Society. Diagnosis, prevention and management of canine heartworm (Dirofilaria immitis) infection in dogs (Batavia, IL, American Heartworm Society Canine Guidelines, American Heartworm Society). http://www.heartwormsociety.orgAccessed August 29, 2011
  40. Jackson RF, Seymour WG, Beckett RS. Routine use of 0.05m g/kg of ivermectin as a microfilaricide. In:  Otto GF editors. Proceedings of the Heartworm Symposium '86. Batavia, IL: American Heartworm Society; 1986;p. 37–39
  41. Plue RE, Seward RL, Acre KE, et al. Clearance of Dirofilaria immitis microfilariae in dogs using 200 mkg/kg ivermectin subcutaneously. In:  Otto GF editors. Proceedings of the Heartworm Symposium '83. Batavia, IL: American Heartworm Society; 1983;p. 153–160
  42. Blagburn BL, Hendrix CM, Lindsay DS, et al. Post-adulticide milbemycin oxime microfilaricidal activity in dogs naturally infected with Dirofilaria immitis. In:  Soll MD editors. Proceedings of the Heartworm Symposium '92. Batavia, IL: American Heartworm Society; 1992;p. 159–164
  43. Case JL, Tanner PA, Keister DM, et al. A clinical field trial of melarsomine dihydrochloride (RM340) in dogs with severe (class 3) heartworm disease. In:  Soll MD,  Knight DH editor. Proceedings of the Heartworm Symposium '95. Batavia, IL: American Heartworm Society; 1995;p. 243–250
  44. Stenzenberger R, Gothe R. Zur adultiziden und mikrofilariziden Therapie naturlich mit Dirofilaria immitis infizierter Hunde mit Immiticide bzw. Ivermectin Tierarztl Prax Ausg K Kleintiere Heimtiere. 1999;27:104–108
  45. Bourguinat C, Keller K, Schenker R, et al. Investigation of genetic changes in Dirofilaria immitis after the use of macrocyclic lactone heartworm preventatives [abstract], in Proceedings of the State of the Heartworm Symposium. In: Batavia, IL: American Heartworm Society; 2010;p. 28
  46. Bourguinat C, Keller K, Geary TG, et al. Geographic genetic polymorphism in Dirofilaria immitis [abstract], in Proceedings of the State of the Heartworm Symposium. In: Batavia, IL: American Heartworm Society; 2010;p. 27
  47. Ardelli BF, Prichard RK. Reduced genetic variation of an Onchocerca volvulus ABC transporter gene following treatment with ivermectin. Trans R Soc Trop Med Hyg. 2007;101(12):1223–1232
  48. McLaren DJ, Worms MJ, Laurence BR, et al. Micro-organisms in filarial larvae (Nematoda). Trans R Soc Trop Med Hyg. 1975;69:509–514
  49. Sironi M, Bandi C, Sacchi L, et al. Molecular evidence for a close relative of the arthropod endosymbiont Wolbachia in a filarial worm. Mol Biochem Parasitol. 1995;74:223–227
  50. Bandi C, Anderson TJ, Genchi C, et al. Phylogeny of Wolbachia in filarial nematodes. Proc Biol Sci. 1998;265:2407–2413
  51. Bandi C, McCall JW, Genchi C, et al. Effects of tetracycline on the filarial worms Brugia pahangi and Dirofilaria immitis and their bacterial endosymbionts Wolbachia. Int J Parasitol. 1999;29:357–364
  52. Langworthy NG, Renz A, Mackenstedt U. Macrofilaricidal activity of tetracycline against the filarial nematode Onchocerca ochengi: elimination of Wolbachia precedes worm death and suggests a dependent relationship. Proc Biol Sci. 2000;267(1448):1063–1069
  53. McCall JW, Genchi C, Guerrero J, et al. Heartworm and Wolbachia: therapeutic implications. Vet Parasitol. 2008;158:204–214
  54. Bazzocchi C, Mortarino C, Grandi G, et al. Combined ivermectin and docycyline treatment has microfilaricidal and adulticidal activity against Dirofilaria immitis in experimentally-infected dogs. Int J Parasitol. 2008;38:1401–1410
  55. Grandi G, Quintavalla C, Mavropoulou A, et al. A combination of doxycycline and ivermectin is adulticidal in dogs with naturally acquired heartworm disease (Dirofilaria immitis). Vet Parasitol. 2010;169:347–351

PII: S1938-9736(11)00081-X

doi: 10.1053/j.tcam.2011.07.001

Topics in Companion Animal Medicine
Volume 26, Issue 4 , Pages 160-172 , November 2011

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