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Natural Transmission of Dirofilaria Immitis by Aedes

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Natural Transmission of Dirofilaria Immitis by Aedes 48 J. Apr. Mosq. CoNrnol Assoc. Vor-.2, No. l NATURAL TRANSMISSION OF DIROFILARIAIMMITIS BY AEDESAEGYPTII C. M. HENDRIX', C. J. BRUNNER3 .qNoL. K. BELLAMY2 ABSTRACT. The Liverpool strain of the mosquito Ardasaegypti was infected with microfilariae of the canine heartworm, Dirofilaria immitis, and was used to transmit heartworm larvae to three dogs. Methods of confirm- ing heartworm infection in these dogs included the rnodified Knott's test, a commercial enzymelinked- immunosorbent assay(ELISA), an indirect fluorescent antibody (IFA) test, and post-mortem examination. INTRODUCTION ously into the canine definitive host (Tulloch et al. 1970, Kotani and Powers 1982). The pur- Ludlam et al. (1970) listed 63 speciesof mos- "complete pose of this experiment was to assessthe ability quitoes in which larval development of Ae. aegypti (Liverpool strain) to transmit in- of Dirofilaria immitis has been reported." Since fections of D. immiti,sto the dog. then, an additional 9 mosquito species capable of supporting larval development of D. immitis to the infective third larval stage within the MATERIALS AND METHODS head or proboscis have been reported (Crans RrrrrNr; TEcHNreuEs.The Liverpool strain and Feldlaufer 1974, Seeleyand Bickley 1974, of Ae. aegyptiwas provided by Dr. McCall, Weinrnann and Garcia 1974, Bickley 1976, John Athens, Georgia. Eggs oviposited on moisr cot- Christensen1977, Mosha and Magayuka 1979, ton batting were hatched in 22 x I I x 5 cm Rogers and Newson 1979, Acevedo 1982, Wal- white enarnelware pans containing distilled ters and Lavoipierre 1982). However, the capa- water at a depth of 4 crn. Food for larval devel- bility of transmitting infective third stage larvae opment was a mixture of I part rat chow, I part of D. immitis to the canine definitive host by brewers' yeast and I part lactalbumin. Pupae rnosquito bite has been dernonstrated with only were collected with a llulb syringe and trans- 7 of these 72 species (Bancroft 1904, Kume and ferred to 185 rnl paper cups; the cups were then Itagaki 1955, Newton 1956, Bemrick and transferred to 30.5 x 30.5 x 30.5 cm mosquito Moorhouse 1968, Bickley er al. 1977, Christen- holding cages (Arnerican Biological Supply, sen 1977, Hendrix et al. 1980). Baltirnore MD, 21228) in an environmental Aedesaegypti (Linnaeus) has been one of the charnber at 26"C, 80% relative hurnidity. and most extensively studied rnosquito species with alternating l2-houl light and dark photo- regard to its role in the larval developrnent of D. periods. Ernerged rnosquitoes were rnaintained irnzitls (Ludlam et al. 1970). Both wlld and lab- in the holding cages on a 5% sucrose solution oratory strains of this rfosquito have been (in a vial with a cotton plug wick). studied with diverse results regarding their Ixpecrrox oF \.roseurrons. The donor dog suitabilities as interrnediate hosts (Buxton and was a 22.7 kg, rnixed-breed female exhibiting Mullen 1981, Tolbert and 1982, Johnson circulating rnicrofilariae of D. immitis on the Sauerrnan and Nayar 1983). rnodified Knott's test (Newton and Wright Although Ae. aegypti has been used exten- 1956). Her circulating rnicrofilaremia level av- sively to study the developrnent of D. immitis elaged 150 rnicrofilariae per 20 p.l of blood. To (Kershaw et al. 1953, Taylor 1960, Singh et al. encourage their feeding on the heartworrn- 1967, McGreevy et al. 1974, Lindernann 1977), infected donor dog, adult female rnosquitoes transrnission of D. immitis to dogs by bites frorn were denied blood rneals for 3 days following infectious Ae. aegypti in the laboratory has not their ernergence. Mosquitoes fed unhindered been demonstrated (Hinrnan 1935). on the donor dog's hind leg for periods ranging Researchers who have utilized Ae. aeglpti for frorn 30 min to I hr. Cages were then returned infecting dogs with the canine heartworrn have to the environrnental charnber to allow the lar- dissected infective third stage larvae fi-orn the val developrnent of D. inmitis to take place mosquito and injected the larvae subcutzrne- within the rnosquitoes -Ip.rxsrrrssroN over the next 14 days. sruDrEs. The test group of 4 litterrnate dogs, three recipients (dogs A, C and I Publication nurnber 1727. Supported in part by a D) and one control (dog B), had spent their research grant-in-aid from Auburn University Col- entire lives in an indool kennel environrnent (a lege of Veterinary Medicine. "bioclean" 2 Department of Pathology and Parasitology, Col- area). Prior to the initiation of the lege of Veterinary Medicine, Auburn University, AL study, blood sarnples fr-orn all dogs were exarn- 36849-3501. ined using the rnodified Knotr's resr and wer-e 3 Department of Microbiology, College of Veteri- negative for rnicrofilariae. Sera frorn each ani- nary Medicine, Auburn Universiry, AL 36849-3501. rnal exarnined for antibodies against adult anti- 49 Mencs, 1986 J. Apr. Mosg. CoNrnoL Assoc. anti- gens of D. immitis using a commercial enzyme- 23 weeks postexposure and for (IFA linked immunosorbent assay(ELISA) (Dirotect' microfilarial antibodies test) at 26 weeks (4 Mallinckrodt, Inc., Bohemia, NY) and for an- postexposure. At necropsy 6 adult female tibodies against microfilariae using an indirect and 2 male) D. immitis were recovered frorn the fluorescent antibodv (IFA) test (Dawe et al. right ventricle and pulrnonary arteries of dog 1980) were antibody-negative. The dogs r,vere D. dogs transferred to individual cages in a confine- By 55 weeks following initial exposure rni- ment area with a screened entryway. Outside A, B and C had not exhibited circulating However, ELISA tests doors were locked and vents sealed to prevent crofilariae of D. immitis. A and C becatne accessof wild infectious mosquitoes to exper- revealed that sera from dogs against adult imental and control animals' weakly positive for antibodies and weeks, Transmission studies were conducted l4 days antigens of D. immitis at 30 29 sera frorn sentry following the mosquitoes' infectious blood respectively, postexposure: on the ELISA meal. One limb of each recipient dog was in- control dog B rernained negative (IFA test) serted through the accesssleeves of the holding test. Anti-microfilarial antibodies 3 dogs at any time cages and mosquitoes fed unhindered for pe- were not detected in these riods ranging from 30 min to I hr. On any during the study. I adult rnale D. immitis succeeding day following the initial 14 day de- At necropsy dog A had C had 2 adult velopmental period, if surviving mosquitoes in the right ventricle while dog No adult D. ira- would feed unhindered on the recipient dogs, fernales in the right ventricle. heart, puhnonary ar- they were perrnitted to do so. Dog A was ex- mitis were present in the of sentry control posed to mosquitoes on 7 occasions,dog C on 4 teries, lungs, or venae cava adult heartworrns occasions,and dog D on 3 occasions.Dog B was dog B nor were aberrant this control anirnal. never exposed to infected caged mosquitoes foJnd in ectopic siteswithin but rernained in the screened confinernent area with her littermates, serving as a sentry control. Pnn.pernxr pERIoD.After the initial exposure DISCUSSION period, all dogs were housed in individual cages of the in- in the rnosquito free environrnent. Beginning 3 Karnnan (1957) reviewed rnuch between weeks postexposure, sera from recipient and forrnation concerning the interactions that control anirnals were collected and frozen at D. immitis and the various rnosquito species hosts' weekly intervals for later analyses using the are capable of serving as interrnediate were ELISA and IFA tests.Three rnonths following \{uch of the data then and since then intricate the initial exposut'e, rvhole blood was collected gathet'ed in studies involving the 4e. ueg;pti at weekly intervals frorn recipient and contl'oL 6ost-p:rr':rsitelelationship between intake on anirnals and exatnined for- rnicrofilar-iae of D. and D. irnmitis: effect of rnicrofilarial 1953)' imrnitis using the rnodified Knotts test. the sulvival of the host (Kersharv et al. larvae NEcnopsr pRocEDURtls.All dogs were rnorphological changes occut-t'ing in reaction to euthanized by lethal injection of sodiurn pen- ('faylor- 1960), encapsulation, host 1977)' ef' tobarbital. Necropsy was perfortned on dog D developing larval stages(Lindernann incubation 29 weeks following initial exposure to infecti- fects o[ tetnperature on the extrinsic of infective ous rnosquitoes,and on dogs A, B and C at 55 (Singh et at. tSOZ;, and etnergence al. weeks postexposut-e. The hearts, pullnonal'y larvie florn the rnouthparts (Mc()r'eevy et of data has alteries, lungs and venae cavurof the recipient 1974). Although a large arnount surveys and control dogs were exarnined for adult D. been gatheled frorn epiderniological immitis. In addition, ectopic sites (brain, eye, (folbert and Johnson 1982, Sauerrnan and etc.) were exarnined for the presence of adult D. \ayar 1983), rnuch has been learned concern- immiti.; in the sently contt'ol anirnzll to ensule ing lalval developrnent within various labor:r- that aberlant adult healtwol'lns lvel'e not pl'e- tor:y stt'ains of Ae. aegypl1. These different' host sent (Otto 1974). str':rinscliffer- rnarkedly with regald to their efficierrcy, i.e. susceptibility velsus refi-actori- ness(Buxton and Mullen l98l). Due to these rvidesplead differ-ences, '4e. aegtpti has been RESUT-'fS utilized to study the genetic bases of suscepti- (Kaltrnan All dogs lernained healthy throughout the lrility to infections rvith D. irnmitis expelittrent. Dog D begatrto exhibit cilculating l95ii. Sulairnitnztnd'fownson 1980)' a rniilofilaliae of D. intmitis apploxirnately 28 Aedesaegypti has long been recognized.as namely in rveeks following the initial exposut'e. Set'utn model for developmental studies, larval developrnent of D. immilis to fi'orn this dog becarne positive fol antibodies suppolting 'fhese l:rlvae at'e againstadult D. irzrnlll.tar.rtigens (E[,ISA test) at the infective thircl lalval stage.
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