Integrated control of ticks and fleas on dogs with particular reference to the prevention of vector-borne diseases 1 Thesis Fourie NIEUW.indd 1 2-9-2015 15:06:40 Copyright © Josephus J. Fourie, 2015 ISBN/EAN: 978-90-393-6407-9 NUR-code: 886 2 Thesis Fourie NIEUW.indd 2 2-9-2015 15:06:40 Integrated control of ticks and fleas on dogs with particular reference to the prevention of vector-borne diseases Geïntegreerde bestrijding van teken en vlooien op honden met nadruk op de preventie van vector-gebonden ziekten (met een samenvatting in the Nederlands) PROEFSCHRIFT ter verkrijging van de graad van doctor aan de Universiteit Utrecht op gezag van de rector magnificus, prof.dr. G.J. van der Zwaan, ingevolge het besluit van het college voor promoties in het openbaar te verdedigen op 2 oktober 2015 des middags te 2.30 uur door JOSEPHUS J. FOURIE geboren op 15 Januari 1981 te Cradock, Zuid Afrika 3 Thesis Fourie NIEUW.indd 3 2-9-2015 15:06:40 Promotoren: Prof. dr. H. P. Haagsman Prof. dr. F. Jongejan 4 Thesis Fourie NIEUW.indd 4 2-9-2015 15:06:40 CONTENTS CHAPTER 1. INTRODUCTION AND LITERATURE REVIEW 9 1.1. Introduction 11 1.2. Ticks 12 1.3. Tick-borne pathogens 16 1.4. Fleas 18 1.5. Flea-borne pathogens 18 1.6. Tick control 20 1.7. Flea control 21 1.8. Mode of action of different classes of acaricides and insecticides 22 1.9. Efficacy and speed of kill 26 1.10. Transmission blocking concept 28 2.0 Aims and Outline of this Thesis 31 References 33 CHAPTER 2. CONTROL OF TICKS AND FLEAS ON DOGS 39 2.1. Fourie JJ, Fourie LJ, Horak IG, Snyman MG. The efficacy of a topically applied combination of cyphenothrin and pyri proxifen against the southern African yellow dog tick, Haema physalis elliptica and the cat fleaCtenocephalides felis. J South Afr Vet Assoc. 2010, 81 (1) : 33-36. 39 2.2. Fourie JJ, Beugnet F, Ollagnier C, Pollmeier MG. Study of the sustained speed of kill of the combination of fipronil/ amitraz/(S)-methoprene and the combination of imida- cloprid/permethrin against Dermacentor reticulatus. Para- site. 2011, 18 (4) : 319-23. 45 2.3. Horak IG, Fourie JJ, Stanneck D. Efficacy of slow-release collar formulations of imidacloprid/flumethrin and delta- methrin and of spot-on formulations of fipronil/(s) - metho- prene, dinotefuran/pyriproxyfen/permethrin and (s) - metho- prene/amitraz/fipronil againstRhipicephalus sanguineus and Ctenocephalides felis felis on dogs. Parasit Vectors. 2012, 22 : 5:79. 53 5 Thesis Fourie NIEUW.indd 5 2-9-2015 15:06:40 CHAPTER 3. PREVENTION OF BABESIA CANIS TRANSMISSION BY TICKS 69 3.1. Jongejan F, Fourie JJ, Chester ST, Manavella C, Mallouk Y, Pollmeier MG, Baggott D. The prevention of transmission of Babesia canis by Dermacentor reticulatus to dogs using a novel combination of fipronil, amitraz and (S)-methoprene. Vet Parasitol. 2011, 179 (4) : 343-350. 79 3.2. Fourie JJ, Stanneck D, Jongejan F. Prevention of transmis- sion of Babesia canis by Dermacentor reticulatus ticks to dogs treated with an imidacloprid/flumethrin collar. Vet Parasitol. 2013, 192 (1-3) : 273-278. 87 3.3. Beugnet F, Halos L, Larsen D, Labuschagné M, Erasmus H, Fourie JJ. The ability of an oral formulation of afoxolaner to block the transmission of Babesia canis by Dermacentor reticulatus ticks to dogs. Parasit Vectors. 2014, 7 (1) : 283. 89 CHAPTER 4. PREVENTION AND SPEED OF EHRLICHIA CANIS TRANSMISSION BY TICKS 97 4.1. Fourie JJ, Ollagnier C, Beugnet F, Luus HG, Jongejan F. Prevention of transmission of Ehrlichia canis by Rhipicep- halus sanguineus ticks to dogs treated with a combination of fipronil, amitraz and (S)-methoprene (CERTIFECT©).Vet Parasitol. 2012, 193 : 223-228. 97 4.2. Fourie JJ, Luus HG, Stanneck D, Jongejan F. The efficacy of Ad vantix© to prevent transmission of Ehrlichia canis to dogs by Rhipi cephalus sanguineus ticks. Parasite. 2013, 20 : 36. 105 4.3. Fourie JJ, Stanneck D, Luus HG, Beugnet F, Wijnveld M, Jongejan F. Transmission of Ehrlichia canis by Rhipicep- halus sanguineus ticks feeding on dogs and on artificial membranes. Vet Parasitol. 2013, 197 (3-4) : 595-603. 115 CHAPTER 5. PREVENTION OF DIPYLIDIUM CANINUM TRANSMISSION BY FLEAS 127 5.1. Fourie JJ, Crafford D, Horak IG, Stanneck D. Prophylactic treatment of flea-infested dogs with an imidacloprid/flume- thrin collar to preempt infection with Dipylidium caninum. Parasitol Res. 2013, 112 : S33-S46. 127 6 Thesis Fourie NIEUW.indd 6 2-9-2015 15:06:40 CHAPTER 6. GENERAL DISCUSSION 143 6.1. Introduction 145 6.2. Pros and cons of spot-on, collars and oral formulations of acaricides 154 6.3. Speed of pathogen transmission 157 6.4. Transmission blocking models 158 6.5. Concluding remarks and future directions 162 References 164 Summary 169 Afrikaanse opsomming 172 Nederlandse samenvatting 175 Acknowledgements 178 Curriculum Vitae 181 List of Publications 182 7 Thesis Fourie NIEUW.indd 7 2-9-2015 15:06:40 8 Thesis Fourie NIEUW.indd 8 2-9-2015 15:06:40 Chapter 1. Introduction and literature review 9 Thesis Fourie NIEUW.indd 9 2-9-2015 15:06:40 10 Thesis Fourie NIEUW.indd 10 2-9-2015 15:06:40 1.1. Introduction According to Saunders Comprehensive Veterinary Dictionary, third edition (2007) page 413, a companion animal is defined as: “dogs, cats, pleasure horses, birds, mice, guinea pigs and more exotic species kept by humans for company, amuse- ment, psychological support, extrovert display and all of the other functions that humans need to share with animals of other species; companions who will not take emotional or psychological advantage of the person and will, for the most part, stay faithful.” Of these, dogs are among the most common companion animals of man. Molecular evidence points to an origin of dogs from the wolf, Canis lupus, more than 14,000 years ago during the hunter-gatherer nomadic period. Less-fearful wolves were thought to be attracted to human settlements to scavenge kills. These less-fearful individuals then may have found utility as early guard dogs, warn- ing settlements through barking of incursions by humans or animals. Over time, these animals became differentiated from the larger autonomous wolf population through natural selection and genetic drift. Selection of pups as pets from these populations based on decreased flight behaviour and increased sociality, two trade- marks of tameness, laid the foundation for domestication. Once humans were able to practice selective breeding based on desired traits like obedient behaviour, the wolf in effect became a dog, ‘man’s best friend’. The large phenotypic variation that is observed in modern dogs has resulted in more than 400 registered breeds today (Driscoll et al, 2009). Because dogs are such loved companion animals, their health and well- being are of great importance to their human companions. Controlling parasites on dogs is therefore important not only because of the detrimental impact on the an- imal’s health, but also the zoonotic risk that some of these parasites pose to their human companions. Dogs serve as hosts for a considerable number of parasites, which include ectoparasites (i.e. fleas, ticks, mites and lice) and endoparasites (e.g. protozoa and helminths). Of these, tick and flea infestations and their associated pathogens are the most prevalent and constitute a major health concern for dogs. 11 Thesis Fourie NIEUW.indd 11 2-9-2015 15:06:40 1.2. Ticks Ticks are obligate, blood-feeding ectoparasites in the phylum Arthropoda. Within the order Parasitiformes, suborder Ixodida, superfamily Ixodoidea, all ticks are in- cluded in three families: Ixodidae, Argasidae and Nuttalliellidae. In these families, the Nuttalliellidae comprises a single species, Nuttalliella namaqua. The remaining two families consist of the hard ticks (Ixodidae) and the soft ticks (Argasidae) (Guglielmone et al, 2010). Ixodid ticks are differentiated from Argasid ticks by the presence of a sclerotized scutum. Fourteen genera are recognized in the family Ixodidae, and species within the genera Ixodes, Rhipicephalus, Dermacentor, Am- blyomma, Hyalomma and Haemaphysalis most frequently infest dogs. The life cycle of ixodid ticks consists of four stages, eggs, six legged larvae, eight legged nymphs and eight legged adult ticks. Depending on the species, ixodid ticks have one- two-or three-host life cycles. All ixodid tick species, which feed on dogs, are characterized by a three-host life cycle (Fig.1). Metastriate ticks which include all genera except Ixodes mate exclusively on the host, whereas in pros- triate ticks, of which Ixodes is the only, gametogenesis already begins during the nymphal to adult moult, resulting in unfed adults sexually active soon after moulting. In some Ixodes species mating takes place off the host, before the ticks have fed, while in others mating takes place on the host. Engorgement of female metastriate and prostriate ticks on the blood of their hosts can be immense, occasion- ally in excess of 100 times their own unfed body weight. After engorgement, female ticks detach and drop from their hosts and commence oviposition, which results in several thousand eggs. The males of most species remain attached for varying periods of time after the females have dropped.Ticks follow two basic strategies to access suitable hosts. A passive (ambush) strategy involves a tick remaining quies- cent in its habitat and depends upon contact with any host that invades this habitat. These ticks are found questing on the vegetation. Active (hunter) host acquisition involves a tick leaving the environment where it was sheltering to actively seek a host. Once a host has been found, tactile stimuli come into play, contributing, along with short-range odourants and body heat, to the selection of a feeding site and the commencement of blood-sucking.