Anthelmintic Resistance in Gastrointestinal Nematodes of Alpacas (Vicugna Pacos) in Australia
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Oorsig/Review Anthelmintic resistance in gastrointestinal nematodes of alpacas (Vicugna pacos) in Australia Mohammed H. Rashid1, Jane L. Vaughan2, Mark A. Stevenson1, Angus J. D. Campbell1, Ian Beveridge1 and Abdul Jabbar1* BACKGROUND Australian alpaca industry is an important In the last three decades, the farming of emerging livestock industry. However, very little domesticated South American camelids (SACs), alpacas (Vicugna pacos) and llamas (Lama glama) has increased in Australia, Europe, New Zealand, is known about the epidemiology and control of wormGINs in (Haemonchus alpacas in Australia. contortus) Recently, was reported the first2. 1,2. case of ivermectin resistance in the Barber’s pole Inthe anUK andintensive the USA, farming due to theirsystem, high-quality alpacas fibreand Australian alpaca farmers revealed that the dose and adaptability to many climatic conditions ofA surveyanthelmintics of the worm used controlfor alpacas practices (e.g. usedone byto common in domestic ruminants; e.g. Haemonchus three times of dose recommended for sheep) and contortusllamas can, Ostertagia be infected ostertagi with both, Trichostrongylus shared (those the existence of other potential risk factors for spp. and Nematodirus spp.) as well as host- the development of AR known for GINs of sheep, Lamanema chavezi) gastrointestinal goats and cattle, could lead to the development of nematodes (GINs)3–5 AR in GINs of alpacas (Rashid et al specific (e.g. data). economic losses from that lowered can cause production significant of , unpublished clinical and subclinical problems,3, 4, 6–8. resulting in The aims of this study were (i) to undertake Outsidefibre, meat South and/or America, leather knowledge on the parasites of SACs is limited. Traditionally, the use witha questionnaire the development survey of to AR obtain in GINs insights of alpacas into farmlevel characteristics that might be associated commonly used method to treat and control anthelmintics against GINs of alpacas in Australia. GINsof chemotherapeutic of domestic ruminants. agents has Similarly, been the farmers most and (ii) to quantify the efficacy of commonly used regularly use various classes of anthelmintics to METHODS control GINs in alpacas and llamas3, 4, although no anthelmintic is registered for use against GINs in SACs in Australia. Given that very little is known Study population 9, farming in Australia mainly occurs in four Australia has various climatic zones, and alpaca registeredabout the pharmacokineticsfor domestic ruminants of drugs at indifferent SACs dosethe off-labelrates recommended use of anthelmintics for goats, insheep alpacas and alpacazones, theherds Mediterranean, are located non-seasonalin the south-eastern rainfall, cattle is commonplace. However, the dose rate(s) statessummer of rainfallNew South and winter Wales rainfalland Victoria, zones. Mostwith and route(s) of administration recommended for fewer in Queensland, Western Australia, South Australia and Tasmania. The majority of alpaca SACs10 as found previously in goats11. Thus, under-dosingsheep might ofnot anthelmintics be effective mayagainst promote GINs thein development of anthelmintic resistance (AR) in supplementaryfarms contain ≤feed 50 animals,(Rashid etwhich al graze year- data).round Alpacason pastures, are routinely with variable vaccinated provision against of of the risk factors for the development of AR in ; unpublishedClostridium GINs ofin sheepSACs as12. Caseunder-dosing reports of is ARin known GINs to of be SACs one perfringens type D, C. tetani, C. novyi type B, 2, Belgium13, C.clostridial septicum anddiseases C. chauvoei (caused). They by are generally Canada14 and the USA15 in various GINs against shorn once annually in spring, although at twohave commonlybeen reported used from classes Australia of anthelmintics, Australia has the largest alpaca population variable timesthroughout the year. Timing and benzimidazoles and macrocyclic 16 lactones. (>450,000) outside South America and the duration of the birthing periods vary between farms but often occur during about two months 4 Volume 23 • Issue 05 • 2019 Faecal egg count reduction test (FECRT) The FECRT was performed on each farm according to the World Association for the Advancement of Veterinary Parasitology (WAAVP) guidelines ruminants18, 19. Both female and male - Huacaya andfor Surithe alpacas,evaluation aged of 3-months anthelmintic to 16-years efficacy were in randomly selected on each farm and allocated to and an untreated control group) comprising 5–15 animals.five or six Six groups anthelmintics (anthelmintic were treatment evaluated groups in this study: (i) monepantel (Zolvix®, Elanco Pty. Ltd., West Ryde, New South Wales, Australia); (ii) a Fig. 1 Map of Australia showing the locations of alpaca farms enrolled in the faecal egg count reduction trials in this study. Each combination of levamisole, closantel, albendazole circle represents one alpaca farm Rutherford, New South Wales, Australia); (iii) closanteland abamectin with sodium (Q-drench®, selenate Jurox (Closicare Pty. Ltd.,Plus in spring. Crias are weaned at an average age of Wales, Australia); (iv) ivermectin (Ivomec®, three months. BoehringerSelenium®, VirbacIngelheim Pty. Ltd.,Pty. Milperra,Ltd., North New SouthRyde, New South Wales, Australia); (v) moxidectin Questionnaire survey The survey aimed to assess current worm control practices of Australian alpaca farmers, (Cydectin® Injection for cattle, Virbac, Pty. Ltd., with an emphasis on the use of anthelmintics. BendigoMilperra, East, New Victoria,South Wales, Australia). Australia); Resistance and (vi) to A questionnaire was conducted using an online ivermectinfenbendazole was (Panacur found up 25®, to the Intervet 9th FECR Pty. trial.Ltd., programme, Research Electronic Data Capture17. Hence, we decided to replace ivermectin with a FECR trials. All anthelmintics were administered practices;The questionnaire (ii) the usecontained of anthelmintics; 30 questions and about (iii) more potent macrocyclic lactone in subsequent (i) farm demography and general husbandry 1.5 times the dose rate recommended for sheep. were close-ended, with a few semi-open (i.e. orally apart from moxidectin (subcutaneously) at agrazing close-ended management. question The with majority the ofaddition questions of a category “other”). An online questionnaire faecalAnimals samples were dosed were individuallycollected from based the on rectum body survey was supplied to 97 alpaca farmers who pre-weight (day using 0) and scales post-treatment where available. (day 11–14) Individual into had responded to a larger survey on more general parasite management in Australia (Rashid et al; methodzip-lock plastic[20] within bags, andseven were days kept of at collection. 4 °C until aspects of alpaca husbandry, worm problems and processed for FEC using a modified McMaster of water added into a 60ml container and soaked Selectionunpublished of farmsdata). Briefly, four grams of faeces were mixed with 11 ml Out of 91 alpaca farms that responded to the survey, 20 farms were selected to take part in 1.27)for 5–30 solution min (45 before ml) was making added a and homogenised 30–45 min later,faecal theslurry. sample Saturated was agitated,sugar (specific and a samplegravity drawn immediately from the suspension using a theirfaecal herd egg count(Fig. 1). reduction The following testing selection (FECRT) criteria based on herd size and the geographical location of 40 and 60 alpacas of different ages and sexes; sieve-top pipette (sieve aperture size 12 meshes were used: (i) the herd was comprised of between per cm), to fill two chambers of a Whitlock egg the 8 weeks prior to the scheduled herd visit; thecounting slide wasslide placed (http://www.whitlock.com.au/ on the stage of a compound (ii) deworming had not been carried out within lightslides/JAWCO_Home.htm). microscope and eggs Afterwere fivecounted. minutes, The (FEC) were greater than or equal to 150 eggs per gram(iii) confirmation (epg) of faeces; that and average (iv) there faecal was egg a historycounts EPG. sensitivity of the McMaster technique was 15 years. When a farmer agreed to participate and Nematode identification of anthelmintic usage on the farm in the last five diagnostic kit (Easy-Plex, AusDiagnostics andmet testedthe first for twoFEC. criteria,Over 50 faecalfarms weresamples tested were to We used a newly established molecular collected from fifteen randomly selected alpacas 21. Pty. Ltd., Beaconsfield, Australia) for the obtain 20 suitable farms for the FECRT trial. identification of common GINs of alpacas 5 Oorsig/Review Faecal DNA was extracted using a method 22. Preand post-treatment faecal samples for each genomicFor primary DNA amplification representing (15each cycles DNA ofsample 10 s orat described previously with few modifications 95 °C, 20 s at 60 °C, and 20 s at 72 °C), 5 μl of sample representing 5–15 individual faecal into 0.2 ml PCR strips and placed into a 24-well samplesgroup were per pooled group. in This order was to achievedobtain one during DNA 5 μl of water (negative control) were dispensed processing of individual faecal samples for FEC thermocycling block in the High-Plex 24 system in the saturated sugar solution to a 50 ml Falcon (AusDiagnostics). Subsequently, the analysis by withdrawing 1 ml of the faeces suspension was executed by the program MT-Assay Setup per treatment group. theSoftware melting (AusDiagnostics). curve analysis wereFollowing performed the first in tube. This process was repeated for each sample round of PCR,