Abbreviations ANOVA Analysis of variance AUC Area Under Curve

Cmax Maximum concentration DRM Doramectin endectocide Macrocyclic lactone antiparasitic against both (some) endoparasites and ectoparasites epg Eggs per gram of faeces FEC Faecal egg count GABA Gamma-amino butyric acid IVM Ivermectin lpg Larvae per gram of faeces ML Macrocyclic lactone MXD Moxidectin po Per os sc Subcutaneous s.e.m. Standard error of the mean tmax Time when maximum concentration is reached after drug administration

14 Rangifer, Special Issue No. 11, 1999 England that he owned 600 reindeer, six of which Introduction were valuable decoy animals used to lure wild reindeer. Reindeer husbandry obviously developed Reindeer, the circumpolar cervid from such hunt with decoy animals (in Vorren & The reindeer genus Rangifer comprises only one Manker, 1976; Skjenneberg, 1984). species, R. tarandus living in the northern The contemporary estimate of the total Rangifer hemisphere, both in the Palaearctic (Eurasian) and population of the world is nearly 8 million animals, Nearctic (American) areas (Banfield, 1961). It half of them semi-domesticated (Staaland & inhabits most of the circumpolar land areas not Nieminen, 1993). About 20% of the semi- covered by permanent ice. The southernmost domesticated reindeer are in Fennoscandia reindeer (apart from those introduced to the (Finland, Sweden and Norway) and 75% in Russia, southern hemisphere) graze in China (50 °N) and and the rest in North America and Greenland, with the northernmost on Svalbard, Greenland and arctic some thousand wild descendants of released semi- islands of Canada, even north of 80 °N. According domesticated reindeer on Iceland, South Georgia to current systematics, there were 12 subspecies of (54°30'S, 37°0'W) and Kerguelen (48°15'S, R. tarandus, but two of them are now extinct (in 69°10'E). Small-scale reindeer herding is also Nieminen, 1994). There is not full agreement about practised in Scotland and Japan (in Nieminen, the number of subspecies, other authors (e.g. Tyler 1993b). & Røed, 1993) count 7 subspecies. The most The main reindeer product is meat, but also important reasons for the evolution of the hides possess a considerable income in Finland subspecies have apparently been the separation of (Nieminen, 1992). In Russia reindeer are still the Asian and American continents and the important draught animals, and they are also milked repeated glacial periods (in Nieminen, 1994). The and used in riding at some locations (Nieminen, Nearctic wild reindeer is called caribou. 1995). Reindeer racing is becoming popular in The semi-domesticated reindeer descends from Fennoscandia, so much so that doping tests have the wild Eurasian mountain or tundra reindeer R. t. been introduced (Nieminen et ai, 1997). Velvet tarandus. There are still some 33 000 wild moun• antlers constitute the major reindeer product in tain reindeer in southern Norway, where they are Alaska (Nieminen & Muhonen, 1996). important game animals (Skogland, 1994). As late Reindeer calves are born mostly in May and as in 1970 it was estimated that there were also 22 early June with a body weight of 4-7 kg, and grow 000 wild reindeer on the Kola peninsula, but the fast during the summer, commonly reaching body number decreased to 2700 in 1984 (in weight of 50 kg or more in September-October. Syroechkovskii, 1995). The semi-domesticated Reindeer seldom deliver twins. In many areas, reindeer has probably also genes from the wild calves are ear-marked in midsummer. To do it, the forest reindeer, R. t. fennicus, with which it readily flock must be rounded up. The next round-ups take cross-breeds. Some years ago, there were about 1 place in autumn or winter, when animals are 000 wild forest reindeer in Finland, partly in a close selected for breeding, and others are slaughtered. neighbourhood of the reindeer husbandry area Those selected to live are often treated with (Kojola, 1995), but the population is growing. A antiparasitics (Kemppainen et al., 1997). relatively recent estimate of the population of this subspecies in Russian Karelia is 6 000 to 10 000 Finnish co-operative reindeer husbandry animals (in Nieminen, 1993a). The wild reindeer The Finnish reindeer husbandry organisation was has always been a popular game animal wherever it founded in the 18th century. The basic unit, the shares habitat with humans. Reindeer hunt was reindeer herding co-operative, is called paliskunta, practised in central Europe before the last Ice Age, which name was first used in the beginning of the and in Norway there is evidence of hunt 10 000 to 19th century. Reindeer are owned by individual 12 000 years ago. herders within a co-operative, but the pastures are common. The co-operatives are mostly separated The semi-domesticated reindeer from each other my means of fences. Presently The reindeer has been crucial to the Saami and there are 56 co-operatives, 40 in Lapland and 16 in other northern peoples and cultures, enabling the the province of Oulu. The Finnish paliskunta has settlement of the barren arctic and subarctic counterparts in Sweden, sameby, and in Norway, regions. The first report on European reindeer reinbeitedistrikt, or siida. The organisation husbandry is obviously from AD 892, when the structures differ, as in the Scandinavian countries Norwegian chieftain Ottar informed King Alfred of the level of co-operation is lower, and reindeer

Rangifer, Special Issue No. 11, 1999 15 husbandry is limited to the indigenous Saami ground, e.g. conservation, forestry, agriculture and people. In Finland anybody (European Economic tourism. Area citizens) living within the reindeer husbandry area and being a member of the local co-operative PARASITE FAUNA OF THE REINDEER AND has a legal right to own reindeer (Huttu-Hiltunen, ANTIPARASITIC MEASURES 1993). In Finland, there are 6800 reindeer owners, and about 800 families live primarily on reindeer A parasite is a symbiont living on the cost of the husbandry, but another 1000 get a considerable part other counterpart of the symbiosis, the host. of their living from reindeer (Anon., 1998). The Reindeer harbour a variety of different parasites reindeer husbandry area now comprises 115 000 (see Halvorsen, 1986). Although viruses, many square kilometres, or slightly over one third of the bacteria and fungi are definitively parasitic, they are country. not handled with in this thesis. So, the parasites The co-operative reindeer herding system has here are (invertebrate) animals living of the proved flexible and has continuously adapted new reindeer. Furthermore, those not practically methods to intensify production. The total number controllable with current macrocyclic lactone (ML) of reindeer in Finland was 37 000 in 1845 (in endectocides are not discussed at all. ML Nieminen, 1993a). During the first half of the endectocides have efficacy against nematodes and 1970s the number oscillated between 100 000 and arthropods, which phyla contain many important 150 000. Because of the launch of new techniques, reindeer parasites. It is worth specially noticing that such as calf slaughter, winter supplementary ML endectocides do not have efficacy against feeding, and antiparasitic treatment, as well as the cestodes, such as Echinococcus and Moniezia use of motorised herding, the amount increased tapeworms, and trematodes, such as the rapidly, reaching 200 000 to 250 000 during the Paramphistomum rumen fluke and liver flukes. The latter half of the 1980's. Between 1970 and 1976, knowledge on the efficacy of ivermectin against the annual number of animals slaughtered averaged reindeer parasite species is discussed in a later 38 000. It peaked in 1990-1991, when 160 000 chapter (page 27), and because other ML reindeer were slaughtered. After that, both the endectocides are newer products, there is no former overwintering population and the amount literature on the use of them in reindeer. slaughtered have diminished. During 1996-1997, 202 000 reindeer were counted alive, 28 000 of Losses estimated to be due to reindeer parasites which were calves. Eighty-eight thousand reindeer (gain of treatment) were slaughtered, whereof 61 000 calves (Anon., It is perhaps principally erroneous to discuss 1998). While calves contributed to less than one parasite-induced losses in reindeer, as the parasites third of the slaughter reindeer in the early 1970's, certainly belong to the ecosystem the reindeer live the current proportion is about three fourths in, almost like weather and vegetation, and are not (Kemppainen et ah, 1997). so easily separable additions. It is therefore better to Carrying capacity of the Finnish reindeer debate in terms of possible gains caused by pastures was clearly exceeded during several antiparasitic treatment. In older literature, however, decades (Kojola & Helle, 1993; Kumpula et ah, attempts to estimate the costs of parasitism were 1997). It has been extended with increased often made. Nordkvist (1967) estimated warbles supplementary feeding and pen-feeding where and throat bots to consume 15-20% of the reindeer winter pastures are scarce (Helle & Kojola, 1993; production income in Sweden, and Saval'ev (1968) Kemppainen et ah, 1997; Nieminen et ah, 1998). In approximated warbles alone to reduce the income addition, the increased slaughter of calves keeps the of the Soviet reindeer husbandry by 25-30%. overwintering population low. To minimise Thinking about such high losses of production, parasite-induced damage to the condition of the control measures might easily appear worthwhile. animals, antiparasitic treatment is used. This may There is, however, very little scientific evidence indirectly help in keeping the overwintering that organophosphate treatments would have breeding stock as small as possible. About 80% of improved the survival or weight gain of reindeer, overwintering reindeer are treated yearly with although several experiments showed a high degree ivermectin (Anon., 1993). Future challenges are in of efficacy against warbles and throat bots sustainability; balancing reindeer husbandry and its (Nordkvist 1967; Klement'eva, 1975; Nieminen et productivity needs with the carrying capacity of the ah, 1980; Persen et ah, 1982). In one experiment, pastures, not forgetting the other needs of the weight loss during winter was higher in famphur treated calves than in untreated ones, but the

16 Rangifer, Special Issue No. 11, 1999 subsequent higher weight gain during summer considered the most important parasites (Watson & compensated the winter weight loss, leading to Charleston, 1985), but also abomasal nematodes slightly higher mean slaughter weights in treated may cause clinical disease (Connan, 1991). animals the next autumn (Persen et a I., 1982). Parasite weight might at least partly have been Brainworm responsible for the higher live weight of untreated A lot of nematode species are known also from the animals in the spring. A single full-grown 3rd stage reindeer, but most of them have usually been warble larva weighs 1.6 to 1.7 g (Nilssen, 1997a). regarded as rather harmless. The most widely Nordkvist (1967) calculated that a normal warble recognised pathogen is probably the brainworm infection could make up a larval mass of about 500 Elaphostrongylus rangiferi, which is blamed for g per reindeer. The probably higher value of intact severe outbreaks of meningoencephalitis after hides from reindeer treated during the previous warm and rainy summers (Handeland & Slettbakk, years might have increased the profitability of 1994). Reindeer brainworms have been studied organophosphate treatment. extensively (e.g. Bakken & Sparboe, 1973; Later, using ivermectin, Nordkvist et al. (1984) Halvorsen, 1986; Handeland & Norberg, 1992; showed significantly lower mean live weight loss Hemmingsen et al., 1993; just to name a few). The (10.2 kg compared with 14.0 kg) in treated than in life cycle of the brainworm is heteroxenous with non-treated reindeer calves during winter. In snails as intermediate hosts and reindeer as another trial, a significant increase in mean live definitive host. The reindeer brainworm can also weight gain of about 3 kg was seen during the infect moose (Steen et al, 1997), sheep and goats subsequent year in treated calves as compared to (Handeland, 1991; Handeland & Sparboe, 1991, non-treated ones (Heggstad et al, 1986). Handeland & Skorping, 1992). In one trial, antiparasitic treatment with ivermectin increased antler symmetry, which was Gastro-intestinal nematodes speculated to be related with reproductive success Reindeer are also known to harbour several species (Folstad eta I., 1996). of abomasal and intestinal nematodes (Bye & Summer treatment of reindeer calves with Halvorsen, 1983; Bye, 1987; Bye et al, 1987; ivermectin or luxabendazole (broad-spectrum Fruetel & Lankester, 1988; Korsholm & Olesen, benzimidazole anthelmintic with efficacy against 1993), but so far there is only little evidence of nematodes, cestodes and trematodes) has in two their clinical importance (Christensson & small trials increased the weight gain of reindeer Rehbinder, 1975; Rehbinder & Christensson, 1977; calves before the slaughter season (Oksanen & Rehbinder & von Szokolay, 1978). However, Nieminen, 1995; Oksanen et al, 1996). This Arneberg et al. (1996) clearly showed that indicates that subclinical parasitism may be a abomasal nematodes depress food intake in growth-limiting factor to reindeer calves, at least if reindeer during late winter. Reindeer calves, born the infection pressure is high. mostly in May, pick up infective stages of gastro• intestinal parasites soon after their birth and Parasite species harbour patent nematode infections as early as late June or early July (Oksanen et al,. 1990). Nematodes The most important gastro-intestinal nematodes Nematodes are commonly considered the most are those in the abomasum (Fruetel & Lancaster, important parasites of domestic ruminants. In cattle, 1988), but reindeer calves have also Nematodirus sheep and goats, gastrointestinal nematodes can and/or Nematodirella nematodes of the small cause even fatal disease or, more commonly, intestine (Bye, 1987; Oksanen et al, 1990). The subclinical infection that leads to impaired reindeer specific species are Nematodirus tarandi production (Urquhart et al., 1987). The most and Nematodirella longissimespiculata, but also important gastrointestinal nematodes are those of other species primarily from other hosts may the abomasum (Ostertagia spp., Haemonchus spp.) parasitise reindeer (Fruetel & Lankester, 1988). but also nematodes of the small intestine Other intestinal nematodes are Capillaria sp. (Trichostrongylus spp., Nematodirus spp., (Christensson & Rehbinder, 1975; Rehbinder & Cooperia spp.) are regarded as important pathogens Christensson, 1977; Nordkvist et al., 1983, 1984) in some areas (Soulsby, 1982). The other important and Trichuris sp. (in caribou, Fruetel & Lancaster, group of parasitic nematodes in domestic ruminants 1988). The life cycles of intestinal nematodes are is the Dictyocaulus spp. lungworms. In farmed red not well-known, but the transmission is probably deer (Cervus elaphus), Dictyocaulus lungworms are direct. It is known that the eggs of Nematodirus

Rangifer, Special Issue No. 11,1999 17 battus of lambs develop further and hatch only after platyrhynchus (Bye & Halvorsen, 1983; Bye et al., winter, but eggs of other species of the genus may 1987) is Marshallagia marshalli, the distribution of hatch during the summer they were produced which is generally considered to be much more (Urquhart et al., 1987). Thus, N. battus from lambs southern in domesticated ruminants (Soulsby, 1982; produce eggs that become infective for the lambs of Barth, 1991). the subsequent year. It is not known whether N. tarandi follow a pattern similar to N. battus or not, Lungworm but the short summer of the Arctic might make that Lungworm infection is common in reindeer and strategy beneficial. may cause serious disease (Kummeneje, 1977; Dau, Pinworms of the genus Skrjabinema live in the 1981; Holmstrom et ai, 1989). The causative caeca of ruminants. Females deposit eggs on the species was earlier identified as Dictyocaulus perianal skin, where they drop off and can be with viviparus, that of bovines, but now the reindeer faecal samples. The parasites are not considered species is most often referred to as D. eckerti pathogenic (Soulsby, 1982), but are occasionally (Skrjabin et ai, 1971; Rahko et al., 1992; Nikander observed in sheep and goats (Borgsteede and &Saari, 1993). Dercksen, 1996). In one experiment, immature and adult Skrjabinema ovis were present in two Vector-transmitted nematodes ivermectin treated goats (DeVaney et ai, 1992). Besides the nematodes infecting reindeer orally, One species of the genus, S. tarandi, is known to there are several known or suspected arthropod occur in reindeer, also in Finland (S. Nikander, vector -transmitted nematode parasite species in unpublished). Eggs of the genus are easily reindeer. Onchocerca tarsicola was commonly recognised because of their highly asymmetrical detected (30%) in tibiotarsal or radiocarpal regions shape. of limbs of 407 Finnish reindeer. The worms were most often found in flat swellings or nodules of Abomasal nematodes connective tissue in membranes surrounding the The most common abomasal nematode species is tendons of the tibiotarsal and radiocarpal joints the reindeer specific Ostertagia gruehneri (Bye & (Bylund et al., 1981). The parasite is transmitted by Halvorsen, 1983; Bye, 1987; Nikander, 1988; simulids (Schulz-Key & Wenk, 1981). Lappnema Fruetel & Lancaster, 1988). Another reindeer auris is a nematode which induces the formation of specific species, O. arctica, is now considered the large fibrotic nodules on the auricles of reindeer. less common morphotype of O. gruehneri Males of the parasite are unknown, and (Lichtenfels et al., 1990). Moreover, many species parthenogenetic reproduction is suspected (Bain & that principally parasitise other cervids or domestic Nikander, 1983). The species has become rare, ruminants have been found in reindeer abomasum perhaps because of endectocide treatment (Pryadko, 1976; Bye & Halvorsen, 1983; Fruetel & (Nikander, 1992). Subcutaneous parasitic nodules Lancaster, 1988; Korsholm & Olesen, 1993). The in the muzzle of reindeer were thought perhaps to life cycle of O. gruehneri is obviously similar to be caused by an Onchocerca nematode (Lisitzin, that of other members of the genus. Seasonal 1964). Both O. tarsicola, E. rangiferi and Setaria inhibition, as known in Ostertagia spp. from tundrae were found in visceral granulomas of domesticated ruminants in temperate areas (e.g. Swedish reindeer (Rehbinder et al., 1979; Michel et ai, 1974; Thomas & Waller, 1979) and Rehbinder, 1990). In Alaska, Setaria. of the reindeer also from deer (Connan, 1991, 1997; Belem et ai, has been identified as Setaria yehi. The parasite has 1993), has also been observed in reindeer been associated with subclinical chronic peritonitis (Nordkvist et al., 1984). The long arctic winter (Dieterich & Luick, 1971). obviously makes this strategy meaningful for parasite (and host) survival. It has been found that Nematocidic treatment the abundance of abomasal nematodes in reindeer Because the brainworm is considered a dangerous calves may be considerably lower than that of adult pathogen, several anthelmintics have been reindeer (Bye & Halvorsen, 1983; Bye, 1987), experimented against it. No efficacy was seen which is in discrepancy with what is known from following treatment with chlorophos, ditrazine domestic ruminants. The importance of milk as a phosphate, phosphamide or tetramisole, while source of nutrition to reindeer calves may explain phenothiazine temporarily reduced their this finding (see Nieminen, 1994). An interesting reproduction (Smirnov, 1976). In one experiment, and surprising abomasal nematode species found in reindeer infected with E. rangiferi were treated the wild polar Svalbard reindeer Rangifer tarandus daily for 10 days with mebendazole given at 6

18 Rangifer, Special Issue No. 11, 1999 mg/kg bodyweight in feed. This treatment the summer (Saveljev, 1968; Anderson et al., eliminated brainworm larval production for at least 1994). The larvae hatch, crawl down the hair and 43 days, but in another group of reindeer a single penetrate the skin (Karter et al., 1992). They dose of mebendazole at 40 mg/kg bodyweight did wander in the connective tissue, and reach the not remove these larvae (Rehbinder et al., 1981). In subcutaneous tissue of the back, where they mature another trial, both mebendazole and fenbendazole to the 3rd instar (Breyev, 1971). During the winter, at 6 mg/kg/day for 10 days had high efficacy they perforate the skin and breath through the hole. against E. rangiferi (Nordkvist et al., 1983). Oral In spring the mature larvae emerge, drop down, tetramisolum at 10 mg/kg 2 or 3 times a year has bury to the ground, where they pupate, and the been empirically observed to eliminate imagos emerge about one month later (Nilssen, Dictyocaulus and Trichostrongylus species from 1997b). The infection intensity in reindeer is often reindeer herds (Kurkela & Kaantee, 1978). high; the average number (150-200) is some ten times higher than that of H. bovis and H. lineatum Arthropods in cattle (Breyev, 1961). Both insects, arachnids and pentatastomids include Warbles are nearly ubiquitous in reindeer. parasites of reindeer. Generally, just the northernmost Arctic herds, and those in the southern hemisphere, are unaffected. Insects They are absent from Svalbard and Iceland Insect parasites of reindeer, excluding harassment (Skjenneberg & Slagsvold, 1968; Saval'ev, 1968; by blood-sucking insects, include lice and oestrid Leader-Williams, 1980; Wahburn et al, 1980). In flies. Sucking lice, Solenopotes tarandi, were the barren ground caribou of the Canadian Beverly originally described in Sweden (Mjoberg, 1915) herd located south from 65 °N, as many as 97 to and are also known from Alaska (Weisser & Kim, 100% of animals sampled had warbles, but in the 1973). Biting lice, Damalinia tarandi, were also Peary caribou on the Canadian Parry Islands (75°N) described in Sweden (Mjoberg, 1916), and are also only 14% were infected (Thomas & Kiliaan, 1990). known from Finland (A. Oksanen, unpublished). A plausible explanation for the absence of warbles The pathogenic effect of lice in reindeer is from the high Arctic regions is the cold climate. unknown. The free-living pupae require at 12 °C not less than There are two oestrid fly species (Diptera: 50 days to develop, while at 27 °C development Oestridae) parasitising the reindeer, the warble fly could take less than 10 days (Nilssen, 1997b). Hypoderma tarandi and the throat bot fly Nordkvist (1967) estimated that normally more Cephenemyia trompe. The imagos of these flies than 95% of reindeer were infected in Sweden. In lack mouth parts, and do not feed. Therefore, the western Finnmark in northern Norway, 99.9% of entire nutritional needs are covered by parasitism 1305 reindeer hides were warbled (Folstad et al., during the larval stage (see Nilssen & Anderson, 1989). In Finland the prevalence and infection 1995b). intensity of reindeer warbles were investigated in adult males, females and calves of six reindeer Warble herding co-operatives (Helle, 1980). A general Larvae of H. tarandi are called warble fly larvae observation was that calves and males were more (e.g. Helle, 1980), subcutaneous gadfly larvae heavily infected than adult females, which is in (Solopov, 1989), warble bots (Nilssen & Haugerud, agreement with the Norwegian results (Folstad et 1995) and grub fly larvae (Nordkvist, 1967). al., 1989). In Finland, both prevalence and Because of simplicity, and consistent with Dieterich infection intensity were lowest in the southernmost & Craigmill (1990) and Vercruysse (1993), they are co-operative located in the forest area, prevalence here called just warbles, even though this word can there in calves being from 42 to 63% and also refer to the whole papule formation, consisting abundance (mean intensity) from 3 (s.e.m. 1) to 11 both of the larva and host tissue reaction. In Latin, (4) during the three year study. In the northernmost reindeer warble was earlier called Oedemagena co-operatives the prevalence was 87 to 100%. tarandi (also in publications I and III), but the Abundance there varied between 23 (6) and 75 (6) inclusion of the species in the genus Hypoderma is larvae. Warbles were thus most common in the now generally accepted (Wood, 1987). northernmost areas. It is possible that the flies find The life cycle of H. tarandi is very similar to each other and the reindeer easier in the open that of other species of Hypoderma (e.g. H. bovis terrain of the north (Helle, 1982). and H. lineatum of cattle). Female warble flies lay Earlier, warbles were often removed mechanical• eggs on hairs of the host, especially on feet, during ly by compressing them between the thumb and

Rangifer, Special Issue No. 11, 1999 19 forefinger in the spring. Bergman (1917) If warbles become less abundant for example experimented with covering the back of reindeer due to antiparasitic treatment, serological tests may with tar to suffocate warbles instead of the be used in early detection of infected animals (see laborious compression. The results were promising, Monfray & Boulard, 1990). but the method never became widely used. Instead, the compression method was still utilised Throat bot sporadically. Even though the procedure was Throat bots are also called nasal bots (Dieterich & laborious, Saval'ev (1968) considered it useful Craigmill, 1990), nostril fly larvae (Helle, 1980), irrespective of other possible control measures. nose bot fly larvae (Nilssen & Haugerud, 1995) and After compression, the warble holes could be nasal warble fly larvae (Saval'ev, 1968). Besides the covered with creolin emulsion (Saval'ev, 1968). scientific name Cephenemyia trompe, also an Another control method of warbles and throat bots erratic form, Cephenomyia trompe, has been used was resting the herd on wet swamps in early (also in publications 1-111). The confusion in the summertime in order to let the emerging larvae scientific name is based apparently on a 150 years drown (Nordkvist, 1967). old mistake (see Zumpt, 1965). After that, both Because of their specific attraction to light names have been used, and the erroneous form coloured reindeer, warble fly females were lured to Cephenomyia has been very common. Modeer (in land on unfolded white hides where they were 1786) is generally considered the author of the easily killed, which was a task of youths (Saval'ev, original description, but as Linné obviously knew 1968). Other prophylactic measures were driving the parasite already in 1722, some scientists have the herd after calving at least 50 to 60 kilometres regarded him as the original author. The away from the place where the parasite larvae were geographical distribution of throat bots follows shed, and not returning to the calving ground before rather closely that of warbles (Bennett & Sabrosky, mid September (Saval'ev, 1968). This kind of 1962; Skjenneberg & Slagsvold, 1968). migration is considered natural to the reindeer Temporally, the life cycle of C. trompe (Folstad et ai, 1991). Hadwen (1926) noticed that resembles that of H. tarandi. The bots mature in Lapland reindeer had fewer warbles than those in tonsil pouches (Rehbinder & Nordkvist, 1983) Alaska, perhaps because the herds were constantly during the spring, drop down to the ground, pupate moving. He also mentioned to have seen dark sheds and emerge as mature flies in the summer. The flies in Finnish Lapland that provided shelter to reindeer have mating places on prominent hill-tops. After against all forms of insect harassment. Such a mating, the female flies expel uterine fluid with «liemu» shed can nowadays be seen at the Siida larvae to the muzzle of reindeer (Anderson & Saami museum in Inari. Also smokes have been Nilssen, 1990). The larvae invade the tonsil pouch, used to repel insects during the warmest summer where the development is very slow in the days (Saval'ev, 1968). On the other hand, carbon beginning (Hadwen, 1926; Nilssen & Haugerud, dioxide has been used to attract warble and throat 1995). Rapid development starts in the spring. bot flies, as well as blood-sucking insects for Earlier, definitive diagnosis of throat bots required scientific purposes (Helle et a I., 1992; Anderson & the slaughter of animals (e.g. Nilssen & Haugerud, Nilssen, 1996). 1995). With the changing reindeer husbandry habits, Before the commercial pharmaceuticals became defined chemical antiparasitics were adopted. In available to reindeer herders, tobacco water was Russia, dichloro-diphenyl-trichloroethane (DDT) used for «deworming» throat bots. It was poured was sprayed together with hexachlorane against into the pharynx via the nostrils or mouth harassment by blood-sucking insects as well as (Nieminen, 1989). Bots could also be removed warble and throat bot flies (Saval'ev, 1968). To manually by inserting a petroleum jelly lubricated treat a herd of 1000 reindeer, 12.5 kg of pure DDT hand into the mouth and pharynx of a well and the same amount of hexachlorane was needed restrained animal. This task was entrusted to small- for one summer season. According to the author, handed women or youths, and could only be carried carefully performed treatment increased the weight out on adult reindeer (Saval'ev, 1968). gain of the animals during the summer by 5 to 6 kg. When throat bot flies were noticed to have The amount of warbles decreased also improving specific mating places, attempts were made to kill the quality of hides. Other insecticides were found the flies there by spraying the mating hilltops with effective as well; both chlorophos and pyrethrum hexachlorane (Saveljev, 1972). The method was (pyrethrin I) were found to act faster than DDT never widely used, as main concern also in Russia (Saval'ev, 1968). was given to the treatment of parasitic stages with

20 Rangifer, Special Issue No. 11, 1999 organophosphates (Nepoklonov et al, 1973). Later, sulphur was placed on the stove to produce sulphur it has been found that mating sites are far too dioxide fumes. The treatment lasted for 40-45 numerous to be practical targets for control (Nilssen minutes and was repeated one week later. Also the & Anderson, 1995a). The mating sites of H. tarandi reindeer harnesses, saddles and accessories were are even more difficult to control in practice fumigated. An important part of mange control was (Anderson et al, 1994). also the isolation of infested animals and herds In the 1950's and 1960's, several systemically (Saval'ev, 1968). administered organophosphates were experimented with in Russia and some of them were found Pentastomids efficacious against reindeer warbles and throat bots Reindeer are parasitised by one member of the (Savel'ev et al, 1972; Nepoklonov et al, 1973). phylum; Linguatula arctica is morphologically Good efficacy of famophos, trichlorfon and close to the widespread (although not prevalent) L. fenthion against these parasites was reported also in serrata of dogs and other species of tropical Sweden (Nordkvist, 1967, 1980). In Finland, the carnivores. L. arctica is called «sinus worm» organophosphates fenthion and famphur were taken because it lives in the paranasal sinuses of reindeer, into practice in the late 1970's (Mykkanen, 1978) especially calves. The species and different aspects and their good efficacy against warbles (Nieminen of life cycle, epidemiology, pathogenity, taxonomy et al, 1980) and throat bots made them popular in a and antiparasitic treatment of L. arctica have been short period until the ivermectin era began. described and reviewed by Haugerud (e.g. 1986, 1989; Haugerud et al, 1993). Arachnids Arachnids can also give trouble to reindeer. Locally No interspecific covariation in Russia, reindeer are known to be parasitised by In one study, there was no association between the both sarcoptic and chorioptic mange mites reindeer brainworm and gastrointestinal nematode (Saval'ev, 1968). Sarcoptes scabiei causes first infection intensities measured as faecal larva and small vesicles but later the affected skin may egg counts (Karter, 1993). Likewise, no become covered by even a few centimetres thick interspecific covariation was found in intensities of scabs. Reindeer suffering from sarcoptic mange the brainworm, abomasal nematodes, warble, throat gradually lose their condition. During winter the bot, and sinus worm in 351 reindeer calves weight loss is rapid, and the affected reindeer may examined post mortem from herds where perish (Saval'ev, 1968). The disease can be antiparasitic treatment had not been performed transmitted to humans, too. Once, the source of (Nilssen et al, 1998). So, a high (or low) warble sarcoptic scabies in Taimyrian reindeer was traced burden is not indicative of the size of the abomasal to infected cattle (Mitskovich & Savel'ev, 1984). nematode burden in the individual. The study also Chorioptic mange mites cause local bald spots indicates transmission, not immunity, to be the key with no thick scabs and are not considered as factor for parasitic infection. serious pathogens as sarcoptic mange mites (Saval'ev, 1968). Rather apathogenic appearing MACROCYCLIC LACTONE ENDECTOCIDES chorioptic mites (Chorioptes texanus) are known from the ears of reindeer in Canada (Sweatman, There are already thousands of publications on the 1958) and Finland (S. Nikander, unpublished). macrocyclic lactone (ML) endectocides. This Apart from that, reindeer parasitic mites are not review is highly selective to include just those known from Fennoscandia. considered pertinent to the introduction to the subject of this thesis. As sarcoptic mange was considered an important reindeer health problem in Russia, means of History of the endectocides commercially available chemotherapy were developed. In spring and summer hexachlorane and hexachlorane-creolin Ivermectin liniments were used, or if the situation was considered really serious the whole animals were The experience with many insecticides, dipped in solution containing the same medication. anthelmintics and antibacterial antibiotics shows In winter, dipping of the reindeer would lead to that revolutionary new drugs may soon lose their chilling, so the animals were treated by fumigation. efficacy as evolution produces pests resistant to the The reindeer was placed in an airtight chamber with new drugs. However, the discovery of the a hole for the head. Inside the chamber, a cast iron extremely high antiparasitic properties of a new stove was heated with timber. A tray filled with group of macrocyclic lactones produced by soil

Rangifer, Special Issue No. 11, 1999 21 actinomycetes opened a totally new era in the griseus ssp. noncyanogenus produces a milbemycin antiparasitic treatment of livestock in the late called nemadectin (apparently nema - nematode, ect 1970's and early 1980's. The group was called - ectoparasites; Zulalian et al., 1994). Chemically avermectins (a - negation, ver - worms, ect - modified nemadectin becomes moxidectin (the ectoparasites, in - pharmaceutical product) (Shoop name from the methoxime substitution of the et al., 1995). The producing actinomycete was carbon C23). Moxidectin is marketed (Cydectin®, thereafter named as Streptomyces avermitilis. The American Cyanamid, now Fort Dodge) world-wide first commercial application, launched in 1981, a for domestic animal endectocide treatment. semisynthetic derivative of avermectin Bj, is called Moxidectin is one hundred fold more lipophilic 22,23-dihydroavermectin B,, or ivermectin. It is a than ivermectin as measured by the standard mixture containing not less than 80% of the octanol/water partitioning ratio. The lipophility of component Bla and not more than 20% of the moxidectin causes that it is preferably stored in fat component Blb, both of which molecules have and this storage probably contributes to the much antiparasitic activity (Shoop et al., 1995). Because longer depletion half life measured in sheep than of the very high commercial success of ivermectin that of ivermectin (Hayes, 1994). (Ivomec®, MSD, now Merial), intense activity was Moxidectin is more efficacious against triggered in the fields of chemistry, pharmacology nematodes in domestic ruminants than ivermectin, and parasitology to find even more effective to the extent that ivermectin resistant nematodes molecules, or at least commercially feasible ones. may appear moxidectin sensitive (Pankavich et al., Since the launch of ivermectin in 1981, until 1992; Craig et al., 1992; Pomroy & Whelan; 1993; 1998, another five commercial ML endectocides Varady et al., 1995) in spite of the probably similar have been introduced for use in production animals. mode of action and demonstrated cross-resistance (Shoop et al., 1993; Le Jambre et al., 1995). The Abamectin long depletion half life causes that the persistent activity of moxidectin against nematode infections Abamectin, or avermectin B1; was developed by the same medical company as ivermectin and is, in domestic ruminants is longer (Taylor et al., 1993; interestingly, a natural fermentation product of S. Hubert et al., 1995). Injectable moxidectin at 200 avermitilis, and the direct raw material of ug/kg is reported to have high efficacy against ivermectin. Like ivermectin, also abamectin is a cattle warbles (Hypoderma lineatum) (Scholl et al., mixture containing not less than 80% of avermectin 1992), but there is also a report on poor efficacy of oral moxidectin at 400 u.g/kg against third instar BIa and not more than 20% of avermectin Blb. Abamectin was registered in 1985 in Australia larvae of the equine bots Gasterophilus spp. (Xiao (Avomec®, MSD) for the treatment of various et al., 1994). In one trial, injectable moxidectin had endo- and ectoparasites in cattle and is now also 96% efficacy against first instars of Oestrus ovis, available in Europe (Enzec®, Janssen) (Heinze- but 100% against second and third instars (Puccini Mutz et al., 1993). The nematocidic and acaricidic et al., 1994). It appears that the anthelmintic properties of moxidectin are more pronounced than activities of abamectin surpass its insecticidic its insecticidal activity (Shoop et al., 1995). Cattle activity (Shoop et al., 1995). Abamectin is also dung has been less toxic against insects following used in crop protection (Dybas, 1989) which may moxidectin than following ivermectin treatment be a cause of environmental concern as much as (Strong & Wall, 1994). avermectin use in farm animals.

Moxidectin Doramectin The next endectocide to reach the market was a The fourth rival in the endectocide market is milbemycin derivative. The milbemycins (milbe - doramectin, 25-cyclohexyl-5-0-demethyl-25-de(l- mite, myc - fungus, in - pharmaceutical product), methylpropyl) avermectin Ala, produced by a like avermectins, are 16-membered macrocyclic mutant strain of S. avermitilis. The generic name lactones. They differ from the avermectins as they obviously does not mean anything, but may give an do not have the bisoleandrosyloxy substituent at the impression of durability. In cattle doramectin has 13-position of the macrolide ring (McKellar, 1994). almost twice as long a half-life as 22,23-

The milbemycins were already detected before the dihydroavermectin Bla, the major component of avermectins, but their full antiparasitic potential ivermectin (Goudie et al., 1993). Doramectin is was not realised immediately. First they were aimed marketed for sc injection (Dectomax®, Pfizer) in against mites in crop production (Shoop et al., sesame oil with ethyl oleate solution which 1995). The actinomycete Streptomyces cyaneo- contributes to low tissue irritability (Wicks et al.,

22 Rangifer, Special Issue No. 11, 1999 1993; Nowakowski et ai, 1995). Doramectin is avermectins (Shoop et al., 1995). In nematodes, claimed to have an antiparasitic spectrum close to low concentrations of ML endectocides have been that of abamectin (Shoop et al, 1995). shown to paralyse pharyngeal pumping, which leads to starving due to the worm's inability to Eprinomectin feed. Higher concentrations inhibit motility, which The latest endectocide was presented in 1996-97. might lead to a faster expulsion because the parasite Eprinomectin (Shoop et al, 1996) comes from the loses its ability to swim against the tide of digesta same pharmaceutical company as ivermectin and (Gill & Lacey, 1998). The expulsion of Ostertagia abamectin, although the company is now called circumcincta takes longer than that of Haemonchus Merial. The generic name eprinomectin is perhaps conforms or Trichostrongylus colubriformis in based on the chemical name 4"-epi-acetylamino- sheep, which has been interpreted to suggest that 4"-deoxy-avermectin B]. To begin with, the main method of expulsion in the first- eprinomectin is only marketed as pour-on mentioned species would be the inhibition of (Eprinex®, Merial). Eprinomectin is a racemic feeding, while the latter species probably are mixture of compounds which comprises not less expelled due to inhibition of motility (Gill & Lacey, than 90% of the component B,a and not more than 1998).

10% of the component B]b. Probably the most obvious practical advantage of the product is its Dosage and efficacy zero milk and meat withdrawal (in the USA). The The manufacturers' dose recommendations are commercial formulation contains 0.5% of based on dose titration trials with various parasite eprinomectin, and the rest is fractionated oils of species. The susceptibility of different parasite natural sources. species and their developmental stages vary a lot. The dose recommended is designed to be effective Mode of action against the least susceptible target parasite species, The mode of action of the different ML in ruminants Cooperia or Nematodirus species. At endectocides is similar at any rate in that it is not the time of the introduction of ivermectin, 90% totally understood (McKellar & Benchaoui, 1996). efficacy was considered very good and 80-90% Efficacy has been demonstrated against nematodes moderately effective (Powers et al., 1982). and arthropods, with some exceptions, such as the However, the endectocides themselves have nematode Thelazia lacrymalis and the mite changed the standards, currently a drug is regarded Ornithonyssus sylviarum (Campbell & Benz, as highly effective if it has over 98% efficacy 1984). Later, ivermectin has been found efficacious against the parasite species in question, effective if against other species of Thelazia (Kennedy et al., the efficacy is 90-98%, and moderately effective if 1994). The efficacy of ivermectin against equine 80-89% (Wood et al, 1995). Against Nematodirus cyathostome larvae is low (Klei et al., 1993), but helvetianus, the efficacy of ML endectocides has that of moxidectin is significantly higher (Xiao et been only moderate (Benz et ai, 1989), with the al., 1994). In one study, no efficacy of even high exception of moxidectin, which has high efficacy doses of ivermectin was seen against various (Flochlay & Deroover, 1997). Before eprinomectin nematodes in domestic fowl (Oksanen & Nikander, none of the drugs had established label claims 1989). Avermectin activity was explained to be against both adult and immature Nematodirus in caused by binding to GABA-mediated synapses cattle. (Bennett, 1986). In vertebrates, there are GABA The recommended dose to domestic ruminants is mediated synapses only within the central nervous the same 200 ug/kg for all the commercial system. Recent evidence shows that avermectins endectocides for subcutaneous injection and oral also interact to a nematode specific glutamate-gated administration, and 500 ug/kg for pour-on chlorine channel distinct from GABA-sensitive application. Eprinomectin is so far only marketed as chloride channels, which is now considered the a pour-on at 500 ug/kg for cattle. main mode of action (Turner & Schaeffer, 1989; For other animal species the dosage Arena et al., 1995). The chloride ion flux into recommendations vary. The least dose widely used neurones is the probable cause of the observed is that of oral ivermectin against canine heartworm paralysis and death of the parasites. However, these microfilariae, given monthly at 6 ug/kg, while may not be the only modes of action. Because of demodectic mange of dogs is treated with an oral the closely similar chemical structure, antiparasitic dose of 600 ug/kg daily even for months (Ristic et spectrum and cross-resistance, it is likely that the al., 1995) The latter is extra-label use, the mode of action of milbemycins is similar to that of manufacturer does not officially recommend

Rangifer, Special Issue No. 11, 1999 23 ivermectin at high doses for dogs and cats, at least oral liquid, pour-on (topical percutaneous), and partly because ivermectin can cause fatal ruminal sustained-release bolus. Common to all intoxications in dogs, especially collies (Paul et al., these application methods is that as an endectocide 1987). The standard dose in swine is 300 ug/kg the drug is designed to act systematically, so it is against all ivermectin sensitive parasites essential that the active ingredient is absorbed to (Sutherland, 1990). the blood circulation, in any case to get maximum In red deer (Cervus elaphus), the subcutaneously activity against parenteral parasites. administered standard dose 200 ug/kg of ivermectin In one trial, the area under the plasma was found to give insufficient nematocidal efficacy, concentration-time curve (AUC) was 5718 (s.e.m. so the authors recommended doubling the dose 1203) ng*h/ml following subcutaneous injection of (Andrews et al., 1993). However, even the double ivermectin at 200 pg/kg to sheep, and 2039 (231) dose 400 pg/kg did not give efficacy comparable ng*h/ml following oral administration at the same with that of 200 ug/kg in cattle. The low efficacy dose (Maniner et al., 1987). The difference here was associated with pharmacokinetics; the peak was 2.8-fold. The AUC in goats after similar oral concentration and AUC in red deer remained administration was only 516 (81) ng*h/ml (Scott et considerably lower than in cattle. It has been al., 1990). Following sc injection to goats, the AUC reported that pour-on eprinomectin at 500 pg/kg of ivermectin was 1440 (144) ng*h/ml (Alvinerie et has high activity against strongyle parasites and al, 1993). The AUC for ivermectin, doramectin, lungworm in red deer (Gogolewski et al, 1997). and moxidectin in cattle following similar sc Ivermectin has been observed to be extremely administrations of commercial preparations was efficacious against cattle warbles, Hypoderma 10790 (1128), 15048 (744), and 5208 (384) lineatum, close relatives of reindeer warbles. A ng*h/ml (Lanusse et al, 1997). In sheep, the AUC high efficacy of injection was reported at a dose of following sc dosing of moxidectin (2696 (499) 0.2 pg/kg - one thousandth of the recommended ng*h/ml) was slightly higher than following oral dose (Drummond, 1984). Ivermectin pour-on at 2 dosing (2373 (375) ng*h/ml) (Alvinerie et al, pg/kg has also been highly efficacious in the 1998). Based on earlier efficacy studies, the authors chemoprophylaxis of cattle warbles (Hypoderma concluded that there was a relationship between bovis and H. lineatum) (Benakhla et al., 1998). plasma concentration and moxidectin efficacy. Plasma concentration (Alvinerie et al., 1998), Pharmacokinetics and route of application and more specifically AUC, is perhaps the best Pharmacokinetics of ivermectin in domestic explanating factor of the level of endectocidic ruminants has been reviewed by Bennett (1986) and efficacy of a given endectocide in a given animal Steel (1993) and of various ML endectocides by species. This interpretation cannot, however, be McKellar & Benchaoui (1996). The ivermectin expanded between different ML endectocides absorbed to the circulation is almost totally (Table 1) because of their different intrinsic excreted in the bile. Because of lipophility of antiparasitic efficacies. Neither is the efficacy ivermectin, the volume of distribution is large, against intestinal nematodes fully explainable with larger in sheep than in cattle (4.6 1/kg versus 1.9 AUC as these parasites also may encounter the 1/kg) (Lo et al., 1985). The larger distribution proportion of orally given drug that is not absorbed volume causes the plasma concentration to be (McKellar et al., 1991). On the other hand, intrinsically lower and the clearance rate more rapid ivermectin was not detected at all in abomasal fluid in sheep than in cattle. The mean volume of of sheep after sc injection at 200 or even 2000 u distribution in cattle was also quite different for g/kg (Bogan & McKellar, 1988). ivermectin (3.35 1/kg), doramectin (2.92 1/kg), and In the world endectocide literature there were moxidectin (13.6 1/kg), respectively (Lanusse et al, 4436 papers listed until mid November 1998 in 1997). The large distribution volumes (especially CAB abstracts only (CAB International, that of moxidectin) are probably caused by Wallingford, Oxon, UK). Most of them report distribution in adipose tissue. The distribution excellent antiparasitic efficacy of one or more volumes vary a lot between different endectocides methods of endectocide application. Some papers and animal species, thus affecting the plasma also describe trials comparing the efficacy of two or concentrations available for parasites. more of the drugs. Relatively few, by contrast, A lot of commercial endectocide preparations compare the efficacy following various methods of have appeared to be used for different animal application of the same drug in ruminants. species, including man. For ruminants the main methods of application are subcutaneous injection, 24 Rangifer, Special Issue No. 11, 1999 Table 1. Some plasma pharmacokinetic parameters of ML endectocides in different ruminants

Species Drug Dose n Cmax tmax AUC Reference (mg/kg) (ng/ml) (h) (ng*h/ml)

Cattle IVM 0.2 sc 5 54.6 35 10 790 Toutain etal. (1988) Cattle IVM 0.2 sc 4 42.8 96 11 016 Lanusse etal. (1997) Cattle IVM 0.2 sc 4 48.2 72 Herder al. (1996) Sheep IVM 0.2 sc 5 30.8 60 5718 Marrineretal. (1987) Goat IVM 0.2 sc 5 6.12 68 1440 Alvinerie et al. (1993) Red deer IVM 0.2 sc 4 15.8 20 Mackintosh et al. (1985) Red deer IVM 0.2 sc 10 15.3 28 Andrews eta!.. (1993) Red deer IVM 0.4 sc 10 28.3 28 Andrews etal. (1993) Sheep IVM 0.2 po 5 22.0 16 2039 Marriner etal. (1987) Goat IVM 0.2 po 6 16.0 <24 516 Scott et al. (1990) Cattle IVM 0.5 topic 4 28.3 48 Herd etal. (1996) Goat IVM 0.5 topic 6 4.00 48 317 Scott et al. (1990) Cattle IVM SRa 4 10.2 924 Herdef al. (1996) Cattle DRM 0.2 sc 20 27.8 72-144 11 400 Nowakowski et al. (1995) Cattle DRM 0.2 sc 4 37.5 144 15 048 Lanusse etal. (1997) Cattle MXD 0.2 sc 3 75.0 4-6 Miller etal. (1994) Cattle MXD 0.2 sc 4 39.4 7.7 5208 Lanusse etal. (1997) Sheep MXD 0.2 sc 5 8.3 21 2696 Alvinerie etal. (1998) Sheep MXD 0.2 po 5 28.1 5.3 2373 Alvinerie etal. (1998)

IVM ivermectin, DRM doramectin, MXD moxidectin a Sustained release bolus, contains 1.72 g of ivermectin and is designed to release 12.7 mg daily for 135 days.

The small number of direct comparisons of persistent efficacy of sc administration against different application methods in domestic Trichostrongylus colubriformis 21 days after ruminants (sheep) indicate a higher efficacy of treatment but no efficacy 21 days after oral subcutaneous compared with oral application treatment (Kerbouef et al., 1995). Persistent (McKellar et al, 1988a; Zajac et al., 1992). efficacy is well-known from cattle treated sc with Subcutaneously applicated ivermectin had a endectocides (e.g. Barth 1983; Armour et al., 1985; persistent efficacy of at least 10 days against Vercruysse et al., 1997; Meeus et al., 1997; Ranjan Haemonchus contortus, Trichostrongylus vitrinus et al., 1997). In one trial, injectable moxidectin was and Cooperia curticei, but orally administered rather effective against first instars of the ovine ivermectin showed no persistent efficacy nasal bot Oestrus ovis, but oral drench was not (Borgsteede, 1993). A persistent efficacy lasting for (Dorchies et al., 1996). Both the therapeutic and one week was also seen for Ostertagia persistent efficacy of ivermectin injection against circumcincta (Grimshaw et al., 1997). There is a 35 O. ovis were higher than those of oral ivermectin day persistent efficacy against O. circumcincta and (Dorchies et al., 1997). The greater efficacy of sc H. contortus of both orally and subcutaneously injected endectocides is related to pharmaco• administered moxidectin in sheep, and a high kinetics; the bioavailability of ruminally

Rangifer, Special Issue No. 11, 1999 25 administered ivermectin was only 25%, whereas Endectocide resistance that of subcutaneously injected ivermectin was Parasite resistance refers to the recommended dose 100% (Prichard et al., 1985). The initial of drug now removing 95% or less of the resident explanation to the low utilisation of orally parasite population (Hennessy, 1997). Resistance is administered drug was that it was probably now considered a major threat to parasite control metabolised in the rumen, but later evidence world-wide (Waller, 1994, 1997). The first reports indicates that ivermectin is bound to the particles of on ML endectocide resistance in nematodes the digesta (Andrew & Halley, 1996). Anyhow, the emerged within 5 years after the introduction of low bioavailability remains a widely accepted fact. ivermectin in 1981. Resistance has been observed In mountain sheep (Ovis canadensis), injectable mostly in Ostertagia and Haemonchus nematodes ivermectin at 200 ug/kg offered an effective means of small ruminants (Gill & Lacey, 1998). of treating lungworm (Protostrongylus species) Endectocide resistance has been observed also in infection (Miller et al., 1987), but orally Cooperia species in a herd of cattle where oral administered ivermectin at approximately 400 ivermectin had been the only anthelmintic used in ug/kg was ineffective (Easterly et al., 1992). the strategic control programme over the previous There are also reports showing that oral two years (Vermunt et al., 1995). Generally, factors application of ivermectin had superior anthelmintic contributing to anthelmintic resistance include efficacy when compared with subcutaneous frequent treatment and under-dosing, while injection. One was in goats and another in alternating between different anthelmintic groups dromedary camels. In goats, the report describes a will slow down the establishment of resistance faecal egg count reduction test showing 94% (Waller, 1990). So far, there are no reports on efficacy of ivermectin injection at 200 ug/kg, endectocide resistance in reindeer parasites; the low compared with 100% efficacy for ivermectin oral efficacy of ivermectin against the brainworm E. formulation, obviously at the same dose rate. No rangiferi is not a sign of resistance as ivermectin details were given on the group sizes. It was has never been regarded as effective against this discussed that Trichostrongylus spp. might have parasite. After treatment of an animal with been the predominant nematodes in the goats endectocides, declining drug levels over time will (Pearson & Rutherford, 1988). In dromedary allow establishment of resistant infective larvae, camels, trichostrongylid egg counts were reduced while still eliminating susceptible larvae. To by 100% when ivermectin was administered orally elucidate the population-level importance of these and by > 88% when given subcutaneously, both at resistant larvae, computer simulations have been the dose of 200 ug/kg. Egg counts of Trichuris sp. performed. The results from such simulations were reduced by > 85% with oral administration, indicate that adult survivors of treatment have much but increased following subcutaneous treatment greater importance than selection of infective larvae (Boyce et al., 1984). In both these cases the by decaying drug concentrations (Dobson et al., parasites in question appear to have been intestinal 1996). The persistent efficacy of endectocides is nematodes which may be affected also by the favourable in preventing resistance, because more unabsorbed fraction of orally given ivermectin. persistent drugs will remove resistant adult parasites more effectively. As anthelmintic Topical pour-on administration of ivermectin to resistance does not disappear spontaneously, it is cattle at a dose of 500 ug/kg has been shown to important to try to prevent its initial establishment cause high antiparasitic therapeutic and persistent (Waller, 1990). activity (Alva-Valdes et al., 1986; Yazwinski et al., 1994; Williams & Broussard, 1995). Also insects may become resistant to Pharmacokinetic studies, however, show that the endectocides. In a trial with house flies resistance maximum plasma concentration and the AUC against abamectin developed rapidly and to a very following such a treatment are smaller than those high level (60 000-fold) (Scott et al., 1991). So far following subcutaneous administration despite the there are obviously no reports on endectocide 2.5-fold dose (Herd et al, 1996). In goats, resistance in oestrid parasites, but there is no reason subcutaneous ivermectin at 200 ug/kg lead to an to believe that development of resistance would not AUC 4.5-fold that after topical administration at be fully possible. 500 ug/kg (Scott et al, 1990; Alvinerie et al., 1993). Gains of endectocidic treatment in domestic ruminants Because of the high antiparasitic efficacy of the ML endectocides, it is not surprising that different

26 Rangifer, Special Issue No. 11, 1999 treatment programs have been observed to increase for example to accidental leaks during production meat production (e.g. Suarez et al, 1991; Baggott or delivery. et al, 1994; Williams et al, 1995) or milk production (Ploeger et al, 1989; Walsh et al, Ivermectin in reindeer 1995). In all of these five papers, pharmaceutical Because antiparasitic treatment of reindeer was a industry is represented, either as authors or subject of common interest (Nieminen et al, 1980; acknowledged, which does not reduce the value of Rehbinder et al, 1981; Persen et al, 1982) at the the individual papers, but indicates that animal time of the introduction of ivermectin, it was health companies have interest in this kind of natural that ivermectin given as a sc injection at the research. Therefore, publication bias appears dose 200 ug/kg was immediately to be evaluated as possible, perhaps some studies with undesired an endectocidic antiparasitic to reindeer. In results of treatment have remained unpublished. Sweden, a trial was done with 37 reindeer calves to compare the efficacy of four antiparasitics Environmental aspects (ivermectin, fenthion, fenbendazole and The possible adverse effects ML endectocides mebendazole) against warbles, throat bots, might have to dung degradation fauna have raised brainworms, lungworms and abomasal and much concern. After the first study (Wall & Strong, intestinal nematodes (Nordkvist et al, 1983). 1987), discussion has been lively. A number of Ivermectin was 100% efficient against warbles, studies have been performed on the degradation of throat bots, lungworms and abomasal and intestinal cattle dung from ivermectin treated animals. Most nematodes (Nematodirus species). The efficacy scientists have found that degradation is retarded against brainworm larvae was lower. This is and insect fauna disturbed in dung following concomitant with results from white-tailed deer ivermectin treatment (e.g. Strong, 1993; Holter et (Kocan, 1985). Fenthion had 100% efficacy against al, 1994). Researchers affiliated to Merial (former throat bots and 86% against warbles, but no MSD) have stressed the importance of methodology efficacy against nematodes, while the when planning such studies (e.g. Barth, 1993). benzimidazoles fenbendazole and mebendazole They showed that in addition to diptera and beetle were 100% efficient against brainworm larvae and larvae, treatment reduced the numbers of dung moderately-highly efficient against other specific nematodes. However, they did not see nematodes. The benzimidazoles had no efficacy retardation in dung degradation (Barth et al, 1994). against warbles or throat bots. The high In a comparison of sustained release bolus, pour-on antiparasitic efficacy of ivermectin was confirmed and subcutaneous injection ivermectin treatments, it in the next trial, performed in 1982-83 (Nordkvist was found that maximum concentration (2 days et al, 1984), which also showed a smaller weight post treatment) in the faeces of pour-on treated loss during winter in ivermectin treated reindeer animals was 12-fold higher than of the sc injected calves than in non-treated ones. To gain approval animals, but after one week the concentrations by the United States Food and Drug Administration declined at a similar rate. The animals treated with (FDA) for ivermectin to be used in reindeer, a a sustained release bolus, by contrast, produced series of trials was performed in Alaska in 1982-83 faeces with a high ivermectin concentration till the (Dieterich & Craigmill, 1990). Ivermectin was end of the trial, 7 weeks post treatment. Both the considered safe to reindeer and efficient against sustained release bolus and pour-on treatments warbles, and the tissue residues decreased rapidly, were considered more ecotoxic than the sc injection approaching zero by day 24. Based on these data, as judged by their higher faecal ivermectin the FDA established a 56 day withholding period concentrations (Herd et al, 1996). This is not (double that of cattle). The next reported trial was surprising, because the total treatment doses are initiated in 1984 in Norway. The live weight of higher. Oral ivermectin formulations were regarded reindeer calves about six months of age, treated as least ecotoxic due to the rapid excretion (Herd, with ivermectin during the autumn increased during 1995). the subsequent year on average 3 kg more than that of similar untreated animals (Heggstad et al, Apparently, no life cycle assessment (LCA) (e.g. 1986). In December, 1990, eighty reindeer calves Consoli et al, 1993) of these compounds/drugs were ivermectin treated in Kautokeino, Norway. In have been published, but obviously, the less the February, 14 of these treated and 19 control calves use, the less the production, and the less the were slaughtered. The efficacy against throat bots environmental concern due to the manufacturing, was 100% and against the sinus worm, Linguatula and the less the risks of environmental damage due arctica, 98% (Haugerud et al, 1993).

Rangifer, Special Issue No. 11,1999 27 The arctic and subarctic dung degradation fauna negligible, because the winter faeces from lichen- can be expected to be less tolerable than that of fed animals did not attract insects during the next more temperate regions. The concern on the summer regardless of ivermectin treatment, possible negative effects of ivermectin treatment obviously due to its nutrient-poor and dry structure. has been discussed in Norwegian newspapers (e.g. The difference in antiparasitic activity of the Berg 1991). Recently, a method was developed to various endectocides and their various formulations analyse ivermectin residues in reindeer faeces in domestic ruminants makes it necessary to (Asbakk et al., 1999), and one trial was done to compare the activity in reindeer, where high investigate the degradation fauna of reindeer faeces efficacy against insect parasites is required. after sc ivermectin injection (Nilssen et al., Because of the inhibited development of hypobiotic submitted). Although measurable concentrations nematode parasite larvae during the time of could be shown in faeces produced for 30 days post treatment (Nordkvist et al., 1984), there are also treatment, the impact on dung insect fauna was special nematocidal efficacy requirements.

28 Rangifer, Special Issue No. 11, 1999 Materials and methods Aims of the research Study design The aims of the present study were: Most of the trials described in these publications were designed for aim #1 (Table 2). Trial I 1. To find ways to optimise the current compared the antiparasitic efficacy of oral (as the endectocidic antiparasitic treatment methods of equine paste formula) and subcutaneous reindeer, taking into account the efficacy of the administration of ivermectin against nematodes and treatment and economical as well as ecological warbles. Work III added pour-on ivermectin, and considerations. The goal was thus to look for the efficacy was also measured against throat bots, best drug and the best way of administration as well according to the method described in paper II (aim as the ideal timing. #2). Paper IV used chemical analyses to explain the differences in antiparasitic efficacy discovered in 2. To develop research methods needed to fulfil trials I and III. Trial V was designed to evaluate a the aim #1. new drug, moxidectin, as a reindeer endectocide. Publication VI described the insecticidic efficacy 3. To investigate, whether summer treatment (against warbles and throat bots) of doramectin in against subclinical infections of calves to be reindeer. Paper VII compared the antiparasitic slaughtered in the autumn might be economically efficacy of oral ivermectin given at different times feasible.

Table 2. Experimental animals and their endectocide treatments.

Paper Untreated group IVM inj. IVM oral IVM topical Other Year 200 ug/kg 200 ug/kg 500 ug/kg treatment

I Aa31(28)b A 31 A 30 (29) 1989-90 n C8 1991 IE A13 A 13 (12) A13 A13 A 13 (10)d 1990-91 IV C5 C5 C4,A6,C5 1991,1993 V A14 (13) A14 A 14(13)e 1991-92 VI A 20 (19) A20f 1994-95 VII A 18 (16) A54(51)g 1995-96 Vin C 177 (75)(8)c C 177 (59) (9) C 175 (62) (9) 1995 a A=adults, C=calves b the number in parenthesis is the final sample size after exclusion of missing animals. L counted alive (breeding replacements). d IVM injection 20 ug/kg,e MXD injection 200 ug/kg,f DRM injection 200 ug/kg, g oral IVM 200 ug/kg either in September, December, or February. IVM ivermectin, DRM doramectin, MXD moxidectin.

Rangifer, Special Issue No. 11, 1999 29 during the autumn or winter. ug/kg (I, HI, IV, VII). Topical pour-on treatment Papers I, HI, V, VI and VII include development was given under the hair coating over the back of methodology to evaluate efficacy against between the shoulder blades ("spot-on") at a dose hypobiotic nematode parasites (aim #2). of 500 pg/kg (III, IV), or as a narrow strip along the One trial (VIII) was performed exclusively for back from withers to the base of tail at the same aim #3. dose rate (IV, VHI). The untreated controls were given no placebo (I, in, V, VH, VHI) or were given Animals and experimental design physiological saline at 1 ml/50 kg sc (VI). Most of the experiments (I to VII) were done in the To investigate the possibilities of endectocides Kaamanen Experimental Reindeer Herd of the used as «growth promoters* in reindeer calves, 529 Finnish Association of Reindeer Herding Co• calves from two herding co-operatives (Palojarvi operatives in Kaamanen, Inari (69°09'N, 27°00'E) and Kemin-Sompio) in Finnish Lapland were during the winters 1989-1990 to 1995-1996. Most allocated systematically to three groups during ear• trials used naturally infected adult hinds (females) marking in July, 1995. One group was left (I, HI, V, VI, VII), but in two trials, also males were untreated, the other was injected subcutaneously included (I, VI). If animals were to be slaughtered, with ivermectin at 200 pg/kg and the third received yearlings were used (II). If frequent blood sampling pour-on ivermectin topically at 500 pg/kg. Carcass was required (III), reindeer calves about 8 months weights of animals slaughtered during the autumn old were used, in addition to Norwegian adult or winter were then compared between treatment reindeer and Swedish yearlings (see below). All groups (VIII). experimental animals were individually marked, either with numbered collars or ear tags, or both. It Examination for adverse reactions is a routine in Kaamanen to gather the herd monthly Because both the standard injection and oral for weighing and occasional blood sampling. There applications of ivermectin had been used in are slightly over 100 hinds in the herd, the number reindeer husbandry and also experimented with in of calves varies a lot between years. The area for the Kaamanen herd (Soveri et ai, 1990), no the herd is about 43 km2 of pine and birch forests specific follow-up for adverse reactions was and fells (Nieminen, 1998). undertaken in the first trial (I), but the animals were The hinds were allocated to the groups using observed in connection with other animal stratified randomisation according to age (I, HI, V, management tasks. In trial (in) with the new topical VII), or just randomically by lot (VI). The calves ivermectin treatment, the animals were released were allocated according to sex and weight (IV). after treatment into an outdoor enclosure where The group size varied between 10 (HI) and 31 (I). they were observed at times for 24 hours. A similar Paper (IV) described three trials; A, five yearlings follow-up for adverse reactions, but of different from Konkamo, Sweden; B, six adult reindeer from durations, was undertaken following moxidectin Dielddasuolo (Tjeld0y), Norway; and C, three and doramectin treatments (V, VI). Were animals groups of five calves each in Kaamanen. found dead due to unknown cause during the experiments, they were autopsied, if possible. Endectocide treatment The endectocidic treatments were performed in Faecal examination for nematode eggs or larvae December (I, HI, V, VI), in November, January or To facilitate the evaluation of nematocidal efficacy, May (IV), in September, December or February faecal egg counts (FEC) were done. The nematode (VII), or in July (VHI). The drugs used were eggs were identified to the genus Capillaria if they ivermectin, Ivomec® 10 mg/ml vet inj., MSD were rough-shelled, about 50 pm in length, dark- (Merial) (I, HI, IV, V, VIH), Ivomec® vet 18.7 mg/g stained, of barrel shape and with slightly protruding pasta (=Eqvalan® paste), MSD (I, in), Ivomec® vet polar plugs, to the genus Skrjabinema if they were mixt. 0.8 mg/ml, MSD (VII), Ivomec® pour-on for typical to the genus: about 50 to 70 pm long, thin- cattle, MSD (III, IV, VHI), moxidectin, Cydectin® shelled and markedly asymmetrical (rather like an 1% vet inj., American Cyanamid (Fort Dodge) (V), orange section), or as trichostrongylids if they were or doramectin, Dectomax® 1% vet inj., Pfizer (VI). indistinguishable from those of the family Subcutaneous injections were given in front of the Trichostrongylidae: oval or ellipsoid, not markedly left shoulder (lateral midline of the neck) at a dose asymmetrical, thin-shelled and length 60 to 100 of 200 pg/kg (I, III, IV, V, VI, VD1) or similarly at a pm. As the trichostrongylid egg counts were dose of 20 ug/kg (III). Oral administration was expected frequently to be negative due to given over the base of tongue at a dose of 200 hypobiosis at the time of treatment in midwinter, 30 Rangifer, Special Issue No. 11, 1999 faecal examination was performed several times Chemical analysis during winter and spring. The FECs were done with To help explain the difference in antiparasitic modified McMaster technique using saturated NaCl efficacy, plasma concentrations were measured solution with sucrose (Christensson et al., 1991), from reindeer calves treated with ivermectin each egg observed representing 40 epg (I, JJT) or 20 administered in different ways (IV). The analyses epg (V, VII). The individual monthly tricho- were performed by Merck Research Laboratories, strongylid FECs were used to calculate Faecal Egg Lauterbach, Germany, using a HPLC (high pressure Count Mean (FECM) (V, VII). Microphotographs liquid chromatographic) method with fluorescence of parasite egg specimens are presented in detection (Downing, 1989). Appendix 2. Brainworm and lungworm larvae were examined Statistical analysis according to a Baermann technique (Holmstrom et Faecal egg counts (FECMs) and animal weights al., 1989) (I, ffl). Larvae were identified as those of were compared by one-way analysis of variance. If the brainworm, Elaphostrongylus rangiferi, if they the group effects were statistically significant (P< were of the proper size (0.3 to 0.4 mm) and had one 0.05), Tukey test was used for pairwise comparison cuticle and the characteristic dorsal spine over the of the group means. In paper VIII, Student's t test, tail. Similar sized larvae with one cuticle, but % test, Mann-Whitney test, and one-way analysis of without the dorsal spine over the tail were classified covariance were performed. The number of warbles as those of the lungworm, Dictyocaulus sp. and throat bots differed so much between treatment (Dictyocaulus eckerti). groups (treatment efficacy often 100%) that it was usually not tested at all. However, in one trial (VI) Warble and throat bot examination the proportion of animals infested with warbles and Warbles were counted as described earlier throat bots was compared by x test. In paper VHI, (Nordkvist, 1967; Dieterich & Craigmill, 1990). In Mann-Whitney test was used to compare the late March - early May, when the larvae had number of warbles. To compare the weights of reached the 3rd instar stage, but before a calves born to hinds treated with untreated controls considerable amount of them had left the host during the different years, Kruskal-Wallis one way (Nilssen & Haugerud, 1994), the backs of the analysis of variance was used. The statistical experimental reindeer were examined visually and analyses were carried out using the Statgraphics® by digital palpation (I, III, V, VI, VII). If the 2.6 program package or the Statistix® software number of warbles exceeded 30, the count was package, either version 3.5, 4.0, or 4.1. One-way done in tens as adjacent warbles might blend analysis of covariance was done with BMDP together and prevent exact enumeration. software. Warbles from the calves slaughtered in January were counted by visual examination of the inside of the skin (VIII). Results The endoscopy method for counting throat bots (JJ) was used in late April or early May (III, V, VI, Adverse reactions VH). No adverse reactions were noticed following any of Animal weighing the ML endectocidic treatments administered in any The Kaamanen reindeer were weighed using an of the various ways of application. The single ovine balance modified to enable the weighing of autopsied animal showed no signs of tissue reindeer (Poldenvale lambway, Precision Weighers, irritation at injection sites. The death was not Reading, England, 1 kg reading intervals) (I, HI, IV, associated with endectocide treatment. V, VI, VH). The new-born calves were weighed within 24 hrs of birth (spring balance, 100 g Efficacy against nematodes intervals) (HI, V, VII). Other than Kaamanen No effect of ivermectin or moxidectin treatment animals were weighed using available apparatus. could be seen against the sporadic Skrjabinema egg The calves in paper VHI were in the trial start production (V). The eggs were found only in April weighed on a standard bathroom balance (1 kg and May, 4 to 5 months post treatment. The reading intervals), and their carcass weights were question remains if the treatment however had had taken from the slaughter records. efficacy, and the egg production was caused by reinfection. In study I, both oral and injected ivermectin reduced the Capillaria egg production. In trial HI, this post-treatment reduction could be

Rangifer, Special Issue No. 11, 1999 31 seen in all the groups, including the untreated the efficacy against throat bots was 92% (IH, data control group. In trial V, both moxidectin and not fully shown). Injectable doramectin at 200 ivermectin appeared to reduce the Capillaria egg pg/kg had 100% efficacy against both warbles and production, but the difference in the egg counts was throat bots (VI). Moxidectin at 200 pg/kg had 93% not significant. In trial VII, Capillaria eggs were efficacy against warbles and 71% against throat detected so infrequently, and in so small numbers, bots (V). that they were totally omitted from the paper. The persistent (prophylactic) efficacy of injected There was a statistically non-significant (200 pg/kg) or pour-on (500 pg/kg) ivermectin reduction of lungworm larva production in animals reduced the number of warbles in hides of reindeer treated with ivermectin. The reduction was more calves treated in midsummer by about 60%. pronounced following injection than oral administration (I). In study HI, the lungworm larva Pharmacokinetics output followed the same pattern as in trial I: the Plasma concentrations were constantly higher in larvae were absent from the samples of February, reindeer calves given ivermectin as sc injection and the mean value remained low (it only equalled than in those that received it either orally or as or exceeded 1 lpg in the orally treated and control pour-on (IV). The mean maximum concentration groups in May). The difference between the following standard sc treatment was about 5-fold treatment groups was not statistically significant, that of the orally treated animals. The concentration but the average larva production was lowest in the also decreased more slowly following sc treatment; standard (200 pg/kg) injection group. The number after 7 days the difference in concentrations was of brainworm larvae in faeces (I, HI) was so low 14-fold between the injection and oral groups. The and their excretion so sporadic that no calculations mean maximum concentration after topical on treatment efficacy were justified, but efficacy treatment varied much between the three trials, the was definitively not very high. highest one was in the animals treated in May Trichostrongylid FEC was reduced by both the (about one third of that of the standard sc treatment sc and oral treatments in trial I. Egg output was first in January). The lowest mean maximum observed in the untreated control group, and concentration was in the animals treated in January followed in successive intervals by the orally (about one twenty-fifth of that of the standard sc treated group and the injection group. The FEC was treatment). No AUC was calculated due to the significantly lower in the injection group than in the small number of sampling times, but it was clearly untreated group in March and June, and in the much larger following sc injection than other injection group than in the oral group in April. No treatments, despite the higher dose given topically. Faecal Egg Count Means (FECM) for individual animals were calculated in this trial. Weight development Similar reduction in trichostrongylid egg output In the first trial (I), the (mostly pen-fed) animals was seen in the next study (in). Egg production of gained weight during the winter, the untreated the standard injection group was first observed in group 4.8 (s.e.m. 1.1) kg, compared with 5.5 (1.3) April, a month later than in the other groups. The and 8.8 (1.5) kg, respectively, for the orally and FECMs of the standard injection group were injection treated hinds. The difference was not significantly lower than those of the other groups. significant in ordinary one-way analysis of The standard sc injection reduced the FECM by variance, but using the treatment as a continuous 80%, both oral treatment and 20 pg/kg injection by variable (0, untreated control; 1, oral treatment; 2, 39%, and the topical pour-on application by 35%. sc injection) the effect of treatment became Injectable moxidectin and ivermectin reduced significant. In the next study (HI), weight loss was the trichostrongylid FECM by 92% and 95%, observed in all the groups between the time of respectively (V). treatment and early April, with no significant In trial VH, oral ivermectin (Ivomec® vet mixt. differences between the groups. In the trial with 0.8 mg/ml, MSD) reduced the trichostrongylid moxidectin and ivermectin injection (V), the mean FECM by 62 to 74%. weight gain between December and April was highest in the untreated group, 1.8 (1.5) kg Efficacy against warbles and throat bots compared to 1.0 (0.8) and 0.8 (1.3) for moxidectin All ivermectin treatments in autumn/winter at 200 and ivermectin treated animals, respectively. The or 500 pg/kg were 100% effective against warbles difference between the groups was not significant. and throat bots (I, HI, V, VH). Injectable ivermectin at 20 pg/kg had also 100% efficacy against warbles, 32 Rangifer, Special Issue No. 11, 1999 Table 3. Mean birth weights (s.e.m.) of reindeer calves born to differently treated Kaamanen hinds.

Study nr. Birth year Untreated control IVM inj. 200 pg/kg Other treatment December HI 1991 5.14(0.32) 5.51 (0.23) 5.53 (0.17)a 5.45 (0.30)b 5.55 (0.25)c V 1992 5.24(0.21) 5.63 (0.29) 5.55 (0.25)d VI 1995 5.79(0.25) 5.47 (0.28)e VH 1996 5.69(0.26) 6.22 (0.26)f 6.65 (0.22) b 6.42 (0.29)8 a IVM injection 20 pg/kg December, IVM oral 200 pg/kg December. IVM topical 500 pg/kg December, MXD injection 200 pg/kg December. : DRM injection 200 pg/kg December, IVM oral 200 pg/kg September. '' IVM oral 200 pg/kg February.

If two extreme weight gain/loss values were Cmax was reached about 1 day after subcutaneous omitted as outliers, the weight gain of the control injection at 200 pg/kg, but in reindeer about 3 days group was 0.5 (0.9) kg, compared to 1.0 (0.8) and after similar treatment. The low plasma 1.7 (1.0) kg for moxidectin and ivermectin treated concentrations in red deer were also associated with animals. In hinds treated orally (Ivomec® vet mixt. insufficient antiparasitic efficacy (Andrews et al., 0.8 mg/ml, MSD) at different times (VII), the mean 1993). weight gain/loss of the groups of hinds varied between a loss of 2.6 kg and a gain of 1.6 kg, the Study methods untreated controls lost 0.1 kg. In the current studies, the treatment efficacy No difference was seen in slaughter weights determination against warbles and throat bots was between reindeer calves treated with ivermectin based on direct parasite counts, which is the most during the summer and those untreated (VIII). reliable basis of efficacy calculation, and thus the method to be recommended (Wood et al., 1995). Birth weights These experiments (III, V, VI, VII) have apparently The mean weight of calves born to treated animals been the first utilisation of the endoscopic method was often higher than that of untreated controls for detecting throat bots in live reindeer (II). The (Table 3). However, the differences between inspection requires special equipment (human treatment groups were not statistically significant. fibreoptic bronchoscope), but, apart from that, is quick, simple and relatively easy to perform. The examination takes generally less than one minute Discussion per animal, and most often the animals do not react to the insertion of the bronchoscope. The necessity to study endectocides in reindeer Because of limited funding, animals could not The differences reported in endectocide efficacy, be slaughtered, so it was essential to be able to use and especially pharmacokinetics (Table 1), between FEC as an indirect measure of nematode parasite various animal species makes it impossible to burden. As the treatments were performed during reliably extrapolate efficacy and pharmacokinetics winter when nematodes are hypobiotic and start to expectations from other ruminants. The closest produce eggs only months later, the common relative to reindeer to which pharmacokinetics data practice of performing FEC reduction test 1-3 was available is the red deer. In this species, the weeks post treatment (e.g. Coles et al., 1992) could C ax m was low, about 15 ng/ml, as compared with not be applied. The spring FECM used in the about 44 ng/ml in reindeer (trial IV). In red deer the Rangifer, Special Issue No. 11,1999 33 current trials has the drawback that reinfection The sc injection at 20 pg/kg in trial III was chosen cannot be excluded as a source of parasite burden to be a dose clearly smaller than the registered one. in any individual animal, or even a group of The broad spectrum of ML endectocides gives animals. However, if the comparison of FECMs can reindeer owners, and especially reindeer show difference between treatment groups, given veterinarians, a new responsibility when compared that the groups are otherwise similar, this difference to insecticide treatments. As the endectocides have has to be caused by differences in treatment high efficacy against various nematode parasites, efficacy. Reinfection can only diminish the the treatment creates a selection pressure on the differences, and the reductions in FECM may be nematode fauna. Some of the reindeer nematodes, smaller than the actual antiparasitic efficacy. like those from other cervids, may also be shared Therefore the differences observed tend to be with domestic ruminants (Nilsson, 1971; conservative estimates. Borgsteede, 1982; Bye & Halvorsen, 1983). The McMaster technique (Christensson et ah, Frequent use of the drugs increases the risk of the 1991) as it was used in the first trials (I, III) had a rise of resistant nematode strains. Even though sensitivity (40 epg) that was later considered reindeer treatment cannot currently be considered suboptimal because of the rather low FECs frequent, it is important to minimise also other common in reindeer during the winter and spring. factors that might favour endectocide resistance. Therefore the technique was modified so that each One of the best-known of them is underdosage egg observed represented 20 epg. The change (Waller, 1990), i.e. treatment that does have lower increased the laboratory work needed, but it killing efficacy than expected. Obviously, the higher the efficacy, the better. increased even more the value of the examination. Together with the calculation of FECM based on In reindeer, probably only intestinal nematodes, several samples, probably a fair measure of the such as Nematodirus, Nematodirella, Capillaria, gastro-intestinal nematode burden was achieved. and Skrjabinema. may be significantly affected by the unabsorbed fraction of orally administered ML Endectocide treatment of reindeer is different from endectocide. The importance of these parasites to domesticated ruminants reindeer health is unknown. Abomasal nematodes The treatment of reindeer with ML endectocides is living in close connection to abomasal mucosa different from their most common use in domestic probably are very little influenced by the drug ruminants as the treatment is directed against both concentration in the bypassing digesta. To ensure insect and nematode parasites. In domestic maximal efficacy of ivermectin treatment against ruminants endectocides are mostly used against warbles, throat bots, sinus worms, lungworms, nematode parasites, in fact they are often referred to abomasal nematodes, brainworms and other as «anthelmintics» in this context. The other use of nematodes, such as Setaria, Onchocerca and endectocides is as an insecticide in herd level or Lappnema, the drug should be given so that larger control programs, e.g. against lice or bovine maximal AUC is achieved, as standard sc injection. warbles. Seldom can the broad spectrum of the It is known that ivermectin treatment decreases compounds be utilised as thoroughly as in the the fertility of surviving (resistant) nematode yearly strategic antiparasitic treatment of reindeer. females (McKellar et ah, 1988b; Le Jambre et al., 1995). Because no animals were killed following Endectocidic efficacy of different ways of treatment in the current studies, actual worm counts application could not be performed. It is therefore not known Antiparasitic treatment of reindeer with ML whether the trichostrongylid gastrointestinal endectocides is a sequel to the organophosphate nematodes were killed after ivermectin (or treatment against warbles and throat bots started in moxidectin) injection or not. However, the time lag Finland in the 1970's. Killing warbles and throat between the treatment and the first recording of egg bots with the current ML endectocides is easy; from production was so long (> 3 months) that a the treatment protocols tried, only moxidectin at reversible reduction in fecundity would perhaps 200 pg/kg did not kill all warbles. The low dose of already have receded. The prepatent period, time ivermectin at 20 pg/kg killed all warbles, but did from infection to the start of egg production, of not have complete efficacy against throat bots. various Ostertagia spp. is about three weeks The endectocide doses used in the current trials (Soulsby, 1982), so, reinfection might well explain are those used in other ruminant species, too. The the trichostrongylid egg production in April-May. sc ivermectin injection at 200 pg/kg is also hi any case, the efficacy of sc ivermectin injection officially registered for use in reindeer in Finland. has been unmistakably superior to that of the other

34 Rangifer, Special Issue No. 11,1999 administration methods. The difference in FECs overwintering population is in the reindeer host. If clearly indicates that oral and topical ivermectin did it was possible to once treat all reindeer, total not have desired nematocidal efficacy. Orally eradication of these parasites would be just a matter applicated ivermectin is mostly adsorbed to ingesta, of antiparasitic efficacy of the treatment, which is and goes therefore into dung. Topically applicated very high for subcutaneously administered ivermectin is very uncertainly absorbed, which may ivermectin. However, all the reindeer are virtually be associated with the thick haircoat and hollow impossible to find during any winter. Moreover, the hairs (Timisjarvi et ai, 1984). wild reindeer populations could still serve as a Unfortunately, market economics strongly affect reservoir. Even though the reindeer husbandry the pricing of different ivermectin preparations. For locally could agree that getting rid of these example in Norway, where both injection, oral nuisances would be a common benefit, such paste, oral mixture and pour-on preparations are agreement would probably not be accepted in all available, a treatment dose (200 pg/kg as injection the reindeer herding areas. The adult flies when or given orally and 500 pg/kg as pour-on) to a 50 attacking reindeer are said to help to collect the kg reindeer calf will cost NOK 8.11 (~EUR 0.94) as animals in flocks (e.g. Nilssen & Haugerud, 1994), sc injection, NOK 12.10 as equine paste, NOK 8.59 which is needed for the ear-marking in the summer. as pour-on, and only NOK 3.72 as oral mixture Some reindeer herders refuse to believe that the (Galligani etal., 1996). The latter price is obviously flies would be totally unnecessary and only harmful so much lower to enable it to compete with for reindeer. People who have lived long with the benzimidazoles as an ovine anthelmintic. The animals may understand that the evolution of the active ingredient is cheapest as pour-on, to symbiosis between the reindeer and its parasites to compensate for the higher dosage; pour-on at 200 the current stage has taken a long time; the parasites pg/kg would cost NOK 3.44 for the same 50 kg are part of the natural biodiversity and should animal. therefore not be eradicated.

Parasite adaptation to the Arctic Economic feasibility Although trichostrongylid eggs cannot be positively Only one of these studies (VIII) was designed to identified to species or even genus, in reindeer measure economic benefit of endectocidic faeces they are mostly Ostertagia gruehneri (Bye, treatment to reindeer, and that trial investigated 1987; Fruetel & Lankester, 1989). The reindeer summer treatment of calves, which is not currently trichostrongylids appear to be well-adapted to the practised in reindeer husbandry. In that trial, no arctic climate by hypobiosis; the development is increase in slaughter weights could be sustained so that egg production is ceased in mid• demonstrated. Because of the rather big sample winter, which obviously saves both the parasites size, it appears very unlikely that the result would and the host. The parasite does not waste energy in have been caused by error alone. All the winter reproduction when the eggs would be deposited on treatment trials were done in the Kaamanen herd, snow, where their chances of development might be which might differ from commercial co-operative small. The host, in turn, would be unnecessarily herds in terms of nutrition and parasitism. stressed by parasite activity in midwinter when food However, it is interesting to note that significant is scarce. It appears that the reindeer Capillaria differences in weight development between parasites do not follow the same pattern, but treatment groups were only seen in one trial (I), and produce eggs in mid-winter. Later, however, the even then not in ordinary analysis of variance. The egg production might decrease, while that of differences in calf birth weights between groups in trichostrongylids increases. The Capillaria pattern trials HI, V, VI and VII were not significant, either. is not as clear as that of trichostrongylids, and the This does not prove wrong the view expressed by factors behind are unknown. many reindeer owners that ivermectin treatment enhances the condition of reindeer and helps the Eradication? animals to survive over winter and produce healthy In many countries, eradication programs have been offspring. However, the lack of significant weight established against cattle warbles (H. bovis and H. gain effects of endectocide treatment indicates that lineatum) These programs are based on the such effects might be dependent on other factors, common conclusion that warbles harm the cattle such as crowding and nutrition. Such management industry enough to justify the costs of the differences may at least partly be the cause of the campaigns (e.g. Tarry et al., 1992). It is common to difference in results in weight gain studies of both reindeer warbles and throat bots that the total reindeer calves following summer antiparasitic

Rangifer, Special Issue No. 11, 1999 35 treatment. Unlike in trial VIII, in the two trials VII might indicate that the active ingredient of the reported from Kaamanen, summer antiparasitic oral ivermectin mixture could be better bioavailable treatment increased the weight gain. Both of those than that of the equine ivermectin paste. That trials were done with a relatively small amount of possible difference might be caused by the mixture animals, so the results may be erroneous. However, bypassing the rumen, as it has been shown that the it appears logical to think that year- and husbandry- biovailability of abomasally applicated ivermectin related differences in parasite burden may have is far higher than that of ruminally applicated. If been the major source of difference in results. This such bypass exists, it should obviously be utilised should get practising veterinarians cautious in thoroughly when ivermectin is administered orally advocating treatment. Both the existing scientific to ruminants, as is now common in sheep industry. results and the costs of treatment should be To assess the relative economic importance of considered. Perhaps in some cases a good various reindeer parasite groups, narrow-spectrum alternative to treatment would be not to treat. After antiparasitics should also be experimented with. all, reindeer meat is, and is expected to be, a natural Benzimidazole compounds do not have insecticidic product, and chemical antiparasitics do not fit well efficacy, so they could be used as anthelmintics, into this image. Ivermectin residues were found in while some insecticides, such as fenthion do not the liver of one reindeer of 35 randomically have anthelmintic efficacy. selected for control by the Finnish National If the nematocidal efficacy of doramectin Veterinary and Food Research Institute in 1997 eventually proves to be equal to that of ivermectin, (Aalto etal., 1998). doramectin is a good alternative in reindeer endectocidic treatment. Based on the knowledge Timing from other animal species, this would not seem It seems that the current «treat them when you catch unlikely. However, it would be wrong to assume them» timing of the endectocide treatment is fully efficacy based on other animal species, so the adequate. Parasites can be effectively treated nematocidal efficacy has to be tested. anytime during the winter although nematodes are Some of the currently commercially available hypobiotic and oestrid fly larvae develop slowly. ML endectocides have not been tested in reindeer at Similar antiparasitic efficacy and small and non• all. Abamectin is obviously a better nematocide significant differences in weight gain/loss and in than insecticide, which might be a benefit in birth weights between groups treated either in reindeer treatment. The interest in under-dosage September, December, or February (trial VII) would be reduced, if its consequences were seen as indicate that the timing of endectocide treatment of warbled animals. However, for abamectin to be reindeer is not critical. useful its insecticidid efficacy should be higher than that of moxidectin. If eprinomectin (as pour- Future research on) is absorbed through the reindeer skin as it is Future research challenges are many. The low designed to do through the bovine skin, it might be insecticidic efficacy of moxidectin in reindeer a good endectocide to reindeer. The general requires an explanation. Was it caused purely by the concern of wasting the active ingredient applies lower intrinsic efficacy of moxidectin against also to reindeer, but not necessarily more than to insects, or did the drug perhaps not reach the cattle. Perhaps eprinomectin also will be marketed parasites? To clarify this, pharmacokinetics of as an injection sometimes, and possibly there will moxidectin in reindeer should be studied. Those be other ML endectocides marketed in the future, studies might also help to understand other too. All of them will apparently have similar mode differences, perhaps still unnoticed. For example it of action, and therefore also cross-resistance will is not known how the nutritional status of animals, exist if it first has been established. To minimise reindeer or other, affects the pharmacokinetics and the risk of endectocide resistance alternative antiparasitic efficacy of ML endectocides. antiparasitic methods should be investigated. Pharmacokinetics of ivermectin in reindeer also need to be worked on further. The results from trial

36 Rangifer, Special Issue No. 11, 1999 the works had already been published, found out the Conclusions possibility to combine them to form this dissertation. He agreed to be my supervisor and suggested Subcutaneous administration additional work to deepen the knowledge of the To direct the endectocide against important economical significance of antiparasitic treatment to parasites, maximal bioavailability of the drug is the reindeer husbandry. needed. Having the standard sc injection as Docent Sven Nikander became formally reference treatment, oral dosing (at least as the responsible to this work only when most of the equine paste) of ivermectin can only be regarded as experiments had already been done, but unofficially he underdosing. To get comparable endectocidic had been involved from the very first trial. I am very efficacy, the oral dose should probably be at least grateful for his kind promise to be my other 3- or 4-fold, which would not be ecologically nor supervisor. Much earlier, as my teacher in parasitology economically feasible. Therefore, oral at the Veterinary College, Sven awakened my interest administration of ivermectin (perhaps all ML in parasitology and taught me to understand the fascination of the parasitic life style. endectocides) to reindeer is principally to be I am grateful to the Faculty of Veterinary Medicine, condemned. which appointed the refereeship of this thesis to The results from these experiments, together docent Timo Helle and doctor Henrik Bjørn. It is with those from many trials in domestic ruminants, difficult to imagine better referees within the fields of raise concern regarding the oral application of ML reindeer research and veterinary parasitology, endectocides to ruminants, a common practice in respectively. sheep husbandry. Is this treatment really directed I am deeply grateful to docent Mauri Nieminen, against relevant parasites? The most important who perhaps knows the reindeer better than anybody ovine parasites are obviously nematodes of the else, except Santa Claus, claimed to be Mauri's elder abomasum, and it is in this group that endectocide brother. Mauri provided me with many good ideas and resistance has been observed. Perhaps the very stimulating discussions. He was my principal co• treatments should be directed more specifically worker in these experiments. against these parasites. Then, the use of oral Doctors of the Young Men's Parasitological administration should be reconsidered in earnest. Association, Sven Nikander, Timo Soveri, and Antti Sukura criticised my texts greatly improving the scientific quality. Timo also co-worked planning many Possible economic benefits of treatment still poorly of the experiments, in addition to assisting in the field. known When I for some years made up the predoctoral The results from the summer ivermectin treatment minority of the Association, I began to feel social of reindeer calves show that it is erroneous to pressure. The Young Male Parasitologists also expect gains based on trials with domestic animals. carefully scrutinised this dissertation, thus The economic feasibility of antiparasitic treatment guaranteeing its contents. Thank you, friends! I also of reindeer is poorly documented and not well- wish to thank the two current applicants for known. These experiments did not clarify the membership in the Association for interesting matter. scientific discussions. I am thankful to my co-authors Kirsi Kumpula, Staffan Bernstad, Hans Søren Norberg, and Harri Acknowledgements Norberg, who helped me to produce this dissertation. First and foremost, I am highly indebted to my dear Jari Ylônen always found the cheapest and most wife and colleague Leena Oksanen, who encouraged practical way to do it. me to write this thesis to have something to celebrate. Doctors Terje D. Josefsen and Morten Tryland, She also provided me with a lot of technical and and other personnel from the Department of Arctic scientific assistance, as well as reviewed my Veterinary Medicine in Tromsø arranged a positive manuscripts again and again cutting off the most and stimulating working atmosphere. Kjetil Asbakk stupid expressions that I tend to use to hide how taught me that the very expensive and imposing HPLC serious I am. apparatus used also to analyse macrocyclic lactones is I am thankful to my parents and colleagues, Aili really very simple in principle. Oksanen and Hans Erik Oksanen, from whom I did I had long discussions with Rolf E. Haugerud on not get enough of fantasy to choose a profession the ethics of antiparasitic treatment and reindeer different from theirs. I am convinced that my choice husbandry. He also reviewed the manuscript. has been ideal for me. My sincere thanks go to professor Hannu Saloniemi, who at a rather late stage, when some of Rangifer, Special Issue No. 11, 1999 37 Svein D. Mathiesen showed me that the Saami Kirsten Zachariassen repaired the English of this reindeer husbandry in Norway is quite different from thesis. I wish to thank her very many. I am also that I knew from Finland. grateful to Rolf E. Haugerud for the Norwegian Most of the experiments were carried out in sammendrag and to Jouni Kitti and Jouni-Antti Vesti Kaamanen using the animals of the Finnish for the Saami coahkkaigeassu. Association of Reindeer Herding Co-operatives. Veijo I highly appreciate the work of the Libraries of the Tervonen's positive attitude and kind permission to Colleges of Veterinary Medicine in Helsinki (now use the animals are greatly appreciated. Faculty) and in Oslo (now The Norwegian School of If Martti and Vàinô Tervaniemi could not find the Veterinary Science); they both managed to find odd last reindeer of the Kaamanen/Kutuharju herd, then it documents following obscure references. was evident that the animal had already moved away Last and least, but growing fast, my wonderful to the evergray lichen pastures. children, Kirsi, Santeri, and Mikko Oksanen, were I am grateful to my consulting statistician, Hanna patient when Papa was in Denmark (Mikko's synonym Oksanen, my sister, who taught me many methods to for «away» at the early phase of the work) and in find the result I already knew was hiding somewhere Finland (at the later stage). I am very grateful for their in the data. tolerance. I owe thanks to the personnel of the Oulu Regional Apart from the mental and functional support listed Laboratory of the Finnish National Veterinary and above, I got salary from my employers, Finnish Food Research Institute for a lot of help, and National Veterinary and Food Research Institute and appreciate the attempts of Riitta Aho, former head of the Norwegian School of Veterinary Science, the laboratory, to establish reindeer research. She also Department of Arctic Veterinary Medicine. I also got encouraged me to increase the tempo when it appeared financial support to these works from my wife Leena, that my writing of this thesis had stagnated, and the Finnish Fund for Veterinary Medicine, the Finnish reviewed the manuscript asking several important Ministry of Agriculture and Forestry, and Norwegian questions. National Centre for Veterinary Contract Research and Although I have certainly already paid my share of Commercial Services Ltd (VESO), Nordic Council for his huge fortune, I still feel obliged to Bill Gates (and Reindeer Research (NOR), as well as from the medical others responsible for the function of the modern companies Orion-Farmos (representing MSD), Pfizer microcomputer). Without my PC, probably neither this and Cyanamid. dissertation nor the enclosed publications would have been published. But, are those numerous software bugs perhaps some kind of parasites?

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40 Rangifer, Special Issue No. 11, 1999 Connan, R. M. 1997. Hypobiosis in the ostertagids animal systemic insecticides. - / Econ. Entomol. of red deer and the efficacy of ivermectin and 11: 402-406. fenbendazole against them. - Vet. Rec. 140: 203¬ Dybas, R. A. 1989. Abamectin use in crop 205. protection. In: W. C. Campbell (ed.). Ivermectin Consoli, F., Allen, D., Boustead, I., Fava, J., and abamectin. Springer-Verlag New York: Weston, R. F., Franklin, W., Jensen, A. A., de 287-310. Oude, N., Parrish, R., Perriman, R., Easterly, T. G., Jenkins, K. J. & McCabe, T. R. Postlethwaite, D., Quay, 15., Séguin, J. & 1992. Efficacy of orally administered ivermectin Vigon, B. 1993. Guidelines for Life-Cycle on lungworm infection in free-ranging bighorn Assessment: A "Code of Practice". Society of sheep. - Wildl. Soc. Bull. 20: 34-39. Environmental Toxicology and Chemistry Flochlay, A. & Deroover, E. 1997. Efficacy of (SETAC) Pensacola, FL, 1993,73 pp. four endectocides against Nematodirus Craig, T. M., Hatfield, T. A., Pankavich, J. A. & helvetianus in cattle: moxidectin, ivermectin, Wang, G. T. 1992. Efficacy of moxidectin doramectin 1 % solutions and moxidectin 0.5 % against an ivermectin-resistant strain of pour-on solution. - Rev. Méd. Vét. 148: 229-234. Haemonchus contortus in sheep. - Vet. Folstad, I. 1986. Hudbrems hos rein. [Reindeer Parasitol. 41: 329-333. warbles] - Ottar (4): 38-44. (In Norwegian). Dau, J. 1981. Protostrongylus, Muellerius & Folstad, I., Arneberg, P. & Karter, A. J. 1996. Dictyocaulus. In: R A Dieterich (ed.). Alaskan Antlers and parasites. - Oecologia 105: 556-558. wildlife diseases. University of Alaska, Folstad, I., Nilssen, A. C, Halvorsen, O. & Fairbanks, Alaska: 141-146. Andersen, J. 1989. Why do male reindeer DeVaney, J. A., Craig, T. M. & Rowe, L. D. (Rangifer t. tarandus) have higher abundance of 1992. Resistance to ivermectin by Haemonchus second and third instar larvae of Hypoderma contortus in goats and calves. - Int. J. Parasitol. tarandi than females? - Oikos 55: 87-92. 22: 369-376. Folstad, L, Nilssen, A. C, Halvorsen, O. & Dieterich, R. A. & Craigmill, A. L. 1990. Safety, Andersen, J. 1991. Parasite avoidance: the efficacy, and tissues residues of ivermectin in cause of post-calving migration in Rangifer! - reindeer. - Rangifer 10: 53-56. Can. J. Zool. 69: 2423-2429. Dieterich, R. A. & Luick, J. R. 1971. The Fruetel, M. & Lankester, M. W. 1989. occurrence of Setaria in reindeer. - /. Wildl. Dis. Gastrointestinal helminths of woodland and 7: 242-245. barren ground caribou (Rangifer tarandus) in Dobson, R. J., Le Jambre, L. & Gill, J. H. 1996. Canada, with key to species. - Can. J. Zool. 67: Management of anthelmintic resistance: 2253-2269. inheritance of resistance and selection with Galligani, G., Borge, M., Brynildsrud, J. & persistent drugs. - Int. J. Parasitol. 26: 993¬ Qvigstad, E.-K. 1996. Felleskatalogen 1996-97 1000. over preparater i veterinærmedisin. [The Dorchies, P., Alzieu, J. P. & Cadiergues, M. C. common catalogue of veterinary medical 1997. Comparative curative and preventive pharmaceuticals 1996-97] Felleskatalogen AS, efficacies of ivermectin and closantel on Oestrus Oslo: 50. (In Norwegian). ovis (Linne 1758) in naturally infected sheep. - Gill, J. H. & Lacey, E. 1998. Avermectin/ Vet. Parasitol. 72: 179-184. milbemycin resistance in trichostrongyloid Dorchies, P., Cardinaud, B. & Fournier, R. nematodes. - Int. J. Parasitol. 28: 863-877. 1996. Efficacy of moxidectin as a 1% injectable Gogolewski, R. P., Plue, R. E., Rugg, D., solution and a 0.1% oral drench against nasal Allerton, G. R., Familton, A. S., Langholff, bots, pulmonary and gastrointestinal nematodes W. & Eagleson, J. S. 1997. Field trials in New in sheep. - Vet. Parasitol. 65: 163-168. Zealand demonstrating the anthelmintic efficacy Downing, G. V. 1989. The determinative method of a topical formulation of eprinomectin in red for assaying ivermectin residues in tissue and deer. Abstracts of the 16th International plasma. In: W. C. Campbell (ed.). Ivermectin Conference of WAAVP, 10-15 August, 1997, and abamectin. Springer-Verlag New York : Sun City, South Africa: 34. 324-335. Grimshaw, W. T., Hong, C. & Hunt, K. R. 1997. Drummond, R. O. 1984. Control of larvae of the Persistent activity of injectable ivermectin common cattle grub (Diptera: Oestridae) with against important gastrointestinal nematodes of sheep. - Vet. Rec. 141: 422-424.

Rangifer, Special Issue No. 11, 1999 41 Hadwen, S. 1926. Notes on the life history of Helle, T. 1980. Abundance of warble fly Oedemagena tarandi L. and Cephenomyia (Oedemagena tarandi) larvae in semi- trompe Modeer. - Parasitol. 13: 56-65. domesticated reindeer (Rangifer tarandus) in Halvorsen, O. 1986. Epidemiology of reindeer Finland. - Rep. Kevo Subarctic Res. Stat. 16: 1¬ parasites. - Parasitol. Today 2: 334-339. 6. Handeland, K. & Norberg, H. S. 1992. Lethal Helle, T. 1982. Peuran ja poron jâljillà. [Tracing cerebrospinal elaphostrongylosis in a reindeer the wild and semi-domesticated reindeer]. calf. - /. Vet. Med. B. 39: 668-671. Kirjayhtyma Oy, Vaasa, Finland. 160pp. (In Handeland, K. & Skorping A. 1992. The early Finnish). migration of Elaphostrongylus rangiferi in Helle, T., Aspi, J., Lempa, K. & Taskinen, E. goats. - /. Vet. Med. B. 39: 263-272 1992. Strategies to avoid biting flies by reindeer Handeland, K. & Slettbakk T. 1994. Outbreaks of - field experiments with silhouette traps. - Ann. clinical cerebrospinal elaphostrongylosis in Zoolog. Fennici 29: 69-74. reindeer Rangifer tarandus tarandus) in Helle, T. & Kojola, I. 1993. Reproduction and Finnmark, Norway, and their relation to climatic mortality of Finnish semi-domesticated reindeer conditions. - /. Vet. Med. B. 41: 407-410. in relation to density and management Handeland, K. & Sparboe, O. 1991.Cerebrospinal starategies. Arctic 46: 72-77. elaphostrongylosis in dairy goats in northern Hemmingsen, W. 1986. Hjememark. [The Norway. - /. Vet. Med. B. 38: 755-763. brainworm], - Ottar 4: 6-10. (In Norwegian) Handeland, K. 1991. Cerebrospinal elapho• Hemmingsen, W., Halvorsen, O. & Skorping, A. strongylosis in sheep in northern Norway. - /. 1993. Migration of adult Elaphostrongylus Vet. Med. B. 38: 773-780. rangiferi (Nematoda: Protostrongylidae) from Haugerud, R. E. & Nilssen, A. C. 1986. Reinens the spinal subdural space to the muscles of bihulemark. [The sinus worm of the reindeer]. - reindeer (Rangifer tarandus). - J. Parasitol. 79: Ottar 4: 22-29. (In Norwegian) 728-732. Haugerud, R. E. 1986. Om Linguatula arc tica, Hennessy, D. R. 1997. Physiology, pharmacology reinens bihulemark. [About Linguatula arctica, and parasitology. - Int. J. Parasitol. 27: 145-152. the sinus worm of the reindeer]. - Rangifer Herd, R. 1995. Endectocidal drugs: ecological Appendix No 1: 80-87. (In Norwegian). risks and counter-measures. - Int. J. Parasitol. Haugerud, R. E. 1989. Evolution of the 25: 875-885. pentastomids. - Parasitol. Today 5: 126-132. Herd, R. P., Sams, R. A. & Ashcraft, S. M. 1996. Haugerud, R. E., Nilssen, A. C. & Rognmo, A. Persistence of ivermectin in plasma and faeces 1993. On the efficacy of ivermectin against the following treatment of cows with ivermectin reindeer sinus worm Linguatula arctica sustained-release, pour-on or injectable formula• (Pentastomida), with a review on ivermectin in tions. - Int. J. Parasitol. 26: 1087-1093. reindeer. - Rangifer 13: 157-162. Holmstrôm, S., Korhonen, P., Nikander, S. & Hayes, P. W. 1994. Moxidectin: understanding the Rahko, T. 1989. Poron keuhkomatotartunnan unique persistent anthelmintic activity of this esiintyminen Suomen Ita-Lapissa. [On the second generation macrocyclic lactone. occurrence of lung worm infection in the Proceedings AVA (Australian Veterinary reindeer in Finnish Eastern Lapland]. - Suom. Association) Canberra, ACT Australia 6th to Elàinlâàkàrilehti 95: 178-181. (In Finnish, with 11th March 1994. English abstract). Heggstad, E., Bø, E. & Lenvik, D. 1986. Holter, P., Strong, L., Wall, R., Wardhaugh, K. Behandling av reinkalver med ivermectin første & Herd, R.. 1994. Effects of ivermectin on levehøst. Effekt på levendevekter andre levehøst. pastureland ecology. - Vet. Rec. 135: 211-212. [Ivermectin treatment of reindeer calves during Hubert, J., Kerboeuf, D., Cardinaud, B. & their first autumn. The impact on body weights Blond, F. 1995. Persistent efficacy of during their second autumn]. - Rangifer moxidectin against Dictyocaulus viviparus and Appendix No 1: 77-79. (In Norwegian). Ostertagia ostertagi in cattle. - Vet. Rec. 136: Heinze-Mutz, E. M., Pitt, S. R., Bairden, D. K., 223-224. Baggott, D. G., Armour, J., Barth, D., Huttu-Hiltunen, V. 1993. Suomen porotalouden Cramer, L. G. 1993. Efficacy of abamectin organisaatio ja hallinto. [The organisation and against nematodes in cattle. - Vet. Rec. 132: 35¬ administration of the Finnish reindeer 37. husbandry]. In: V. Huttu-Hiltunen, M.

42 Rangifer, Special Issue No. 11, 1999 Nieminen, A. Valmari & B. Westerling (eds.) (Ovibos moschatus) and caribou (Rangifer Porotalous. [Reindeer husbandry]. Painatus- tarandus groenlandicus) in West Greenland. - keskus, Helsinki, Finland: 32-56. (In Finnish). Rangifer 13: 185-189. Karter, A. J. 1993. Reindeer, parasites and Kummeneje, K. 1977. Dictyocaulus viviparus anthelmintic treatment: an epidemiological, infestation in reindeer in northern Norway. - ecological and evolutionary prospective. PhD Acta Vet. Scand. 18: 86-90. dissertation, University of California, Davis, Kumpula, J., Colpaert, A., Kumpula, T. & 1993, 153 pp. Nieminen, M. 1997. Suomen poronhoitoalueen Karter, A. J., Folstad, I. & Anderson, J. D. 1992. talvilaidunvarat. [The winter pasture resources Abiotic factors influencing embryonic of the Finnish reindeer management area]. development, egg hatching, and larval Riistan- ja kalantutkimus, Helsinki, Finland, orientation in the reindeer warble fly, 1997. 43 + 34 pp. (In Finnish, with English Hypoderma tarandi. - Med. Vet. Entomol. 6: summary). 355-362. Kurkela, P. & Kaantee, E. 1978. Antiparasitic Kemppainen, J., Nieminen, M. & Rekila, V. effect of tetrasolium (INN) on reindeer (Rangifer 1997. Poronhoidon kuva. [The image of reindeer tarandus tarandus L.) in enclosure conditions husbandry]. Riista- ja kalatalouden with special reference to Oedemagena tarandi. - tutkimuslaitos, Helsinki, Finland, 1997, 142 pp. Zentralbl. Veterinarmed. B. 25: 81-87. (In Finnish). Lanusse, C, Lifschitz, A., Virkel, G., Alvarez, Kennedy, M. J., Holste, J. E. & Jacobsen, J. A. L., Sanchez, S., Sutra, J. F., Galtier, P. & 1994. The efficacy of ivermectin (pour-on) Alvinerie, M. 1997. Comparative plasma against the eyeworms, Thelazia gulosa and disposition kinetics of ivermectin, moxidectin Thelazia skrjabini in naturally infected cattle. - and doramectin in cattle. - /. Vet. Pharmacol. Vet. Parasitol. 55: 263-266. Ther. 20: 91-99. Kerboeuf, D., Hubert, J., Cardinaud, B. & Le Jambre, L. F., Gill, J. H., Lenane, I. J. & Blond-Riou, F. 1995. The persistence of the Lacey, E. 1995. Characterisation of an efficacy of injectable or oral moxidectin against avermectin resistant strain of Australian Teladorsagia, Haemonchus and Tricho- Haemonchus contortus. - Int. J. Parasitol. 25: strongylus species in experimentally infected 691-698. sheep. - Vet. Rec. 137: 399-401. Leader-Williams, N. 1980. Observations on the Klei, T. R., Chapman, M. R., French, D. D. & internal parasites of reindeer introduced into Taylor, H. W. 1993. Evaluation of ivermectin at South Georgia. - Vet. Rec. 107: 393-395. an elevated dose against encysted equine Lisitzin, P. 1964. Histological study of a parasitic cyathostome larvae. - Vet. Parasitol. 47: 99-106. nodule in the subcutaneous tissue of the muzzle Klemenfeva, E. V. 1975. [Field trials of Warbex of a reindeer (Rangifer tarandus). Preliminary for control of Oedemagena tarandi}. - Trudy report. - Nord. Vet.-Med. 16: 390-395. Vsesoyuznyi Nauchno issledovatel'skii Institut Lo, P.-K. A., Fink, D. W., Williams, J. B. & Veterinarnoi Sanitarii. 51: 154-155. (In Russian, Blodinger, J. 1985. Pharmacokinetic studies of with English abstract). ivermectin: effects of formulation. - Vet. Res. Kocan, A. 1985. The use of ivermectin in the Comm. 9: 251-268. treatment and prevention of infection with Mackintosh, C. G., Mason, P. C, Manley, T., Parelaphostrongylus tenuis (Dougherty) Baker, K. & Littlejohn, R. 1985. Efficacy and (Nematoda, Metastrongyloidea) in white-tailed pharmacokinetics of febantel and ivermectin in deer (Odocoileus virginianus Zimmermann). - J. red deer (Cervus elaphus). - iV. Z. Vet. J. 33: Wildl. £>w 21: 454-455. 127-131. Kojola, I. 1995. Peura palasi kotiin. [The wild Marriner, S. E., McKinnon, J. & Bogan, J. A. forest reindeer back home]. - Suomen Luonto 54 1987. The pharmacokinetics of ivermectin after (11): 30-34. (In Finnish). oral and subcutaneous administration to sheep Kojola, I. & Helle, T. 1993. Regional differences and horses. - J. Vet. Pharmacol. Ther. 10: 175¬ in density-dependent mortality and reproduction 179. in Finnish reindeer. - Rangifer 13: 33-38. McKellar, Q. A. & Benchaoui, H. A. 1996. Korsholm, H. & Olesen, C. R. 1993. Preliminary Avermectins and milbemycins. Invited review. - investigations on the parasite burden and J. Vet. Pharmacol. Ther. 19: 331-351. distribution of endoparasite species of muskox

Rangifer, Special Issue No. 11,1999 43 McKellar, Q. A. 1994. Chemotherapy and delivery Mykkanen J. 1978. Poron loistorjunnasta. [On systems - helminths. - Vet. Parasitol. 54: 249¬ antiparasitic treatment of reindeer]. - Poromies 258. 45 (3): 12-14. (In Finnish). McKellar, Q. A., Bogan, J. A., Horspool, L. & Nepoklonov, A. A., Bryushinin, P. I. & Shal'kov, Reid, K. 1988b. Effect of ivermectin on the E. N. 1973. [An effective means against the reproductive potential of Cooperia curticei. - reindeer warble-fly]. - Veterinariya (12): 65-66. Vet. Ree. 122: 444. (In Russian). McKellar, Q. A., Jackson ,F., Coop, R. L., Nieminen, M. & Muhonen, H. 1996. Alaskan Jackson, E. & Scott, E. 1991. Effect of luonto ja poronhoito. [The Alaskan nature and parasitism with Nematodirus battus on the reindeer industry]. - Poromies 63 (4): 33-39. (In pharmacokinetics of levamisole, ivermectin and Finnish). netobimin. - Vet. Parasitol. 39: 123-136. Nieminen, M. 1989. Loistorjunnan merkitys. [The McKellar, Q., Marriner, S. & Bogan, J. 1988a. relevance of antiparasitic treatments]. Comparison of ivermectin, oxfendazole and Poromies 56 (3): 28- 36. (In Finnish). levamisole for use as anthelmintics during the Nieminen, M. 1992. Porontaljoille ja -nahoille periparturient period in sheep. - Vet. Ree. 122: parempaa laatua ja arvoa. II. Kurmutonta nappa- 558-560. ja mokkanahkaa ulkomaille. [Increasing the Meeus, P. F., De Bont, J. & Vercruysse, J. 1997. quality and value of reindeer hides. II. Export of Comparison of the persistent activity of warble-free leather and suede].. - Poromies 59 ivermectin, abamectin, doramectin and (6): 26- 27. (In Finnish). moxidectin in cattle in Zambia. Vet. Parasitol. Nieminen, M. 1993a. Poronhoidon historia. [The 70: 219-224. history of reindeer herding] In: Huttu-Hiltunen Michel, J. F., Lancaster, M. B. & Hong, C. 1974. V, Nieminen M, Valmari A, Westerling B. (eds) Studies on arrested development of Ostertagia Porotalous. [Reindeer husbandry]. Painatus- ostertagi and Cooperia oncophora. - J. Comp. keskus, Helsinki, Finland: 9-20. (In Finnish). Pathol. 84: 539-554. Nieminen, M. 1993b. Eri maiden poronhoito. Miller, J. A., Oehler, D. D. & Scholl, P. J. 1994. [Reindeer husbandry in different countries]. In: Moxidectin: pharmacokinetics and activity V. Huttu-Hiltunen, M. Nieminen, A. Valmari & against horn flies (Diptera: Muscidae) and B. Westerling (eds.) Porotalous [Reindeer trichostrongyle nematode egg production. - Vet. husbandry]. Painatuskeskus, Helsinki, Finland: Parasitol. 53: 133-143. 21-31. (In Finnish). Miller, M. W., Hobbs, N. T., Rutherford, W. H. Nieminen, M. 1994. Poro. Ruumiinrakenne ja & Miller, L. L. W. 1987. Efficacy of injectable elintoiminnat. [Reindeer. Anatomy and ivermectin for treating lungworm infections in physiology] Mauri Nieminen. Rovaniemi. 1994 mountain sheep. - Wildl. Soc. Bull. 15: 260-263. 169 p. (In Finnish). Mitskovich, V. Yu. & Savel'ev, V. D. 1984. Role Nieminen, M. 1995. Ratsuporoista teurasporoihin - of wild reindeer in the epizooty of parasitic poro hyotyelaimena pohjoisilla alueilla. [From diseases in Taimyr. In: E. E. Syroechovskii (ed.) riding-reindeer to slaughter animals - reindeer Wild reindeer of the Soviet Union. Translated utilisation in the northern areas]. - Poromies 62 from Russian. Amerind Publishing Co, New (6): 22-28. (In Finnish). Delhi, 1984: 109-112. Nieminen, M., Maijala, V. & Soveri, T. 1998. Mjöberg, E. 1915. Über eine neue Gattung und Art Lukijalle. [To the reader] In: M. Nieminen, V. von Anopluren. [On a new sucking louse genus Maijala & T. Soveri. Poron ruokinta. [Feeding and species]. - Entomol. Tidjskr. 36: 282-285. of reindeer] Riista- ja kalatalouden (In German). tutkimuslaitos, Helsinki, Finland 1998: 4-5. (In Mjöberg, E. 1916. Studien über Mallophagen und Finnish). Anopluren. [Studies on biting and sucking lice]. Nieminen, M., Poso, R. & Soveri, T. 1997. -Arkiv förZoologi 13: 66-68. (In German). Kilpaporoissa ei kiellettyja aineita. [Racing Monfray, K. & Boulard, C. 1990. Preliminary reindeer doping-free]. - Poromies 64 (2): 44-45. evaluation of four immunological tests for the (In Finnish). early diagnosis of Hypoderma tarandi causing Nieminen, M., Timisjarvi, J. & Laitinen, M. hypodermosis in reindeer. - Med. Vet. Entomol. 1980. The effects of antiparasitic treatment on 4: 297-302. the condition of semi-domesticated reindeer

44 Rangifer, Special Issue No. 11, 1999 (Rangifer tarandus). - Rep. Kevo Subarctic Res. Treatment of reindeer with ivermectin- effect on Stat. 16: 23-26. dung insect fauna. Submitted. Nikander, S. & Saari, S. 1993. Dictyocaulus Nilsson O. 1971. The inter-relationship of eckerti in the respiratory tract of reindeer. endoparasites in wild cervids (Capreolus Proceedings of the 14th International capreolus L. and Alces alces L.) and domestic Conference of the World Association for the ruminants in Sweden. - Acta Vet. Scand. 12: 36¬ Advancement of Veterinary Parasitology, 68. Cambridge, 8-13 August, 1993: 291. Nordkvist M. 1980. The larvicidal effect of Nikander, S. 1988. Abomasal helminths of cervids fenthion 50 % treatment on warble and nostril in Finland. Abstracts, Nordic Congress on Game fly larvae in reindeer. - Vet. Med. Rev. (2): 131¬ Research, Espoo 5.-9. September, 1988: 44. 134. Nikander, S. 1992. Kuumakorvan eli vartin Nordkvist, M. 1966. Renens sjukdomar. In: aiheuttaja (Lappnema auris) - maassamme Ekonomisk renskôtsel, LTs forlag, 1966: 106¬ uhanalainen laji? [The causative agent of wart- 141. (In Swedish). ear (Lappnema auris) - a threatened species in Nordkvist, M. 1967. Treatment experiments with Finland?] - Poromies 59 (6): 22-24. (In Finnish). systemic insecticides against the larvae of the Nilssen, A. C. & Anderson, J. R. 1986. Reinens reindeer grub fly (Oedemagena tarandi L.) and svelgbrems. [Throat bot of the reindeer]. - Ottar the reindeer nostril fly (Cephenomyia trompe L.) 4: 30-37. (In Norwegian) -Nord. Vet.-Med. 19: 281-293. Nilssen, A. C. & Anderson, J. R. 1995a. Flight Nordkvist, M., Christensson, D. & Rehbinder, C. capacity of the reindeer warble fly, Hypoderma 1984. Ett fàltavmaskningsfôrsôk med ivermectin tarandi (L.), and the reindeer nose bot fly, (MSD) på renar. [A deworming field trial with Cephenemyia trompe (Modeer) (Diptera: ivermectin (MSD) in reindeer]. - Rangifer 4 (2): Oestridae). - Can. J. Zool. 73: 1228-1238. 10-15. (In Swedish, with English abstract). Nilssen, A. C. & Anderson, J. R. 1995b. The Nordkvist, M., Rehbinder, C, Christensson, D. mating sites of the reindeer nose bot fly: not a & Rônnbâck, C. 1983. A comparative study on practical target for control. - Rangifer 15: 55-61. the efficacy of four anthelmintics on some Nilssen, A. C. & Haugerud, R. E. 1994. The important reindeer parasites. - Rangifer 3 (2): timing and departure rate of larvae of the warble 19- 38. fly Hypoderma (=Oedemagena) tarandi (L.) and Oksanen, A. & Nieminen, M. 1995. The influence the nose bot fly Cephenemyia trompe (Modeer) of summer ivermectin treatment on the growth (Diptera: Oestridae) from reindeer. - Rangifer of reindeer calves. Abstracts of the 2nd 14: 113-122. International Arctic Ungulate Conference. Nilssen, A. C. & Haugerud, R. E. 1995. Fairbanks, Alaska, 13-17 August, 1995: 10. Epizootiology of the reindeer nose bot fly Oksanen, A. & Nikander, S. 1989. Ivermectin as a Cephenemyia trompe (Modeer) (Diptera: bird anthelmintic - trials with naturally infected Oestridae) in reindeer, Rangifer tarandus (L.) in domestic fowl. - /. Vet. Med. B. 36: 495-499. Norway. - Can. J. Zool. 73: 1024-1036. Oksanen, A., Nieminen, M., Soveri, T., Nilssen, A. C. 1997a. Factors affecting size, Kumpula, K., Heiskari, U. & Kuloharju, V. longevity and fecundity in the reindeer oestrid 1990. The establishment of parasites in reindeer flies Hypoderma tarandi (L.) and Cephenemyia calves. Proceedings of the 6th workshop on trompe (Modeer). - Ecologic. Entomol. 22: 294¬ reindeer research, Tromsø, Norway, 8-10 304. October, 1990. - Rangifer, Special Issue No 5: Nilssen, A. C. 1997b. Effect of temperature on 20- 21. pupal development and eclosion dates in the Oksanen, A., Soveri, T. & Nieminen, M. 1996. reindeer oestrids Hypoderma tarandi and Impact of broad-spectrum anthelmintic treatment Cephenemyia trompe (Diptera: Oestridae). - in the summer on the weight gain of reindeer Environ. Entomol. 26: 296-306. calves. Brief communication. - Rangifer 16: Nilssen, A. C, Haugerud, R. E. & Folstad, I. 151-154. 1998. No interspecific covariation in intensities Paliskuntain yhdistys. 1992. Suomen of macroparasites of reindeer, Rangifer tarandus porotalous. [The Finnish reindeer industry]. (L.). - Parasitology 117: 273-281. Kemi 1992. 24 pp. (In Finnish). Nilssen, A. C, Asbakk, K., Haugerud, R. E., Pankavich, J. A., Berger, H. & Simkins, K. L. Hemmingsen, W. & Oksanen, A. 1999. 1992. Efficacy of moxidectin, nemadectin and

Rangifer, Special Issue No. 11,1999 45 ivermectin against an ivermectin-resistant strain slaughtered reindeer bulls. - Nord. Vet.-Med. 29: of Haemonchus contortus in sheep. - Vet. Rec. 556-557. 130: 241-243. Rehbinder, C. & Nordkvist, M. 1983. Paul, A. J., Tranquilli, W. J., Seward, R. L., Lokalisationen av svalgkormflugans Todd, K. S. Jr. & DiPietro, J. A. 1987. (Cephenomyia trompe L) larver i svalget på ren i Clinical observations in collies given ivermectin en tidigare okånd tonsillavåvnad (Tonsilla orally. - Am. /. Vet. Res. 48: 684-685. pharyngis dorso-medialis). [The localization of Pearson, A. B & Rutherford, D. M. 1988. the larvae of the nostril fly (Cephenomyia Ivermectin injection less effective in goats than trompe L) in the pharynx of reindeer in an earlier oral treatment. - Surveillance 15: 22. unknown tonsil tissue]. - Rangifer 3: 46-49. (In Persen, E., Jacobsen, E., Lenvik, D. & Swedish, with English summary). Skjenneberg, S. 1982. Forsøk med behandling Rehbinder, C. & von Szokolay, P. 1978. The av reinkalver mot reinbremslarver (Oedemagena presence of gastric parasites in winter- tarandi L og Cephenomyia trompe L). Effekt på slaughtered reindeer. - Nord. Vet.-Med. 30: 214¬ kalvenes kondisjon målt med levende vekt og 216. overlevingsevne. [Weight development and Rehbinder, C. 1990. Some vector borne parasites survival rate of reindeer calves treated against in Swedish reindeer (Rangifer tarandus Oedemagena tarandi L and Cephenomyia tarandus L.). - Rangifer 10: 67-73. trompe L. - Rangifer 2: 39-49. (In Norwegian, Rehbinder, C, Christensson, D. & Forssell, I. with English summary). 1979. Investigations on parasitic visceral Ploeger, H. W., Schoenmaker, G. J., granulomas in reindeer. - Nord. Vet.-.Med. 31: Kloosterman, A. & Borgsteede, F. H. 1989. 282-283. Effect of anthelmintic treatment of dairy cattle Rehbinder, C, Forssell, I., Nordkvist, M. & von on milk production related to some parameters Szokolay, P. 1981. Effekten av mebendazol på estimating nematode infection. - Vet. Parasitol. Elaphostrongylus rangiferi hos ren. [Efficacy of 34: 239-253. mebendazole on Elaphostrongylus rangiferi in Powers, K. G., Wood, I. B., Eckert, J., Gibson, reindeer. - Nord. Vet.-Med. 33: 150-158.(In T. & Smith, H. J. 1982. World Association for Swedish, with English summary). the Advancement of Veterinary Parasitology Ristic, Z., Medleau, L., Paradis, M. & White- (W.A.A.V.P.) guidelines for evaluating the Weithers, N. E. 1995. Ivermectin for treatment efficacy of anthelmintics in ruminants (bovine of generalized demodicosis in dogs. /. Am. Vet. and ovine). - Vet Parasitol 10: 265-284. Med. Assoc. 207: 1308-1310. Prichard, R. K., Steel, J. W., Lacey, E. & Saval'ev, D. V. 1968. Control of warble flies and Hennessy, D. R. 1985. Pharmacokinetics of bloodsucking Diptera. In: P. S. Zhigunov (ed.) ivermectin in sheep following intravenous, intra- Reindeer Husbandry. Translated from Russian. abomasal or intraruminal administration. - /. Israel Program for Scientific Translations Vet. Pharmacol. Therap. 8: 88-94. Jerusalem 1968. pp 294-311. Puccini, V., Giangaspero, A. & Fasanella, A. Savel'ev, D. V., Kurzaev, G. M., Solomakha, A. 1994. Efficacy of moxidectin against Oestrus I. & Kadnikov, V. V. 1972. [The effectiveness ovis larvae in naturally infested sheep. - Vet. of Baytex against the reindeer warble-fly]. - Rec. 135: 600-601. Veterinariya. (12): 76-78. (In Russian). Rahko, T., Saari, S. & Nikander, S. 1992. Saveljev, D. V. 1968. [Seasonal variation in the Histopathological lesions in spontaneous activity of gadfly attacs on reindeer]. - dictyocaulotic pneumonia of the reindeer Veterinariya 24: 53-54. (In Russian). (Rangifer tarandus tarandus L.). - Rangifer 12: Saveljev, D. V. 1971. Kiiliåisten biologia ja taistelu 115-122. niita vastaan [Biology of oestrid flies and the Ranjan, S., Trudeau, C, Prichard, R. K., fight against them]. - Poromies (6): 6-9. (In Daigneault, J. & Rew, R. S. 1997. Nematode Finnish) reinfection following treatment of cattle with Scholl, P. J., Guillot, F. S. & Wang, G. T. 1992. doramectin and ivermectin. - Vet. Parasitol. 72: Moxidectin: systemic activity against common 25-31. cattle grubs (Hypoderma lineatum) (Diptera: Rehbinder, C. & Christensson, D. 1977. The Oestridae) and trichostrongyle nematodes in presence of gastro-intestinal parasites in autumn- cattle. - Vet. Parasitol. 41: 203-209.

46 Rangifer, Special Issue No. 11,1999 Schulz-Key, H. & Wenk, P. 1981. The Solopov, N. V. 1989. Features of the ecology of transmission of Onchocerca tarsicola juvenile forms of subcutaneous gadfly in (Filarioidea: Onchocercidae) by Odagmia ornata reindeer - Soviet J. Ecol. 19: 299-304. and Prosimulium nigripes (Diptera: Simuliidae). Soulsby, E. J. L. 1982. Helminths, arthropods and -J.Helminthol. 55: 161-166. protozoa of domestic animals. 7th ed. Bailliere Scott, E. W., Kinabo, L. D. & McKellar, Q. A. Tindall., London, 1982 809 pp. 1990. Pharmacokinetics of ivermectin after oral Soveri, T., Nikander, S. & Nieminen, M. 1990. or percutaneous administration to adult milking Efficiency of parenteral and oral ivermectin goats. Vet. Pharmacol. Therap. 13: 432-435. treatment on parasites in reindeer. - Rangifer Scott, J. G., Roush, R. T. & Liu, N. 1991. Special Issue No 4: 64. Selection of high-level abamectin resistance Steel, J. W. 1993. Pharmacokinetics and meta• from field-collected house flies, Musca bolism of avermectins in livestock. - Vet. domestica. - Experientia 47: 288-291. Parasitol. 48: 45-57. Shoop, W. L., Egerton, J. R., Eary, C. H., Steen, M., Blackmore, C. G. & Skorping, A. Haines, H. W., Michael, B. F., Mrozik, H., 1997. Cross-infection of moose (Alces alces) Eskola, P., Fisher, M. H., Slayton, L., Ostlind, and reindeer (Rangifer tarandus) with D. A., Skelly, B. J., Fulton, R. K., Barth, D., Elaphostrongylus alces and Elaphostrongylus Costa, S., Gregory, L. M., Campbell, W. C, rangiferi (Nematoda, Protostrongylidae): effects Seward, R. L. & Turner, M. J. 1996. on parasite morphology and prepatent period. - Eprinomectin: a novel avermectin for use as a Vet. Parasitol. 71: 27-38. topical endectocide for cattle. - Int. J. Parasitol. Strong, L. & Wall, R. 1994. Effects of ivermectin 26: 1237-1242. and moxidectin on the insects of cattle dung. - Shoop, W. L., Haines, H. W., Michael, B. F. & Bull. Entomol. Res. 84: 403-409. Eary, C. H. 1993. Mutual resistance to Strong, L. 1993. Overview: the impact of avermectins and milbemycins: oral activity of avermectins on pastureland ecology. - Vet. ivermectin and moxidectin against ivermectin- Parasitol. 48: 3-17. resistant and susceptible nematodes. - Vet. Rec. Staaland, H. & Nieminen, M. 1993. World 133: 445-447. reindeer herding: origin, history, distribution, Shoop, W. L., Mrozik, H., Fisher, M. H. 1995. economy. Proceedings, World Conference on Structure and activity of avermectins and Animal Production, Edmonton, Canada: 161¬ milbemycins in animal health. - Vet. Parasitol. 203. 59: 139-156. Suarez, V. H., Bedotti, D. O., Larrea, S., Busetti, Skjenneberg, S. 1984. Reindeer. - In: I. L. Mason M. R. & Garriz, C. A. 1991. Effects of an (ed.). Evolution of domesticated animals, integrated control programme with ivermectin Longman Ltd, London. 128-138. on growth, carcase composition and nematode Skjenneberg, S. & Slagsvold, L. 1968. Reindriften infection of beef cattle in Argentina's western og dens naturgrunnlag. [Reindeer husbandry pampas. - Res. Vet. Sci. 50: 195-199. and its ecological principles]. Universitets• Sutherland, I. H. 1990. Veterinary use of forlaget Oslo/Bergen/Tromsø. 332 pp. (In ivermectin. - Acta Leiden 59: 211-216. Norwegian). Syroechovskii, E. E. 1995. Wild reindeer. Skogland T. 1994. Villrein. Fra urinnvåner til Translated from Russian. Science Publishers, miljøbarometer. [From aboriginals to Inc., New Hampshire. 290 pp. environmental barometre] Teknologisk Forlag, Tarry, D. W., Sinclair, I. J. & Wassail, D. A. Drammen. 143 pp. (In Norwegian). 1992. Progress in the British hypodermosis Skrjabin, K. I., Shilobalova, N. P. & Shults, R. S. eradication programme: the role of serological 1971. Dictyocaulus eckerti. In: K. I. Skrjabin et surveillance. - Vet. Rec. 131: 310-312. al. (eds.). Dictyocaulidae, Heligmosomatidae Taylor, S. M., Edgar, H. & Kenny, J. 1993. and Ollulanidae of animals. Israel Program for Prophylactic efficacy of moxidectin for Scientific Translations, Jerusalem: 29-34. periparurient ewes and mid-summer Iambs. - Smirnov, Yu. 1976. [Study of the efficacy of some Vet. Rec. 133: 270-271. anthelmintics in Elaphostrongylus infections in Thomas, D. C. & Kiliaan, H. P. L. 1988. Warble Rangifer tarandus]. - Sbornik Nauchnykh Rabot infestations in some Canadian caribou and their Murmanskoi Olenevodcheskoi Opytnoi Stantsii significance. Proc. 5th International Reindeer/ (3): 58-61. (In Russian). Caribou Symposium Arvidsjaur, Sweden 18-22

Rangifer, Special Issue No. 11, 1999 47 August, 1988. - Rangifer Special Issue No. 3: Walsh, A., Younis, P. J. & Morton, J. M. 1995. 409-417. The effect of ivermectin treatment of late Thomas, R. J. & Waller, P. J. 1979. Field pregnant dairy cows in south-west Victoria on observations on the epidemiology of abomasal subsequent milk production and reproductive parasites in young sheep during winter and performance. - Aust. Vet. J. 72: 201-207. spring. - Res. Vet. Sci. 26: 209-212. Washburn, R. H., Klebesadel, L. J., Palmer, J. Timisjårvi, J., Nieminen, M. & Sippola, A.-L. S., Luick, J. R. & Bleicher, D. P. 1980. The 1984. The structure and insulation properties of warble-fly problem in Alaska reindeer. - the reindeer fur. - Comp. Biochem Physiol 79A: Agroborealis (Jan): 23-28. 601-609. Watson, T. G. & Charleston, W. A. G. 1985. The Turner, M. J. & Schaeffer, J. M. 1989. Mode of significance of parasites in farmed deer. In: P. F. action of ivermectin. In: W. C. Campbell (ed.). Fennessy & K. R. Derw (eds.). Biology of Deer Ivermectin and abamectin. Springer-Verlag New Production. Roy. Soc. N. Z. Bull. 22: 105-117. York Inc. 1989, 73-88. Weisser, C. F. & Kim, K. C. 1973. Rediscovery of Tyler, N. & Røed, K. 1993. Utbredelse og Solenopotes tarandi (Mjoberg, 1915) klassifisering av reinsdyr. [Distribution and (Linognathidae: Anoplura), with ectoparasites of classification of reindeer]. - Ottar 195, 1993: 3¬ the barren ground caribou. - Parasitology 66: 10. (In Norwegian). 123-132. Urquhart, G. M., Armour, J., Duncan, J. L., Williams, J. C. & Broussard, S. D. 1995. Dunn, A. M. & Jennings, F. W. 1987. Persistent anthelmintic activity of ivermectin Veterinary Parasitology. Longman Scientific & against gastrointestinal nematodes of cattle. - Technical Harlow. 286 pp. Am. J. Vet. Res. 56: 1169-1175. Vårady, M., Praslicka, J. & Corba, J. 1995. Williams, J. C, Loyacano, A. F., Broussard, S. Efficacy of moxidectin against multiple resistant D. & Coombs, D. F. 1995. Effect of treatment Ostertagia spp. in lambs. - N. Z. Vet. J. 43: 89¬ with an ivermectin sustained-release bolus on 90. productivity of stocker beef calves. - Vet. Vercruysse, J. 1993. Synopsis. In: Veterinary Parasitol. 58: 75-82. Parasitology, Special Issue: Doramectin - a Wood, D. M. 1987. Oestridae. - In: J. F. McAlpine novel avermectin. - Vet. Parasitol. 49: 1-3. (ed.). Manual of Nearctic Diptera. Vol 2. Vercruysse, J., Claerebout, E., Dorny, P., Monog. No. 28. Agriculture Canada, Ottawa, Demeulenaere, D. & Deroover, E. 1997. Ont. pp. 1147-1158. Persistence of the efficacy of pour-on and Wood, I. B., Amaral, N. K., Bairden, J. L., injectable moxidectin against Ostertagia Duncan, J. L., Kassai, T., Malone, J. B., ostertagi and Dictyocaulus viviparus in Pankavich, J. A., Reinecke, R. K., Slocombe, experimentally infected cattle. - Vet. Rec. 140: O., Taylor, S. M. & Vercruysse, J. 1995. 64-66. World Association for the Advancement of Vermunt, J. J., West, D. M. & Pomroy, W. E. Veterinary Parasitology (W.A.A.V.P.) second 1995. Multiple resistance to ivermectin and edition of guidelines for evaluating the efficacy oxfendazole in Cooperia species of cattle in of anthelmintics in ruminants (bovine, ovine, New Zealand. Vet. Rec. 137: 43-45. caprine). - Vet. Parasitol. 58: 181-213. Vorren, 0. & Manker, E. 1976. Samekulturen. Xiao, L., Herd, R. P. & Majewski, G. A. 1994. Universitetsforlaget. (In Norwegian). Comparative efficacy of moxidectin and Wall, R. & Strong, L. 1987. Environmental ivermectin against hypobiotic and encysted consequences of treating cattle with the cyathostomes and other equine parasites. - Vet. antiparasitic drug ivermectin. - Nature 327: 418¬ Parasitol. 53: 83-90. 421. Yazwinski, T. A., Featherston, H., Tucker, C. & Waller, P. J. 1990. Resistance to chemotherapy: Johnson, Z. 1994. Residual nematocidal What are the risks for the reindeer industry? - effectiveness of ivermectin in cattle. - Am. J. Rangifer, Special Issue No 4: 14-18. Vet. Res. 55: 1416-1420. Waller, P. J. 1994. The development of Zajac, A. M., Thatcher, C. D., Brock, R. A., anthelmintic resistance in ruminant livestock. - Umberger, S. H. & Notter, D. R. 1992. Acta Trop. 56: 233-43. Comparison of ivermectin formulations in an Waller, P. J. 1997. Anthelmintic resistance. - Vet. ovine parasite control programme. - Vet. Rec. Parasitol. 72: 391-405; discussion 405-12. 130: 353-354.

48 Rangifer, Special Issue No. 11, 1999 Zulalian, J., Stout, S. J., daCunha, A. R., Garces, Asbakk, K., Bendiksen, H. R. & Oksanen, A. T. & Miller, P. 1994. Absorption, tissue 1999. Ivermectin in reindeer faeces distribution, metabolism, and excretion of determination by HPLC. - J. Agric. Food Chem. moxidectin in cattle. - /. Agric. Food Chem. 42: 47: 999-1003. 381-387. Zumpt, F. 1965. Myiasis in man and animals in the old world. Butterworth & Co. Ltd., London 1965.

Rangifer, Special Issue No. 11, 1999 49 Appendixes

Appendix 1. Names of some important nematode and arthropod reindeer parasites in some languages.

Latin English Norwegian Swedish Finnish Saami Ostertagia medium løpe-rundmark löpmagsmask juoksutus- civzzamähtu gruehneri stomach worm mahamato Dictyocaulus lungworm lungemark lungmask keuhkomato geahpesmähtu eckerti Elaphostrongylus brainworm hjernemark hjärnmask aivomato liw'zamähtu rangiferi Hypoderma warble, grub fly hudbrems hudbroms, kurmu, gurbmä-loddi, tarandi' renstyng kurmupaarma låvzå Cephenemyia throat bot, nasal svelgbrems, svalgkorm, saulakka, njunne-loddi, trompe'" bot nesebrems nässvalgstyng saulalintu, savla Solenopotes sucking louse blodlus blodlus täi varradihkki tarandi Damalinia tarandi biting louse pelslus pälslus väive nåhkedihkki Linguatula sinus worm bihulemark, näshälemask kielimato njunnemåhtu, arcticaA neseflyndre njunneguovdni (Bergman, 1916; Nordkvist, 1966; Skjenneberg & Slagsvold, 1968; Nilssen & Anderson, 1986; Folstad, 1986; Hemmingsen, 1986; Haugerud & Nilssen, 1986; Paliskuntain yhdistys, 1992; J. Kitti, pers., comm. 1998, English names from the text). a Formerly regarded as D. viviparus, the bovine lungworm. b Formerly called Oedemagena tarandi. c Often used the erroneous form Cephenomyia trompe. d Often in older literature erroneously called L. serrata, the canine sinus worm.

50 Rangifer, Special Issue No. 11, 1999 Appendix 2. Photomicrographs of parasite eggs and larvae in reindeer faeces and photographs of other reindeer parasites (diagnostic aids).

1-2. Gastro-intestinal trichostrongylid. 3. Nematodirus sp. Seen almost exclusively in reindeer calf faeces. 4. Skrjabinema sp. 5. Capillaria sp., together with Eimeria sp. coccidia oocysts. 6. Moniezia sp. (Cestode). Seen almost exclusively in reindeer calf faeces. 7. Linguatula arctica (Pentastomid). 8. Elaphostrongylus rangiferi \\, dorsal spine not easily visible in print, therefore enlargened. Scale bar 100 pm for Figures 1-8. 9. Fibrous tissue caused by Lappnema auris in the auriculum of reindeer («wart-ear» or «hot ear»). 10. Histological section of fibrous tissue caused by Lappnema auris. Numerous parasites in capillaries (arrows). H-E staining. 11. Warbled reindeer hind in early May. The barren female has lost its antlers. 12. Warbled reindeer hide slaughtered in May. Inside view. 13. Cross-section of the skin of a reindeer calf, died in March, partly due to heavy warble infection. 14. Massive throat bot infection (101 bots) in a reindeer calf killed in May. 15. Throat bots seen in reindeer by fibreoptic pharyngoscopy. 16. Linguatula arctica from a reindeer calf slaughtered in May. Scale bar 8.5 cm.

Rangifer, Special Issue No. 11, 1999 51