Printer Friendly

Epizootiology of Elaphostrongylus alces in Swedish moose.

ABSTRACT: A total of 961 harvested and 241 unharvested moose (Alces alces) carcasses and parts from throughout Sweden were examined for Elaphostrongylus alces from 1985 to 1989. When available, the central nervous system and skeletal muscles were searched for adult nematodes, and lungs and feces were examined for first-stage larvae. The parasite was distributed throughout Sweden with highest prevalence (56%) in the central region and lowest in the south (13%). Prevalence was highest in calves and old moose (>9 years) and lowest in middle-aged animals (5-9 years), with no statistical difference between sexes, although prevalence trended higher in young males. Body condition and abundance of Elaphostrongylus alces were negatively correlated, and condition was poorer in unhar-vested than harvested moose. A short (39-73 days) prepatent period was documented, and calves as young as 1.5 months were infected. These results indicate the importance of continued surveillance of Elaphostrongylus alces, particularly because a warming climate will likely increase abundance of intermediate mollusk hosts and possibly cause increased infection of moose.

Key words: Alces alces, climate, body condition, Elaphostrongylus alces, intermediate host, gastropods, moose, prepatent period, protostrongylidae, Sweden

The moose (Alces alces) population in Scandinavia began to rise in the 1970s, peaking in the mid-1980s in Sweden. With few large predators at that time, it was not unusual to find dead or sick animals (Hornberg 2001, Steen et al. 2005), and in the 1980-1990s, high mortality was noted in both Swedish and Norwegian moose, as well as in semi-domestic reindeer (Rangifer tarandus). A previously unknown disease, elaphostrongylosis (Steen and Rehbinder 1986, Stuve 1986), was reported in the 1980s and sick animals were characterized by locomotive abnormalities such as ataxia, incoordination, swaying of the hindquarters, broad and stamping gait, and a certain way of hypermetria that suggested paralysis of ascending proprioceptive nerve fibers (Steen and Roepstorff 1990). A previously undescribed species of elaphostrongyline nematode with a dorsal-spine larva, Elaphostrongylus alces (Steen et al. 1989) was invariably associated with sick and dead moose (Steen and Rehbinder 1986).

Parasites of the genera Parelaphostrongylus and Elaphostrongylus belong to the subfamily Elaphostrongylinae (Protostrongylidae, Metastrongyloidea, Nematoda). Species of the genus Parelaphostrongylus (P. tenuis, P. odocoilei, P andersoni) affect the central nervous system (CNS) and skeletal muscle fasciae of Nearctic cervids in North America including white-tailed deer (Odocoileus virginianus), black-tailed deer (O. hemonious hemonious), mule deer (O. h. columbianus), and occasionally wapiti (Cervus canadensis) and moose (Alces alces spp.). Species of Elaphostrongylus (E. alces, E. cervi, E. panticola, E. rangiferi) affect the CNS, the peripheral nerve system (PNS), and the skeletal muscle fasciae in Eurasian cervids including moose, red deer (Cervus elaphus), maral deer (C. e. sibiricus), roe deer (Capreolus capreolus), and reindeer (Lankester 2001). In the New World, as in the Old World, central nervous disorders and mortality occur in wild cervids infected with elaphostrongyline nematodes (Anderson 1964, Lankester 2001, 2010). Representatives of the genera Elaphostrongylus and Parelaphostrongylus are also harmful to domestic ruminants (Lankester 2001).

Both Elaphostrongylus spp. and Parelaphostrongylus spp. develop from the first to third larval stage ([L.sub.1]-[L.sub.3]) in their gastropod intermediate host, and develop from the [L.sub.3] to the adult ([L.sub.5]) stage in their cervid (final) host (Olsson et al. 1998, Olsson 2001). Specific identification of adult protostrongylids and first-stage larvae ([L.sub.1]) in feces of Swedish moose was a result of multiple studies. The morphology of E. alces was initially described by Steen et al. (1989) and (Steen and Johansson 1990), and subsequent comparison of specific proteins in protostrongylid [L.sub.1] indicated that [L.sub.1] and adult E. alces had the same protein pattern in moose, but differed from the [L.sub.1]s and adult protostrongylid parasites in other wild ruminants (Steen et al. 1993). Experimental infection of captive moose indicated that [L.sub.1] collected from wild moose caused elaphostrongylosis, and [L.sub.1] excreted from infected and sick moose and transmitted to terrestrial snails (Arianta arbustorum) in which larvae develop (Lankester et al. 1998), were identified as E. alces using genomic DNA (Gajadhar et al. 2000) and single-strand conformation polymorphism (SSCP) analysis (Chilton et al. 2005, Huby-Chilton et al. 2006). Collectively, these studies indicate that protostrongylid larvae in Swedish moose are E. alces. Given the prevalence and deleterious effect of this disease, our objective was to determine if E. alces is related to age, sex, condition, and geographic distribution of moose in Sweden.


Sweden was divided into 6 regions from the far north (69[degrees]03'36"N 20[degrees]32'55"E) to the far south (55[degrees]20'13"N 13[degrees]21'34"E)to determine the distribution and prevalence of elaphostrongylosis (Fig. 1). Sweden is sheltered by the Scandinavian mountains and has a continental climate with large differences in temperature and precipitation between summer and winter, and a relatively small amount of precipitation (Swedish Meteorological and Hydrological Institute [SMHI]). Summer temperatures are similar to those in North America and Asia at similar latitude, although due to the Gulf Stream, winter in Sweden is typically milder (SMHI 2015).


Hunting begins on the first Monday of September in northern Sweden, on the second Monday of October in the south, and seasons end in December or January (Swedish Association for Hunting and Wildlife Management 2015). Prior to the hunting seasons (1986 and 1987), we sent hunters report cards (hunting site, sex, and approximate age) and wrapping materials to pack body parts (i.e., lungs, feces, spinal cords, and mandibles). Moose carcasses and parts (n = 1137) were examined in 5 consecutive years (1985-1989); 896 (79%) were associated with harvested moose (1986, 1987, 1989) and 241 (21%) were from non-harvested animals (i.e., euthanized or found dead; 1985-1989). We used 1020 lungs and 1084 fecal samples to identify presence of elaphostrongylid [L.sub.1], 655 spinal cords (membranes) to identify presence of adult worms, and 636 mandibles to measure fat content (Table 1).

Age was determined by dental wear (Gasaway et al. 1978) or from information provided by hunters; 151 animals were not aged due to lack of information. Five age classes were established: 1) calves were [less than or equal to]12 months), 2) yearlings were >12 and [less than or equal to]24 months, 3) young animals were >24 months and [less than or equal to]5 years, 4) middle-aged animals were >5 and [less than or equal to]9 years, and 5) old animals were >9 years. Sex was determined from the whole carcass or hunter information.

Evaluation of body condition was by visual inspection, location, and appearance of body fat (n = 948), and/or by measuring fat content (%) in mandible bone marrow (n = 636; Engelsen Etterlin et al. 2009). Three categories of condition were established: normal, poor (below normal), and emaciated (lack of adipose tissue). The fat content in bone marrow was measured with standard techniques under specified assay conditions and techniques (NMKL No 131, Nordic Committee on Food Analysis 1989) and also used to assign condition: normal = 75-94%, poor = 16-<75%, and emaciated = 0.4-<16% fat content. Assigning condition from visual inspection (without measuring fat content) was considered reliable because of the strong correlation between the condition category assigned from fat measurements and visual inspection of the same animals ([R.sub.s] = -0.801, P < 0.001, n = 592).

Bodies/parts were inspected for adult E. alces worms and [L.sub.1] with necropsy procedures described previously (Steen and Rehbinder 1986, Steen et al. 1997, 1998) and included examination of muscle fasciae, the cranial cavity, brain, and spinal cord membranes and epidural space of the spinal cord (Steen and Rehbinder 1986, Steen et al. 1997). Lungs from all animals were palpated and inspected for nodules, and 20 g samples of minced lungs and feces were processed to detect [L.sub.1] (Baermann 1917). [L.sub.1]s were identified as protostrongylids quantified in a counting chamber under a stereo microscope, expressed as larvae per gram of wet feces (lpg), and classified into 7 levels of relative abundance ranging from none (0) to heavy (6) (National Veterinary Institute, Sweden). There were 4 categories of infection: 0 = uninfected, 1 = in the epidural space but not in lungs or feces, 2 = in lungs but not feces, and 3 = in feces. Animals were categorized as either infected or uninfected (presence or absence of [L.sub.1] and/or E. alces worms) for certain statistical comparisons (e.g., sex or age groups, prevalence in population or region),

Data management and statistics

Data were tested for normal distribution and seasonal variation, and if not normally distributed, normality was achieved with log-transformation. A peak function analysis was used to identify the best fit to the relationship between bone marrow fat and season (TableCurve software, Systat 2002). A mean value was calculated for harvested animals and this value was applied together with the individual values for remaining animals. The residuals for all animals were calculated (harvested moose were not combined as above), and adjusted values were calculated by adding the residual to the common mean. This produced a few values >100% that were not further corrected in subsequent analyses. Bone marrow fat (adjusted for seasonal variation) was subsequently analysed using generalized linear models. Body condition was also analysed with generalized linear models, modeling the probability of being in normal condition (see above) assuming a binary distribution of the response variable. The total parasite infection or parasites found in either the lungs, feces, or in the epidural space were similarly corrected, and the probability of being infected was tested with respect to 3 predictors (age, sex, region).

The age when calves were infected was estimated with birth date information from each county. Comprehensive data were available from 5 counties: Vasterbotten (AC in Region 1), Vastra Gotaland (O in Region 4), Kalmar (H in Region 5), Kronoberg (G in Region 5), and Sodermanland (D in Region 4) (Fig. 1). In 3 counties (H, G, and D) the mean value + SD (Malmsten 2014) was used as the birth date, and in 2 counties (AC and O) the mean value + SD was estimated (Broberg 2004). Birth dates for the counties without data were estimated using a multiple imputation (PROC MI in SAS statistical software, SAS 2014) with a Markov chain Monte Carlo method in which longitude and latitude of resident cities were used with the number of imputations set to 60. Other than 3 counties with a minor inconsistency (3-4 days), the approach produced an acceptable trend of earlier birth dates in southern Sweden, and the dates corresponded well with the span of birth dates reported by a national hunting organization (Swedish Association for Hunting and Wildlife Management 2015) (Table 2).

The mean category of infection (0-3) in each age group was calculated to illustrate the relationships among age (mean age of group), category of infection, and body condition. These values were used to develop a contour graph using SigmaPlot software (Systat 2008) where body condition, age group, and infection category were interpolated.


Infection, age and sex

Age of moose was skewed towards young animals (Table 1), and age in the two groups (harvested and unharvested) was not distributed evenly. Unharvested moose were older than those harvested for combined age classes, calves, and by sex (Table 3). The average age of harvested animals (n = 761) was 10.4 months (95% CI = 9.6-10.4; range = 0-15 years), and 22.3 months (CI = 17.4-28.4; range = 0-20 years) for unharvested animals (n = 227). Females were older in the yearling, middle-aged, and combined age groups.

A slight majority (57%) of the harvested sample (n = 896) was infected with [L.sub.1] and/or adult E. alces worms. The prevalence was similar between sexes in each age class for [L.sub.1] in lungs, [L.sub.1] in feces, and adult worms in the epidural space of the spinal cord (Fig. 2). There was a tendency (P = 0.074) toward higher prevalence in males than females in the young age class. Worms were found in the epidural space of the spinal cord in animals 3 months to 2 years old, but not in animals 3 to 9 years old; worms were found in a single 10-year old moose. The abundance of [L.sub.1] in lungs (n = 784) was high in calves and yearlings, lower at 3-4 years of age, and minimal in adults.

Nearly the entire sample (98%) of unhar-vested moose (n = 241) was infected with E. alces (Fig. 3). Worms were found in the epidural space of the spinal cord in 3 month to 4 year-old animals. The average age of infected calves was 4.8 months (95% CI = 4.7-4.9). No worms were found in the epidural space of the spinal cord in 5-9 year-old moose, but worms reappeared at 10-16 years of age.

The prevalence of adult worms in the epidural space of the spinal cord was 36% in the combined data (harvested and unhar-vested, n = 655); the prevalence of [L.sub.1] in lungs (n = 1020) and feces (n = 1084) was 64 and 53%, respectively. The prevalence (worms/[L.sub.1]) was 66% overall; 88% in old moose, 74% in yearlings, 67% in calves, 55% in young, and 48% in middle-aged animals. There were differences (P < 0.001) in frequency of infection among age groups; the oldest animals had the highest frequency of infection ([L.sub.1]) and the middle-aged the lowest. The frequency of worms in the epidural space of the spinal cord was high in calves/yearlings, leveled out at 4 years, and then was not identified until 10-16 years at low frequency. The abundance of [L.sub.1] in lungs of old animals was at the highest level (6).

Body condition

Body condition of harvested animals (n = 981) was either normal (40% overall, 24% calves) or poor (59%, 75% calves). In unharvested moose (n = 227), body condition was normal in 38% overall, with calves and old animals lower; 25% calves, 45% young, and 29% old animals were in normal condition.

For all moose, body condition and category of infection were correlated ([R.sub.s] = 0.215, P < 0.001). In separate age classes, this correlation was found in yearlings ([R.sub.s] = 0.262, P < 0.001, n = 239), young ([R.sub.s] = 0.463, P < 0.001, n = 67), middle-aged ([R.sub.s] = 0.441, P = 0.002, n = 47), and old animals ([R.sub.s] = 0.456, P = 0.003, n = 40), but not in calves ([R.sub.s] = 0.054, P = 0.239, n = 471). For all moose, body condition was correlated inversely with category of infection ([R.sub.s] = 0.084, P = 0.025, n = 721); separate correlations were found in yearlings ([R.sub.s] = 0.213, P = 0.002, n = 227) and young animals ([R.sub.s] = 0.398, P = 0.011, n = 40). Figure 4 illustrates the probability of normal body condition relative to age and category of infection, indicating that calves have poor body condition regardless of category of infection, and that some middle-aged animals have normal body condition despite high abundance of [L.sub.1] in feces. Old individuals were generally in normal body condition if not infected, although few were without infection.

Bone marrow fat content (n = 615) varied annually (Table 4, Fig. 5). On average, harvested animals had higher fat content (93%, 95% CI = 91-96) than unharvested animals (70%, CI = 66-75) with values corrected for time of year, sex, and age class (Table 4). In a combined sample, a negative correlation was found between bone marrow fat content and category of infection ([R.sub.s] = -0.212, P < 0.001, n = 635). This negative correlation was found in calves ([R.sub.s] = -0.131, P = 0.020, n = 319), yearlings ([R.sub.s] = -0.223, P = 0.002, n = 193), young ([R.sub.s] = -0.618, P < 0.001, n = 46), and old ([R.sub.s] = -0.736, P < 0.001, n = 21), but not middle-aged moose ([R.sub.s] = -0.319, P = 0.062, n = 35).

Time of infection

The earliest identification of a calf diagnosed with elaphostrongylosis was at ~1.5 months on 21 July in Region 3, County of Uppsala (Table 5). The abundance of [L.sub.1] was category 6 in the lungs and 4 in feces, and the calf was in normal body condition. The earliest calf death where worms were found in the epidural in the spinal cord was on 10 October (~4 months old) in Region 2, County of Varmland; the abundance of [L.sub.1] was category 6 in the lungs and 3 in feces.

Worms were first found in harvested calves on 15 September (~3 months old). The abundance of [L.sub.1] was category 0 in the lungs and 6 in feces. First stage larvae (infection intensity = 6) were found in lungs from 14 August (~2 months old) to 4 June the following year (~12 months old). Abundance of [L.sub.1] in calves ranged from categories 1-6 by 2 months old, and the lung infection remained high; 81% had an [L.sub.1] abundance category of 4-6 in the first year. The excretion of larvae began at a low level (2) on 14 August, and calves continued to excrete larvae throughout the first year at all levels of abundance (1-6).

The prevalence of infection in harvested moose (n = 896) differed among regions (Fig. 6), ranging from 13% in southernmost Region 6 to 56% in Region 3 (Fig. 1 and Table 2). Infection was most prevalent in central Sweden, least prevalent in southern Sweden, and similar (P < 0.05) in southern and northern Sweden.


Although parasites at low abundance are generally less harmful to their host, when the host population increases rapidly, as with Swedish moose in the 1970-80s (Hornberg 2001, Steen et al. 2005), an increasing risk to the individual and host population is possible (Toft 1991). The proportion of elaphostrongylosis (symptoms of nervous disorder and/or emaciation) varies among age-classes in moose, with young animals more prone to illness (Steen et al. 2005). Similarly, we found that E. alces worms located in the epidural space of the spinal cord were more prevalent in calves and yearlings, and only occasionally found in adults. The high abundance measured in young animals may simply reflect that the Swedish moose population is skewed towards young animals (Sand et al. 2011). Conversely, abundance of [L.sub.1] in lungs and feces was highest in old moose, and lowest in young and middle-aged moose.

Both Stuve (1986) and Steen et al. (2005) suggested that E. alces most frequently infects males and young animals; however, we found no difference in the abundance within the epidural space, lungs, or feces between sexes or age groups of harvested moose, only a tendency toward males in the young age group. Similarly, male reindeer calves with dominant mothers had higher abundance of E. rangiferi than female calves, and it was suggested that because these calves had better access to forage, they were at greater risk of ingesting infected gastropods (Halvorsen 1986a). Calf weight is dependent on summer browse availability in a cow's home range, with access to and quality of forage related to its relative status (Saether and Heim 1993). Stuve (1986) attributed the difference in infection rate between sexes in older moose to physiological changes associated with the rut, as suggested with reindeer (Halvorsen 1986b).

A novel finding of our study was that [L.sub.1] were found in lungs and feces of calves by 21 July, and adult worms in the epidural space by 15 September, or ~50-100 days after birth (Broberg 2004, Malmsten 2014). This prepatent period aligns with experimental infections of E. alces in moose in which patent infection was realized 39-73 days post-infection (Steen et al. 1997). Because calves sample vegetation in the first days of life to promote development of rumen microbes (Syroechkovsky et al. 1989), their potential to exposure to E. alces [L.sub.3] is almost immediate. Not surprisingly, adult E. alces were identified in the epidural space of the caudal vertebral canal in 2 other calves harvested in September (Handeland and Gibbons 2001). Further, calves and yearlings were most frequently infected in the epidural space of the spinal cord which seemingly corroborates that moose shed most E. alces [L.sub.1] during their early years, after which a sharp drop in larval shedding and low numbers of adult worms in older animals occur (Stuve 1986, Steen et al. 2005).

In both harvested and unharvested moose, E. alces worms were found in the epidural space of the spinal cord of animals aged 3-4 months to 4 years, not in middle-aged animals, and again at 10-16 years. Conversely, high levels of larvae were found in lungs and feces irrespective of age. We believe that the low frequency of worms in older animals, despite having [L.sub.1] in lungs and shed larva, is due to migration from the CNS/PNS into the muscle fasciae, as with some other elaphostrongylins (Lankester 2001).

The pattern of E. alces adults migrating out to the muscle fasciae, presumably due to an immune response in the epidural space (Steen et al. 1997, 1998), differs somewhat from that of E. rangiferi, E. cervi, and P. tenuis. The latter are believed to remain in the CNS as adult worms during their entire life (in the subdural or subarachnoid space, inside the meninges), although E. rangiferi also migrates to the muscle fasciae (Hemmingsen et al. 1993). E. rangiferi, E. cervi, and P. tenuis may realize an immuno-logical harbor within the CNS, as might P. andersoni that is associated with blood vessels and connective tissues where females deposit eggs (Lankester 2001). We hypothesize that E. alces worms are attacked by the immune system in the epidural space, and they migrate to the muscle fasciae where, with lower immunological defense, they deliver most of their larvae.

After ingestion, [L.sub.3] migrate from the gastrointestinal (GI) tract to the perineal cavity along the mesenchyme nerves, and into the abdominal wall associated with the more posterior lateral nerves. It is likely that E. alces does not need to enter the CNS parenchyma to develop to the 5th stage (adult), as other Elaphostrongylus spp., but remains epidurally-associated with lateral nerves of the PNS and finally migrates to the muscle fasciae (Olsson et al. 1998). The lack of worms in the epidural space of the spinal cord in moose during their prime could be explained by this migration; however, it could also reflect an immune response to prevent reinfection as described for P. andersoni that realizes declining larval output as deer age with few adult worms in deer >1 year old. Further, repeated infection in white-tailed deer resulted in sharp decline in larval numbers and a strong cellular response to adult worms (Lankester 2001). Worms in the epidural space of older moose could simply be a reinfection associated with a weaker immune system, or an initial infection. Whether some [L.sub.3]s migrate directly to muscle fasciae without being associated with neural tissue is unknown.

Infected animals, on average, had lower body condition than uninfected animals except for middle-aged animals in their prime. Calves were in poorer condition regardless of category of infection (as expected for young, growing animals), middle-aged were likely in normal condition despite high shedding rate of [L.sub.1] in feces, and old individuals were in normal condition if uninfected. Thus, infection, not age per se, seemed to reflect relative body condition. However, individual variation of immunological response to the parasite presumably exists because some individuals die young, others remain in normal condition through prime, and old animals are increasingly susceptible.

In contrast with E. alces, no protostrongylid [L.sub.1] of E. cervi were recovered from Iberian red deer fawns (Cervus elaphus hispanicus) (Vicente and Gortazar 2001). Prevalence of E. cervi [L.sub.1] increased with age of deer (Vicente et al. 2006) which is opposite to our findings with E. alces in moose; both had higher infection rates in young males than females. The E. cervi pattern corresponds with that in reindeer in which E. rangiferi infects the host late in the season, remaining at the same intensity for at least 3 years (Halvorsen et al. 1985).

It appears that E. cervi and E. rangiferi have more similar and longer evolutionary relationships to each other and their respective hosts than E. alces. Moose have a long, independent evolutionary history from the Alceini and the Plio-Pleistocene, suggesting a peculiar adaption and habitat restriction of the species (Niedzialkowska et al. 2014), and presumably, a relatively short evolutionary period with E. alces that could be less adapted with its host than E. cervi and E. rangiferi. It is possible that E. alces is more pathogenic to its host because both harvested and unharvested moose of below normal or emaciated body condition were infected with E. alces. In 2-year old moose, Stuve (1986) found that infected moose were lighter (carcass weight) than uninfected moose, yet conversely, Steen et al. (1997) found that moose experimentally infected with E. alces retained normal weight when fed ad libitum. It remains unclear, however, if poor body condition is an indirect or direct effect of the parasite, that emaciation is either directly caused by an inflammatory response due to an epidural localization, or that elaphostrongylosis causes locomotor disorders making it difficult to move and feed (Steen and Rehbinder 1986, Steen and Roepstorff 1990, Steen et al. 2005).

In summary, different morphology (Steen et al. 1989, Steen and Johansson 1990, Gibbons et al. 1991, Lankester et al. 1998), genetics (Gajadhar et al. 2000, Chilton et al. 2005, Huby-Chilton et al. 2006), location (Steen et al. 1997, 1998) (epidural for E. alces, subdural/subarachnoid for E. rangiferi), and life span and host age relationships with infection (Lankester 2001) suggest different, and perhaps, ongoing evolutionary adaption in Elaphostrongylus species with their hosts. Of further consequence is that rising temperatures, and a warmer and wetter climate are predicted to increase habitat, distribution, and abundance of mollusk hosts (Halvorsen and Skorping 1982, Halvorsen et al. 1985), which in turn could lead to higher infection rates in cervids (Handeland and Slettback 1994, Halvorsen 2012). Although moose are not necessarily in poor condition when infected with E. alces, condition and parasite abundance were correlated. We therefore suggest continued surveillance of this disease and its specific consideration in management of moose in Sweden.


We thank W. E. Faber, Department of Natural Resources, Central Lakes College, Brainerd, Minnesota, USA for his feedback on the manuscript. We are grateful for all technical help and assistance from employees, and earlier employees H. Mann, S. Persson, and I. Forssell at the Department of Parasitology, National Veterinary Institute and Swedish University of Agricultural Sciences, Uppsala, Sweden. Last, but not least, we thank Swedish hunters for their help and cooperation in data collection. Financial support for this study was provided by the Swedish Environmental Protection Agency, Stockholm, Sweden.


ANDERSON, R. C. 1964. Neurological disease in moose experimentally infected with Pneumostrongylus tenius from white-tailed deer. Veterinary Pathology 1: 289-322. doi: 10.1177/030098586400100402.

BAERMANN, G. 1917. Eine einfache Metode zur Auffindung von Ancylostoma-(Nematoden-) Larven aus Erdproben. Mededeel uithet Geneesk Lab. te Wel-tevreden, Feestbundel, Batavia, pp. 41-47 (in German).

BROBERG, M. 2004. Reproduction in Moose: Consequences and Conflicts in Timing of Birth. Doctoral Thesis, Gothenburg University, Gothenburg, Sweden.

CHILTON, N. B., F. HUBY-CHILTON, M. W. LANKESTER, and A. A. GAJADHAR. 2005. A method for extracting genomic DNA from individual elaphostrongyline (Nematoda: Protostrongylidae) larvae and differentiation of Elaphostrongylus spp. from Parelaphostrongylus spp. by PCR assay. Journal of Veterinary Diagnostic Investigation 17: 585-588. doi: 10.1177/104063870501700612.

ENGELSEN ETTERLIN, P., A. NEIMANIS, D. GAVIER-WIDEN, and C. HARD AF SEGERSTAD. 2009. Postmortal Hullbe-domning av Hull Hos Tamdjur och Vilda Djur (Postmoral Examination of Body Condition in Pet Animals and Wildlife). National Veterinary Institute, Uppsala, Sweden (in Swedish).

GAJADHAR, A., T. STEEVES-GURNSEY, J. KENDALL, M. LANKESTER, and M. STEEN. 2000. Differentation of protostrongylid dorasal-spined larvae by PCR Amplication of ITS-2 Rdna. Journal of Wildlife Diseases 36: 713-722. doi: 10.7589/0090-3558-36.4.713.

GASAWAY, W. C., D. B. HARKNESS, and R. A. RAUSCH. 1978. Accuracy of moose age determinations from incisor cementum layers. Journal of Wildlife Management 42: 558-563. doi: 10.2307/3800818.

GIBBONS, L. M.,O. HALVORSEN, andG. STUVE. 1991. Revision of the genus Elaphostrongylus Cameron (Nematoda, Metastrongyloidea) with particular reference to species of the genus occurring in Norwegian cervids. Zoologica Scripta 20(1): 15-26. doi: 10.1111/j.1463-6409.1991.tb00272.x.

HALVORSEN, O. 1986a. On the relationship between social status of host and risk parasitic infection. Oikos 47: 71-74. doi: 10.2307/3565921.

--. 1986b. Epidemiology of reindeer parasites. Parasitology Today 12: 334-339. doi: 10.1016/0169-4758(86)90053-0.

--. 2012. Reindeer parasites, weather and warming of the Arctic. Polar Biology 35: 1209. doi: 10.1007/s00300-012-1209-0.

--, and A. SKORPING. 1982. The Influence of temperature on growth and development of the nematode Elaphostrongylus rangiferi in the gastropods Arianta abustrum and Euconulus fulvus. Oikos 38: 285-290. doi: 10.2307/3544666.

--, A. SKORPING, and K. HANSEN. 1985. Seasonal cycles in the output of first stage larvae of the nematode Elaphostrongylus rangiferi from reindeer, Rangifer tarandus tarandus. Polar Biology 5: 49-54. doi: 10.1007/BF00446045.

HANDELAND, K., and L. M. GIBBONS. 2001. Aspects of the life cycle and pathogenesis of Elaphostrongylus alces in moose (Alces alces). Journal of Parasitology 87: 1054-1057. doi: 10.1645/0022-3395 (2001)087[1054:AOTLCA]2.0.CO;2.

--, and T. SLETTBAKK. 1994. Outbreaks of clinical cerebrospinal Elaphostrongylosis in reindeer (Rangifer tarandus tarandus) in Finnmark, Norway, and their relation to climatic conditions. Journal of Veterinary Medicine B 41(1-10): 407-410. doi: 10.1111/j.1439-0450.1994.tb00244.x.

HEMMINGSEN, W., O. HALVORSEN, and A. SKORPING. 1993. Migration of Adult Elaphostrongylus rangiferi (Nematoda: Protostrongylidae) from the spinal subdural space to the muscles of reindeer (Rangifer tarandus). Journal of Parasitology 79: 728-732. doi: 10.2307/3283612.

HUBY-CHILTON, F., N. B. CHILTON, M. W. LANKESTER, and A. A. GAJADHAR. 2006. Single-strand conformation polymorphism (SSCP) analysis as a new diagnostic tool to distinguish dorsal-spined larvae of the Elaphostrongylinae (Nematoda: Protostrongylidae) from cervids. Veterinary Parasitology 135: 153-162. doi: 10.1016/j.vetpar.2005.08.001.

HORNBERG, S. 2001. Changes in population density of moose (Alces alces) and damage to forests in Sweden. Forest Ecology and Management 149: 141-151. doi: 10.1016/S0378-1127(00)00551-X.

LANKESTER, M. W. 2001. Extrapulmonary lungworms of cervids. Pages 228-278 in W. M. Samuel, A. A. Kocan, and M. Pybus, editors. Parasitic Diseases of Wild Mammals, 2nd edition. Iowa State University Press, Ames, IA.

--. 2010. Understanding the impact of meningeal worm, Parelaphostrongylus tenuis, on moose population. Alces 46: 53-70.

--, I.-M. C. OLSSON, M. STEEN, and A.A. GAJADHAR. 1998. Extra-mammalian larval stages of Elaphostrongylus alces (Nematoda: Protostrongylidae), a parasite of moose (Alces alces) in Fennoscandia. Canadian Journal of Zoology 76: 33-38. doi: 10.1139/z97-168.

MALMSTEN, J. 2014. Reproduction and health of moose in southern Sweden. Doctoral Thesis, Swedish University of Agricultural Sciences, Uppsala, Sweden.

NIEDZIALKOWSKA, M., K. J. HUNDERTMARK, B. JEZDRZEJEWSKA, K.NIEDZIALKOWSKI, V. E. S IDOROVICH, M. GORNY, R. VEEROJA, E. J. SOLBERG, S. LAAKSONEN, H. SAND, V. A. SOLOVYEV, M. SHKVYRIA, J. TIAINEN, I. M. OKHLOPKOV, R. JUSKAITIS, G. DONE, V. A. BORODULIN, E. A. TULANDIN, and W. JEZDRZEJEWSKI. 2014. Spatial structure in European moose (Alces alces): genetic data reveal a complex population history. Journal of Biogeography 41: 2173-2184. doi: 10.1111/jbi.12362.

NORDISK METODIK-KOMMITTE for LIVSMEDEL (NORDIC COMMITTEE on FOOD ANALYSIS). 1989. SBR (Schmid-Bondzynski-Ratslaff), No. 131. Esbo, Finland. (accessed July 2015).

OLSSON, I.-M. 2001. Elaphostrongylus alces--transmission, larval morphology and tissue migration. Veterinary Medicine Licentiate Thesis, Swedish University of Agricultural Sciences, Uppsala, Sweden.

--, M. W. LANKESTER, A. A. GAJADHAR, and M. STEEN. 1998. Tissue migration of Elaphostrongylus spp. in guinea pigs (Cavia porcellus). Journal of Parasitology 84: 968-975. doi: 10.2307/3284629.

SAETHER, B. E., and M. HEIM. 1993. Ecological correlates of individual variation in age at maturity in female moose (Alces alces); the effects of environmental variability. Journal of Animal Ecology 62: 482-489. doi: 10.2307/5197.

SAND, H., N. JONZEN, H. ANDREN, and J. MANSSON. 2011. Strategier for beskattning av alg. (Strategies for Moose Management). Forest Facts, Report from the Swedish University of Agricultural Sciences, No. 2 4, p 4 (In Swedish).

SAS 2014. Version 9.4 TS Level 1M0, X64_7PRO platform, SAS Institute Inc., Cary, North Carolina, USA.

STEEN, M., C. G. M. BLACKMORE, and A. SKORPING. 1997. Cross-infection of moose (Alces alces) and reindeer (Rangifer tarandus) with Elaphostrongylus alces and Elaphostrongylus rangiferi (Nematoda, Protostrongylidae): effects on parasite morphology and prepatent period. Veterinary Parasitology 71: 27-38. doi: 10.1016/S0304-4017(97)00013-7.

--, A. G. CHABAUD, and C. REHBINDER. 1989. Species of the genus Elaphostrongylus, parasite of Swedish Cervidae. A description of E. alces n. sp. Annales de Parasitologie, Humanie et Comparee 64: 134-142.

--, AND C. JOHANSSON. 1990. Elaphostrongylus spp. from Scandinavian cervidae--a scanning electron study (SEM). Rangifer 10: 39-46. doi: 10.7557/

--, I.-M. OLSSON, AND E. BROMAN. 2005. Diseases in a moose population subjected to low predation. Alces 41: 37-48.

--, S. PERSSON, AND L. HAJDU. 1993. Protostrongylidae in Cervidae and Ovibus moscatus; a clustering based on isoelectric focusing on nematode proteins. Rangifer 13: 221-223. doi: 10.7557/

--, AND C. REHBINDER. 1986. Nervous tissue lesions caused by elaphostrongylosis in wild Swedish moose. Acta Veterinaria Scandinavia 27: 326-342.

--, and L. ROEPSTORFF. 1990. Neurological disorder in two moose calves (Alces alces L.) naturally infected with Elaphostrongylus alces. Rangifer, Special Issue 3: 399-406. doi: 10.7557/

--, I. Y. WARSAME, and A. SKORPING. 1998. Experimental infection of reindeer, sheep and goats with Elaphostrongylus spp. (Nematoda, Protostrongylidae) from moose and reindeer. Rangifer 18: 73-80. doi: 10.7557/

STUVE, G. 1986. The prevalence of Elaphostrongylus cervi infection in moose (Alces alces) in southern Norway. Acta Veterinaria Scandia 27: 397-409.

SYROECHKOVSKY, E. E., E. V. ROGACHEVA, and L. A. RENECKER. 1989. Moose husbandry. Pages 369-386 in R. J. Hudson, K. R. Drew, and L. M. Baskin, editors. Wildlife Production Systems. Economic Utilization of Wild Ungulates. Cambridge University Press, Cambridge, England.



SYSTAT. 2002. Table Curve 2D, version 5.01. SYSTAT Software Inc., San Jose, CA.

--. 2008. SigmaPlot for Windows version 11.0, Build SYSTAT Software Inc., San Jose, California, USA.

TOFT, C. A. 1991. An ecological perspective: the population and community consequences of parasitism. Pages 319-343 in C. A. Toft, A. Aeschlimann, and L. Bolis, editors. Parasite-Host: Association Coexistence or Conflict? Oxford University Press, Oxford, England.

VICENTE, J., I. G. FERNANDEZ DE MERA, AND C. GORTAZAR. 2006. Epidemiology and risk factors analysis of elaphostrongylosis in red deer (Cervus elaphus) from Spain. Parasitology Research 98: 77-85. doi: 10.1007/s00436-005-0001-2.

--, and C. GORTAZAR. 2001. High prevalence of large spiny-tailed protostrongylid larvae in Iberian red deer. Veterinary Parasitology 96: 165-170. doi: 10.1016/S0304-4017(00)00425-8.

Margareta Steen (1), Ing-Marie Olsson Ressner (2), Bodil Olsson (3), and Erik Petersson (4)

(1) Department of Anatomy, Physiology and Biochemistry, Swedish University of Agricultural Sciences, P. O. Box 7090, SE-750 07 Uppsala, Sweden; (2) Swedish Chemicals Agency (KemI), P. O. Box 2, SE-172 13 Sundbyberg, Sweden; (3) TNS Sifo, P.O. Box 115 00, SE-404 30 Gothenburg, Sweden; (4) Department of Aquatic Resources, Swedish University of Agricultural Sciences, SE-178 93 Drottningholm, Sweden

Corresponding author: Margareta Steen, Department of Anatomy, Physiology and Biochemistry, Swedish University of Agricultural Sciences, PO. Box 7068, SE-750 07 Uppsala, Sweden,

Table 1. Total number of moose (harvested/unharvested) and sample
location/type--epidural space of the spinal cord (epidural), lungs,
feces, mandibles--used to study Elaphostrongylus alces in Sweden,

              Moose    Epidural  Lungs    Feces    Mandibles

 Males        386/87   173/85    343/84   369/85   260/36
 Females      456/147  223/144   404/145  427/145  262/57
 Unknown       54/7     23/7      37/7     49/7     21/-
Age group
 Calves       457/107  187/103   392/102  434/103  270/48
 Yearlings    227/36   113/36     52/12   220/36   182/11
 Young         40/27    23/27     39/27    38/27    36/10
 Middle aged   31/19    27/19     28/19    26/19    30/5
 Old            6/37     4/37      6/37     6/37     5/16
 Unknown      135/14    65/13    110/14   123/14    20/1
Total         896/241  419/236   784/236  847/237  543/93

Table 2. Prevalence of Elaphostrongylus alces (adjusted for Julian
date and age of the sampled moose) and birth date of moose in Swedish
counties. Birth dates marked with an asterisk are observed values;
others are estimated (see Data management and statistics).

Region  County                   Mean prevalence (%)   N

1         AC    Vasterbotten          43.8              82
1         BD    Norrbotten            51.4              13
1          Z    Jamtland              53.5               8
1          Y    Vasternorrland        58.2              21
2          W    Dalarna               63.2              32
2          X    Gavleborg             67.7             457
2          S    Varmland              49.4              36
3          B    Stockholm             61.7               2
3          C    Uppsala              100.0               3
3          T    Orebro                67.4              17
3          U    Vastmanland           79.3              15
4          D    Sodermanland         100.0               5
4          E    Ostergotland          27.6              12
4          O    Vastra Gotaland       53.9              12
5          F    Jonkoping             39.1              16
5          G    Kronobergs            28.2              10
5          H    Kalmar                32.2              11
6          K    Blekinge              37.4               5
6          M    Skane                    0               8
6          N    Halland               41.5              12

Region  Birth date (Julian date)  Birth date

1           167*                   16 June
1           168                    17 June
1           171                    20 June
1           164                    13 June
2           160                     9 June
2           157                     6 June
2           159                     8 June
3           149                    29 May
3           152                     1 June
3           156                     5 June
3           154                     3 June
4           148*                   28 May
4           150                    30 May
4           153*                    2 June
5           151                    31 May
5           144*                   24 May
5           143*                   23 May
6           140                    20 May
6           144                    24 May
6           146                    26 May

Table 3. Age in months (mean and 95% CI) of Swedish moose examined for
Elaphostrongylus alces, 1985-1989. The column to the far right gives
level of significance between harvested and euthanized + dead moose
(for the last three rows the t-tests are performed on log transformed
data; the data presented in the table are back-transformed values). If
all sexed animals are combined, the sexes differed in age (P < 0.05).

Age class                Sex

Calves                   Females
                         All calves ([double dagger])
Yearlings (*)            Females
Young                    Females
                         Combined ([double dagger])
Middle-aged (*)          Females
                         Combined ([double dagger])
Old                      Females
                         Combined ([double dagger])
All females ([section])
All males ([section])
All moose

Age class                  Harvested          Unharvested

Calves                     4.3 (4.1-4.4)        8.5 (8.1-8.8)
                           4.2 (4.0-4.4)        8.1 (7.8-8.4)
                           4.2 (3.5-5.0)        8.3 (6.6-9.9)
Yearlings (*)             18.4 (17.7-19.0)     19.2 (17.5-20.9)
                          17.7 (17.0-18.4)     17.3 (15.6-19.0)
                          18.0 (16.9-19.1)     18.3 (15.4-21.1)
Young                     46.5 (42.8-50.4)     47.4 (43.0-51.7)
                          42.0 (36.9-47.1)     44.6 (37.4-51.8)
                          44.7 (42.0-47.4)     46.2 (42.9-49.5)
Middle-aged (*)           90.3 (85.0-95.5)     93.4 (86.7-100.2)
                          84.0 (74.4-93.6)     76.8 (65.5-88.1)
                          89.0 (86.0-92.1)     89.1 (85.1-93.0)
Old                      144.0 (106-181.7)    154.2 (141.3-167.2)
                         120.0 (144.6-195.4)  144.0 (100.5-187.5)
                         146.0 (139.1-152.9)  153.4 (150.6-156.2)
All females ([section])   12.3 (10.7-14.1)     29.6 (21.0-41.6)
All males ([section])      9.0 (8.0-10.0)      14.2 (10.7-18.7)
All moose                 10.4 (9.6-11.4)      22.3 (17.4-28.4)

Age class                t-value

Calves                   22.3, P < 0.001
                         21.1, P < 0.001
                          4.28, P < 0.001
Yearlings (*)             0.91, P = 0.362
                          0.36, P = 0.716
                          0.17, P = 0.863
Young                     0.28, P = 0.782
                          0.58, P = 0.562
                          0.70, P = 0.481
Middle-aged (*)           0.74, P = 0.461
                          0.98, P = 0.333
                          0.01, P = 0.994
Old                       0.52, P = 0.606
                          0.56, P = 0.580
                          1.94, P = 0.053
All females ([section])   4.73, P < 0.001
All males ([section])     3.92, P = 0.004
All moose                 5.74, P < 0.001

(*) Sexes differ by age class (all causes of death included).
([double dagger]) Includes individuals not sexed.
([section]) Sexes differ with all age classes combined.

Table 4. Analysis of bone marrow fat (%) and body condition of
harvested and unharvested moose, Sweden, 1985-1989. Values are mean
[+ or -] SE with sample size in parentheses. Pair-wise comparisons
(t-values) of harvested and unharvested animals are provided in each
age group (raw). Means denoted by the same letter in each column
(percent fat and body condition separately) were not different
(P < 0.05). The values for percent fat are adjusted for time of year
causing certain values to be >100% (see Data management and

Variable             Age class          Harvested

Bone marrow fat (%)  Calves        83.6 [+ or -] 0.8a (270)
                     Yearlings     97.1 [+ or -] 0.9b (182)
                     Young         98.7 [+ or -] 2.1b (36)
                     Middle aged   99.6 [+ or -] 2.3b (30)
                     Old          104.6 [+ or -] 5.7b (5)
                     All animals   96.7 [+ or -]1.3 (523)
Probability of       Calves         0.17 [+ or -] 0.03a (368)
normal condition     Yearlings      0.48 [+ or -] 0.04b (204)
                     Young          0.50 [+ or -] 0.11bc (40)
                     Middle aged    0.74 [+ or -] 0.12c (30)
                     Old            0.84 [+ or -] 0.17abc (6)
                     All animals    0.33 [+ or -] 0.02 (648)

Variable              Euthanized or dead           Statistic

Bone marrow fat (%)  60.5 [+ or -] 1.8a (48)     t = 11.6 P < 0.001
                     69.9 [+ or -] 3.8b (11)      t = 6.88 P < 0.001
                     83.6 [+ or -] 4.0c (10)      t = 3.32 P < 0.001
                     77.4 [+ or -] 5.7bc (5)      t = 3.62 P < 0.001
                     63.3 [+ or -] 3.2ab (16)     t = 6.34 P < 0.001
                     70.9 [+ or -]1.7 (92)       t = 11.6 P < 0.001
Probability of        0.25 [+ or -] 0.06a (102)   z = 0.81 P = 0.420
normal condition      0.30 [+ or -] 0.12c (35)    z = 1.19 P = 0.235
                      0.47 [+ or -] 0.15b (27)    z = 0.25 P = 0.800
                      0.64 [+ or -] 0.21b (17)    z = 0.34 P = 0.734
                      0.12 [+ or -] 0.06ab (34)   z = 2.53 P = 0.012
                      0.29 [+ or -] 0.05 (215)    z = 0.56 P = 0.578

Table 5. Age (in days) of moose calves infected by Elaphostrongylus
alces, Sweden, 1985-1989.

Parasite          Mean age          Min  Max
location   N      [+ or -]SD        age  age

Epidural  281  140.8 [+ or -] 20.0   50  215
Lung      348  140.2 [+ or -] 20.8   50  215
Feces     416  141.0 [+ or -] 17.6  101  215
COPYRIGHT 2016 Alces
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2016 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Steen, Margareta; Ressner, Ing-Marie Olsson; Olsson, Bodil; Petersson, Erik
Article Type:Report
Geographic Code:4EUSW
Date:Jan 1, 2016
Previous Article:Provincial population and harvest estimates of moose in British Columbia.
Next Article:Recruitment of winter ticks (Dermacentor albipictus) in contrasting forest habitats, Ontario, Canada.

Terms of use | Privacy policy | Copyright © 2019 Farlex, Inc. | Feedback | For webmasters