Infection with brainworm (Elaphostrongylus rangiferi) in reindeer (Rangifer tarandus ssp.) in Fennoscandia

Abstract

Sami reindeer herders have considerable traditional knowledge about a neurological reindeer disease resembling elaphostrongylosis, but the causative agent was not identified prior to the description of the brainworm Elaphostrongylus rangiferi in Russia in 1958. Elaphostrongylosis was quickly recognised as a serious cause of reindeer morbidity and mortality. The ecology, epidemiology and pathophysiology of the disease were studied in Sweden and Norway during the 1960s and in particular the 1970s to 1990s. In Finland, elaphostrongylosis was not recognised as an important disease for Finnish reindeer husbandry, even though the presence of brainworm infection has been documented. Brainworm has an indirect lifecycle with snail and slug intermediate hosts. The free-living L1 larvae have extremely good freeze tolerance and can survive > 360 days at - 80 °C in water (solid ice). Even though reindeer brainworm is clearly well adapted to the Arctic chill, the lifecycle stages outside the reindeer final host are sped up at warmer environmental temperatures. Arctic summer temperatures are close to the developmental threshold of the parasite in the intermediate gastropod hosts (8-10 °C), and the parasite has typically had a 2-year life cycle. Disease outbreaks generally occur during the winter following the infection of reindeer with infected snails and slugs during the summer and autumn. Warmer summers result in faster development of brainworm larvae in the intermediate hosts. Clinical symptoms have been seen reported as early as August, such as in the outbreak in Trøndelag, Norway in 2018. The reindeer brainworm is also a cause of conflict between reindeer herders and small ruminant farmers, because it can cause severe disease in goats and sheep, which share pasture with reindeer. Many knowledge gaps remain if we wish to successfully predict and mitigate for large-scale outbreaks in a future with a predicted warmer, wetter and wilder climate.

Keywords: Climate change; Diagnosis; Epizootic; Goat; Lifecycle; Neurological disease; Pathogenesis; Protostrongylid; Rangifer tarandus tarandus; Sheep; Treatment.

Fig. 1

Lifecycle of Elaphostrongylus rangiferi, brainworm, with reindeers as the final host and with slugs and snails as the intermediate host

Fig. 2

a Reindeer showing neurological signs suggestive of clinical elaphostrongylosis with the characteristic kyphotic stance (courtesy of Kjell Handeland); b reindeer showing circling behaviour with Elaphostrongylus infection (courtesy of Morten Tryland)

Fig. 3

Photomicrographs showing histopathological changes in the brain of a reindeer infected with Elaphostrongylus rangiferia Multiple nematodes and associated inflammation in the meninges covering the cerebellum. The haemorrhage was caused by the euthanasia (Obj. 2.5×). (b) Detail of a showing the cellular infiltrate around the nematodes (Obj. 20×). c Longitudinal sections of nematodes (black arrows) (Obj. 10×). d Transverse section of a nematode and mononuclear cell response in the meninges of the cerebellum (Obj. 20×). a–d haematoxylin and eosin

Fig. 4

Adult Elaphostrongylus nematodes in muscle fascia (Courtesy of Kjell Handeland). The thin dark threadlike parasites can be seen coiled in the centre of the image

Fig. 5

Photomicrographs showing histopathological changes in the lungs of a reindeer infected with Elaphostrongylus rangiferi. a Heavily infected area with multiple transverse as well as longitudinal larvae (black arrows) and eggs (blue arrow). Mononuclear cells and giant cells (grey arrow) surround the parasites. b An area less infected. A coiled larva (black arrow) as well as several eggs (blue arrows) are seen. Mononuclear cells are present in the interstitium. a, b Obj. 10×, haematoxylin and eosin

Fig. 6

Elaphostrongylus rangiferi larva at L1 development stage. The larva has been fixed in ethanol prior to photography

Fig. 7

Time taken for Elaphostrongylus rangiferi L1 larvae to develop to L3 at different temperatures. Temperature data for Trøndelag, Norway was used to show fluctuations in mean monthly environmental temperature (for 2018–2019; data from http://www.yr.no) and the developmental threshold times indicated [50] (reproduced with permission of Dr. Hannah Vineer, University of Liverpool). Also shown are the peak periods for brainworm L1 larval output by male and female reindeer [29]

Fig. 8

Photomicrographs showing histopathological changes in the spinal cord of a goat infected with Elaphostrongylus rangiferi. a, b foci of malacia in spinal cord white matter due to nematode migration. c Transverse sections of adult nematodes in the white matter. a: Obj. 2.5×; b: Obj. 10×; c: Obj. 20×. a–c: Haematoxylin and eosin

Fig. 9

The number of elaphostrongylosis cases in the period 2000–2019 diagnosed at the Norwegian Veterinary Institute by species (reindeer, goat, sheep). The diagnosis is based on the detection of histopathological changes and nematodes in the central nervous system combined with the presence of clinical signs. However the species of Elaphostrongylus involved was not further identified. We cannot rule out that some of the small ruminant cases in particular could potentially be caused by other brainworm species like E. cervi (from red deer) or E. alces (from moose) especially in areas where grazing does not overlap with reindeer