Myxomatosis is an infectious disease caused by the myxoma virus (MYXV), which has very high mortality rates in European wild rabbits (Oryctolagus cuniculus). While sporadic cases of myxomatosis have also been reported in some hare species, these lagomorphs are considered to have a low susceptibility to MYXV infection. In the present study, we describe the spatiotemporal evolution and main epidemiological findings of novel hare MYXV (ha-MYXV or MYXV-Tol) epidemics in Iberian hares (Lepus granatensis) in Spain. In the period 2018-2020, a total of 487 hares from 372 affected areas were confirmed to be MYXV-infected by PCR. ha-MYXV outbreaks were detected in most of the Spanish regions where the Iberian hare is present. The spatial distribution was not homogeneous, with most outbreaks concentrated in the southern and central parts of Spain. Consecutive outbreaks reported in the last two years suggest endemic circulation in Spain of this emerging virus. A retrospective study carried out just after the first epidemic period (2018-2019) revealed that the virus could have been circulating since June 2018. The number of outbreaks started to rise in July, peaked during the first half of August and October and then decreased sharply until January 2019. The apparent mean mortality rate was 55.4% (median: 70%). The results indicated high susceptibility of the Iberian hare to ha-MYXV infection, but apparent resistance in the sympatric hare species present in Spain and less infectivity in European rabbits. The novel ha-MYXV has had significant consequences on the health status of Iberian hare populations in Spain, which is of animal health and conservation concern. The present study contributes to a better understanding of ha-MYXV emergence and will provide valuable information for the development of control strategies. Further research is warranted to assess the impact of this emerging virus on wild lagomorph populations and to elucidate its ecological implications for Iberian Mediterranean ecosystems.

Monitoring of emerging myxoma virus epidemics in Iberian hares (Lepus granatensis) in Spain, 2018-2020.

MYXOMATOSIS is a disease of wild European and domestic rabbits ( Oryctolagus cuniculus ) caused by infection with myxoma virus, which is found naturally in some Sylvilagus rabbit species of South America and California. Sylvilagus species show few clinical signs. However, myxomatosis was introduced into Australia (1950), continental Europe (1952), Great Britain (1953) and Ireland (1954). This was as a control method for wild European rabbits. The initial mortality in Great Britain was 99 per cent. Myxomatosis is normally transmitted between host rabbits when virus particles adhere to the piercing mouthparts of a biting insect vector. In Great Britain the rabbit flea ( Spilopsyllus cuniculi ) is the most important vector of the disease. Other blood-sucking insects may play a minor role as vectors in some circumstances.

Myxomatosis has rarely been reported in the European brown hare ( Lepus europaeus ). Initial experimental inoculation in 1937 of wild-caught brown hares in Australia using virulent myxoma virus from rabbits failed to elicit disease …

MYXOMATOSIS Confirmation of myxomatosis in a European brown hare in Great Britain

In late 2018, an epidemic myxomatosis outbreak emerged on the Iberian Peninsula leading to high mortality in Iberian hare populations. A recombinant Myxoma virus (strains MYXV-Tol and ha-MYXV) was rapidly identified, harbouring a 2.8 kbp insertion containing evolved duplicates of M060L, M061L, M064L, and M065L genes from myxoma virus (MYXV) or other Poxviruses. Since 2017, 1616 rabbits and 125 hares were tested by a qPCR directed to M000.5L/R gene, conserved in MYXV and MYXV-Tol/ha-MYXV strains. A subset of the positive samples (20%) from both species was tested for the insert with MYXV being detected in rabbits and the recombinant MYXV in hares. Recently, three wild rabbits were found dead South of mainland Portugal, showing skin oedema and pulmonary lesions that tested positive for the 2.8 kbp insert. Sequencing analysis showed 100% similarity with the insert sequences described in Iberian hares from Spain. Viral particles were observed in the lungs and eyelids of rabbits by electron microscopy, and isolation in RK13 cells attested virus infectivity. Despite that the analysis of complete genomes may predict the recombinant MYXV strains’ ability to infect rabbit, routine analyses showed species segregation for the circulation of MYXV and recombinant MYXV in wild rabbit and in Iberian hares, respectively. This study demonstrates, however, that recombinant MYXV can effectively infect and cause myxomatosis in wild rabbits and domestic rabbits, raising serious concerns for the future of the Iberian wild leporids while emphasises the need for the continuous monitoring of MYXV and recombinant MYXV in both species.

https://www.mdpi.com/1999-4915/12/10/1127/pdf

Detection of recombinant Hare Myxoma Virus in wild rabbits (Oryctolagus cuniculus algirus).

Although there are around 40 species of hares in the world divided into three different genera (Lepus, Caprolagus, and Pronolagus), only six species inhabit Europe, all belonging to genus Lepus. The conservation status of these six species was recently revised in the International Conservation Union (IUCN) Red List of Threatened Species. Lepus castroviejoi and L. corsicanus were attributed the status of “vulnerable”. The other four species, L. europaeus, L. timidus, L. capensis, and L. granatensis, were considered of “least concern” although a declining trend was recognized for the last two species’ wild populations. Here we review the major threats to the hare species in Europe, with emphasis on infectious diseases. Furthermore, we present the sanitary data regarding the Iberian hare populations from Portugal, which were severely affected by the emergence of a naturally occurring recombinant myxoma virus (MYXV), first reported in mid-2018. The recent detection in 2019 of a leporid herpesvirus (LeHV-5), which pathogenicity appears to be exacerbated in MYXV-infected hares, brings additional concerns to the health and conservation of the Iberian hare.

/pdf/the-health-and-future-of-the-six-hare-species-in-europe-a-2fd71snjbv.pdf

The Health and Future of the Six Hare Species in Europe: A Closer Look at the Iberian Hare

Myxomatosis is an emergent disease in the Iberian hare, having been considered a rabbit disease for decades. Genome sequencing of the strains obtained from Iberian hares with myxomatosis showed these to be distinct from the classical ones that circulated in rabbits since the virus introduction in Europe, in 1952. The main genomic difference in this natural recombinant hare myxoma virus (ha-MYXV) is the presence of an additional 2.8 kb region disrupting the M009L gene and adding a set of genes homologous to the myxoma virus (MYXV) genes M060R, M061R, M064R, M065R and M066R originated in Poxviruses. After the emergence of this recombinant virus (ha-MYXV) in hares, in the summer of 2019, the ha-MYXV was not detected in rabbit surveys, suggesting an apparent species segregation with the MYXV classic strains persistently circulating in rabbits. Recently, a group of six unvaccinated European rabbits (Oryctolagus cuniculus cuniculus) from a backyard rabbitry in South Portugal developed signs of myxomatosis (anorexia, dyspnoea, oedema of eyelids, head, ears, external genitals and anus, and skin myxomas in the base of the ears). Five of them died within 24-48 hr of symptom onset. Molecular analysis revealed that only the recombinant MYXV was present. This is the first documented report of a recombinant hare myxoma virus in farm rabbits associated with high mortality, which increases the concern for the future of both the Iberian hare and wild rabbits and questions the safety of the rabbit industry. This highlights the urgent need to evaluate the efficacy of available vaccines against this new MYXV.

Recombinant myxoma virus infection associated with high mortality in rabbit farming (Oryctolagus cuniculus).

Myxomatosis was detected in Iberian hares (Lepus granatensis) in Portugal, October 2018, following its emergence in Spain 3 months earlier. Here, we describe the epidemiological, molecular and anatomo-histopathological data of the first two cases. Myxoma virus DNA was detected in the eyelids, nose and perineal region in both hares. It was also detected in the lungs of hare 1 and in the spleen and liver of hare 2. The genomic insertion identified in strains from Spain was confirmed in both strains suggesting a common origin for the Iberian viruses. Gross lesions in hare 1 included palpebral oedema and conjunctival mucopurulent discharge, common in both forms of the disease in rabbits. Hare 2 presented eyelid thickening with small diffuse nodules. Histopathology of the eyelids showed extracellular myxoid matrix in hare 1 and purulent dermatitis in hare 2. Both animals exhibited good body condition, suggesting a short course of the disease and higher virulence of the virus towards the Iberian hare.

Madelena Monteiro

Papers

First cases of myxomatosis in Iberian hares (Lepus granatensis) in Portugal