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GB Emerging Threats

Quarterly Report

Small Ruminant Diseases

Safeguarding

public and

animal health

editor:

tel:

fax:

email:

Amanda Carson, APHA Penrith

+ 44 (0) 1768 885295

+ 44 (0) 1768 885314

Amanda. [email protected]

Quarterly Report: Vol 19 : Q4 Oct - Dec 2015

Contents Page

Introduction & overview 2

New & re-emerging diseases and threats 4

Ongoing new and re-emerging disease investigations 4

Unusual diagnoses 6

Changes in disease patterns and risk factors 7

Horizon Scanning 14

Diagnostic Submissions Trend

Publications

15

21

Highlights Page

Polyarteritis nodosa 6

Spinal Cord Compression Following Vaccination 6

Plant Poisonings 12

VIDA diagnoses are recorded on the APHA FarmFile database and SAC Consultancy: Veterinary Services LIMS database and comply with agreed diagnostic criteria against which regular validations and audits are undertaken. The investigational expertise and comprehensive diagnostic laboratory facilities of both APHA and SAC C VS are widely acknowledged, and unusual disease problems tend to be referred to either. However recognised conditions where there is either no diagnostic test, or for which a clinical diagnosis offers sufficient specificity to negate the need for laboratory investigation, are unlikely to be represented. The report may therefore be biased in favour of unusual incidents or those diseases that require laboratory investigation for confirmation. APHA VICs have UKAS Accreditation and comply with ISO 17025 standard. SAC C VS have UKAS accreditation at their central diagnostic laboratory and at the Aberdeen, Edinburgh, Perth, Ayr, Dumfries, Inverness, St Boswells and Thurso Disease Surveillance Centres which comply with ISO 17025 standard. From September 2014 APHA contracted the services of partner Post-mortem providers. From April 2015, these services were provided by the Royal Veterinary College, the University of Bristol, University of Surrey, the Wales Veterinary Science Centre and SACCVS. These providers contribute to the VIDA diagnoses recorded on the APHA FarmFile database and comply with agreed diagnostic criteria. To achieve a VIDA diagnosis, all testing must be carried out by a laboratory with ISO 17025 accreditation.

GB Emerging Threats Quarterly Report Small Ruminant Diseases Vol 19 : Q4 Oct - Dec 2015

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INTRODUCTION

This report contains analysis of disease data from APHA, SAC Consulting: Veterinary Services (SAC CVS) division of Scotland’s Rural College (SRUC) and partner post-mortem providers (SAC CVS, University of Bristol Veterinary School, Royal Veterinary College, University of Surrey and Wales Veterinary Science Centre) from samples submitted in the fourth quarter of 2015 compared to the equivalent quarter of previous years. It aims to identify emerging small ruminant disease related threats. The production of the report is underpinned by a large quantity of surveillance data and information, compiled as part of the Defra Plant and Animal Health and Animal Health and Policy Implementation Directorates. Further information can be found at http://ahvla.defra.gov.uk/vet-gateway/surveillance/index.htm.

OVERVIEW

Issues & Trends

Weather

In contrast to the generally settled weather of September and October, November was notably unsettled,

and the UK was affected by the season's first three named storms Abigail, Barney and Clodagh which

brought some strong winds and heavy rain. December was an exceptional and record-breaking month.

The UK was in a warm and moist tropical air mass for most of the month, bringing unseasonably mild

conditions to England and Wales, although Scotland and Northern Ireland were colder at times,

particularly in the second week. It was also exceptionally wet and often windy, with frequent deep

depressions and frontal systems - including storms Desmond, Eva and Frank - bringing record-breaking

rainfall over much of Scotland, Wales and northern England. Severe flooding affected Cumbria for much

of December, and became widespread across North Wales, northern England and Scotland after

Christmas (Fig 1)

Farmers suffering from uninsurable losses can apply for a grant of up to £20,000 from the Farming

Recovery Fund, which the government had extended to cover farmers in Lancashire and Yorkshire, as

well as Cumbria and Northumberland

The government extended its Farming Recovery Fund for flood-hit growers and livestock producers.

Originally launched to help farmers hit by Storm Desmond in Cumbria, Northumberland and parts of

Lancashire, the fund has been extended to cover all of Lancashire and Yorkshire too

Farmers affected by flooding will be able to claim grants of £500-£20,000 to cover the cost of restoring

their farmland. This includes:

The restoration of productive stock proof grassland

The restoration of productive arable and horticultural land

The restoration of field access or track ways, fencing or gates or water troughs

The restoration of drainage on flood-damaged holdings

Damage to agricultural machinery that cannot be insured

Damage to agricultural buildings that cannot be insured

Survey carried out by the Cumbria Farmer Network

Approximately 1,000 farmers were contacted by the Cumbrian Farm Flood Action Group following the

December floods with 144 of them reporting a collective £1.7 million in losses. Defra has estimated

that 650 Cumbrian farms were affected by storm damage, meaning the survey represents detailed

information from a third of those farms. Data collection was funded by the Prince’s Countryside Fund, the

http://ahvla.defra.gov.uk/vet-gateway/surveillance/index.htm

http://ahvla.defra.gov.uk/vet-gateway/surveillance/index.htm


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survey was conducted by The Farmer Network and Westmorland Agricultural Society with analysis

carried out by the NFU.

Of the 1,000 farmers contacted, 220 completed a detailed survey and the findings have now been

analysed.

• 63% of those surveyed lost sections of watercourse bank sides

• 37% have lost walls

• 14% have lost hedgerows

• 38 farmers reported a total of 701 sheep deaths and 16 farmers reported 189 sheep missing

• 53% reported river stone/gravel deposit and 22% have had land slips

Fig 1. Provisional rainfall percent of average map for December 2015 & Provisional mean temperature anomaly (difference from 1981-2010 average) map for December 2015

Industry

The fourth quarter of 2015 began with prices falling back below the same period last year after a more

positive situation seen in towards the end of the third quarter of the year. After this decline seen at the

beginning of the fourth quarter prices began to rise. This was the trend seen for much of the rest of the

quarter, with the strongest gains seen during December. One reason for the rise in prices seen in the

final quarter of 2015 was a decline in lamb slaughterings seen during the period, with numbers back by

over 250,000 head (-7%) compared to the same period in 2014. As supplies began to fall, UK retail

demand grew in September and remained continually above year earlier levels through to the end of the

year. Sales at a retail level were poor during the summer due to competitions from other meats. However

sales got a boost in the fourth quarter helped by lower retail prices and a promotional campaign. The

value of the euro also declined during the period, making UK sheep meat more competitive on the global

market. Combined with this there was also the seasonal uplift in prices due to higher demand for the

Christmas period, leading prices to strengthen further. However throughout the period prices remained

well below levels seen in the previous year. The market for skins remained weak during the period.

Moving into 2016 prices have continued to increase as slaughterings have remained below year earlier

levels, while the strength of the pound has continued to decline. Mark Koslowski AHDB Beef & Lamb


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Farmer incomes may also have been affected by a delay in the Single Farm Payment to some farms.

Most affected were payments to farmers with common grazing.

NEW AND RE-EMERGING DISEASES AND THREATS

Monitoring the trends in diagnoses of known diseases cannot, by definition, detect either new diseases or changes

in endemic diseases that would prevent a diagnosis from being reached (for example a change in the pathogen

that compromised the usual diagnostic test). Such new or emerging diseases would probably first be detected by

observation of increased numbers of submissions for clinical and/or pathological syndromes for which a diagnosis

could not be reached in the normal way. Submissions for which no diagnosis is reached (DNR) despite testing

deemed to allow reasonable potential for a diagnosis to be reached are regularly analysed to look for increases in

undiagnosed disease which could indicate the presence of a new or emerging disease. Undiagnosed disease

submissions are summarised broadly by the clinical presentation of disease and, once this has been determined by

further investigation, the body system affected. Both groups are investigated and trends in the levels are compared

over time.

Data recording by APHA and SACCVS was harmonised from 2007. The Species Expert Group reviews trends in

VIDA DNR data each quarter with the aim of providing information on potential new or emerging diseases or

syndromes. ‘Prior years’ refers to pooled data for 2010-2014 for GB VIDA data.

Supplementary analysis of APHA DNR data is also undertaken using an early detection system (EDS). This uses

a statistical algorithm to estimate an expected number of DNR reports and a threshold value. If the current number

of DNR reports exceeds the threshold (i.e. exceedance score>1), this indicates that the number of reports is

statistically higher than expected. When this EDS identifies categories of submissions where the threshold DNR

has been exceeded, the Species Expert Group reviews the data to investigate further. This review may involve

assessment of individual DNR submissions. Where this DNR analysis finds no evidence of a new and emerging

threat or other issue, the detail of these reviews in response to thresholds being exceeded may not be reported

here.

SMALL RUMINANTS: DETECTION OF ACTUAL AND POTENTIAL NEW AND (RE)

EMERGING DISEASE THREATS IN 2015

The Small Ruminant Expert Group (SRSEG) maintained a spreadsheet of potential threats to small

ruminants during 2015. Twenty seven threats were identified in 2015, 10 were threats which are present

in GB small ruminants. Information from surveillance partners or non-submission data sources detected

2 of the 29 threats while eleven were detected by post-mortem submissions to APHA, SAC CVS or a

third party PM provider and a further thirteen were detected from analysis of Scanning Surveillance

submission data or non-PM submissions. Fourteen were raised with the Veterinary Risk Group as either

threats or points for information. The work of the Surveillance Laboratory Services Department is

integral to threat detection through its veterinary investigative, diagnostic and laboratory testing roles.

Links with other areas of expertise within APHA have been essential in investigating and characterising

threats identified. The groups who liaised on specific threats are detailed in the spreadsheet and include

Virology, Bacteriology, Sequencing, Pathology, Antimicrobial Resistance, Toxicology/food safety, non-

statutory zoonoses, International Diseases Monitoring and Exotic Diseases Teams. A variety of means

of disseminating data have been used with presentations at meetings being prominent, also disease

alerts and information sheets, these having the advantage of rapid production and direct dissemination

to target audiences


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Analysis of Diagnosis Not Reached (DNR)

Sheep & Goats

There are no indications of any new or emerging disease syndrome. There was no significant change in the overall %DNR and no significant increases for any of the presenting signs or syndromes.

ONGOING NEW AND RE-EMERGING DISEASE INVESTIGATIONS

Threat of increased resistance to multiple classes of anthelmintics in nematodes of GB sheep

Anthelmintic resistance (AR) is perhaps one of the most significant threats to the UK sheep industry and

has become a major problem for small ruminant producers throughout the world. In January 2016, the

APHA Small Ruminant Expert Group (SRSEG) highlighted this threat to the Veterinary Risk Group

(VRG). This was prompted by the report of a recent industry-funded (HCC/Meat promotion Wales)

survey of 47 sheep flocks in Wales during 2014 and 2015. The results indicated 94% of farms studied

have evidence of resistance to Benzimidazole (1-BZ), while 68% of farms have resistance to Levamisole

(2-LV) anthelmintic groups. Resistance was also detected on 51% of farms to Ivermectin (macrocyclic

lactone, 3-ML) and 19% of farms tested demonstrated evidence of resistance to Moxidectin (3-ML)

(http://hccmpw.org.uk/farming/projects/anthelmintic_resistance_project/). This confirmed an increase in

resistance compared to previous studies in England and Wales (Jones and others 2012; Mitchell and

others 2010).

This study is representative of wider concerns relating to AR and studies conducted in Scotland and

Northern Ireland support the findings. Anthelmintic resistance was also raised by the UK representative

at the November 2015 European Food Safety Authority (EFSA) Animal Health and Welfare risk network

meeting at which other Member States expressed similar concerns.

Two new classes of anthelmintic have become available as Prescription Only Medication-Veterinary

(POM-V) in the last 6 years, namely Group 4 AD (monepantel) and Group 5 SI (derquantel) classes. It is

important that use of these new classes is in line with Sustainable Control of Parasites (SCOPS)

principles particularly as isolated cases of resistance to monepantel in nematodes have arisen in various

countries including the Netherlands, New Zealand and Uruguay. These isolated cases were generally

associated with a very high historical frequency of monepantel use on the premises (Mederos and others

2014; Van den Brom and others 2015). (Scott and others 2013) Severe resistance to monepantel in

more than one nematode species after being administered for less than two years on the affected farm

has also been reported (Scott and others 2013).

Triclabendazole resistance (RCVZ-R) has been reported in fluke (Gordon and others 2012). Fluke is a

zoonotic disease, so the wider issue of AR also has potential low level public health implications. The

continuing requirement to control sheep scab is likely to lead to greater use of MLs. Such increased use

of MLs to control scab may inadvertently promote resistance in gastro-intestinal nematodes.

There is the opportunity to slow the progression towards multiple AR. SCOPS advice

(http://www.scops.org.uk) is available to vets and farmers and provides detailed advice to mitigate the

risk of introduction or development of AR. This helps raise awareness but is only effective if applied on

farm.

In January 2016, the APHA Small ruminant expert group agreed to raise this threat at the next Sheep

Health and Welfare Group meeting (February 2016) to highlight to industry to potentially fund a similar

study to assess the scale of resistance to different anthelmintic groups in sheep in England, and provide

evidence and pressure for action. APHA's role is primarily promoting awareness of this threat, assessing

http://hccmpw.org.uk/farming/projects/anthelmintic_resistance_project/

http://www.scops.org.uk/


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worm burdens and AR by testing, and providing advice on such testing. A presentation was given by the

Head of APHA’s Surveillance Intelligence Unit at the Animal Health Distributors Association annual

conference in January 2016 to raise awareness. Communications planned by SREG will refer to the

industry-funded study in Wales and highlight the issue of AR in sheep in internal and external

communications. The challenges to the sheep sector of ensuring advice reaches sheep keepers and

influencing farmer behaviour are acknowledged. Much of the work is reliant on industry leadership

working together with others including the Sheep Veterinary Society, veterinary practitioners,

Responsible Use of Medicines in Agriculture Alliance (RUMA), SCOPS and Animal Medicines Training

Regulatory Authority (AMTRA).

UNUSUAL DIAGNOSES

Polyarteritis nodosa

A post-mortem examination undertaken by Ben Strugnell at Farm Post-mortems Ltd at the John Warren

Fallen Stock site in Hamsterley led to an investigation into Polyarteritis nodosa (PAN).

Two unrelated lambs were presented on separate occasions from a farm breeding replacement breeding

sheep from Beltex and Texel breeding ewes. A 10-month-old ewe appeared “hunched” before death and

had recently been examined for lameness and a second 7-month-old Texel ram lamb had exhibited ill-

thrift and diarrhoea prior to death.

On gross post-mortem examination notable features in the female lamb included poor body condition,

haem-abdomen and marked peri-duodenal haemorrhage and a 5 cm long fusiform aneurysmal dilation

of up to 1 cm in diameter of the gastroduodenal artery. The male lamb had poor body condition,

moderate subcutaneous oedema, and moderate generalised lymphadenopathy and diffuse thickening of

the small intestinal wall.

Histopathology was carried out by Mark Wessels of Finn Laboratories who described a necrotising

arteritis in the small to medium arteries in the small intestine, abomasum, mesentery, kidney and heart

confirming a diagnosis of PAN.

No BVDV or BDV viral nucleic acid was detected using PCR nor was specific viral nucleic acid detected

using micro-array by the APHA laboratory at Weybridge.

This is unusual as in sheep PAN is considered rare and sporadic; however, a further case on the same

farm has recently been submitted for examination and collaborative investigations continue between

Farm Post-mortems Ltd, Finn Laboratories and APHA to try to determine if an underlying cause can be

identified to explain these cases.

Spinal Cord Compression Following Vaccination

A live ewe was submitted to APHA Thirsk from a lowland flock of 1000 ewes. The group had recently

received a footrot vaccine. Four-to-seven-days post vaccination three animals in the group were unable

to stand and showed twitching muscles. The ewe was bright, alert and responsive, but could not stand

unless supported due to marked paresis/paralysis of the forelimbs. Post-mortem examination revealed

three small encapsulated abscesses within the subcutaneous tissues of the left side of the neck at the

level of the first cervical vertebra. In addition, there was extensive inflammation of the neck muscles on

that side which had extended to involve the atlas bone at the atlanto-axial joint. Histopathological

examination of the spinal cord identified degenerative changes to the nerves compatible with the

compression of the spinal cord. It was suggested that the compression at these sites was the result of

the inflammatory changes observed in the body of the atlas and muscles of the neck, respectively. The

severity of the pathology in the nerves was deemed sufficient to have caused the clinical signs and was

most likely to be associated with the recent vaccination given the clinical history.


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CHANGES IN DISEASE PATTERNS AND RISK FACTORS

This section of the report gives information on occurrence of selected diseases. The data originate from submissions and are summarised and presented according to the diagnosis reached and assigned as a VIDA code. Our charts show the number of diagnoses (numerator) as a proportion of the number of submissions in which that diagnosis was possible (denominator), for all of GB, England & Wales and for Scotland. The bars indicate the 95% confidence limits. Note that the y-axis of the charts varies and therefore care must be taken when comparing individual charts.

Metabolic disease

Ill Thrift

Ill thrift was a common presenting sign in lambs, and sometimes ewes, for submissions and

investigations this quarter. Investigations revealed combinations of PGE, liver fluke, iodine deficiency

and/or trace element deficiencies (especially cobalt). In some case of PGE, resistance was suspected.

This illustrates the need for proper investigations to clearly establish the cause or causes involved in this

common presentation to ensure that appropriate treatment or management changes can be applied.

Skin

A skin condition due to coagulative necrosis of unknown cause was reported by the SAC CVS during

November. Several animals in a group of six-month-old cheviot lambs had developed swollen heads

after moving from a linked holding in the Highlands. Malignant oedema was suspected and treatment

with penicillin and corticosteroids resulted in some improvement. One animal was submitted to Perth

Disease Surveillance Centre for investigation and the main finding was crusting and peeling of the skin

around the muzzle, eyes and ears. Secondary bacterial infection was evident but there were no

significant findings on bacteriology. Histopathology found the ear lesions to be consistent with

coagulative necrosis with extensive bacterial invasion. There was no significant epithelial damage to

suggest photosensitisation and the findings were considered suggestive of ischaemic damage. The

possibility of the changes occurring secondary to septicaemia was suggested. Ergotism was considered

unlikely as no other body sites were affected.

Sheep scab was confirmed in a flock of 1000 sheep where 500/650 ewes were affected. The ewes

were at grass (fenced by electric fence) surrounded by maize crop. Clinical signs were particularly

severe as there were limited available areas to use as scratching posts and this was the first time this

group of ewes had been infected with scab so had no immunity. Purchased sheep were thought to be

the likely source of infection as there were no other sheep in the vicinity. The ewes were immediately

dipped as they were going to the ram the next week and there was cessation of clinical signs almost

instantly with 60% served in the first five days.

Parasitology

Parasitic Gastroenteritis

Parasitic gastroenteritis accounted for 31% of diagnosable submissions (146 incidents) in the fourth

quarter (October to December 2015). This is a reduction from the same quarter in 2014 for APHA, but

similar to that recorded by SAC CVS in that year (Fig 2). Incidents were recorded in store lambs or

replacement ewe lambs and there was often a history of recent ineffective treatment, suggestive of


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resistance to benzimidazoles and macrocyclic lactones. Few farmers are aware of the anthelmintic

classes that are efficacious on their holding.

Fig 2: Incidents of PGE in Sheep as % of diagnosable submissions in Q4 2004 - 2015

Acute fasciolosis

Both for the fourth quarter Fig 3 and annual percentage diagnoses Fig 4 there was a significantly higher

rate for Scotland than for England and Wales. This could be related to the weather conditions preceding

the last quarter, and the survival of infective metacercariae on pasture. Met. Office data show that, for

the UK as a whole, the percentage rainfall was 198% higher in 2015 than the average for the years

1961-9190, and the figure was 225% for Scotland. A wet spring in Scotland was followed by a very wet

November and December. These weather conditions favoured the life cycle of the parasite, particularly

in Scotland.

A further comment from SAC CVS also highlighted the possibility that farmers who treated early in

September were caught out by disease appearing later in November and December when the weather

was ideal for persistence of large numbers of infective metacercariae on the pasture, to cause acute

infection.

Fig 3: Incidents of Acute Fasciolosis in Sheep as % of diagnosable submissions in Q4 2004 – 2015


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Fig 4: Incidents of Acute Fasciolosis in Sheep as % of diagnosable submissions in 2004 - 2015

Chronic fasciolosis

A similar trend in percentage diagnosis for chronic fasciolosis can be seen for Scotland in the fourth

quarter Fig 5, and is again likely to be related to the warm wet spring and November and December

Fig 5: Incidents of Chronic Fasciolosis in Sheep as % of diagnosable submissions in Q4 2004 - 2015

Reproductive & Mammary disease

No statistical significant increases for any of the diseases monitored. The submission of abortion

material from sheep occurs predominantly in the first two quarters of the year.

Respiratory disease

The annual figure for pneumonia NOS recorded by APHA was markedly increased from 46 cases in

2014 to 62 in 2015. The 2015 quarter 4 figure was consistent with 2014 for both APHA and SAC CVS.

The only repetitive recorded diagnoses within NOS during 2015 were 7 diagnoses of coagulase positive


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Staphylococcus/Staphylococcus aureus pneumonia and 7 diagnoses of Bibersteinia trehalosi

pneumonia. Numerous cases were likely bacterial pneumonia with no identification of significant

organisms either due to contaminant growth or prior antimicrobial treatment likely inhibiting organism

growth.

Mycobacterium bovis spoligotype 10 was isolated from a poor doing ewe in a flock of 1000, where two

large caseous lesions were found in a left lung lobe during a practitioner post mortem.

Systemic disease

Bibersteinia trehalosi

There was an increase in Bibersteinia trehalosi cases reported by APHA this quarter (n=22), which

represented 13.75% of diagnosable submissions, when compared to quarter 4 in 2014 (n=18), with

5.37% of diagnosable submissions. Bibersteinia trehalosi cases for 2015 for GB were 3.87% of

diagnosable submissions (74 cases, compared to 71 cases in 2014). . In the UK systemic pasteurellosis

affects sheep of six to nine months of age during October, November and December. The onset of

disease frequently coincides with the feeding of turnips or a change in diet. Control may be achieved by

vaccination. Minimising stress should be a major part of flock management particularly with

environmental and nutritional changes in the autumn.

Bibersteinia trehalosi was cultured from a six-month-old lamb. Six animals had died suddenly from this

flock of 500 at the beginning of October. The lambs were weaned at the end of July and had been given

a trace element dose and wormer at the end of September. At post-mortem examination there were

necrotic erosions on the tongue and proximal oesophagus which suggested systemic Bibersteinia

trehalosi. Fig 6.

Fig 6. Necrotic erosions on the tongue and proximal oesophagus caused by Bibersteinia trehalosii.

Widespread haemorrhages were present throughout the carcase. Bibersteinia trehalosi was cultured

from liver, lung and spleen.

A flock submitted three carcases to Ayr following the death of 15 lambs over a three day period.

Bacteriology revealed B. trehalosi septicaemia in one and Yersinia pseudotuberculosis septicaemia in

the other two. A concurrent Anaplasma phagocytophilium (tick borne fever) was confirmed in these

animals, which as an immunosuppressant is likely to have predisposed to the bacterial septicaemias.

Yersinia pseudotuberculosis is sporadically isolated from sheep abortion cases but is rarely encountered

causing a septicaemia. It is important as a potential zoonosis.


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Visceral Caseous Lymphadenitis

An adult ewe was submitted for post-mortem examination from a flock of 50 to investigate ill-thrift. The

farmer reported a decrease in body condition in the flock over the preceding weeks, which was not

associated with any particular clinical signs. Abscesses containing green/yellow inspissated

mucopurulant material were found within the skin; the subcutaneous tissues of the ventral body wall;

within the mediastinum and affecting approximately 75% of the left lung and 15% of the right lung (Fig 7

& Fig 8). A pure growth of Corynebacterium pseudotuberculosis was cultured from one of the swabs

confirming caseous lymphadenitis. Trueperella pyogenes was also cultured in a mixed growth from the

lung. Visceral caseous lymphadenitis (CLA) is considered an unusual finding in the UK. It is uncertain

why a visceral distribution has been less common in the UK when compared to other endemic countries,

with possible strain variation or management influences suggested as potential reasons. Visceral CLA is

particularly important due to an increased impact on sheep health and because the lesions are grossly

indistinguishable from tuberculosis. This case illustrates the importance of culturing to confirm the

diagnosis and sampling from more than one site as mixed infections can occur.

Fig 7: Abscess within right lung Fig 8: Mediastinal abscess

Enteric disease,

Bolus injuries

Cases where incorrect dosing of trace element boluses causes injury, irritation, pain and inflammation,

secondary infections, haemorrhages and death continue to be detected. The usual finding is a

penetrating injury in the oropharynx with the bolus lodged in the tissues adjacent to the oesophagus.

There is usually a delay of several days before clinical signs are seen. In all cases it was suggested to

review the dosing methods.

Toxicity

The Chemical Food safety report for the quarter is published at

https://www.gov.uk/government/publications/chemical-food-safety-reports

Lead

A raised kidney lead concentration was detected in a six to eight-month-old lamb that died as a result of

ill thrift and lungworm infection. The kidney lead concentration from this lamb was 42.7 µmol/kg DM,

https://www.gov.uk/government/publications/chemical-food-safety-reports


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equivalent to 1.60 mg/kg WM. The source of lead was suspected to be of geochemical origin. There

were approximately 70 other lambs in the group which had been on the same grazing since September

2015. There were also twenty cattle on the farm that were grazing in the same area. The livestock were

removed from this field. APHA recommended that the potentially lead-exposed groups (both lambs and

cattle) observe a sixteen week withdrawal and that after this period cohorts from the two groups are

blood tested to establish whether there is evidence of lead exposure and whether further risk

management measures may be required. Minimal measures would likely require animals to be sold

and/or slaughtered into the food chain with FCI requiring offal to be discarded.

Botulism suspected as the cause of weakness, ataxia and death in ewes.

Botulism was diagnosed in a flock of 450 ewes with access to five grass fields. Five ewes showed signs

of weakness and died following spreading broiler litter on neighbouring grassland fields. The first death

occurred four days after spreading. The boundary fence between some of the fields was reported to be

poor (a single strand of sheep wire netting) and broiler litter was observed to have breached the

boundary fence allowing the sheep direct access to broiler litter. No carcase material was present in the

broiler litter. The sheep were immediately moved away from the source. The farmer was advised that no

clinically affected sheep should be presented to the food chain and that any recovering animals should

observe a further eighteen day restriction following the cessation of clinical signs.

Copper

FSA/APHA incident trigger is when the liver copper concentration exceeds 500 mg/kg WM.

Especially in sheep, chronic copper poisoning can also occur when liver concentrations of copper are

well below this incident trigger value. The same food safety advice is still provided. The APHA

reference interval for liver copper concentrations in sheep is 300 to 8000 µmol/kg DM, equivalent to

approximately 5 to 125 mg/kg WM.

There was an increase in copper toxicity cases reported by APHA this quarter (n=9), which represented

4.48% of diagnosable submissions, when compared to quarter 4 in 2014 (n=5), with 1.50% of

diagnosable submissions. It is an unusual time of year to see copper toxicity cases, as in most flocks

there would usually have been limited concentrate feeding by this time. Copper toxicity cases for 2015

for GB was 2.34% of diagnosable submissions (57 cases, compared to 41 cases in 2014). This is the

highest annual number recorded when taken as a percentage of diagnosable submissions, and suggests

there needs to be a greater awareness of the risks of over-supplementation in sheep.

Plant poisoning

Bog asphodel poisoning

Post mortem examination was carried out on the sixth six-month-old lamb from a total of 100 to develop

clinical signs of photosensitisation, including swollen faces, lips and ears with oozing yellow serum and

yellow mucous membranes. The lambs affected were from different groups but all grazing fields across

Dartmoor with exposure to Bog asphodel (Narethecium ossifragum). The likely demise of the animal

examined was confirmed as a terminal E.coli septicaemia with gross evidence of a fibrinous peritonitis,

pleuritis and pericarditis; however, a severe underlying liver pathology with jaundice, discoloured urine

and raised liver enzymes was confirmed which was consistent with a diagnosis of secondary

photosensitisation.


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Pieris poisoning

Two separate incidents of Pieris poisoning were reported. Poisoning with these plants, which are

members of the Ericaceae family, is due to grayanotoxins, which are known to bind sodium channels in

excitable cell membranes exerting their effect on nerve, heart and skeletal muscle tissues.

Following the moving of approximately seventy ewes to away ground, several were found dead and

bloated and another approximately six were found recumbent and dribbling from their mouths. There

was evidence that they had broken into an adjoining garden and eaten plants there. At post mortem

examination all three ewes examined had a large number of leaves present in their rumen contents.

Some leaves had smooth edges and some were serrated. Some were yellow in colour, others green.

There were also numerous pale seed heads present. The finding of large numbers of leaves together

with seed heads that resembled those seen on Pieris plants is consistent with clinical signs and death in

these animals due to Pieris poisoning. There was also evidence of previous fluke infection but this would

not have been responsible for the clinical signs and death in these animals.

Pieris poisoning was diagnosed in a group of about fifty ewes. Seven presented with clinical signs and

several died. Clinical signs included vomiting/depression/excitation and some showed hind leg paresis,

dragging their hind legs. Diagnosis was made based on clinical signs and exposure to the cut plant (Fig

9).

Fig 9 Pieris leaves from the rumen of a sheep.

Acorn (oak) poisoning

Two separate incidents of acorn poisoning were reported. The main toxic principles are considered to be

tannic acid and its metabolites gallic acid and pyrogallol, all of which are nephrotoxic.

Acorn poisoning was diagnosed as the cause of death of one ewe from a group of twenty. The ewes had

been at grass but because this was poor had recently been brought inside and fed haylage. This ewe

was seen to have diarrhoea but after housing showed rapid weight loss and inappetance. At post

mortem examination there were ulcers observed on both sides of the tongue and the mucosa of the

ventral oesophagus. The rumen content was watery with green fibre and white pale pieces of material

suggestive of broken up acorns. There were a few ulcers on the mucosal surface of the abomasum. The

large intestine content was scant with longitudinal haemorrhages on the mucosa of the large intestine.

The ulceration of the tongue, oesophagus and abomasum is consistent with the ewe being uraemic


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when it died and this was confirmed with high aqueous humour urea and creatinine. The kidney cortices

were pale, supporting a nephropathy.

Farmers and vets should be aware of the seasonal hazard of plant poisonings, particularly as pasture

and grass quality reduces, and animals seek other sources of forage. Equally, animals may be

accidentally exposed after storms (e.g., fallen acorns), due to dumping of green waste (e.g., yew

clippings), or by gaining access to marginal grazing through damaged fencing.

Urinary disease, Nervous disease, Musculo-Skeletal disease

No statistical significant increases for any of the diseases monitored.

Zoonoses

The annual report on zoonoses in the United Kingdom (UK) includes a summary of reported cases

of zoonotic infection in humans and animals during 2014. The data have been compiled from

statutory notifiable or reportable disease reports, national scanning surveillance systems, national

laboratory reporting, control programmes, research programmes and from data submitted to the

European Community via the Trends and Sources Report under the Zoonoses Directive 2003/99, by

agencies contributing to the Report.

https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/488376/zoonoses-annual-

report-2014.pdf

HORIZON SCANNING International Disease Monitoring

Blue tongue Outbreaks continue to be reported in France, Eastern Europe and Italy Fig 10. It has been an unusually

mild winter so there will still be vector activity and virus circulation. As animals are moved off upland

pasture and into housing while the winter temperatures drop there may still be vectors present in the

sheds so some cases may still be reported.

France has continued to report BTV-8 over the winter months; there are now 191 affected holdings in Central and Southern France, mainly cattle.

Using a combination of modelling and expert opinion APHA have estimated the risk to the UK over the

coming months and this has been presented in the risk assessment available at:

https://www.gov.uk/government/publications/qualitative-risk-assessment-bluetongue-virus-btv-8-entry-

into-the-uk.

There is considerable uncertainty at present and the risk will change as the season progresses, so this

assessment will be updated accordingly.

The area most at risk from midge-borne incursion will be the South and Southeast of England.

Incursion and spread will depend on the weather (wind direction and temperature) and the immune

status of the livestock exposed.

Vaccination is the best control option and will have the dual benefit of reducing both viraemia (preventing

onward transmission) and clinical signs in the individual animal.

For information on Bluetongue disease please see: https://www.gov.uk/guidance/bluetongue.

https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/488376/zoonoses-annual-report-2014.pdf

https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/488376/zoonoses-annual-report-2014.pdf

https://www.gov.uk/government/publications/qualitative-risk-assessment-bluetongue-virus-btv-8-entry-into-the-uk

https://www.gov.uk/government/publications/qualitative-risk-assessment-bluetongue-virus-btv-8-entry-into-the-uk

https://www.gov.uk/guidance/bluetongue


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Fig 10: BTV in Europe Feb 2016

Diagnostic submission trend

Contributors of diagnostic submission data include APHA VI Centres, SAC CVS Disease Surveillance

Centres and partner post-mortem providers. It is worth noting that a submission may be comprised of a

number of carcases submitted for examination, therefore these do not represent a count of carcases

received.

A new format has been developed to show submission throughput by type, by country, submissions by

syndrome and submissions by mapped regions.

Throughput Sheep Diagnostic Submissions Throughput

Table 1 describes the sheep submissions by Carcase, Fetus and other submission by Country for Q4

2015. A comparison is made to show the percentage of submissions as compared to the average of the

equivalent quarters for the previous 2 years and average of the equivalent quarters for the previous 5

years.

For carcase submissions in England the trend is to a reducing number 50% compared to the previous 5

years and 58% compared to the previous 2 years. Carcase submissions in Scotland and Wales remains

relatively stable and above 80% compared to the average of previous years.

For fetus submissions again the trend is for a decreasing number of submissions from England and also from Wales. In Scotland the number of fetus submissions is increasing. For other submissions the number from England is over 80% in comparison to the average of previous years. In Scotland there is an increase in submissions in comparison to the previous 5 years average.


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In England and Wales the reductions in carcase and fetus submissions may reflect the changes to the network of centres offering post-mortems and the Small Ruminant Expert Group will continue to monitor these trends as the new providers in England and Wales develop their services. Table 1. Submissions by Country for Q 4 2015

Carcase Foetus/Stillborn Other

Total

Q4 Q4

Subs 2015 v Prior2

2015 v Prior 5

Q4 Subs

2015 v Prior2

2015 v Prior 5

Q4 Subs

2015 v Prior2

2015 v Prior 5

Subs 2015 v Prior2

2015 v Prior 5

England 99. 58. % 50. % 11. 67. % 37. % 433. 81. % 85. % 543. 75. % 73. %

Wales 37. 100. % 80. % 4. 133. % 38. % 86. 56. % 52. % 127. 66. % 57. %

Scotland 150. 84. % 80. % 14. 187. % 167. % 242. 88. % 97. % 406. 88. % 91. %

Unknown 2. 36. % 56. % 1. 100. % 167. % 39. 83. % 122. % 42. 79. % 116. %

288. 73. % 66. % 30. 107. % 61. % 800. 79. % 84. % 1,118. 78. % 77. %

Table 2 describes the Annual sheep submissions by Carcase, Fetus and other submissions by Country for 2015. A comparison is made to show the percentage of submissions as compared to the average of the previous 2 years and average of the previous 5 years. The Annual comparison shows that there has been a greater reduction in the submission of carcases from England, reducing to 55% compared to the previous 2 years and 42% compared to the previous 5 years. In Wales and Scotland the reduction in carcase submissions is much less and for Wales is the same when compared to the previous 2 years. The Annual comparison for fetus submissions shows a reducing trend across all countries overall reducing to 83% compared to the previous 2 years and 7% compared to the previous 5 years. For other submissions there is an overall downward trend in submissions for all countries to 85% compared to the previous 2 years and 81% compared to the previous 5 years. Again this probably reflects the changes in the provision of services which will be monitored. Table 2 .Annual Submissions by Country


Total

Annual 2015 Subs

2015 v

Prior2

2015 v

Prior 5

2015 Subs

2015 v

Prior2

2015 v Prior 5

2015 Subs 2015 v Prior2

2015 v Prior 5

Subs 2015 v Prior2

2015 v Prior 5

England 491. 55. % 42. % 474. 82. % 69. % 2,478. 84. % 86. % 3,443. 78. % 73. %

Wales 200. 100. % 73. % 95. 76. % 57. % 884. 85. % 86. % 1,179. 86. % 80. %

Scotland 846. 90. % 88. % 347. 83. % 78. % 1,336. 94. % 97. % 2,529. 91. % 91. %

Unknown 20. 78. % 71. % 18. 180. % 108. % 311. 107. % 116. % 349. 107. % 112. %

1,557. 76. % 64. % 934. 83. % 71. % 5,009. 88. % 90. % 7,500. 85. % 81. %

Goat Diagnostic submissions throughput Table 3 describes the goat submissions by Carcase, Fetus and other submission by Country for Q4 2015. A comparison is made to show the percentage of submissions as compared to the average of the equivalent quarters for the previous 2 years and average of the equivalent quarters for the previous 5 years. The number of goat submissions for carcase, fetus and other is relatively small. Nevertheless the overall trend for carcases and other submissions is a declining number in comparison the previous years. It is not unexpected that there have been no fetus submissions in the quarter in Scotland and Wales given the smaller populations in these countries.


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Table 3. Submissions by Country for Q 4 2015


Total

Q4 Q4

Subs 2015 v Prior2

2015 v Prior 5

Q4 Subs

2015 v Prior2

2015 v Prior 5

Q4 Subs

2015 v Prior2

2015 v Prior 5

Subs 2015 v Prior2

2015 v Prior 5

England 13. 65. % 69. % 5. 200. % 147. % 43. 39. % 45. % 61. 46. % 52. %

Wales 1. 200. % 125. %

2. 25. % 22. % 3. 33. % 29. %

Scotland 3. 60. % 75. %

13. 96. % 120. % 16. 86. % 108. %

Unknown 1. 100. % 250. %

8. 62. % 63. % 9. 64. % 69. %

18. 68. % 75. % 5. 167. % 139. % 66. 46. % 52. % 89. 51. % 57. %

Table 4 describes the Annual goat submissions by Carcase, Fetus and other submissions by Country for 2015. A comparison is made to show the percentage of submissions as compared to the average of the previous 2 years and average of the previous 5 years. The Annual comparison shows that there has been and overall reduction in the number of carcase and other submissions across the counties. Annually the number of fetus submissions has increased compared to previous years although the numbers remain low such that meaningful interpretation is difficult. Table 4. Annual submissions by Country


Total

Annual 2015 Subs

2015 v

Prior2

2015 v

Prior 5

2015 Subs

2015 v

Prior2

2015 v Prior 5

2015 Subs 2015 v Prior2

2015 v Prior 5

Subs 2015 v Prior2

2015 v Prior 5

England 60. 66. % 61. % 23. 200. % 139. % 306. 55. % 59. % 389. 59. % 61. %

Wales 7. 156. % 88. % 1. 100. % 83. % 48. 117. % 85. % 56. 120. % 85. %

Scotland 11. 67. % 79. % 5. 125. % 227. % 73. 83. % 88. % 89. 82. % 90. %

Unknown 2. 80. % 111. %

49. 64. % 60. % 51. 64. % 61. %

80. 70. % 66. % 29. 176. % 145. % 476. 62. % 64. % 585. 65. % 66. %

Diagnostic Submissions by syndrome Sheep & Goat syndromic submissions Table 5 shows the profile of syndromes for all sheep diagnostic submissions for each year and table 6 for goats, to show up if the mix is changing over time. The syndrome comes entirely from the classification to which the VIDA diagnosis code belongs. For unknown these represent all diagnostic codes where the disease type is unknown or the diagnosis is not applicable. In goats there has been an increase in enteric diagnoses which has reduced the number of unknowns in comparison to previous years which is difficult to explain as there have been no new diagnostic tests The same information in the form of a bar graph for sheep is shown in Fig 11 and for goats in Fig 12. As expected the highest number of submissions relate to reproductive disease making up a quarter of all submissions on 2015. The spike of reproductive submissions in 2012 is likely to reflect the arrival of Schmallenberg virus in the UK


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Table 5. Sheep diagnostic submissions by syndrome

.

Fig 11. Graph showing percentage of sheep diagnostic submissions by syndrome per year

Table 6 Goat diagnostic submissions by syndrome


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Fig 12. Graph showing percentage of Goat diagnostic submissions by syndrome per year

Table 7 shows the profile of syndromes for sheep carcases (including fetuses) for each year, and Table 8 for Goats to show up if the mix is changing over time. Again as expected there are a higher number of carcases submissions to investigate reproductive conditions in sheep and enteric conditions for goats. Table 7. Sheep carcase and fetus submissions by syndrome

Table 8. Goat carcase and fetus submissions by syndrome


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Maps The map Fig 13 showing submissions for sheep and goats has been developed in collaboration with the

Data Systems Group GIS team at APHA Weybridge, who generate the outputs to support the work of the

SIU in evaluating the coverage of scanning surveillance activities in England and Wales.

Submission data was extracted from the VIDA database in order to include submissions to the diagnostic

laboratories of the Scottish Agricultural College (SAC) from holdings in England and Wales and are

limited to those holdings that could be georeferenced.

Demographic data on the underlying population of holdings by species is based on the work of the

Livestock and Demographic Data Groups and derived from Sheep and Goats: Agricultural Survey

extracts as at December 2014.

The submission ratio for each species is the proportion of holdings that submitted at least one carcase

or diagnostic sample in the reference period over all holdings of that species in the spatial unit county.

The 2015 maps are the first draft of the coverage outputs incorporating underlying population data.

Future enhancements are planned to incorporate data on other sources of surveillance information, from

within and external to APHA, such as statutory disease notifications, inspection visits or submissions to

other diagnostic laboratories.

The distribution broadly reflects the density of the population of sheep Fig 14.

Fig 13 Spatial distribution of Small Ruminant submissions Fig 14 GB Sheep population density


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Publications of interest Sheep and goats papers published by APHA staff October - December 2015

AYLING R 2015 Mycoplasma infections in goats and other species. Goat Veterinary Society Journal

31, 66.

Benavides J; GONZALEZ L; Dagleish M; Perez V 2015 Diagnostic pathology in microbial diseases of

sheep or goats. Veterinary Microbiology 181 (1-2) 15-26.

Chong A; Kennedy I; Goldmann W; Green A; GONZALEZ L; JEFFREY M; Hunter N 2015 Archival

search for historical atypical scrapie in sheep reveals evidence for mixed infections.Journal of General

Virology 96 (10) 3165-3178.

GEORGE A 2015 Tuberculosis in goats. Goat Veterinary Society Journal 31, 32-37.

Houston F; Goldmann W; Foster J; GONZALEZ L; JEFFREY M; Hunter N 2015 Comparative

susceptibility of sheep of different origins, breeds and PRNP genotypes to challenge with bovine

spongiform encephalopathy and scrapie. PLoS ONE 10(11): e0143251.

JEFFREY M; WITZ JP; MARTIN S; HAWKINS SAC; BELLWORTHY SJ; DEXTER GE; THURSTON L;

GONZALEZ L 2015 Dynamics of the natural transmission of bovine spongiform encephalopathy within

an intensively managed sheep flock. Veterinary Research 46:126.

MANSFIELD KL; Balseiro Morales A; JOHNSON N; Ayllon N; Hofle U; Alberdi P; Fernandez de Mera

IG; Garcia Marin JF; Gortazar C; de la Fuente J; FOOKS AR 2015 Identification and characterization

of a novel tick-borne flavivirus subtype in goats (Capra hircus) in Spain. Journal of General Virology 96

(7) 1676-1681.

McCutcheon S; Blanco ARA; Tan BC; GONZALEZ L; MARTIN S; Mallinson G; Appleford NE; Turner

ML; Manson JC; Houston EF 2015 A prion reduction filter does not completely remove endogenous

prion infectivity from sheep blood. Transfusion 55 (9) 2123-2133.

Nicholas RAJ; AYLING RD; ROSALES RS; Myerscough C 2015 Investigation of severe coughing and

ill thrift in adult hill sheep associated with Mycoplasma ovipneumoniae. Veterinary Record Case

Reports 3 (1) e000255.

Parida S; Muniraju M; Mahapatra M; Muthuchelvan D; Buckowski H; BANYARD AC 2015 Peste des

petits ruminants. Veterinary Microbiology 181 (1-2) 90-106.

Other publications of interest

Barwell, R., Eppleston, J., Watt, B. & Dhand, N. K. Foot abscess in sheep: Evaluation of risk factors and management options. Preventive Veterinary Medicine Bellet, C., Woodnutt, J., Green, L. E. & Kaler, J. (2015) Preventative services offered by veterinarians on sheep farms in England and Wales: Opinions and drivers for proactive flock health planning. Prev Vet Med 122, 381-388


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Cumbassá A; Barahona MJ; Cunha MV; Azórin B; Fonseca C; Rosalino LM; Tilburg J; Hagen F; Santos AS; Botelho A (2015) Coxiella burnetii DNA detected in domestic ruminants and wildlife from Portugal. Veterinary Microbiology 180 (1–2) 136-141 Duron, O., Sidi-Boumedine, K., Rousset, E., Moutailler, S. & Jourdain, E. (2015) The Importance of Ticks in Q Fever Transmission: What Has (and Has Not) Been Demonstrated? Trends in Parasitology 31, 536-552 Deng, H., Dam-Deisz, C., Luttikholt, S., Maas, M., Nielen, M., Swart, A., Vellema, P., Van Der Giessen, J. & Opsteegh, M. (2016) Risk factors related to Toxoplasma gondii seroprevalence in indoor-housed Dutch dairy goats. Prev Vet Med 124, 45-51 Joulie, A., Laroucau, K., Bailly, X., Prigent, M., Gasqui, P., Lepetitcolin, E., Blanchard, B., Rousset, E., Sidi-Boumedine, K. & Jourdain, E. (2015) Circulation of Coxiella burnetii in a Naturally Infected Flock of Dairy Sheep: Shedding Dynamics, Environmental Contamination, and Genotype Diversity. Appl Environ Microbiol 81, 7253-7260 King B; O’Shea Brown T; Tarlinton R; Daly JM (2015) Seroprevalence of Schmallenberg virus in the United Kingdom and the Republic of Ireland: 2011–2013. Veterinary Microbiology 180 (1–2) 36-40 Lambton SL; SMITH RP; GILLARD K; HORIGAN M; FARREN C; PRITCHARD GC (2015) Serological survey using ELISA to determine the prevalence of Coxiella burnetii infection (Q fever) in sheep and goats in Great Britain. Epidemiology and Infection 144 (1) 19-24 Lewis C (2015) Sheep scab - a history.2015 Goat Veterinary Society Journal 31, 50-53 Meadows, S., Jones-Bitton, A., Mcewen, S., Jansen, J. & Menzies, P. (2015) Coxiella burnetii seropositivity and associated risk factors in sheep in Ontario, Canada. Preventive Veterinary Medicine 122, 129-134 Meyers MT; Bahnson CS; Hanlon M; Kopral C; Srisinlapaudom S; Cochrane ZN; Sabas CE; Saiyasombat R; Burrough ER; Plummer PJ; O'Connor AM; Marshall KL; Blitvich BJ (2015) Management factors associated with operation-level prevalence of antibodies to Cache Valley Virus and other bunyamwera serogroup viruses in sheep in the United States. Vector-Borne and Zoonotic Diseases 15 (11) 683-693 Peperkamp, N. H., Luttikholt, S. J., Dijkman, R., Vos, J. H., Junker, K., Greijdanus, S., Roumen, M. P., Van Garderen, E., Meertens, N., Van Maanen, C., Lievaart, K., Van Wuyckhuise, L. & Wouda, W. (2015) Ovine and Bovine Congenital Abnormalities Associated With Intrauterine Infection With Schmallenberg Virus. Vet Pathol 52, 1057-1066 Schoenlaub L; Elliott A; Freches D; Mitchell WJ; Zhang G (2015) Role of B cells in host defense against primary Coxiella burnetii infection. Infection and Immunity 83 (12) 4826-4836 Sidi-Boumedine K; Adam G; Angen Ø; Aspán A; Bossers A; Roest H-J; Prigent M; Thiéry R; Rousset E (2015) Whole genome PCR scanning (WGPS) of Coxiella burnetii strains from ruminants. Microbes and Infection 17 (11–12) 772-775 Vasileiou NGC; Fthenakis GC; Papadopoulos E (2015) Dissemination of parasites by animal movements in small ruminant farms. Veterinary Parasitology 213 (1–2) 56-60

Winter, J. R., Kaler, J., Ferguson, E., Kilbride, A. L. & Green, L. E. (2015) Changes in prevalence of, and risk factors for, lameness in random samples of English sheep flocks: 2004–2013. Preventive Veterinary Medicine 122, 121-128


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References

GORDON, D., ZADOKS, R., SKUCE, P. & SARGISON, N. (2012) Confirmation of triclabendazole resistance in liver fluke in the UK. Veterinary Record 171, 159-160

JONES, J., PEARSON, R. & JECKEL, S. (2012) Suspected anthelmintic resistance to macrocyclic lactones in lambs in the UK. Veterinary Record 170, 59-60

MEDEROS, A. E., RAMOS, Z. & BANCHERO, G. E. (2014) First report of monepantel Haemonchus contortus resistance on sheep farms in Uruguay. Parasit Vectors 7, 598

MITCHELL, E. S. E., HUNT, K. R., WOOD, R. & MCLEAN, B. (2010) Anthelmintic resistance on sheep farms in Wales. Veterinary Record 166, 650-652

SCOTT, I., POMROY, W. E., KENYON, P. R., SMITH, G., ADLINGTON, B. & MOSS, A. (2013) Lack of efficacy of monepantel against Teladorsagia circumcincta and Trichostrongylus colubriformis. Veterinary Parasitology 198, 166-171

VAN DEN BROM, R., MOLL, L., KAPPERT, C. & VELLEMA, P. (2015) Haemonchus contortus resistance to monepantel in sheep. Vet Parasitol 209, 278-280

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