The Animal and Plant Health Agency (APHA) is an executive agency of the Department for Environment, Food & Rural Affairs, and also works on behalf of the Scottish Government and Welsh Government.

Editor: David Welchman Phone: 02080 267640

Email: David.Welchman@apha.gov.uk

GB avian quarterly report Disease surveillance and emerging threats

Volume 23: Q2 – April-June 2019

Highlights Page Avian influenza update in Europe 3

Focal duodenal necrosis in layers 7

Intestinal spirochaetosis in rheas 7

Multilocus sequence typing (MLST) scheme for M. gallisepticum 8

Infectious coryza in small chicken flocks 11

Contents

Introduction and overview .................................................................................................... 1

New and re-emerging diseases and threats ........................................................................ 3

Unusual diagnoses .............................................................................................................. 7

Changes in disease patterns and risk factors ...................................................................... 8

Horizon scanning ............................................................................................................... 11

References ........................................................................................................................ 12

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Introduction and overview This quarterly report reviews disease trends and disease threats for the second quarter of 2019, April to June. It contains analyses carried out on disease data gathered from APHA, SAC Consulting: Veterinary Services (SAC CVS) division of Scotland’s Rural College (SRUC) and partner post mortem providers and intelligence gathered through the Avian Expert Group. In addition, links to other sources of information including reports from other parts of the APHA and Defra agencies are included. A full explanation of how data is analysed is provided in the annexe available on GOV.UK. https://www.gov.uk/government/publications/information-on-data-analysis

Issues & Trends Industry trends – chick and poult placings Broilers There was a 0.9% decrease in placings of broiler chicks from UK hatcheries during June 2019 compared with June 2018 (Fig 1), at 85.0 million chicks, representing an average of 21 million chicks per week for the quarter. Although slightly lower than the corresponding figures for 2018, placings remain at a historically high level. Fig 1: Average number of broiler chicks placed per week from UK hatcheries

Turkeys There was an increase of 13.0% in the number of turkey poults placed during June 2019 compared with June 2018 (Fig 2), at 1.5 million, representing an average of 0.27 million poults placed per week for the quarter.

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Fig 2: Average number of turkey poults placed per week in the UK by UK hatcheries

Layers

The number of layer chicks placed during June 2019 was 11.0% lower than the corresponding figure for June 2018, at 3.2 million chicks (Fig 3). However UK packing station egg throughput in Q2-2019, at 7.9 million cases, was 0.5% higher than in Q1-2019 and 3.3% higher than Q2-2018, reflecting a continued increase in packing station throughput compared to historic levels. Free range eggs accounted for 53.2% of eggs packed in Q2-2019, compared with 52.4% in Q2-2018. For the eighth consecutive quarter, free range egg output during Q2-2019 exceeded enriched colony system output (by 11.6% of total throughput); barn and organic production remained at low levels although there continued to be a rise in both categories of egg cases packed compared with the previous four quarters. Average UK farm gate prices for eggs in Q2-2019 were 2.4% higher than the preceding quarter, and 2.0% higher than Q2-2018. Fig 3: Average number of layer chicks placed per week in the UK by UK hatcheries

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The poultry industry statistics are available online at: Poultry and poultry meat statistics: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/818187/poultry-statsnotice-18jul19.pdf [accessed 5 August 2019] Egg statistics: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/822349/eggs-statsnotice-01aug19.pdf [accessed 5 August 2019]

New and re-emerging diseases and threats Please refer to the annexe on GOV.UK for more information on the data and analysis.

Highly Pathogenic Avian influenza (HPAI) in the UK and Europe

There were no outbreaks of Highly Pathogenic Avian Influenza (HPAI) in poultry in the UK during Q2-2019 and no detections in wild birds in the UK.

There have been no further cases of H5N6 HPAI in wild birds in Denmark since the case in a common buzzard (Buteo buteo) in January 2019, as described in the previous quarterly report (APHA 2019a).

The most recent outbreaks of H5N8 HPAI identified in Bulgaria were in April 2019 and affected a fattening duck flock (detected through active surveillance), a 37-bird backyard chicken flock with high mortality, and two laying chicken flocks. In the laying flocks, one involved a primary outbreak in a flock of 70,000 birds showing clinical signs of depression and raised mortality whilst a secondary outbreak in a flock of 168,000 birds was detected by active surveillance. These two farms shared some common services and personnel. These cases are summarised in https://ec.europa.eu/food/sites/food/files/animals/docs/reg-

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com_ahw_20190411_hpai_bul.pdf under the regulatory committee presentations at https://ec.europa.eu/food/animals/health/regulatory_committee/presentations_en There have been no further H5 HPAI outbreaks confirmed in South-Eastern Russia since January 2019. The latest updated situation assessment (dated 19 July 2019) is available at https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/821261/uoa-hpai-europe.pdf and concludes that “Currently the risk of HPAI in wild birds in the UK is LOW (i.e. no change).” However it remains possible that there may be incursions of H5 viruses in wild waterfowl via migration pathways in the autumn and therefore “we recommend that all poultry keepers stay vigilant and make themselves aware of the latest information on gov.uk, particularly about recommendations for biosecurity and how to register their flocks using the simplified forms now available.”

Low Pathogenicity Avian Influenza in Europe An outbreak of notifiable H5 Low Pathogenicity Avian Influenza (LPAI) was confirmed in Denmark in June, in a mallard breeding flock, following a positive surveillance result. This follows two LPAI outbreaks in Denmark in February and March. The case is summarised at https://ec.europa.eu/food/sites/food/files/animals/docs/reg-com_ahw_20190708_lpai_dan.pdf Outbreaks of non-notifiable H3 LPAI were identified in Belgium (West and East Flanders), with the first case having occurred in a free range chicken layer flock in January. The farm was voluntarily depopulated by the farmer but was infected again in April, and this was followed by a rapid increase in cases with 71 outbreaks confirmed by mid-June. Six outbreaks were fully confirmed by PCR as H3N1. The clinical signs seen in the outbreaks were listed as follows: • Eggshell defects (discolouring)

• Depression in the birds

• Severe drop in egg production

• Severe drop in feed intake

• Increasing mortality (25-30%), up to 60%

• Sometimes slowly spreading

• Sometimes no clinical signs at all

• Delayed restart of laying after recovery and low egg production

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The virus was confirmed to be a low pathogenicity strain with an intravenous pathogenicity index (IVPI) of 0.13 and genetically related to a strain isolated from a wild bird in the Netherlands in 2017. It shows adaptation to chickens, with a predilection for the ovary and oviduct and has also been detected by PCR in brain tissue. The outbreaks have affected 27 chicken breeder farms, 30 laying chicken farms, seven turkey farms, six broiler units and one ostrich farm. No common links have been identified between the farms, and no common pathogens other than H3N1. A range of temporary control measures have been put in place, including enhanced surveillance and biosecurity measures. These findings are reported at https://ec.europa.eu/food/sites/food/files/animals/docs/reg-com_ahw_20190612_lpai_bel.pdf Non-notifiable H3N1 LPAI was also confirmed in May in an 8,000-bird breeding chicken flock in northern France, following an increase in mortality (100 in three days), respiratory disease and an egg drop of 5 per cent. This was followed later in May by an outbreak in two 10,000 bird breeder flocks on one site 2.2km from the first outbreak, with increased mortality (15 per cent in five days), respiratory signs and progressive egg drop. The flocks on both sites derived from the same hatchery and also had other links, including shared vaccination teams and feed transport and links with Belgium. A third outbreak was confirmed in another, nearby breeder flock in early June. In all three outbreaks voluntary depopulation was undertaken followed by cleansing and disinfection, with no state funding. These outbreaks are summarised at https://ec.europa.eu/food/sites/food/files/animals/docs/reg-com_ahw_20190708_lpai_fra.pdf A drop in egg production and an increase in mortality were also features of H6N1 and H4N6 LPAI outbreaks reported in the literature and summarised in the previous quarterly report (APHA 2019a). Newcastle disease

There were no Newcastle disease outbreaks reported in Europe during the quarter, the last outbreak having been in Bulgaria in January.

Avian notifiable disease exclusion testing scheme (‘Testing To Exclude’, TTE, Testing For Exclusion) in Great Britain (GB) The scheme started in May 2014 (Gibbens and others 2014) and is ongoing (http://apha.defra.gov.uk/vet-gateway/tte/nad.htm; accessed 20 February 2019). There were two exclusion testing investigations during Q2-2019 with the details summarised in Table 1. The scheme is very valuable in enabling possible LPAI to be investigated where it is considered to be a differential diagnosis for the clinical signs seen in birds on a site. The scheme currently only applies to chickens and turkeys. The cases shown below, which tested negative for avian notifiable disease, represented the 32nd and 33rd cases investigated since the inception of the scheme in 2014.

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Table 1: Summary of findings from the Notifiable Avian Disease Exclusion Testing Scheme, Q2 – 2019 Species and purpose (where information available)

Clinical details Cloacal and oropharyngeal swabs taken

Results Outcome

Chickens – free range layers

Drop in egg production, some reduction in feed intake

Yes Negative M-gene (AI virus) PCR results

Avian notifiable disease excluded

Chickens – broiler breeders

Drop in egg production.

Yes Negative M-gene (AI virus) PCR results

Avian notifiable disease excluded. A management issue was suspected as the principal underlying cause

Differential diagnosis of negated notifiable disease report cases in GB This scheme was introduced in autumn 2018 to offer differential diagnostic testing through APHA and its partners in cases where suspicion of Notifiable Avian Disease (NAD) has been reported, but subsequently negated either on clinical grounds or following laboratory testing. The scheme is also available for Testing to Exclude cases (see above) where notifiable disease has been negated by laboratory testing. The scheme is described in more detail by Welchman and others (2019). Table 2 (below) summarises the outcome of cases investigated from April to June 2019 inclusive. Table 2: Summary of findings of differential diagnostic testing of negated notifiable avian disease report cases in GB.

Species of poultry and purpose

Summary of clinical signs/history

Samples examined Summary of findings and diagnosis

Chickens, show/breeding, originally 105 birds

35 died over 10 days, swollen heads, sneezing, gasping, dullness, deaths

4 x culled chickens for post-mortem examination

Mild superficial pharyngitis in one bird (perhaps caused by abrasion due to coarse feed and secondary bacterial invasion); Marek’s disease identified by histopathology in one bird.

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Broiler chickens Two houses of 40,000 birds showed loose droppings, dullness, reduced mobility, inappetance and up to 8% mortality.

cloacal & oropharyngeal swabs for IBV PCR testing

IBV detected on PCR testing – suspected IBV nephritis

Pigeon paramyxovirus investigations There were four submissions of material from pigeons or doves tested for Pigeon Paramyxovirus-1 (pAAvV-1 (formerly PPMV-1)) at APHA Weybridge during the quarter as suspect report cases, three in April and one in June. Cloacal swabs from two of these cases were positive by PCR and virus isolation for pAAvV-1.

Other diseases

Focal duodenal necrosis in layers

This case was described in the APHA disease surveillance report for June (APHA 2019b). Elevated mortality in colony layer chickens at point of lay was investigated by post mortem examination which revealed frothy caecal contents, with abnormal intestinal thickening, gas bubbling in the mid intestine, and increased mucoid content in some birds. In very fresh carcases, lesions were visible in the duodenum suggestive of possible focal duodenal necrosis (FDN). Histopathological examination of the duodenal lesions showed changes consistent with FDN, with multifocal necrosis of the villi and numerous clostridial-like organisms visible. The aetiology of FDN remains uncertain but the disease is associated with the presence of Clostridium colinum infection or with toxin-producing Clostridium perfringens strains (Franҫa and others, 2016). It is reported in layer chickens, under a variety of management types, and can result in decreased egg production and lower egg weights, and may represent a mild form of necrotic enteritis which is more often seen in younger birds. Although the risk factors contributing to FDN remain unknown, the use of antibiotic in affected flocks is reported to be one means of effective treatment. FDN has been regarded as one of the top five diseases affecting layer chickens in the United States (Franҫa and others 2016), but has rarely been reported in Great Britain.

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Unusual diagnoses Intestinal spirochaetosis in rheas

Two cases of intestinal spirochaetosis were investigated in young rheas (Rhea sp) in two separate small, privately owned collections, as reported in the APHA disease surveillance report for April (APHA 2019c). The first case was a six-month-old rhea submitted for post mortem examination following sudden death. It was the second to die on the holding, with the first displaying haemorrhagic diarrhoea before death. The gross pathology findings included severe thickening and necrosis of the caecal and rectal mucosa with an overlying diphtheritic membrane (Fig 4). Brachyspira hyodysenteriae was isolated in anaerobic culture from a mucosal scrape. In the second case, an eight-month-old rhea was submitted as the second on the farm to be found dead unexpectedly and post mortem findings were similar to those described above. Histopathology on the affected intestine identified a very severe subacute necrotising typhlocolitis with spirochaetes and B. hampsonii was subsequently confirmed by culture. Severe intestinal spirochaetosis is a recognised cause of death in juvenile rheas (Hampson 2013) and has been recorded on the VIDA database on seven occasions since 2008. B hyodysenteriae. has been implicated in the past but B. hampsonii has not been described previously in rheas, and was also identified for the first time by APHA in a pig in a different region in England (APHA (2019) GB Emerging Threats quarterly report – pigs, April-June – to be published). Close contact with infected pigs is thought to be a risk factor in the spread of B. hyodysenteriae to rheas, but this was not the case on these two holdings and whole genome sequencing showed that these isolates are distinct from sequenced GB pig B. hyodysenteriae isolates and the pig-derived B. hampsonii. Wild waterfowl, other wild birds and rodents are also known to be carriers of potentially pathogenic Brachyspira spp.; disease associated with B hyodysenteriae has been described in domestic ducks (Glávits and others 2011) and B. hyodysenteriae was recovered at a high isolation rate in both farmed and wild mallards (Anas platyrhynchos) in Sweden (Jansson and others 2004). B. hampsonii has been isolated from wild mallards and greylag geese (Anser anser) in Spain (Martinez-Lobo and others 2013) and from lesser snow geese (Chen (or Anser) caerulescens caerulescens) in Canada (Rubin and others 2013). However no surveys have been carried out for brachyspiral infection in wild waterfowl in the UK.

Fig 4: Large intestine of a rhea showing severe necrotic changes associated with spirochaete infection.

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Changes in disease patterns and risk factors Please refer to the annexe on GOV.UK for more information on the data and analysis.

Multilocus sequence typing (MLST) scheme for Mycoplasma gallisepticum

Mycoplasma gallisepticum (MG) is of worldwide importance as a pathogen of various bird species, principally as a cause of respiratory disease and infectious sinusitis. Previously various DNA fingerprinting methods have been used to differentiate between different strains of MG, including between field and vaccine strains. However a multilocus sequencing (MLST) method has now been developed to distinguish between strains and has the advantage of high discriminatory power and good reproducibility (Bekő and others 2019), with the use of six housekeeping genes. A total of 130 samples from different countries were examined by this technique, yielding 57 sequence types (STs). The samples included several from the UK and assessment of supplementary data published with the paper indicated that these comprised six chicken strains (dating from 2007 to 2012) categorised as ST14, a turkey strain from 1999 (ST 52), three partridge strains from 1994, 2006 and 2008 (STs 55, 42 and 56) and 13 partridge and pheasant strains from 2016-2017, all of which were categorised as ST29. The latter were collected as part of a British Veterinary Poultry Association (BVPA) project on respiratory disease in gamebirds (Welchman unpublished; APHA 2017, APHA 2019d). Samples from a chicken from Italy (2012) and a partridge from France (2012) were also identified as ST29. The identification of the 13 recent gamebird strains as ST29 indicates that, when assessed by this MLST technique, they represented a single type which differed from previous strains detected in the UK and which may have emerged in recent years. These and other gamebird strains arising from the BVPA project are also being examined by a further technique, core genome MLST which has been used for molecular typing of MG (Ghanem 2018). The results of this will be reported in due course and will provide additional information on the identity of current UK gamebird strains.

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Diseases of small and backyard flocks: Marek’s disease

The GB avian disease surveillance dashboard for non-commercial and small chicken flocks (https://public.tableau.com/profile/siu.apha#!/vizhome/AvianDashboard/Overview) shows that Marek’s disease (MD) has been the commonest disease diagnosed in this type of flock since 2007. Diagnoses have been associated with a variety of main clinical signs, of which the commonest is wasting (loss of body condition) (Fig 5)

Fig 5: Main clinical sign reported for cases of Marek’s disease in non-commercial and small chick flocks from the GB avian disease surveillance dashboard

VIDA data show an apparent increase in the number of incidents of MD diagnosed in 2019 in GB (Fig 6), indicating that the disease continues to be diagnosed in chickens in general, not only in small non-commercial flocks.

Fig 6: Annual VIDA incidents of Marek’s disease diagnosed in chickens since 2007 (data for 2019 are up to the end of June).

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The prevalence of MD in small flocks in GB is mirrored in recent reports of the causes of mortality in backyard poultry in eight states of the USA (Cadmus and others 2019) and in Ontario, Canada (Brochu 2019). In a survey of backyard chicken post-mortem examinations in the USA, MD was the commonest cause of mortality in all eight states, and was diagnosed in 22 per cent of birds overall. This was attributed to lack of vaccine uptake and, where vaccine was used, to late administration (at one- or two-day old rather than in ovo) delaying the development of immunity. MD was also the most commonly diagnosed primary viral disease in the survey in Ontario.

Cadmus and others (2019) suggested that further education of small flock owners is required on the importance of only purchasing MD-vaccinated birds, and of vaccinating any chicks they hatch themselves. Compared with a general reduction of disease in commercial poultry, disease has persisted in backyard flocks. Several factors were considered to have interfered with reducing disease in backyard flocks and the control of preventable diseases, including mixing of different species and breeds, contact with wild birds and other wildlife, movements of backyard birds between different premises and events, poor husbandry, weaknesses in biosecurity and disease prevention measures by owners and unwillingness to seek veterinary advice. The provision of poultry medicine resources to practising veterinarians would benefit veterinary care for backyard owners. Further research would benefit not only backyard flocks but potentially also commercial flocks because of the risk of spread of infectious disease between backyard and commercial premises. The factors highlighted by Cadmus and others (2019) are also relevant in the UK as well as in the USA.

A very recent publication (Mescolini and others 2019) described sequence analysis of the meq gene of MD virus (Gallid alphaherpesvirus 2, GaHV-2), which is correlated with virulence of the disease, in 19 Italian backyard flocks. The isolates were obtained from 2015 to 2017 from flocks showing clinical signs or lesions of MD. The study revealed the circulation of both high and low virulence strains of GaHV-2 in Italian backyard flocks. As well as the circulation of different strains, the variability in disease presentation could also have been attributable to different genetic susceptibilities to MD in different breeds of chicken, as well as differing immune status in the birds. The opportunities for the spread of GaHV-2 between birds, for example at shows, was also emphasised. It was suggested that backyard flocks could act as a reservoir of different GaHV-2 strains and there is the potential for these to be transmitted to other flocks, including commercial flocks, by wild birds acting as carriers.

Horizon scanning Novel orthoreovirus (avian reovirus) variant detected in China

Orthoreoviruses are recognised as the cause of a variety of diseases in poultry, including arthritis/tenosynovitis. New strains are reported to have emerged in flocks despite the use of vaccination. The isolation of a new strain from synovial fluid and tendon samples from

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the progeny of a vaccinated broiler breeder flock in China has been reported by Chen and others (2019). The strain was able to break through vaccinal protection and cause disease in the chicks despite a high level of maternal antibody. Experimental infection of broiler chicks with the new strain (designated LY383) resulted in lesions of tenosynovitis in the inoculated birds. The new strain was distinct both from vaccine strains and previously described field strains. Other new strains of orthoreovirus (avian reoviruses, ARV) have been described previously, for example in Korea (Noh and others 2018) and Canada (Ayalew and others 2017) and concern has been expressed that commercial vaccines may not provide sufficient protection against new field isolates. Analysis of the Sigma C gene of ARV, in particular, has shown significant genetic heterogeneity between current isolates, which can be divided into six clusters (I to VI), all of which are potentially pathogenic (Ayalew and others 2017). Further commercial vaccines may need to be developed to protect against the emerging strains. Further investigation is required to monitor whether emerging strains such as these are present in Great Britain.

Infectious coryza (Avibacterium paragallinarum) in small chicken flocks

Infectious coryza is principally a respiratory disease of worldwide economic importance, caused by the fastidious organism Avibacterium paragallinarum. Because of its fastidious nature, difficulty in isolation and identification and the confounding presence of other bacteria, it is more readily identified by PCR testing than by culture. A real-time (RT) PCR was used to screen small chicken flocks in California (Clothier and others 2019). RT-PCR testing was carried out on both sinus and tracheal swabs and 294 samples were collected: 30 per cent were positive for A. paragallinarum, with the highest detection rate in birds less than 12 months of age. Tracheal swabs had a higher detection rate than sinus swabs. Only 46.5% of positive samples were from birds with a history of respiratory disease. Co-infection with other agents was detected in 30 per cent of PCR-positive birds, most commonly with Mycoplasma gallisepticum and/or M. synoviae. A. paragallinarum was thus shown to be present commonly in small chicken flocks, including in birds not showing respiratory signs, and this was considered a potential threat to commercial poultry.

A. paragallinarum was first confirmed in the UK in a small hobby breeder flock in 2010 (Welchman and others 2011) but has only infrequently been identified in subsequent years, which may be due to the difficulty in culturing the organism and the current lack of an available PCR test. However the findings by Clothier and others (2019) suggest that A. paragallinarum could be contributing significantly to respiratory disease in small flocks in the UK, and that improved surveillance is required.

References

APHA (2017) GB Emerging Threats Quarterly Report - Avian Diseases, vol 21, Q2 (April-June 2017), page 9

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https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/642180/pub-survrep-a0217.pdf (Accessed 9 August 2019) APHA (2019a) GB Emerging Threats Quarterly Report - Avian Diseases, vol 23, Q1 (January-March 2019), pages 3-4 https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/806086/pub-survrep-a0119.pdf (accessed 9 August 2019) APHA (2019b) Focal duodenal necrosis in layers. Veterinary Record 185, 13 http://dx.doi.org/10.1136/vr.l4533 APHA (2019c) Intestinal spirochaetosis in rheas. Veterinary Record 184, 547-548 http://dx.doi.org/10.1136/vr.l2018 APHA (2019d) Mycoplasma gallisepticum in pheasants and partridges. Veterinary Record 184, 433 http://dx.doi.org/10.1136/vr.l1595 AYALEW, L.E., GUPTA, A., FRICKE, J., AHMED, K.A and five others (2017) Scientific Reports 7, 3565 DOI:10.1038/s41598-017-02743-8

BEKŐ, K., KREIZINGER, Z. SULYOK, K.M. and 9 others (2019) Genotyping of Mycoplasma gallisepticum by multilocus sequence typing. Veterinary Microbiology 231, 191-196 https://doi.org/10.1016/j.vetmic.2019.03.016

BROCHU, N.M, GUERIN, T., VARGA, C.V., LILLIE, B.N., BRASH, M.L. & SUSTA, L. (2019) A two-year prospective study of small poultry flocks in Ontario, Canada, part 2: causes of morbidity and mortality. Journal of Veterinary Diagnostic Investigation 31, 336-342

CADMUS, K.J., METE, A., HARRIS, M. ANDERSON, D. and 7 others (2019) Causes of mortality in backyard poultry in eight states in the United States. Journal of Veterinary Diagnostic Investigation 31, 318-326

FRANCA, M., BARRIOS, M.A., STABLER, L., ZAVALA, G., SHIVAPRASAD, H.L. and 3 others (2016) Association of Beta2-Positive Clostridium perfringens Type A with Focal Duodenal Necrosis in Egg-Laying Chickens in the United States. Avian diseases 60, 43-49 GHANEM, M., WANG, L., ZHANG, Y., EDWARDS, S., LU, A., LEY, D. & EL-GAZZAR, M. (2018) Core genome multilocus sequencing typing: a standardised approach for molecular typing of Mycoplasma gallisepticum. Journal of Clinical Microbiology 56, 1-11 https://doi.org/10.1128/JCM.01145-17 GIBBENS, N., BROWN, I.H. & IRVINE, R.M. (2014) Testing for exclusion of notifiable avian disease. Veterinary Record 174, 534-535 GLÁVITS, R., IVANICS, É., THUMA, Á., KASZANYITSKY, É. and 4 others (2011) Typhlocolitis associated with spirochaetes in duck flocks. Avian Pathology 40, 23-31

HAMPSON, D.J. (2013) Avian Intestinal Spirochetosis. In Diseases of Poultry, 13th Edn, ed Swayne, D.E. Wiley-Blackwell, pages 1003-1004.

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JANSSON, D. JOHANSSON, K.-E., OLOFSSON, T., RÅSBACK, T. and 4 others (2004) Brachyspira hyodysenteriae and other strongly β-haemolytic and indole-positive spirochaetes isolated from mallards (Anas platyrhynchos). Journal of Medical Microbiology 53, 293-300 MARTINEZ-LOBO FJ, HIDALGO Á, GARCĺA M, ARGŰELLO H, and 3 others (2013) First Identification of “Brachyspira hampsonii” in Wild European Waterfowl. PLoS ONE 8(12): e82626. doi:10.1371/journal.pone.0082626 MESCOLINI, G., LUPINI, C., FELICE, V., GUERRINI, A. and 3 others (2019) Molecular characterization of the meq gene of Marek’s disease viruses detected in unvaccinated backyard chickens reveals the circulation of low and high-virulence strains. Poultry Science 98, 3085-3092 http://dx.doi.org/10.3382/ps/pez095 NOH, J.-Y., LEE, D.-H., LIM, T.-H.and 3 others (2018) Isolation and genomic characterization of a novel avian orthoreovirus strain in Korea, 2014 Archives of Virology 163, 1307-1316 https://doi.org/10.1007/s00705-017-3667-8 RUBIN, J.E., HARMS, N.J., FERNANDO, C., SOOS, C. and 3 others (2013) Isolation and characterization of Brachyspira spp. Including “Brachyspira hampsonii” from Lesser Snow Geese (Chen caerulescens caerulescens) in the Canadian Arctic. Microbial Ecology (2013) 66:813–822 DOI 10.1007/s00248-013-0273-5 WELCHMAN, D., KING, S.A., WRAGG, P., WOOD, A.M and 4 others (2011) Infectious coryza in chickens in Great Britain. Veterinary Record 167, 912-913 WELCHMAN, D., HANSEN, R. & SCHOCK, A. (2019) Differential diagnosis of negated avian notifiable disease cases in Great Britain. Veterinary Record 184, 276 http://dx.doi.org/10.1136/vr.l938

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