Perhaps the above is one of the best available epidemiological explanations for the outbreak of PPMV1 in Australia?
PPMV1 (Pigeon paramyxovirus) was first reported in Shepparton, some 200 km from Melbourne in a flock of Persian High Flyers. On 2/9/2011 a veterinarian in Melbourne, that had consulted Persian High Flyer pigeon lofts suffering high mortality for a week since the 27/8/11, was alerted by a call from Vic DPI informing him about the diagnosis of PPMV1 in Shepparton. The 'penny dropped'. PPMV1 was not a DDx previously considered as in his words "this virus did not occur in Australia". A virus that has never before been reported in Australia- PPMV1 of European origin (genotype VI of APMV1) had arrived on our shores. Soon the old rivalry between Sydney and Melbourne takes a new dimension - Which city had it first?
They could not agree where the capital should be. Could they agree on the origin of PPMV1?
To add to the confusion the pigeon paternity in Melbourne were informed by a respected veterinarian that the virus may have been introduced on the "wings of waterfowl migrating up the east coast of Australia".
With rumours and innuendoes reigning supreme, the epidemiology of pigeon paramyxovirus in Australia remains obscure unless poetry is your cup of tea. Even the epidemiologist's dearest friend - time, may not provide further clues.
From the 27/8/11 the veterinarian in Melbourne had been investigating cases of high mortality in domestic pigeons with up to 120/130 mortalities in one case and 29/50 in another case. Circo virus, Adeno virus and Herpes viruses were all considered but not Newcastle disease or PPMV1 since, as the veterinarian wrote to his clientele "the virus did not occur in Australia". Specimens submitted to a private pathology provider for histopathology provided no useful clues. Perhaps a few questions could be asked but there are so many other riddles that perhaps it would serve no purpose to tackle any more mysteries.
During the week of the 28/8/11 the Melbourne clinic admitted many other pigeon clients and their birds had potentially been exposed to the virus during their visit. When the "penny dropped" these clients were advised to isolate the birds that visited the surgery, normally a smart recommendation but in this case the birds had already been placed with other pigeons in the lofts with ample potential opportunity to infect others with PPMV1. One of the birds, a racing pigeon admitted for surgery while some of the PPMV1 birds were hospitalised, indeed came down with the disease and ultimately infecting the entire loft.
It became apparent that the infected pigeons originated from a pet shop in Melbourne North West. This shop has extensive lofts and provides fanciers with a venue to sell their excess pigeons on consignment. A significant mortality was experienced in the shop starting on the 29/8/11. According to the Melbourne veterinarian's notes, believing that the mortality was due to Circo virus, the shop owner contacted his customers inviting them to collect their pigeons. Whether it was Circo virus or PPMV1; the poor understanding of infectious diseases and biosecurity principles is apparent.
In his account of the outbreak in Melbourne the veterinarian also stated that "Vic DPI quickly and efficiently handled the first 2 lofts but left the management of the other lofts to their owners".
It is possible to understand why the eradication of the disease was deemed at early stages to be considerably difficult or practically impossible and why vaccination was viewed as the most appropriate means of controlling the disease.
The Victorian DPI web site provided the following advice to pigeon owners;
"There is no efficacy nor safety data for Poultry Newcastle disease vaccines in pigeons. It is strongly recommended that pigeon owners considering the use of Newcastle disease vaccine do so in consultation with their Veterinarian.
Isn't there a pigeon paramyxovirus vaccine available overseas?
There is a registered pigeon vaccine available in some countries. DPI remains strongly supportive of efforts to import a pigeon specific PMV1 vaccine from Europe. One vaccine company, with the support of various industry bodies, applied to import that vaccine, and APMVA assessed the vaccine as safe and efficacious. However, the application has not been given quarantine approval. It seems unlikely that a pigeon specific vaccine will become available in Australia in the near future".
At the time of the initial round of outbreaks in Victoria in August - September, the disease was not notifiable in Victoria, Tasmania, NT and ACT. Across Australia the disease was not covered by EADRA cost sharing agreement and the pigeon sector was not a party to official deliberation on aspects of control, surveillance or eradication of the disease.
In the absence of immediate legislative powers to eradicate the disease, the stated primary objective of "identifying the extent of the disease and limiting its spread where possible" may have been a realistic objective provided a pigeon PPMV1 vaccine became available in the shortest time or the efficacy and safety of the poultry NDV vaccines were demonstrated within a few weeks rather than 10 months after the beginning of the outbreak.
Limiting the spread of the outbreak was only possible if a suitable vaccine became available and was used quickly by a large percentage of the industry. As evident from the Victorian web site and the web sites of other jurisdictions there was an understandable reluctance by jurisdictions to promote the use of the poultry NDV vaccines available in Australia and a significant reluctance by the pigeon sector to use the vaccines. An overseas, efficacious inactivated pigeon vaccine that has been used extensively around the world was deemed of questionable safety by AQIS and meanwhile PPMV1 was spreading.
The inability to access pigeon vaccines is probably the most critical aspect in the PPMV1 saga. The impact was not only on the control of the disease but also, very likely, on the welfare of pigeons and their owners. It raises an interesting conundrum about the relative importance of veterinary obligations, especially during emergency situations and adherence to strict letters of protocols. It raises an ethical dilemma about the 'power to kill animals' and the obligation to protect where possible.
My miniscule knowledge of the pigeon world was a poor match to my knowledge of Newcastle disease in poultry and PPMV1. It became apparent as time progressed and my knowledge improved that the pigeon sector in Australia, especially the racing sector, was fragmented and with multi-layers of politics, animosity, rivalry and other well known human traits. It also became clear that the pigeon sector in NSW was bewildered by the response in Victoria and frustrated by the forlorn hope of gaining access to good pigeon PPMV1 vaccines that were available overseas.
In an effort to inform the pigeon sector in NSW of developments in Victoria and to clarify interstate movement restrictions, I slowly accumulated a list of emails and contact was established with sectors and individuals in the industry. The sector was predominantly hungry for information and at the same time not shy of spreading information quickly but sometimes inadvertently also inaccurately. Rumours and some very interesting "fish tales" were interwoven with facts in such a delicate framework that separation was almost impossible without a hefty measure of trust. Getting accurate and quick information to the sector was a prime objective for successful communication. I do not believe that this has been achieved for the entire sector.
I also became acquainted with the magical history of the pigeon and although this diminutive creature is no match for the stature and muscular equine architecture, nevertheless a soft spot was developing inside me for this bird and its unsurpassed determination and service to humanity. It was later in the midst of the outbreak in NSW that the sadness, depth of the potential consequences as well as the enduring and endearing nature of the Australian spirit became clearer to me when I met a flyer that served in the Australian signal core in Papua New Guinea during World War 2. He was an officer in the Australian Corps of Signals Pigeon Service. His loft in Sydney became infected with PPMV1 and to witness a life time of dedication to a hobby and a glorious loft being decimated by the disease was a sad experience.
The Australian War Memorial web site4 perhaps tells a story that we should remember when we are inclined to classify the pigeon as a pest or when we do risk assessments, ponder vaccination risks and decide the faith of animals by actions or inactions.
"The 8th Australian Pigeon Section was sent to Port Moresby in December 1942 to support operations on the Kokoda Trail. The pigeons were trained to carry a message for up to 120 miles (193 km) at an average speed of 30 miles per hour (48km/hr). They were particularly useful in emergency situations when no other method of communication was available.
In 1943, a British organisation, the People's Dispensary for Sick Animals (PDSA), began awarding the Dickin Medal to "animals displaying conspicuous gallantry and devotion to duty while serving or associated with any branch of the Armed Forces or Civil Defense Units". It is regarded as the 'animal's Victoria Cross'. Two Australian pigeons were awarded the Dickin Medal in February 1947."
From its first appearance in Victoria in August 2011 until 16th November 2011, 50 infected premises were reported in the Melbourne area as well as 6 detections among wild pigeons in the same areas. The Victorian approach consisted of detection, quarantine, tracing and surveillance. Initially the Victorian DPI recommended that shows, other gathering and racing be avoided and later (30/9/12) a ban was placed by it on the movements, shows, racing etc of pigeons.
Other jurisdictions placed restrictions on movements of pigeons and equipment from Victoria, while SA placed restrictions on movements of pigeons from all jurisdictions, later seeking harmonisation of movement restrictions across Australia.
Clinical signs - NSW
The following signs were reported from NSW outbreaks:
In one flock of 12 feral pigeons that were monitored; one pigeon was reported sick, taken to a vet, PPMV1 was confirmed and the pigeon recovered. No others were reported sick or dead in the 2 weeks following this incident. However subsequently multiple mortalities were reported among feral pigeons in Haberfield.
NSW Pathology/Post Portem
Post-mortem findings were inconsistent and varied from not significant or mild. Presence of petechial haemorrhages over the heart and darkish congested lungs were noted in some pigeons. Mottled, congested liver was reported in some pigeons. Spleen was enlarged in some but normal in other pigeons and also crop and stomach either empty or with food contents in others. Air-sac appearance was generally normal and green diarrhoea was present in some. Swabbing of affected pigeons produced pinkish tinged cloacal swab indicating inflamed intestines. With time I could predict the PCR results from the pinkish tinge of the swab.
The difference in the clinical signs experienced by pigeons infected with PPMV1 in Victoria and NSW is an interesting aspect with some possible impact on the understanding of the epidemiology of the disease. The absence of nervous and respiratory signs in pigeons infected with PPMV1 in NSW and the relatively lower level of mortality reported in most flocks in NSW (higher than 50% in Victoria) may also be reflected in the clinical manifestations in wild pigeons in NSW and with lower rate of mortality it is possible that some feral pigeon mortality has gone unnoticed. No mass mortality of pigeons, similar to the 600 mortality in Geelong, has been reported in NSW and investigations of reported cases of sporadic mortality in feral pigeons yielded no evidence of PPMV1 until November 2012.
The change in pattern between the clinical signs in NSW and Victoria is not easily explainable but is consistent with other reported PPMV1 cases1. Differences in clinical signs between regions were reported in chickens during the NDV outbreaks in NSW during 1998-2002 (Arzey, unpublished data). In some regions nervous signs predominated and in others respiratory signs predominated.
Different disease patterns were also recognised in Europe between 1983, 19841 with nervous signs predominant in 1983 changing to predominantly GI manifestations in 19842 and currently a combination of the 1983 and 1984 patterns. It is also interesting that no respiratory signs were reported in Europe with PPMV1.
Vaccination, in principle, is one of the most effective tools to deal with PPMV1 especially when the prime stated objective is limiting the spread of the outbreak.
The disease was deemed fairly early to be ineradicable and in such circumstances the only strategy available was to minimise the spread and prevent the disease through vaccination.
No pigeon vaccine was available in Australia. However, at least 2 inactivated pigeon PPMV1 vaccines produced by reputable international manufacturers and widely used in Europe and USA were on offer, requiring approval by APVMA and AQIS.
Despite support from various jurisdictions, the poultry industry and lobbying by the pigeon sector, to date, neither of the 2 vaccines has been approved for use in Australia. I still remain puzzled and with a slight vertigo as to the risk from these imported inactivated vaccines but nevertheless the debate should have been extended to include ramifications of not vaccinating vs the risk from inactivated vaccines being possibly, but yet most unlikely, contaminated with extraneous agents.
As the Australian Poultry Veterinary Association Chair of the Committee on Exotic diseases and Importation I have argued the toss many times against importation of certain products but I could not fathom the arguments against the importation of these 2 widely used inactivated vaccines when such vaccines were required urgently and when at stake was possible impact on native pigeons and other native birds in Australia, not to mention possible mutation to virulene in poultry.
I could not avoid pondering quietly whether the same approach would prevail if PPMV1 affected horses?
The available chicken Newcastle disease vaccines were of unknown efficacy or safety in pigeons, a point that was repeatedly emphasised by jurisdictions from the beginning of the outbreak in Victoria in their posted web advice to pigeon fanciers. Consequently there was little enthusiasm shown by the pigeon fraternity to adopt vaccination and reluctance by governments to promote the use of the Australian NDV poultry vaccines in pigeons.
At the behest of CCEAD, a trial was conducted in Victoria by a private veterinarian to assess the efficacy and safety of the Australian chicken NDV vaccines in pigeons. In February 2012, six months after the beginning of the outbreak, the results of the first trial using the Australian NDV chicken vaccines on pigeons was reported and unfortunately the results as measured by NDV HI antibodies in vaccinated pigeons demonstrated a very poor outcome - no response. The trial was conducted by a veterinarian with sound knowledge of pigeons but limited knowledge and experience with NDV vaccine administration.
The results of these trials were extremely disappointing. It was not until the first outbreak of PPMV1 in NSW that preliminary results of the second vaccination trial with chicken NDV vaccines (this time conducted under close supervision of a poultry veterinarian) became available and allowed a proactive approach to vaccination. However, valuable time and the confidence of the pigeon sector was lost while PPMV1 became more and more entrenched in domestic and feral pigeons in Victoria and in NSW.
At this stage, in February 2012 the infection was widespread among domestic pigeons in Victoria and multiple detections in wild pigeons had been reported in Victoria.
It had taken 6 months to reach this milestone - a failed trial, done by a veterinarian with no experience with NDV vaccination, presumably, assuming that vaccination of birds with either a live or inactivated NDV vaccines is a simple task that every veterinarian is amply qualified to perform effectively. I refuse to accept the other possible explanation proposed by a few pigeon fanciers that PPMV1 in pigeons was of little national importance and any solution that required no government $ input was gladly adopted.
Was the inability of the vaccines to induce immunity in the pigeons a reflection of poor technique or a reflection of inappropriate vaccines?
Some failure to appreciate the susceptibility of live vaccines to chlorinated water could have been encountered during the first trial but what was the explanation for the failure of the inactivated poultry vaccine, given by injection, to induce any measurable immunity in the pigeons during the trial?
This question remained unanswered but after 6 months of consistent governmental advice to pigeon owners that no data is available on the efficacy or safety of the Australian NDV vaccines in pigeons, suddenly, evidence was found in the scientific literature to indicate that poultry vaccines can work effectively on pigeons and NDV HI titres (the ultimate indicator for inactivated vaccine efficacy) are inconsequential. This apparently coincided with AQIS' final rejection of the application by Pfizer to import their pigeon inactivated vaccine. With some extensive experience evaluating the efficacy and safety of poultry vaccines for APVMA, I could not precisely follow the rationale. Veterinarians servicing the pigeon sector were dubious about the ability of the chicken vaccine to perform in pigeons although some overseas anecdotal data indicated that chicken vaccines "worked on pigeons in other countries". But were they identical vaccines to the Australian NDV vaccines?
Vaccination of pigeons was a controversial subject among pigeon fanciers in Victoria with some swearing that they will kill their pigeons before giving them chicken vaccines. "Chickens do not fly said one flyer" "I do not want to see my pigeons turning into Henny Penny" said another.
Contradicting recommendations were given by veterinarians in Melbourne and Sydney and more than acquiring a sense of urgency about protecting their birds, some fanciers were extremely concerned about the effect of the vaccine on the ability of pigeons to race while others were adamant that any vaccinated pigeon should not be allowed to fly because it will infect all other racing pigeons.
The end result was that confusion and misconceptions reigned supreme and vaccination with poultry NDV vaccine was very slow to take off.
The Victorian Homing Association commissioned a second trial to evaluate the efficacy and safety of the poultry NDV vaccines on pigeons. This trial was supervised by a poultry veterinarian. The second trial indicated dramatically different results and a more optimistic outcome; reporting NDV HI titres in the range of 16 to 256 following 2 applications of inactivated poultry NDV vaccines.
At last there was a technical capacity to confidently advise veterinarians and owners of pigeons that the chicken vaccines are likely to provide good protection but one of the most valuable elements of disease control had been lost - precious time.
The results of the second vaccine trial coincided with the appearance of PPMV1 in Sydney in a fancy flock of pigeons but the uptake of vaccination in NSW was sluggish at this stage and those that contemplated vaccination did so to protect only their breeders. The fancy pigeons (the first infected loft in NSW) with the consent of the owner were culled but perhaps too much hope was placed on the culling as the ultimate tool rather than contemplating vaccination at the same time. Like the fanciers in Victoria, flyers in NSW extracted all sort of "gems" on Google and from other sources indicating side effects and other possible negative effects with the poultry NDV vaccines and the reluctance to vaccinate the racing birds was based on the belief that the vaccination will affect the performance negatively during the race.
It was not until the detection of PPMV1 in Sydney among racing birds and imposition of movement restrictions that the attitude changed.
By 13/8/12 more than 600 pigeon lofts had been fully vaccinated in NSW and all racing pigeons in Sydney that were members of the Cumberland Federation were vaccinated.
Vaccination was also carried out on infected lofts. Mixed results were reported with clinical signs being evident in some of the lofts more than 50 days post first vaccination. However mortality stopped. Virus was still circulating in these flocks 60 days post vaccination as evident from PCR results on cloacal swabs. The prevalence was low among the sampled birds and the titre of the virus detected was also low. This clearly demonstrates that vaccinated pigeons can carry and shed the virus albeit at lower titres.
After the first wave of PPMV1 outbreaks between July and August 2012, a second wave occurred between October and November 2012. None of the newly infected lofts in October or November 2012 were vaccinated or had completed a full vaccination program on all birds. The last reported incident in domestic pigeons on the 14/11 was in a loft where young pigeons received only one course of inactivated vaccine. The last reported PPMV1 incident in NSW was dated 7/12/12 and involved feral pigeons in the Ashfield municipality. It followed a previously reported PPMV1 infection in wild pigeons in the Elizabeth Bay area.
The outbreaks and presence of PPMV1 in feral pigeons appears to be still restricted to the Sydney area. For how long?
Did the outbreak of PPMV1 merit special consideration and importation of reputable inactivated overseas pigeon vaccines?
Should it take more than 6 months to conduct efficacy and safety trials with the Australian poultry vaccines and who should conduct such trials?
The balance between the risk from imported reputable vaccines and man's obligation to protect animals under their care can be viewed as a philosophical issue but it has far reaching practical ramifications that we may encounter in the future with other minor species and other vaccines. Even following the positive results from the efficacy study in Victoria, a significant number of pigeon owners was reluctant to vaccinate their pigeons, preferring to wait for the pigeon vaccine to be registered.
The approach to the control of PPMV1 in Australia has been partially fragmented and lacked clear vision. The reasons are partially associated with the fact that the status of regulation in each jurisdiction was different and the entity was not recognised as an emergency disease, nor was it covered by cost sharing arrangements. Control was further complicated by the fragmentation of the sector and the difficulty to establish effective communication with the industry in each jurisdiction and nationally.
While eradication may not have been practical, effective early control with vaccination was feasible provided either a pigeon specific vaccine was allowed into the country or provided the efficacy of the Australian chicken NDV vaccines in pigeons was demonstrated at early stages of the outbreak, enabling wide vaccination uptake.
Depopulation of infected flocks in NSW was carried out on the first 2 infected lofts. This was done following the owner's agreement to depopulate. Some incentives were offered to owners by members of the pigeon sector in NSW and it also became apparent that considerable pressure was exerted on the owners to agree to depopulation. Once it became clear that the spread associated with the Mudgee race was significant no further depopulation was carried out. Infected lofts were placed in quarantine and the conditions included keeping the pigeons restricted to the loft (no exercise). The control measures and the movement controls that were introduced in NSW aimed at the imposition of restrictions for a period of 6 - 8 weeks, allowing the sector to vaccinate pigeons at least twice before racing and shows could commence.
After the 13/8/12 movement restrictions were revoked and while the disease remained notifiable, no quarantine was imposed on newly infected lofts.
Several other issues have risen during the outbreaks in Victoria and NSW. These include; fragmented approach to control, lack of knowledge of the epidemiology and ecology of feral pigeons and their interactions with other birds, lack of knowledge of the industry, difficulties in communication with the broader pigeon owners community and possibly low level of empathy with the industry.
It is beyond the scope of this paper to discuss these issues in detail but it was apparent that lack of knowledge of the industry and its practices affected the understanding of various elements of risk and control. It was clear that very little knowledge is available in Australia about the feral pigeon population, its size, scale of movements and habitat. This lack of knowledge impacted on the ability to understand risks and on decisions to view PPMV1 as being endemic perhaps prematurely.
In some respects the pigeon sector is viewed as a leisure sector or hobby sector. This does not help to understand the enormous impact that the outbreaks and movement restrictions that followed had on many individuals and clubs.
Many other issues should be mentioned;
The ability of a clinic to cope with an outbreak of an exotic disease and yet function normally and effectively maintain good biosecurity, the approach and preparedness to exotic disease in non-main stream species of animals, obtaining critical information during significant outbreaks of disease, capturing of pet shops in the biosecurity net, the practicality of Quarantine, the margins of errors in risk assessments and acceptable risks during emergency disease outbreaks, the role of governments and the role of the private sector and, delivering effective service to the community with ever decreasing resources.
The source of the Victorian outbreak has not been elucidated. The first outbreak in Sydney in fancy pigeons in May was most likely as a result of the introduction of pigeons from Victoria but the primary source(s) of the outbreaks in Sydney in racing pigeons from June onwards remains unclear. The majority of the outbreaks in NSW were predominantly traced to a common race or to tossing (several lofts exercising). More questions than answers remain as to whether the Earlwood loft diagnosed on the 28/6 was indeed the index case and from where and how it acquired the infection. It is clear that the Mudgee race and/or the tossing of pigeons on the 20/6, where the Earlwood loft participated, could be regarded as a likely infection source to others but the lack of widespread infection among participants in the Mudgee race is enigmatic when it is considered that 400 odd lofts participated in the race (approximately 7000 pigeons) and only 8 racing lofts in total succumbed to the infection (2 infected lofts did not participate in the race or tossing).
The impact on native fauna was dealt with through the 21st century unquestionable tool - risk assessments conducted by the Australian Wildlife Health Network. The risks were based on several parameters like diet, and number of sightings and conservation status It was apparent that native or Australian birds that had pigeons as a significant element of their diets were not considered to be of high status on the conservation list and many other Australian birds that would be susceptible to PPMV1 had few opportunities for contact with domestic or feral pigeons due to different habitats. However, there is little doubt that several native pigeons and doves are likely to regularly interact with feral pigeons. The nomadic nature of some and ability to travel long distances also make some vulnerable - like the diamond dove, Bronzewing pigeons, fruit doves, pied imperial pigeon and a few others. Australia has 25 species of pigeons and doves and the future impact of widespread PPMV1 outbreaks or the disease becoming endemic has not been explored beyond the rudimentary. How critical were the first 6-7 months of PPMV1 spreading in Victoria and subsequently in Sydney to the survival and future ecological fate of some of Australian native birds is a question that may take years to be answered.
Perhaps it is worthwhile to quote Australia's Nobel Prize laureate, Dr Peter Doherty;
"Apart from their obvious aesthetic value, birds control insects, distribute seeds and pollens, clean up the environment and move nutrients from the oceans to the land. They are our not so distant relatives and deserve our regard. And it is time to give them more consideration" 3
Have we shown sufficient consideration to the pigeon or more so to the Australian native bird fauna?
The moral support and help from Dr Amanda Lee during some of the more demanding days of the outbreaks in Sydney is greatly appreciated.