May 20, 2013 - Abstract. Pet birds are a not-so-well known veterinarian's clientship fraction. Bought individually or in couples, as families often do (which is a lucrative business for pet shops or local breeders) or traded (sometimes illegally) for
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Sep 16, 2002 - Jennifer K. Meece, PhD, Center for Tropical Disease Research and Training, University of Notre Dame, Notre Dame, Indiana and Clinical ...
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Feb 11, 2014 - 2014 Japanese Society of Tropical Medicine. Abstract: This review presents a comprehensive picture of the zoonotic parasitic diseases in Egypt, with partic- ular reference to their relative prevalence among humans, animal reservoirs of
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affected with erysipelas resulting in significant economic losses (Wang et al., 2010). Odontocete cetaceans are highly susceptible to E. rhusiopathiae, and infections have been reported since the 1950s (Seibold and Neal, 1956;. Simpson et al., 1958;
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James V. Conlana,*, Banchob Sripab, Stephen Attwoodc,d, Paul N. Newtone,f a School of Veterinary and Biomedical Sciences, Murdoch University, South Street, Murdoch, WA, Australia b Tropical Disease Research Laboratory, Department of Pathology, Facult
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Summary. This paper discusses food-borne zoonotic diseases by considering contemporary influences on food safety and examining pathogens at the human/animal interface. The authors also discuss the epidemiological surveillance of food-borne illnesses
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Environmental Health Perspectives â¢ VOLUME 118 | NUMBER 8 | August 2010. 1109. Review ..... Two short (~ 1 km) routes (one heavy traffic, one mixed) ... UK. 7-mile journey from village to Huddersfield, cycle along a major highway and a separate bic
released a âCitizen's Audit of Eramet Mariettaâ. (Neighbors for Clean Air 2006) during a press conference held at the site of a newly installed. ATSDR air monitor located in close prox imity to the ferro manganese refinery. The. Cincinnatibased O
aerosols of ovalbumin with 0.03 or 0.4 mg. MEHP/m3 (Hansen et al. 2007). Although no effects were observed on lung function para- meters or in the levels of IgE or IgG2, the levels. Jaakkola and Knight. 846. VOLUME 116 | NUMBER 7 | July 2008 â¢ Envi
Escherichia coli O157:H7 strains transmitted from wild passerines (European
starlings mostly) to cattle and then introduced into the food chain has been reported
in several studies [92-94]. Lack of hygiene and the absence of quarantine (especially
concerning imported birds), and dirty food and water sources seem to be the most
probable origin of infection with these zoonotic pathogens. Besides, the potential
transmission from wild birds to open-air aviaries hosted petbirds (via faecal drops)
should be considered (Boseret, pers. obs.). However, reports of transmission of these
bacteria from pet birds to humans still lack in the literature.
Viral diseases 3.2.1
Highly pathogenic avian influenza A H5N1 has been in the world health focus since
the years 2000’s outbreaks. Perkins et collaborators , demonstrated in 2003 that
the avian influenza A virus H5N1 after intranasal administration was able to induce
clinical symptoms leading to death in petbirds species like zebra finches and common 18
budgerigars, which are very common hosts of domestic ornamental aviaries, as well
as in wild species like house sparrows and european starlings, usually living close to
human habitations . Several studies demonstrated the important role of
migrating birds as pathogens vehicles all over the world [21, 96, 97], being putatively
able to infect wild indigenous birds (house sparrows, european starlings), these latter
possibly contaminating petbirds living in open air aviaries . This virus could also
spread from endemic countries [12, 16] to other locations through international trade
of exotic birds [15, 16, 22]. In relation with this fact, markets where live birds are sold
appear to represent a great risk for zoonotic transmission as demonstrated by several
authors [12, 13]. This is indeed noticeable that Asian owners seemed to be, even at
the peak of the H5N1 outbreak, unaware of the zoonotic risks this kind of business
could cause [12, 13] and this was also the case in Western countries as hybrids
between canaries and different wild passerines were and are still sold on public
markets (Boseret, pers. inform.). Illegal bird importation can also induce a risk as
suggested by Van Borm and collaborators .
West Nile Fever is an emergent vector-borne zoonosis in which birds, e.a. house
sparrows, play a key role as main and amplifying reservoir hosts . The virus
responsible for this disease is a flavivirus (Flaviviridae) known under the name of
West Nile Fever Virus (WNV) which was isolated from numerous passeriform
species, including canaries , as well as psittacines . Birds, most of the time
are subclinically affected , but can however develop a clinical form of the disease with
ocular and neurologic symptoms . Usutu virus (USUV) is another mosquito-borne
flavivirus of African origin. This avian virus is transmitted by arthropod vectors
(mainly mosquitoes of the Culex pipiens complex). Since 2001, death of birds 19
especially passerines have been associated with infection by USUV [99, 100] . It is
well known that free-living birds, including migratory species, have the potential to
disperse certain pathogenic microorganisms . Usutu virus has recently been
detected in Europe and is spreading through Austria, Hungary, Italy, Spain and
Switzerland, causing disease in birds and humans . Following the same pattern
than the West Nile Fever virus, USUV is a candidate as emerging pathogen in Europe
and the consequences for human health safety have to be considered [49, 53]. Open
air aviaries are common in our countries and could be an important feeding source
for mosquitoes, which could then inoculate the virus to humans
Proventricular dilation disease (PDD) is a disease in petbirds and, as it could be
frequently lethal, PDD is considered as a major threat to aviculture . This
syndrome is associated with inflammation of the nervous system and
gastrointestinal dysfunction as well as neurologic changes like seizures. Recently,
the cause of this disease has been attributed to a novel bornavirus, the Avian
Borna Virus (ABV) . However, there is no evidence of ABV cross-species
transmission and the zoonotic potential of this family of viruses remains unclear
Newcastle disease, caused by avian paramyxovirus (APMV) was also described in
petbirds [56, 91, 104]. Transmission to humans could also be possible, with
conjunctivitis  but the most important consequence would be spreading of the
infection among poultry breeding by the intermediary of human, wildbirds
(especially pigeons) or maybe insects mechanical vectors like the house fly (Musca
domestica)  20
Parasitic/fungal diseases 3.3.1
Toxoplasmosis is a well-known human disease, responsible for abortion or
congenital malformations in human. Although less documented than through the
cat-cycle transmission, Toxoplasma gondii has also been described as an important
pathogen for canaries, finches and budgerigars [106, 107], inducing blindness
among other symptoms. However, transmission to humans appears to be mostly
unlikely, as the birds don’t excrete T. gondii in faeces (implying no risk of
contamination by lack of hygiene or fecal matter manipulation). Indeed, Toxoplasma
gondii should be found in internal organs and muscles, butas these birds are usually
not bred in an alimentary purpose, this eliminates then the possibility of a
contamination by raw or undercooked flesh eating (Losson, pers. comm).
Pigeons are known to be reservoirs of pathogenic yeasts, like Cryptococcus
neoformans, which is described to cause opportunistic infections in humans .
However less is known on the role that might play petbirds in such zoonotic
transmission. Several studies have demonstrated the presence of C. neoformans in
parrots, little petbirds like canaries, budgerigars or lovebirds and cockatiels [109,
110]. As it has been discussed above, petbirds, moreover housed in outdoor aviaries
and then in contact with wild pigeons’ droppings, could be a potential health hazard
for humans as Cryptococcus neoformans reservoirs.
Despite a relatively poor documentation on petbirds parasitic diseases, giardiosis,
aspergillosis and cryptosporidiosis have been reported in these avian populations,
both in chronic and in acute infections. Favorisating conditions could be high-
density populations, stress, adaptation to new environment or prolonged periods in
confined housings. Transmission to human often results from faeces
manipulation or lack of hygiene [41, 56, 90].
Avian giardiasis is caused by two different Giardia species: G. ardeae and G. psittaci.
G. psittaci has been demonstrated to be responsible for fatal infections in
budgerigars , but is not transmissible to humans. The species responsible for
zoonotic infections is Giardia duodenalis, causing generally a self-limited illness,
sometimes asymptomatic, characterized by diarrhoea, abdominal pain and weight
loss.  G. duodenalis is divided into eight genotypes or “Assemblages”, among
whose Assemblages A and B appear to be responsible for human infections .
Interestingly, these genotypes have been isolated in faeces of different avian species,
without leading to the development of clinical symptoms. Birds seem then more
likely to serve as mechanical vectors of cysts and oocysts.
In birds, Cryptosporidium infection leads to intestinal, respiratory or nephrotic
symptoms and could be caused by three distinct species: C. galli, C. meleagridis and
C. baylei. The two latter have been described as possible zoonotic agents, though in a
low frequency in comparison with other species such as C. hominis or C. parvum
. The main human population at risk are very young children (first exposure,
lack of hygiene) and immunocompromised individues such as HIV-positive patients,
who will develop gastro-intestinal lesions but also infections of other organs such as
pancreas, liver and sometimes respiratory tract . Cryptosporidium parvum has
been isolated in faeces of various avian species, conforting the possibility of zoonotic
parasites shedding and transmission by birds. 
Aspergillosis has been frequently isolated from pet birds  , in both acute
(severe respiratory condition with lethargy and changes in vocalization) and
chronic forms (more often fatal because of its long-term development). However,
human infection would rather come from environmental origin, and therefore be
considered as a minor zoonotic threat, apart eventually from human
immunocompromised patients .
4. Guidelines to prevent transmission from birds to humans
One interesting document to start with is the “Compendium of Measures To Control
Chlamydia psittaci Infection Among Humans (Psittacosis) and Pet Birds (Avian
Chlamydiosis), 1998” edited by the Centre for Diseases Control in 1998 .
The transmission of zoonotic pathogens from animals to humans could be easily
decreased by applying some elementary hygiene principles. A few recommandations
could be delivered to the owner by the bird seller like the following ones:
Clean clothing and shoes after any contact with other birds (bird club meeting, bird fair, live poultry).
Wash hands before and after handling birds (including cages cleaning).
Look out every day to cages, food and water; to be sure they are clean (including
perches, feeding cups, etc.). 23
When giving fruits or vegetables to birds, discard the rotten remainings.
Change bath pots every day and let them available to birds only one hour/day (to
avoid the bathing waste water to become a reservoir for pathogens).
Wash cages once a week.
Preserve food in clean and sealed containers.
Clean and disinfect every aviary items before use.
Usually, birds breeders are correctly aware of these precautions; the risk is however
higher in the case of family pets bought for the first time in a decorative purpose or
as present for the children, especially when either parents or kids haven’t been
informed about the cited above elementary advices.
Birds’origin traceability :
In the case of birds bred in the country wherein they are sold (e.g. little birds like
canaries, finches, budgerigars), they are usually provided without any certificate or
identification (apart from a legband with the breeding identification number).
Sellers are supposed to keep an accurate traceability of their stocks, but there is as
far as we know no legal obligation of the seller to give any documents to the buyer.
About exotic pet birds issued from importation, laws differ from countries, but in a
general view, a vet certificate, a passport and an importation authorization have to
be delivered with the birds. As said before, smuggled birds represent a high risk of
zoonoses introduction. In Europe, exotic bird importation from non EU countries is
forbidden and animals imported from other EU-members countries should have an
international passport, a correct identification and a veterinary certificate of good
health (Directive 91/496/CE).
However on the owner point of view, there are some recommandations to be aware
of after buying a new pet bird.
If the birds comes from another country, request certification from the seller that
these were legally imported (eventually ask for official documents) and were
healthy prior to shipment (certified by an official veterinarian).
Schedule an appointment with a veterinarian.
Isolate new birds from other birds for a quarantine time determined by the
Restrict access to birds from people owning birds too.
Keep birds away from other birds (e.g. in the gardens).
Awareness of sickness signs
Breeders usually know the sickness signs of a bird, even if they could be somehow
difficult to detect. But for non initiated people, like sellers in animal shops or new
owners, this could be difficult to see whether their birds are healthy or ill.
Prevention tools and information should then be provided by the breeders to people
they are selling/giving their animals. Veterinarians also should better inform
owners for example by providing documentation on warning signs of infectious bird
diseases. If unusual signs of disease or if unexpected deaths occur in a breeding, the
owners should then warn their avian veterinarian.
Biosecurity and hygiene precautions in big facilities
When of sufficient size, a Hazard Analysis and Critical Control Points (HACCP) plan
could be applied in breeding facilities and in selling facilities. To quarantine newly
incoming birds is an absolutely necessary precaution. These animals should be kept
in clean cages for a duration estimated by the sanitary veterinarian, and pathogens
and/or pests absence (including D. gallinae) should be carefully checked. CDC
recommends at least a quarantine of 30-45 days when Chlamydophila psittaci
infection is suspected . For example, one should check these different control
1. Direct birds’ environment : -
Presence/absence of D. gallinae in the quarantine cages after at least one week,
which is the time needed by the parasite to accomplish a complete reproduction
cycle, from egg to egg . For example, the acarids could be easily found on
feedballs, perches or on the removable bottom sandtray. An easy test is to push
strongly with the thumb on dirty spots pasted on the reverse face of this tray and
scratch them from left to right (or vice versa). If a bloody smear does appear, this
would be an efficient sign that blood-fed parasites did begin to colonize cages’
anfractuosities (Boseret, pers. obs.).
Color/consistency/quantity of droppings: for example, a yellow stain should
suggest campylobacteriosis, a liquid consistency should refer to salmonellosis or
other enterobacteriaceae infections .
Transport cages: were they soiled or clean? Presence of dead birds?
2. Birds : general examination
Presence/absence of other pests’ species living most of their time on the host, e.g.
at the calamus of the feathers (like Ornithonyssus sylviarum), at the edge of the
beak or in the leg’s scales (like Knemidokoptes pilae, which is a non zoonotic
mange agent) or in another part of the body (e.g. ticks, lice). Broken feathers or
feather-loss could indicate pruritus and discomfort, other indicators of
ectoparasites infestation . Ectoparasites are considered by many breeders to
be a good indicator of inadequate hygiene and management and their detection
therefore could awake attention of the owner on the health status of their
infested incoming birds.
General state of the birds (good/bad)
Perching/ lying at the bottom of the cage
Normal activity/apathic, rolled in ruffled feathers
In social groups/isolated
Good respiratory state/nasal-ocular discharge, open beak
641 642 643
Plumage aspect: are the birds in molting period? How is the molting: homogenous and bilateral/heterogenous and asymmetric
3. Quarantine facilities hygienic state:
Frequence and efficiency of cages/walls/floor/shells disinfection
Food storage (access to mice, rats?)
Environmental conditions: temperature, humidity, duration of light hours
This list is not exhaustive and a complete list of adequate control points has to be
determined in function of the kind and size of breeding, facilities conformation,
season, frequence of birds movements, etc. The above recommendations should
however constitute a basis of elementary examinations to be performed in every
In case of a high level of risk or when a doubt emerges relatively to the birds’ health
state, the following laboratory analyses could be performed:
654 655 656 657 658
1. Individu level: necropsy of a dead or a sacrificed sick individu, performed along with bacterial analyses of intestinal content or other organs presenting lesions. 2. Group level: Bacterial analyses of cloacal or/and oral swabs of a birds sample bunch (one-to-ten, one-to-fifteen…). 3. Vector level: molecular analyses of vectors found on birds and/or in the cages, to
detect specifically zoonotic agents: Chlamydophila psittaci, west nile fever, etc…
The first two types of analyses could be an interesting investment and couldn’t be
too much expensive (less than 100 euros/birds’ bunch).
However, molecular analyses are on another financial level. One should recommend
them in particular cases, first when birds are about to be handled by owners, like
parrots, parakeets or cockatiels, second when the pathogen targeted is of zoonotic
non negligeable importance. For example, tuberculosis detection has to be carried
out with a critical mind, as false negative do occur. On another hand, as surveillance
of zoonoses is a European legal obligation (Directive 2003/99/EC), testing birds
could be systematically included in national surveillance programs, a fortiori when
human health is estimated to be put at risk, and then could then grant the breeders
with a official budget intervention. 28
Another suggestion to diminish the costs at a local level would be to perform such
tests in multiplex series, allowing breeders to share somehow elevated costs. But all
these possibilities involves a complete change of mind and implies a broader
transparency in these kind of breedings, which still lacks even in our high-controlled
countries (Boseret, pers. inform.).
When birds are proved to be healthy, then they could be introduced in their
definitive facilities. Outcoming birds should be submitted to similar sanitary
Moreover, the precaution of all-in/all-out replacement system, already applied in
poultry exploitations, should be carried out in petbirds breedings too. For example,
only birds of the same age should be kept in the same location, and when moved, the
facility should be disinfected carefully before welcoming a new flock.
In selling facilities, where birds from different origins could be mixed up, only
replace them when the whole flock has been sold and the cages cleaned with ad hoc
disinfectants. One interesting initiative would be to create a certificate of « good
health » to moving flocks, but as many animals are sold in non-official ways (e.g.
private breedings, markets), this couldn’t be not so easy to put in place.
Control point should be also implemented on bird’s fairs. Sanitary certificates could
be an obligatory document to provide to authorities to allow the breeder to attend
This review aimed to present a non-exhaustive panorama of data relative to
petbirds-human pathogen transmission. Different situations have been illustrated in
this short review: familial households, breeding or selling facilities, bird fairs,
international trade and the wildbirds’problematic of reservoirs. Although this
represents a minor part of the companion animals’ vet clientship, petbirds’ diseases
with zoonotic potential shouldn’t be neglected or underestimated, considering the
major health impact on the population, including children. Referring to Pastoret and
Vallat zoonoses classification, petbird zoonoses own to the most threadful diseases
types: 2 and 2+ (see table 3; ). Vets could then play an important role in
educating pets (including birds) owners.
On an another point of view, pathogens’ shedding by wild passerine birds could be
responsible of maintaining infection in domestic birds pools, such as openair
aviaries or poultry breedings, and could have important economic impacts. The
presence of Salmonella species in starling faeces and in cattle feeding operations
reported e.a. by Carlson and collaborators is a good example of a under-known
reservoir phenomenon. Another example is the role of birds, among which
passerines, as amplifying hosts for some vector-borne zoonotic emerging viruses.
Open air aviaries are not protected from mosquitoes, and ornamental birds have
been showed to be able to act the same way than their wild counterparts. Migrating
birds are also a sanitary concern, as these birds could spread a high variety of
pathogens by solely defecating above outdoor aviaries wherein petbirds are housed.
Thus these birds concentration could become a non negligible reservoir of
pathogens, contributing to maintain and spread infection in human population.
Referring on vectors, D. gallinae following author’s advice is an underestimated
concern – probably too many times misdiagnosed - in petbird medicine as well as in
small avian breedings, as the parasite could be carried and transferred from one
species to another, mostly by inert materials such cages, perches, water or feed
bowls, etc. and eventually by the intermediaire of man. Threatening pathogens like
C. psittaci or Salmonella ssp. were reported to be carried by the mite and transmitted
to petbirds, which could then infect either their owners or their cagemates. In
addition, sanitary state of petbird owning and trade is rather unclear in many
countries. HACCP or other quality control plans (ISO, AFNOR…) are applied by the
Federal Agency for Food Safety Chain (FAFSC) in Belgian poultry breedings, but not
in « backyard poultry flocks » or in local passerine breedings. Legislation does exist
e.g. on international trade but despite this, illegal introduction of birds in our
countries still remains a threat for human health when considering the highly
pathogenic agents that could be brought in our frontiers (e.g. avian influenza A virus
H5N1 or chlamydophilosis).
Therefore, investigate the health status of pet birds, facilities, avian exploitations
and owners should be an interesting starting point to define human health risks
encountered (from family to breeding scale), to propose economic and sanitary
prevention measures (e.g. biosecurity, prophylaxy, hygiene) in an interest of health
protection and economic improvement. This investigation could be a good picture
illustrating the concept of « Animals + Humans = One Health ».
The author(s) declare that they have no competing interests.
GB and CS fixed the design of the study; GB has realized the literature research and
analysis; BL, ET, JM and CS have been involved in revising the manuscript critically
for important intellectual content; CS has given final approval of the version to be
GB is doctor in veterinary medicine and defended a PhD on songbirds’behavior and
health status. She is currently studying zoonoses transmitted by birds, especially
petbirds, in CS research unit.
BL, ET, JGM and CS are professors and heads of respectively parasitology, virology,
bacteriology and epidemiology and risk analysis sections of the department of
infectious and parasitic diseases, (Faculty of Veterinary Medicine, University of
Liège, Belgium) and therefore provided the author with expert advices on diseases
discussed in this manuscript.
We would like to acknowledge the team of the UREAR-ULg unit for their kind
support in this redacting process, Drs Dal Pozzo, Humblet and Martinelle.
761 762 763
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1072 1073 TABLES 1074 Table 1: main pet bird species following International Ornithologic Congress (IOC) 1075 classification 3.1 (2012) Order
Canari/serin des canaries
Pinson des arbres
Diamant à longue queue
Diamant de Gould
Bengali/moineau du japon
African or Timneh grey parrot
Gris du Gabon
Table 2: main transmission routes of diseases
Non contagious diseases
Example in petbirds
West Nile Fever
1079 1080 1081 1082 1083
Table 3: classification of emerging zoonoses