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Chlamydophila psittaci in zoo parakeets: the risk for visitors
Keywords
Chlamydophila psittaci, zoo, parakeet, risk assessment, clearview, visitors, chlamydiosis
Summary
This research was aimed at investigating the risk for visitors of zoos in relation to Chlamydophila psittaci. This is a
gram negative obligate intracellular bacterium which can be transmitted from birds to humans. The research took
place in a zoo in the Netherlands. To investigate the prevalence of C. psittaci in the population of birds, cloacaswabs
were taken of 32 birds and a Clearview Chlamydia MF test and PCR were performed on these samples. To evaluate the
compliance in hand washing observations of the visitors were done. One bird tested positive on a species specific
Chlamydia PCR, but negative for Chlamydophila psittaci with real-time PCR. The prevalence of C. psittaci in this sample
population of birds was low compared to the prevalence found in other studies in other bird populations. A maximum
number of eight birds (8 %) could be diseased with this sample size. Exact infectious doses for humans are not known.
Although the attack rates in reported outbreaks are not extremely high there is evidence that as little as a single
contact might result in zoonotic transmission and consequent disease. The severity of the consequent disease can be
high but a majority of people will only suffer from flu like symptoms. 346 visitors were observed, hand washing was
performed by 18 (5,2 %) of them. The compliance in hand washing of visitors in this study was extremely low
compared to other studies. In conclusion, with a maximal prevalence of eight percent, the risk of exposure for visitors
is relatively small. But since severe symptoms upon infection might develop, preventive measurements to reduce the
risk of transmission of the disease are absolutely necessary.
Introduction
Most zoos are constantly improving and renewing their exhibits. As a part of this more and more
zoos offer their visitors a chance to watch the exhibited animals up close. Sometimes the visitors
are even allowed to enter animal exhibits for the ultimate experience. Although this contributes
to educational purposes and to the experience and amusement of visitors it also poses some
risks. For instance, a zoo in the Netherlands recently opened a bird exhibit with several species
of psittacine birds. These birds can carry C. psittaci, a bacterium that can cause disease in both
birds and humans. Visitors might be at risk of being infected upon contact with the birds.
Chlamydophila psittaci is a gram negative obligate intracellular bacterium. 7, 9, 26 Currently at
least eight serovars and nine different genotypes of C. psittaci are known. These are the
genotypes A-F, E/B, M56 and WC. Some genotypes are more or less host specific, others can
infect a range of different animal species. Genotype A, B and F are usually associated with
psittacine birds.23, 25
In general, the bacterium has been detected in about 465 species from 30 different bird orders.
The prevalence that can be found in groups of psittacine birds differs significantly between
researches. In a research in which necropsy was performed on 533 psittacine birds in Texas,
18,2 percent of the birds were infected with C. psittaci. In an investigation among birds in
breeding facilities in Belgium, 19,2 percent of 308 birds tested positive on PCR for C. psittaci. 165
asymptomatic birds in Poland were tested with PCR and 10,3 percent were positive. In a
research in Brazil, an average prevalence of 35,8 percent was observed in three breeding
facilities. 5, 18, 19, 27
Infected birds shed the bacteria through faeces and nasal discharge. Fecal shedding can be
intermittent and periods of active bacterial excretion can last for up to several months
depending on type of strain, infectious dose and host immune system. Shedding in clinically
healthy birds can be induced by stress. Stress can be induced by reproduction, poor nutrition,
transportation, overcrowding and improper husbandry.4, 7, 23 The incubation period differs
between strains and depends on the infectious dose, but can range from several days to several
weeks.7, 9, 23 Both clinically and subclinically infected birds can shed the bacterium and pose a
threat to both humans and other animals.3, 21 Once C. psittaci is introduced in a population of
birds, other birds can be infected by inhalation or ingestion of contaminated materials. Vertical
transmission and transmission in the nest to fledglings can occur. Ectoparasites have been
shown to transmit the disease between birds, but they probably act as a mechanical factor.
Furthermore, birds can become infected through contaminated water. 3, 9, 21, 26
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In psittacine birds the disease associated with C. psittaci infection is called psittacosis. Some
infected birds may show no clinical signs. Clinical manifestations of the disease range from mild,
nonspecific signs to severe disease and even death. 4, 7, 23, 24
Humans infected with C. psittaci can also be asymptomatic. In most humans the disease
manifests with mild, flu-like symptoms such as coughing, fever, shivering, headache, sore throat
and photophobia.26 Respiratory disease can give rise to symptoms like breathing difficulty and
chest tightness. In severe cases the disease becomes systemic, with pneumonia and sometimes
even multiple organ failure. Endocarditis, myocarditis, hepatitis, pancreatitis,
keratoconjunctivitis, encephalitis, reactive arthritis, anemia and neurological and renal
complications can sometimes be seen. Infection might cause abortion in pregnant women.
Infections with C. psittaci are rarely fatal when antibiotic therapy is available. The disease occurs
most frequently in people between 35 and 55 years of age. 6, 7, 12, 21, 23, 24 The incubation period
ranges from several days up to two weeks, but longer periods can also occur.10, 2123
Humans can be infected by inhalation of infectious particles via aerosols from urine, dried faeces
or respiratory tract secretions, mouth to beak contact, being bitten by an infected bird, and
direct contact with contaminated excretions. C. psittaci is generally transmitted to humans via
inhalation of infectious dust particles and aerosols.7, 10, 21
The aim of this study was to assess the risk for zoo visitors with relation to Chlamydophila
psittaci.
Materials and methods
The research took place in a zoo in the Netherlands. The zoo attracts around 650.000 visitors
per year, covers an area of about 19 ha and houses almost 130 species of animals. In this zoo, a
new climbing route for children through the bird exhibit was recently opened. When following
the route, visitors get the chance to see the birds up close. The construction is largely made out
of ropes and ends in a slide. Visitors also have access to the exhibit via a ground route. Several
psittacine birds are housed in the exhibit, including the following species; Cockatiel (Nymphicus
hollandicus), Monk Parakeet (Myiopsitta monachus), Rose-ringed Parakeet (Psittacula krameri),
and Burrowing Parrot (Cyanoliseus patagonus). The birds are sampled biannually to assess their
health status. Six months prior to this research, the birds had been given a doxycycline
treatment.
Diagnosing a suspected bird with C. psittaci can be difficult, especially in the absence of clinical
signs. A combination of tests is widely recommended. 7, 23 Although culture has historically been
considered the golden standard, it might not be as sensitive as Polymerase chain reaction (PCR)
which has recently been developed for C. psittaci. 22, 23, 26 The most specific PCR’s are directed at
the ompA gene, a specific topic on the C. psittaci genome. It has four regions which are specific
for a distinct type of serovar, and so even the serovar of the agent can be determined by some
PCR’s. 7, 22, 23
To investigate the prevalence of C. psittaci in the population of birds, samples were taken of a
number of birds and a combination of two tests was performed on these samples. A Clearview
Chlamydia MF test (Inverness Medical Innovations Australia Pty Ltd, Sinnamon Park) had
formerly been utilized by the zoo to monitor the birds. Therefore this test was used together
with PCR in this research. The Clearview test is an immunoassay test using a genus specific
epitope, and was originally designed to detect Chlamydia trachomatis in humans.
Based on results found in other bird populations and the fact that the birds had been given
doxycycline treatment prior to this research, which would result in a lower prevalence, the
predicted prevalence was at least eight percent, and it was calculated that 32 birds had to be
sampled. Birds were caged overnight by closing the exit of their inner exhibit. After that, the
birds were captured and two cloacaswabs were taken from each bird. The ring number was
noted down and the swabs were assigned a number, with each number corresponding with one
specific bird and two cloacaswabs. After this was done the bird was let free. The swabs were
randomly assigned to a test. One swab was sent to IDEXX (IDEXX Vet Med Lab, Hoofddorp) for
PCR and the Clearview test was performed on the second one.
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Hand hygiene is one commonly accepted way to reduce the risk of getting infected with all kinds
of infectious agents. 1, 16, 17, 28 A hand washing facility was available for visitors of the climbing
route so the risk of infection could be decreased. To evaluate the compliance in hand washing
observations of the visitors were done.
Observations of the visitors were carried out during two hours on two successive days. Visitors
that entered the exhibit via the climbing route were counted, and the number of visitors that
washed their hands was also observed. It was not possible to distinguish between hand washing
with or without soap.
Results
Out of the 32 birds that were sampled, one bird tested positive on a species specific Chlamydia
PCR. However, this bird tested negative for Chlamydophila psittaci with real-time PCR. With the
species specific PCR it was not possible to differentiate between C. abortus, C. felis and C. caviae.
None of the Clearview test results were positive. For the detection of C. psittaci, the tests showed
100 percent agreement. No birds were ill before, during or after the time of the research.
In two consecutive days 346 visitors were observed. During the first observation period, 105
visitors were seen and hand washing was performed by none of them. During the second
observation period, 241 visitors were monitored and hand washing was performed by 18 of
them. In total, 18 (5,2 %) out of 346 visitors washed their hands during the time of observation.
Discussion
The prevalence of C. psittaci in this sample population of birds was low compared to the
prevalence found in other studies in other bird populations.4, 5, 18, 27 This may be due to a good
feeding program, which included a high quality seed diet. Also, the birds were all captured and
given a preventive doxycycline treatment about 6 months prior to this research.
Approximately 100 birds were housed in the exhibit, and none of the sampled birds were found
positive for C. psittaci. Using Win Episcope 2.0 it was calculated that with the used sample size of
32 birds, the confidence interval would be 96,02 in case of a prevalence of eight percent. So with
95 percent confidence it can be said that a maximum number of eight birds could be diseased
with this sample size. All birds in the exhibit were clinically healthy. Whether or not clinically
healthy and clinically diseased animals shed the same amount of bacteria when infected is not
known. Because C. psittaci can be shed intermittently, it might be that there were infected birds
that were not actively shedding during sampling. Also, birds that were healthy during the
research might become infected again. The population of birds used in this research was not
completely closed, as contact with wild birds is possible as it is an open aviary. Wild birds are
supposed to form a reservoir through which captive birds can become infected.3, 9 Therefore it
cannot be said that the risk of exposure for visitors is neglectable.
C. psittaci is generally transmitted to humans via aerosols and dust particles. 21 This means that
the distance from the visitors to the birds would need to be much larger in order to prevent
possible transmission. This would conflict with educational and entertainment purposes. The
ventilation in the exhibit is excellent, as it is an open aviary. Since investigated outbreaks are
frequently associated with poor ventilation, this might be a factor related to exposure.2, 14
However, this has never thoroughly been investigated.
One bird was found positive on a Chlamydophila species specific PCR, but not on the C. psittaci
specific PCR. All Chlamydophila species are potentially zoonotic, but little is known about the
transmission of C. abortus, C. caviae and C. felis from other animals to birds, and from birds to
humans. There might be a potential risk for the visitors that come in contact with this infected
bird, but as the other Chlamydophila species are considered less contagious than C. psittaci it
would be a small risk.21 However, there should be further research on this topic.
It is impossible to make a definitive quantitative risk assessment based on the literature
available. This is because the exact infectious doses for humans are not known. Therefore, in
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this article the focus will be on a qualitative risk assessment. The infectious dose depends on the
virulence of the strain involved and the number of bacteria transmitted. Some serovars of C.
psittaci are thought to be very infectious for humans.21 Indeed, a relation with exposure to birds
can not in all cases be made. Thus, even short exposure can result in infection.15, 23, 24 When
psittacosis is common in a population of birds the number of diseased humans in contact with
this bird population can be fairly high. In a bird park in Japan, 17 people became ill upon contact
with diseased birds. At a bird fair in the Netherlands, 25 people were diseased after participating
or visiting the fair. In France, 33 out of 86 investigated persons were probably infected after
visiting a local bird fair.2, 13, 14 In the USA 66 human cases were reported between 2005 and 2009.
Studies that were performed on larger populations of humans suggest that the incidence of C.
psittaci might be higher than expected based on reported cases alone.9, 10, 24
9, 10, 24
9, 10, 24
In a research among 450 healthy participants 12,7 percent tested positive for C. psittaci DNA.
Most at risk were people having daily or weekly contact with psittacine birds and racing pigeons.
It might be that people in frequent contact with birds are more at risk, but experience milder
forms of disease. 10, 23, 27
In previous researches of psittacosis outbreaks, 34 and 38 percent of the tested human
population was infected.2, 11 However, the persons involved had had close contact with possibly
infected birds or had been in the same space as the suspected birds for longer periods of time. In
the study at an outbreak in a bird show in the Netherlands the attack rate was higher in persons
with prolonged contact with the supposedly diseased birds than in visitors of the show. The
attack rates were 39 percent and three percent respectively.13
Although the attack rates in outbreaks are not extremely high there is evidence that as little as a
single contact might result in zoonotic transmission and consequent disease.11, 14 This should be
taken in consideration.
The severity of the consequent disease can undoubtedly be high, although a majority of people
will only suffer from flu like symptoms. Whereas fatalities are rare because of sufficient
treatment possibilities there are cases of severe disease in which hospitalization in an intensive
care unit was necessary.8, 11, 24 Then there is a large group of persons that has symptoms not
severe enough to require intensive care but that will require hospitalization or need to consult a
doctor. Children do not seem to be more at risk than adults. Some articles even suggest that
children are less likely to develop severe symptoms than adults.7, 24 The median ages per year of
psittacosis reports in the Netherlands from 2004 to 2011 ranged from 59 to 60.20 This confirms
the ages in which the highest incidence can be seen as reported by Stewardson and Grayson.24
Although rare, cases of pregnant women suffering abortion have also been reported. 12, 21
To reduce the risk for visitors of being infected, a sink and soap dispenser were placed at the end
of the climbing route to create an opportunity for visitors to wash their hands.
The compliance in hand washing of visitors in this study was extremely low. Other studies in
petting zoos have shown a wide range of hand hygiene compliance among visitors, ranging from
0 to 77 percent. In most petting zoos the mean value ranged from 30,9 to 58 percent.1, 28 So the
number of visitors performing hand hygiene in this study was below average. There are several
explanations for this.
It has to be noted that during the first observation it was cold and it was raining. This might have
contributed to the low number of visitors washing their hands; zero out of 105 visitors washed
their hands during this observation.
Most of the visitors that washed their hands were parents encouraging their children to do the
same. Few to no children washed their hands without the encouragement of a parent. As most of
the visitors of the climbing route were children on their own, with their parents waiting for them
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near the exit, hand washing was not performed by most of the children visiting the climbing
route. The sink was placed on such a level that children may encounter difficulties reaching it.
Hand hygiene is considered a great preventive measure against lots of transmissible diseases. 1,
16, 17, 28 However, it is not known whether or not it is effective against C. psittaci, since no studies
have investigated the relation between the performance of hand washing and the incidence of
infection with C. psittaci.
This study has apparent restrictions. Infective doses are not known, so no definitive quantitative
risk assessment could be made. The collected observational data were limited and collected in
conditions in which visitors are possibly less likely to perform hand hygiene.
A little calculation to establish the hypothetical risk for visitors of this specific zoo can be
made with the data derived from previously described outbreaks. In the outbreak at the bird
fair in the Netherlands, three percent of the visitors became ill after visiting the show. No
birds were reported ill in this case.13 As no bird tested positive in this zoo, we will take a low
estimate of three percent of visitors getting infected in this zoo for the calculation. We will
assume that 50 percent of the visitors of the zoo will visit the climbing route. Then on a
arbitrary day about 900 visitors will visit the climbing route. This is 50 percent of about 1800
visitors per day, which is based on 650.000 visitors per year. It can then be calculated that 27
people, three percent out of 900, will get infected. It has never been thoroughly investigated
how many infected people will actually become diseased. If 30 percent of the infected visitors
would develop symptoms then eight visitors per day would get ill from visiting the climbing
route. But this is only an estimation. If the birds in the exhibit would show signs of
psittacosis, the visitors would be at a significant higher risk of getting infected. During an
outbreak in the Netherlands in 2005 where some birds tested positive, 34 percent of the
tested human population was infected with Chlamydophila. Ten persons became ill, with
symptoms ranging from headache to sepsis and multi organ failure, three of them had to be
hospitalized.11 However, it is highly unlikely that visitors that develop symptoms will relate
them to their visit to the zoo, since the incubation time ranges from several days to several
weeks.9, 23 Only cases of severe disease where hospitalization is needed will be investigated
and possibly linked to the zoo.
Conclusion
The aim of this study was to assess the risk for zoo visitors with relation to Chlamydophila
psittaci. With the obtained results it can be said that the exposure for visitors is low. This is
mainly because the prevalence of Chlamydophila psittaci in the birds of maximal eight percent is
low. The zoo where this research was carried out attracts on average approximately 1800
people daily, and a considerable amount of these will visit the climbing route. Although the
overall risk of transmission of C. psittaci is small, there is a reasonable chance that some of these
visitors will get infected with C. psittaci.
The severity of the disease ranges from mild to severe, but most infections go by unnoticed. The
chance that a visitor infected with C. psittaci will develop severe disease is small, but it still might
happen that a visitor gets very ill, and this will have grave consequences.
So the risk is restricted, but there is some risk for visitors of getting infected with C. psittaci.
Therefore, measures to reduce the risk of transmission of the disease are absolutely necessary.
Acknowledgements
Financial, field and technical support was provided by DierenPark Amersfoort, and in particular
T. Hendrikse. Financial and technical support was further provided by the Institute for Risk
Assessment Sciences, division Veterinary Public Health at the Utrecht University. Special thanks
to E.C. Keessen and I.M van Veen, who provided useful assistance in various aspects of this study.
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