Ectoparasites from Feral Pigeons: Impact on Humans
Ectoparasites from Feral Pigeons: Impact on Humans
Introduction
Feral pigeons (Columba livia Gmelin, 1789) are among the most successful
avian settlers in our cities. They are distributed worldwide and live close to the
human population. The average feral pigeon population is around 1 pigeon per
10–20 city inhabitants. The world population is therefore estimated to be
between 165 and 330 million individuals. Feral pigeons bring pleasure to people
who feed them, but the large food supplies provided by pigeon friends and food
leftovers, together with the absence of enemies, allows the development of large
populations that can cause various problems. An individual feral pigeon
produces around 12 kg of excrement each year soiling buildings and public
areas. Large quantities of droppings accumulate in particular in its roosting and
breeding places. Pigeon feces provide ideal conditions for the growth of mould
fungi that damage construction, as e.g. stone and concrete, leading to erosion of
historic buildings and monuments. The damage caused by an individual feral
pigeon has been estimated to be EUR 23.7– 33.5 per year. In the USA, feral
pigeons cause an estimated USD 1.1 billion per year in damages. These damage
costs do not include the damages associated with their role as reservoirs and
vectors for diseases. Suitable nesting sites are rare in most cities, leading to
intense competition and overcrowding at breeding sites which produces poor
living conditions due to social stress, diseases and parasites.
Feral pigeons can pose various health hazards to man and his domestic
animals. In feral pigeon populations so far 109 different pathogenic agents that
can infest humans have been recorded, but only 7 have in fact been transmitted
to humans, causing a total of 230 reported infections. These were Chlamydophila
psittaci with 101 cases and 2 fatal courses, Histoplasma capsulatum with 91
cases, Cryptococcus neoformans with 11 cases and 2 fatal courses, Aspergillus
sp. with 13 cases and 9 fatal courses, Candida sp. with 12 cases and Toxoplasma
with 1 case. 229 of 230 infections were transmitted by the airborne route and
can therefore be prevented by hygienic precautions in most cases when handling
pigeons and their excrements. Only 1 case has been described where the patient
was infected by the cutaneous route. An HIV-positive former intravenous drug
addict presented with a primary cutaneous Cryptococcus’s after an injury
inflicted by pigeons nesting in an abandoned house. Exposure to pigeons and
their effluents can cause ‘pigeon breeder’s lung’, a hypersensitivity reaction
causing allergic alveolitis provoked by inhaled pigeon antigens. To date a total of
9 cases, 1 with fatal outcome, have been reported due to feral pigeons.
Many wild-living species have a parasitic fauna comparable to the feral
pigeons, but no other species lives as closely to humans. They use various
building structures for roosting and breeding, and therefore their parasites and
pathogens are at close distance to humans, presenting a serious health risk. We
report a case of concomitant infestation with Dermanyssus gallinae, Argas
reflexus and Cimex lectularius due to feral pigeons using a balcony for roosting.
To our knowledge, this is the first reported case where one individual has
concurrently been attacked by 3 different ectoparasites deriving from feral
pigeons. In a review we point out the importance of feral pigeons and their
ectoparasites for dermatologists.
Case Report
A 26-year-old American female student had suffered from a cat dander allergy
and from cat flea Ctenocephalides felis infestation in the past. On April 5, 2009
she moved into an apartment on the 4th floor of an old carelessly renovated
apartment building, where the former tenant had fed a group of 8–10 feral
pigeons on her balcony. The pigeons used the balcony as an overnight roost and
most likely for breeding. The floor of the balcony was completely covered with a
layer of feces and feathers of about 5 cm height that was removed by the former
tenant before the patient moved into the apartment. Ten days later, she awoke
4–5 times with a ‘burning feeling’ on the legs. In the morning she first noticed an
exanthema that consisted of hundreds of small itching papules on the legs,
forearms, loin and abdomen. The next day she found high numbers of insects
she later identified as bedbugs. The following night she suffered from general
symptoms such as fatigue, weakness, dizziness, tachycardia and thoracic
oppression and slept against her habit more than 14 h. The general symptoms
disappeared on the next day. Two days later she presented to her general
practitioner who diagnosed a ‘rash’ and a nodule with a central sting on the
forearm and who prescribed fexofenadine. For the following 2 months she only
noticed sporadic stings.
Preparing a lecture on the feral pigeon problem, she came across articles on
hygienic problems deriving from feral pigeons. By an internet search she
identified insects she found on the floor, on a water bottle and near her clock
radio as bedbugs C. lectularius which she disposed of by vacuum cleaning. Later,
she clearly identified bedbugs from specimens of our parasite collection. In the
morning she noted additional stings in a disseminated distribution that had
occurred during the night. These stings were different from the stings of the first
infestation as they occurred as larger linearly assorted urticarial and papular
stings. During the night she found another 3 bedbug’s C. lectularius beside the
bed that she immediately disposed of by vacuum cleaning. In addition she
discovered a hiding place of bedbugs in her clock radio, which by pushing a
button could be forced to leave this only electric apparatus in the room. She then
disposed of the clock radio including the bugs in a plastic bag.
Her 25-year-old partner who occasionally stayed overnight with her was also
infested with red mites and presumably with bedbugs but not with pigeon ticks.
He showed papules on the legs, abdomen, breast and general symptoms such as
fatigue, weakness, dizziness, dyspnea, palpitations and heat waves that
disappeared within 1 day. He did not consult a physician. On the upper side of
her mattress that lay directly on the floor, she detected pigeon ticks Argas
reflexus that she also disposed of with a vacuum cleaner. She and her partner
moved to the living room for sleeping to escape further stings and because of the
fear of infestation. On April 27, a pest controller performed a disinfestation of
the balcony and the apartment with dichlorvos, deltamethrin and pyrethrum. He
confirmed the presence of pigeon ticks and red mites. On the floor and at the
glazed door between the balcony and the bedroom, hundreds of red mites
crawled about. This glazed door did not fit completely, which allowed parasites
to enter the bedroom from the balcony. A final check was performed 1 week later.
Two weeks later, she applied to one of us (Haag-Wackernagel) for an interview
concerning her lecture on feral pigeons and brought the parasites she had
recovered from the vacuum cleaner. The parasitological determination confirmed
pigeon ticks (Fig. 1) and red mites (fig. 2). One tick (9.36.1 mm) showed remains
of blood and had bursted when aspirated, an unfed tick of 4.93 mm was alive.
Later, she found 8 additional dead pigeon ticks on her balcony, one of them
engorged with blood. The red mites were partly engorged with blood which was
visible from the dark-brown-colored intestine. On her left forearm she had an
excoriated nodule of 7 mm in diameter with a perifocal erythema (fig. 3). On the
legs she still had small excoriated papules caused by the mite stings (fig. 4).
On May 16, she installed a bird net to prevent the pigeons from using the
balcony as overnight roost. Nine weeks after the first infestation she still found
red mites in the bedroom and living room. Every 3 days she used a pyrethrum
spray around the balcony door to kill invading mites. Since the disinfestation by
the pest controller, the number of stings had decreased but still occurred in
lower numbers, preferentially on the legs. On June 10, after more than 2 months
of parasite attacks, we performed a detailed on-site search. On the balcony we
found living pigeon ticks (fig. 5) and dead red mites in wall chinks and gaps of
the glazed door. We found tick feces around holes and chinks of the wooden
coverings and the walls as well as at the opened bathroom window where 2 feral
pigeons were roosting. All other balconies and window ledges of the house
including the neighboring houses were fouled with pigeon feces and on 2
balconies pigeon nests were present. The 46-day-old pigeon tick sting of the
patient was still painful on palpation and showed a persistent inflammation (fig.
3). As an ad hoc measure, we placed a glue barrier to test whether parasites still
invaded the apartment. We advised the patient to contact her landlord to claim
complete disinfestation and renovation including sealing of all gaps and chinks
and a disinfestation or removal of the canopy covering the balcony. Two weeks
later, she brought 4 living pigeon ticks she had found on the balcony and the
glue tapes placed in front of the glazed door. The 108-cm-long and 6-cmwide
tape contained 60 red mites, confirming a continued invasion from the balcony.
The largest distance a mite covered from the edge before having been caught in
the glue was 23 mm. As a preventive measure she vacuum-cleaned daily to
remove invading red mites and used an insecticide spray around the balcony
door every 3 days. Since our on-site visit, she was not stung any more.
Fig. 1. Pigeon ticks Argas reflexus found in the bedroom selected from the
vacuum cleaner by the patient. The tick below is engorged with blood and burst
when aspirated, the upper starving tick is intact.
Fig. 2. Red mites Dermanyssus gallinae, some engorged with blood (dark
brown intestine)
Fig. 3. (a) 25-day-old sting of the pigeon tick Argas reflexus . (b) The same sting
when 46 days old.
For an infestation, the parasite has to cover the distance to the human
host. There a two principal ways. In the first case the patient actively comes in
contact with the source of infestation. All reported cases of such human activity
leading to an infestation with feral pigeon parasites concerned the red mite D.
gallinae. For example, Przybilla et al. described a young woman who was stung
by red mites when removing a feral pigeon nest from a toilet, and Baselga et al.
reported a case where a young woman brought a radio with red mites from the
attic where feral pigeons lived. She and her brother were subsequently infested
with the mites. One of us (Haag-Wackernagel) was attacked by hundreds of red
mites shortly after a pigeon loft keeper had put a plastic bag with pigeon feces
harboring the parasites in front of his office. In all other cases the parasite
actively covered the distance to the human host from feral pigeon breeding or
resting sites. Auger et al. [42] reported a hospital infection in 10 patients by D.
gallinae from feral pigeon nests on galleries, window ledges and air conditioners.
The patients acquired the stings while walking in the galleries.
Winkler reported a hospital infection where D. gallinae entered the patients’
rooms through ventilation openings and attacked 12 patients, one suffering over
500 bites. Cafiero et al. reported several cases from Southern Italy where
humans were attacked by red mites which all derived from abandoned feral
pigeon nests. In Zurich (Switzerland) in 1930, many inhabitants panicked when
an article in a local newspaper reported an outbreak of an infestation caused by
the red blood mite. The feral pigeons were shot and the human population was
advised not to feed pigeons as it was believed that even feeding pigeons might
lead to infestations. The parasite can be easily removed from the patient by
showering or a full bath. In most cases, medical treatment is not necessary. If
treatment of mite bites is needed, antihistamines and mild topical corticosteroids
typically bring rapid relief. Elimination of the mite from the patient’s environment
is usually curative since they are only temporary visitors to the human skin and
incapable of living and reproducing on the human host. Roaming mites in
human living space can easily be removed with a vacuum cleaner or treated with
a nontoxic insecticide spray as e.g. pyrethroids.
Pigeon nests should be completely removed and treated with insecticides
before disposal to prevent further infestations as the parasites may leave the
waste bins. To prevent further nesting and roosting, access to buildings should
be obstructed, and ledges and other structures should be protected with pigeon
deterrent systems or structural restrictions. The Northern Fowl Mite
Ornithonyssus sylviarum the northern fowl mite is a common, bloodsucking
parasite that occurs on the plumage of the chicken in temperate regions
throughout the world. It also affects pigeons and many wild birds. The northern
fowl mite is very similar to D. gallinae and therefore often confused with it. The
entire life cycle of Ornithonyssus sylviarum usually takes place on the host.
Under high infestations the parasite can also be found in nest debris from where
it can emigrate to human habitations. Up to date only 1 case has been reported
where the mite emigrated from an abandoned feral pigeon nest together with D.
gallinae and caused a nosocomial infection in a hospital. The Pigeon Tick Argas
reflexus the most important ectoparasite, even the most significant health hazard
posed by feral pigeons, is the soft tick A. reflexus (fig. 9). It is a temporary,
bloodsucking ectoparasite of pigeons occurring in various parts of Europe, the
Near East and the USA. This originally Mediterranean tick species was probably
introduced to central Europe by humans together with the domestic pigeon. A.
reflexus is a widely present tick at breeding sites of feral pigeons and is harbored
by most feral pigeon populations. The tick is brownish, and unfed 4–15 mm long,
6–8 mm wide and 1–2 mm thick (fig. 9). It’s typical habitat comprises pigeon
nesting sites where the ticks seek shelter in crevices of walls or in slits in wood
in the vicinity.
Discussion
We describe a case where a female patient was concurrently attacked by 3
different ectoparasites deriving from feral pigeons. Pigeon ticks and red mites
were determined by us, bedbugs by the patient. The symptoms of stings
described by the patient are consistent with stings of bedbugs. She recognized
the bedbugs by an internet search and from specimens of our collection, so her
identification can be considered to be confirmed. The patient and her partner
suffered from hundreds of red mite stings simulating a generalized exanthema.
It is well known that these mites infest humans by hundreds. A report described
a hospital infection with red mites where a patient suffered from 500 stings. The
general symptoms described are difficult to interpret. Most likely it is an
inflammatory response of the organism to foreign proteins. In this case the cause
of the dermatosis could only accidentally be diagnosed as a zoonosis due to feral
pigeons. The ectoparasites of feral pigeons attack their human hosts preferably
during the night and hide following their blood meal. Patients show nonspecific
clinical signs that are very difficult to assign due to the problems of detection of
the parasites and accurate identification of the species as well as relating the
symptom to be due to a parasitization. Most dermatologists are aware of
dermatoses associated with burrowing parasites as e.g. Sarcoptes scabiei, but if
the dermatitis is caused by zoonotic ectoparasites it is often misdiagnosed. In
the cases reported by Cafiero et al, diagnoses were consistently generic and even
when the eruption was attributed to acariasis, the possibility of zoonosis was not
suspected. The patients often received symptomatic therapy, e.g. cortisone and
tranquilizers, without a proper diagnosis.
Additionally, none of the consulted physicians advised patients to inspect their
homes for parasites. Physicians should be aware of the possibility of an
infestation with parasites deriving from feral pigeons. In cases with dermatosis
of unclear etiology of patients living in urban areas, a zoonosis caused by feral
pigeon ectoparasites should always be considered. Patients should be carefully
interrogated to ask for feral pigeons close to their habitation, especially when
they live in the uppermost apartment or directly under the roof. In the case of a
suspicion, parasites can be caught for determination by a glue barrier that can
be placed around the bed, e.g. with double-sided adhesive tape normally used to
affix carpets. If the parasites are identified, a careful search in the living space
of the patient, including house facade, balconies and ledges, ventilation
openings, air conditioner inlets etc., should be performed. Inside buildings
particular electrical devices and other warm areas are preferred by pigeon
parasites, as they are adapted to the pigeon’s body temperature of 42 ° C.
Ectoparasites are able to cover relatively large distances. Hence, adjoining
houses and backyards have also to be considered as areas where feral pigeons
could live as a source for ectoparasites. Even feral pigeons that only stay
temporarily in an area can be a source of a parasitic infestation. Williams
reported a case where feral pigeons congregated to drink from small pools on an
uneven flat roof where water accumulated following rain. Red mites emigrated
from the pigeons and invaded an apartment where 2 women were in fasted. If
the source is localized, the whole area has to be disinfested by a pest controller.
To prevent feral pigeons from further using a building, bird proofing by
appropriate deterrent systems or architectural measures has to be carried out.
A first measure often applied is the aspiration of the parasites with a vacuum
cleaner. As shown in figure 1 engorged ticks do not survive aspiration because
of bursting whereas starving ticks remain sound and could be able to leave the
vacuum cleaner and could lead to infestation. Survival of aspiration and leaving
the vacuum cleaner is known from bedbugs, whereas red mites are too delicate
to resist. Aspiration of parasites without immediate disinfestation or safe
disposal of the content of the cleaner bag bears the risk of reinfestation. In cases
where the source of an ectoparasite infestation is not detectable and
reinfestations occur, the patients have to leave their habitation as an ultimate
measure. This has to be recommended when recurrent anaphylactic reactions
due to pigeon tick infestations occur. Miadonna et al. escribed a case where a
patient changed his residence after having developed an anaphylactic shock
consisting of dyspnea and hypotension due to pigeon tick bites. Till now more
than 370 infestations of humans due to feral pigeons have been reported. In 71%
of these cases, the sources of infestations were nests on the building shell or
inside buildings. In the present case, the pigeons used a balcony after having
been attracted by food provided by the former tenant. To support a population
of ectoparasites, a continuous supply of hosts must be guaranteed. Buildings
infested with feral pigeons for longer than 1 year or breeding sites populated with
more than 50 feral pigeons are at high risk of harboring pigeon ticks. Hence, it
is surprising that only few pigeons using a small balcony were the source of
infestations with 3 parasite species. To our knowledge only 1 case has been
reported where more than 1 parasite species were transmitted from feral pigeons
to humans. Vargo et al. described a hospital infection with 2 mite species, D.
gallinae and O. sylviarum, which originated from an abandoned pigeon nest.
Even a single abandoned feral pigeon nest can be the cause for the emigration
of ectoparasites and infestation of humans as demonstrated for red mites and
pigeon fleas. From domestic pigeons it is known that the birds leave their
breeding sites when parasite populations are very high. Such emigrating
individuals transport parasites to new places. Emigrating young birds occupying
new breeding sites additionally play an important role in the dissemination of
parasites. Feral pigeon colonies close to human habitations bear a latent risk of
parasitic infestations and are difficult to prevent. The real cause of the problem
is the high feral pigeon populations in our cities due to a large food basis provided
deliberately by pigeon feeding or accidentally by discarded food. Infestations of
humans with feral pigeon parasites are therefore only one side of the problem
linked with the overpopulation by these birds in our cities. Sustainable solutions
can only be reached by integrative measures as e.g. public edu cation and
feeding restrictions.
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