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CLASSIFICATION AND PREVALENCE OF FOOT LESIONS IN
CAPTIVE FLAMINGOS (PHOENICOPTERIDAE)
Adriana M. W. Nielsen, D.V.M., Søren S. Nielsen, D.V.M., Ph.D., Catherine E. King, M.Sc., and
Mads F. Bertelsen, D.V.M., D.V.Sc., Dipl. A.C.Z.M.
Abstract: Foot lesions can compromise the health and welfare of captive birds. In this study, we estimated the
prevalence of foot lesions in captive flamingos (Phoenicopteridae). The study was based on photos of 1,495 pairs of
foot soles from 854 flamingos in 18 European and two Texan (USA) zoological collections. Methodology for
evaluating flamingo feet lesions was developed for this project because no suitable method had been reported in the
literature. Four types of foot lesions were identified: hyperkeratoses, fissures, nodular lesions, and papillomatous
growths. Seven areas on each foot received a severity score from 0 to 2 for each type of lesion (0 5 no lesion, 15
mild to moderate lesion, 2 5 severe lesion). The prevalence of birds with lesions (scores 1 or 2) were 100%, 87%,
17%, and 46% for hyperkeratosis, fissures, nodular lesions, and papillomatous growths, respectively. Birds with
severe lesions (score 2) constituted 67%, 46%, 4%, and 12% for hyperkeratosis, fissures, nodular lesions, and
papillomatous growths, respectively. Hyperkeratosis and nodular lesions were most prevalent on the base of the
foot and the proximal portion of the digits, likely reflecting those areas bearing the most weight. The second and
fourth digits were most affected with fissures and papillomatous lesions; these areas of the foot appear to be where
the most flexion occurs during ambulation. The study demonstrates that foot lesions are highly prevalent and
widely distributed in the study population, indicating that they are an extensive problem in captive flamingos.
Key words: Flamingos, foot lesions, foot pad dermatitis, Phoenicopterus, prevalence.
INTRODUCTION
Foot lesions in captive flamingos (Phoenicop-
teridae) constitute a long recognized problem,1,15
although they have not received much attention
in the literature. Severe foot lesions compromise
animal welfare and can be a port of entrance for
bacterial infections, potentially leading to joint
infections and septicemia.15
Pododermatitis is a major problem in indus-
trial poultry farming.8,9 A high prevalence of foot
lesions has also been reported in captive raptors,19
as well as in penguins in zoo collections.13,20,23
Foot lesions have been observed in a wide range
of other birds in captivity.1,4,11,14,16 Despite a high
purported occurrence, no reports on the preva-
lence or etiology of foot problems in flamingos
exist in the literature. The aim of this study was
to estimate the prevalence of foot lesions in
captive flamingos in Europe. Secondary objec-
tives were to classify the lesions into type and
severity and to determine the areas of the foot
most frequently affected by lesions.
MATERIALS AND METHODS
Study population
The study population was a convenience
sample from the target population (i.e., captive
flamingos in Europe). A request for personnel to
submit photographs of the soles of the feet of
flamingos in their zoo collections was posted on
the European Association of Zoos and Aquari-
ums (EAZA) Bird Taxon Advisory Group’s
email list server. Furthermore, two zoos located
in eastern Texas (USA) were included to present
data from zoos facing different climatic and
geographic factors.
Twenty zoos contributed to the study by
providing photos of the plantar surface of both
feet of every flamingo in their collection. Photos
were collected from 2003 through 2008 and were
either taken by local zoo staff or by the authors.
Flamingos were generally photographed when
handled for other purposes, such as vaccination,
blood sampling, or wing feather clipping. Only
photographs of good quality, in which the
plantar surface of the feet was visible and the
individual unequivocally identified (leg band or
transponder number) were included. Four fla-
mingo species were represented: Caribbean fla-
mingo (Phoenicopterus ruber, n 5 137), Chilean
flamingo (Phoenicopterus chilensis, n 5 319),
greater flamingo (Phoenicopterus roseus, n 5
367), and lesser flamingo (Phoeniconaias minor,
n 5 30). The number of birds in the different age
From the Center for Zoo and Wild Animal Health,
Copenhagen Zoo, Roskildevej 38, DK-2000 Frederiks-
berg, Denmark (A. Nielsen. Bertelsen), the Department of
Large Animal Sciences, University of Copenhagen,
Grønnegaardsvej 8, DK-1870 Frederiksberg, Denmark
(S. Nielsen), and the Animal Department, Fuengirola
Zoo, c/ Camilo Jose Cela, 6–8, 29640 Fuengirola
Malaga, Spain (King). Correspondence should be
directed to Dr. A. Nielsen ([email protected]).
Journal of Zoo and Wildlife Medicine 41(1): 44–49, 2010
Copyright 2010 by American Association of Zoo Veterinarians
44
groups were: ,1 year: 5; 1–3 years: 106; 4–9 years:
178; 10–19 years: 166; 20–29 years: 151;
$30 years: 77; and unknown age: 171. The photo
material consisted of 1,495 observations of 854
different birds. Some flocks had been photo-
graphed more than once, in different years,
different times of the year, or both.
Lesions and scores
Foot lesions were classified as belonging to one
of four pathoanatomical categories: hyperkera-
toses, fissures, nodular lesions (NLs), and papil-
lomatous growths (PGs; Fig. 1). More than one
type of lesion could occur simultaneously on the
same foot and within the same area. Each foot
was divided into seven areas: the base and the
weight-bearing areas of the second (D2), third
(D3), and fourth (D4) digits, both proximally and
distally. Each area was given a severity score
from 0 to 2 for each type of lesion. Score 0 was
given when no lesion was present. For hyperker-
atoses, score 1 was given when the epithelium was
flattened or slightly overgrown and score 2 was
given when marked overgrowth was present. For
fissures, score 1 represented fissures less than
2 mm deep, whereas fissures deeper than 2 mm
were classified as score 2. Closed NLs without
exposed necrotic tissue were given a score of 1,
and open NLs with exposed necrotic tissue
received a score 2. Papillomatous growths were
classified as score 1 for small, fingerlike prolifer-
ations and score 2 for clusters or lumps of
proliferations. Areas not visible in the photo
because of overlap of feet, fingers covering the
area, and so on were recorded as missing
observations. All photos were scored by the same
observer (AMWN). The protocol for scoring was
developed for this study because no existing
methods used for other birds were applicable for
scoring all four types of lesions seen in flamingos.
Statistical analyses
The prevalence of hyperkeratoses, fissures,
nodular lesions, and papillomatous growths was
assessed by randomly selecting one assessment
date per flamingo. The prevalence was then
calculated as the proportion of flamingos with
lesions (scores 1 or 2) and as the proportion of
flamingos with severe lesions (score 2 alone) for
the four types of lesions.
Subsequently, it was determined by logistic
regression (with the Genmod procedure in SAS v.
9.1, SAS Institute, Cary, NC 27526, USA) that
lesion scores between affected areas for left and
right feet for each type of lesion were not
different. Therefore, left and right feet were
pooled for further analyses. Then, the propor-
tions affected by each of the four lesion types
were calculated for each area on the foot.
RESULTS
The overall prevalence of the four lesion types
were 100% for hyperkeratoses, 87% for fissures,
17% for NLs, and 46% for PGs. The prevalence
of flamingos affected with hyperkeratoses, fis-
sures, NLs, and PGs per participating zoo is
shown in Table 1. The distribution of lesions on
different areas of the feet is shown in Table 2 for
each lesion type.
DISCUSSION
The prevalence calculations provided here
demonstrate that foot lesions frequently occur
in captive flamingos in European zoo collections.
This report is, to our knowledge, the first major
Figure 1. Classification of foot lesions in captive flamingos: a. hyperkeratosis; b. fissures; c. nodular lesions;
and d. papillomatous growths.
NIELSEN ET AL.—FLAMINGO FOOT LESIONS 45
epidemiological collection of such prevalence
data. This study was based on photos of flamingo
feet, some of which were taken and submitted by
local zoo staff. Disadvantages of using photos
include the inability for the observer to palpate
lesions and differences in quality of photos.
However these drawbacks were outweighed by
the ability to obtain a large sample size, and to
allow uniform objective scoring by the same
observer at the same time.
Severity scoring is a common way to system-
atically evaluate foot lesions in birds, and a
number of different grading systems have been
developed in the poultry industry,3,9,12,17,18,24 as
well as in raptor medicine,5,21 to evaluate severity
of foot lesions. Because no pre-existing system
Table 1. Prevalence (%) of flamingos affected by hyperkeratoses, fissures, nodular lesions, or papillomatousgrowths among 854 flamingos in 20 zoological collections.
Location n
Prevalence (%)
Hyperkeratoses Fissures Nodular lesions Papillomatous growth
Score1+2 Score 2
Score1+2 Score 2
Score1+2 Score 2
Score1+2
Score2
European zoos
Amersfoort Zoo 63 98 25 87 21 2 0 13 0
Antwerp Zoo 15 100 100 100 87 47 27 93 67
Augsburg Zoo 20 100 100 100 100 15 5 5 0
Avifauna 16 100 75 100 44 6 0 25 0
Burgers Zoo 73 100 95 96 79 44 10 93 32
Copenhagen Zoo 45 100 51 87 60 0 0 67 27
Dublin Zoo 76 100 36 75 20 4 0 7 0
Durrell 50 100 34 66 8 4 0 8 0
Edinburgh Zoo 19 100 79 100 68 11 0 21 0
Givskud Zoo 19 100 53 84 32 37 26 37 5
Helsinki Zoo 17 94 18 76 29 0 0 18 0
Jerez Zoo 47 100 51 89 32 15 0 32 2
Kolmarden Zoo 30 97 70 87 70 0 0 47 3
Odense Zoo 58 100 88 97 69 2 0 93 34
Parken Zoo 42 100 62 95 24 5 0 90 5
Riga Zoo 43 100 91 79 40 44 2 19 5
Rotterdam Zoo 127 100 90 84 50 35 9 48 14
Twycross Zoo 34 100 82 94 62 15 3 71 6
Total 794 100 67 87 46 17 4 46 12
Texan zoos
Ellen Trout Zoo 17 100 47 35 0 47 35 6 0
Houston Zoo 43 100 67 72 0 42 26 7 0
Table 2. Percentage of area affected by hyperkeratoses, fissures, nodular lesions, and papillomatous growthsamong 854 flamingos.
Position on foota
Area affected (%)
Hyperkeratoses Fissures Nodular lesions Papillomatous growths
Score 1+2 Score 2 Score 1+2 Score 2 Score 1+2 Score 2 Score 1+2 Score 2
Base 38 6.0 9.1 1.8 3.8 0.9 11 2.0
Proximal D2 95 45 39 14 6.3 0.9 30 4.6
Proximal D3 81 13 22 7.1 1.6 0.9 11 1.3
Proximal D4 87 29 32 12 6.0 1.0 25 5.5
Distal D2 17 1.1 17 2.0 0.3 0.0 9.3 0.3
Distal D3 51 6.0 40 12 0.5 0.4 22 2.0
Distal D4 44 6.3 50 14 0.4 0.1 12 0.7
a D2, second digit; D3, third digit; D4, fourth digit.
46 JOURNAL OF ZOO AND WILDLIFE MEDICINE
existed that was useful for flamingos, a system
was developed. The four categories of lesions
used in this study were chosen based on clinical
experience and after a cursory review of the first
500 photos collected. Retrospectively, all lesions
seen in this study fit into one of the four
categories, supporting this classification method-
ology. The scale, with scores from 0 to 2, was
chosen as a compromise between the attempt to
obtain a fairly differentiated diagnosis and to
minimize the number of borderline scores.
Scoring can result in misclassification bias
because of the observer’s subjective assessment.
To minimize errors, each of the seven weight-
bearing areas on each foot was given a separate
score for each type of lesion, and all photos were
scored by the same observer.
Foot lesions affected nearly all the flamingos,
in that hyperkeratosis was observed in 100% of
the flamingos in this survey and also affected
more than half of the weight-bearing areas on the
foot soles. Hyperkeratosis is not believed to cause
pain or facilitate infections, and in our experi-
ence, it is likely clinically insignificant. However,
hyperkeratosis could potentially develop into
other types of lesions, as similar lesions pro-
gressed to severe fissures in an experimental study
on turkeys.2
The high prevalence (87%) of birds with
fissures was unexpected, particularly as 46% of
the birds had deep fissures (score 2), which are
presumably painful and constitute a possible port
of entry for infections.
Although fissures apparently similar to those
of flamingo feet observed in chickens and turkeys
have been described as pododermatitis or foot
pad dermatitis,2,10 these terms are generally used
to refer to abrasions, necroses, ulcers, or ‘‘bum-
bles’’ on the soles of poultry feet,17,18,24,25 rather
than fissures.
In poultry, wet or alkaline litter is considered
to be among the main risk factors in development
of these lesions.2,10 This seems counterintuitive in
flamingos because these wetland birds normally
inhabit very alkaline water and mud flats.7,24
However, the prevalence of fissures in wild-
ranging flamingos is unknown, and the effect of
wet and alkaline litter on flamingo feet has not
been studied.
NLs were less prevalent (19%), and only 6% of
the birds had severe nodular lesions. The tendency
was strong for the affected birds to be clustered in
a few collections with a high prevalence of this
lesion form, suggesting the presence of a local risk
factor. Despite the inconsistent definition of
‘‘bumblefoot’’ in birds, nodular lesions in flamin-
gos appear analogous to most lesions described as
‘‘bumblefoot’’ in the literature20,22 and likely
constitute the most chronic and clinically severe
lesion in the study. Interestingly the NLs found in
the Texan zoos were markedly larger (up to 3 cm
in diameter) than in the European zoos.
PGs affected nearly half (43%) of the birds, but
severe lesions were relatively scarce (11% of birds,
2% of areas). These lesions were often associated
with fissures (data not shown), and large
proliferations (score 2) might promote an unnat-
ural weight distribution on the foot. Lesions
described in poultry as ‘‘cauliflower-type prolif-
erations’’10 are very likely comparable to PGs in
flamingos. The etiology has not been established
for these lesions, but in raptors, a similar type of
lesion was described as ‘‘benign papillomata of
possible viral etiology,’’18 and viruslike particles
have been isolated from proliferative pododer-
matitis in a wild northern gannet (Morus
bassanus).6 However, preliminary investigations
into a viral etiology with the use of multiply
primed rolling-circle amplification for papilloma-
viral DNA on a subset of affected flamingos were
negative (Hans Stevens, Rega Institute for
Medical Research, Laboratory of Clinical Virol-
ogy, Leuven, Belgium, unpubl. data).
The analysis of anatomical distribution of
lesions (Table 2) showed several interesting trends.
Hyperkeratosis was most prevalent on the
proximal portion of the digits, likely reflecting
those areas bearing the most weight. The distal
portion of D2 was least affected and probably
carries the least weight. Although the prevalence
was much lower, NLs roughly showed the same
distribution, suggesting that there might be one or
more coinciding risk factors. For fissures, D2 and
D4 were most affected, whereas the base and D3
(central digit) were spared. This pattern of
distribution likely reflects the areas of the foot
where the most flexion occurs during ambulation.
A somewhat similar pattern was seen with PGs,
perhaps suggesting a link between these two types
of lesions. If PGs have a viral etiology, fissures
could be speculated to be a port of entry; however,
there is little evidence to support this at this time.
It is noteworthy that certain collections might
be severely affected by one type of nonhyperker-
atosis lesion (fissures, NLs, or PGs) and almost
free from another. This suggests different etiolo-
gies for the different lesions and that, presum-
ably, important management factors, such as
water quality, substrate, temperature, and so on,
might have different levels of risk for these
NIELSEN ET AL.—FLAMINGO FOOT LESIONS 47
different lesion types. The two Texan zoos
diverged from the European pattern in having a
remarkably high prevalence of NLs and an
almost complete lack of PGs and severe fissures,
again suggesting the influence of environmental,
management, or both factors.
This study clearly illustrates that foot lesions
are highly prevalent in captive flamingos. Some
of these lesions are likely to pose a significant
threat to animal welfare for these birds. The
implications of this are great because flamingos
are so commonly kept in zoos and in private
collections throughout the world. Almost 7,000
flamingos reside just in EAZA-affiliated zoos,
and approximately 70% of EAZA-affiliated zoos
hold flamingos. More research into the etiology
of these lesions, including the significance of
various management factors, is obviously war-
ranted and is highly encouraged.
Acknowledgments: The authors thankfully ac-
knowledge the staff of Antwerp Zoo, Augsburg
Zoo, Biopark Valencia, Burgers Zoo, Colchester
Zoo, Copenhagen Zoo, Cotswold Zoo, Dieren-
park Amersfoort, Dublin Zoo, Durrell Wildlife
and Conservation Trust, Ellen Trout Zoo,
Givskud Zoo, Helsinki Zoo, Houston Zoo, Jerez
Zoo, Kolmarden Zoo, Odense Zoo, Parken Zoo,
Riga Zoo, Royal Zoological Society of Scotland,
Rotterdam Zoo, Safari Beekse Bergen, Safari de
Peaugres, Twycross Zoo, Valencia Zoo, Vogel-
park Avifauna, and Zoo de la Palmyre and thank
Hans Stevens for viral analyses.
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Received for publication 17 July 2009
NIELSEN ET AL.—FLAMINGO FOOT LESIONS 49