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 (AdrianaMWN@gmail.com).

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.

LITERATURE CITED

1. Abrey, A. 2000. The management of a multi-

species bird collection in a zoological park In: Tully, T.

N., M. P. C. Lawton, and G. M. Dorrestein (eds.).

Avian Medicine. Reed Educational and Professional

Publishing Ltd., Butterworth-Heinemann, Woburn,

Massachusetts. Pp. 364–385.

2. Chavez, E., and F. H. Kratzer. 1972. Prevention

of foot pad dermatitis in poults with methionine. Poult.

Sci. 51: 1545–1548.

3. Chavez, E., and F. H. Kratzer. 1974. Effect of diet

on foot pad dermatitis in poults. Poult. Sci. 53: 755–760.

4. Coles, B. H. 1985. Clinical examination. In:

Sutton, J. B., and S. T. Swift (eds.). 2007. Avian

Medicine and Surgery. Blackwell Science Inc., Malden,

Massachusetts. Pp. 40–55.

5. Cooper, J. E. 1978. Veterinary aspects of captive

birds of prey. Standford Press, Saul, Glouchestershire,

United Kingdom.

6. Daoust, P., D. Wadowska, F. Kibenge, R. P.

Campagnoli, K. S. Latimer, and B. W. Ritchie. 2000.

Proliferative pododermatitis associated with virus-like

particles in a northern gannet. J. Wildl. Dis. 36: 378–382.

7. del Hoyo, J. 1992. Family Phoenicopteridae. In:

del Hoyo, J., A. Elliot, and J. Sargatal (eds.).

Handbook of the Birds of the World, vol. 1. Lynx

Edisions, Barcelona, Spain. Pp. 508–526.

8. Ekstrand, C., and B. Algers. 1997. Rearing

conditions and foot-pad dermatitis in Swedish turkey

poults. Acta Vet. Scand. 38: 167–174.

9. Ekstrand, C., B. Algers, and J. Svedberg. 1997.

Rearing conditions and foot-pad dermatitis in Swedish

broiler chickens. Prev. Vet. Med. 31: 167–174.

10. Greene, J. A., R. M. McCracken, and R. T.

Evans. 1985. A contact dermatitis in broilers—

clinical and pathological findings. Avian Pathol. 14:

23–38.

11. Harcourt-Brown, N. H. 2000. Bumblefoot. In: J.

Samour (ed.). Avian Medicine. Mosby Elsevier, Edin-

burgh, United Kingdom. Pp. 126–130.

12. Harms, R. H., B. L. Damron, and C. F.

Simpson. 1977. Effect of wet litter and supplemental

biotin and/or whey on the production of foot pad

dermatitis in broilers. Poult. Sci. 56: 291–296.

13. Hawkey, C., H. J. Samour, G. M. Henderson,

and M. G. Hart. 1985. Haematological findings in

captive gentoo penguins (Pygoscelis papua). Avian

Pathol. 14: 251–256.

14. Hogan, L. S., and L. D. Craig. 1987. Successful

treatment of bumblefoot in canaries. Mod. Vet. Pract.

68: 30.

15. Humphreys, P. N. 1975. Pathological conditions.

In: Kear, J., and N. Duplaix-Hall (eds.). Flamingos. T.

and A. D. Poyser, Berkhamsted, Hertfordshire, United

Kingdom. Pp. 199–202.

16. Humphreys, P. N. 1996. Wing and leg problems.

In: Beynon, P. H., N. A. Forbes, and N. H. Harcourt-

Brown (eds.). Manual of Raptors, Pigeons and

Waterfowl. British Small Animal Veterinary Associa-

tion Ltd., Glouchestershire, United Kingdom. Pp. 311–

314.

17. Mayne, R. K., R. W. Else, and P. M. Hocking.

2007. High litter moisture alone is sufficient to cause

footpad dermatitis in growing turkeys. Br. Poult. Sci.

48: 538–545.

18. Nagaraj, M., J. B. Hess, and S. F. Bilgili. 2007.

Evaluation of feed-grade enzyme in broiler diets to

reduce pododermatitis. J. Appl. Poult. Res. 16:

52–61.

19. Naldo, J. L., and J. H. Samour. 2004. Causes of

morbidity and mortality in falcons in Saudi Arabia. J.

Avian Med. Surg. 18: 229–241.

20. Reidarson, T. H., J. McBain, and L. Burch.

1999. A novel approach to the treatment of bumblefoot

in penguins. J. Avian Med. Surg. 13: 124–127.

21. Remple, J. D. 1993. Raptor bumblefoot: a new

treatment technique. In: Redig, P., J. E. Cooper, J. D.

Remple, and B. Hunter (eds.). Raptor Biomedicine,

vol. 27. Chiron Publications Ltd. Keighley, West

Yorkshire, United Kingdom. Pp. 154–155.

22. Remple, J. D., and A. A. Al-ashbal. 1993.

Raptor bumblefoot. Another look at histopathology

and pathogenesis. In: Redig, P., J. E. Cooper, J. D.

48 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Remple, and B. Hunter (eds.). Raptor Biomedicine,

vol. 17. Chiron Publications Ltd., Keighley, West

Yorkshire, United Kingdom. Pp. 92–93.

23. Sladen, W. J. L., J. J. Gailey-Phipps, and B. J.

Divers. 1979. Medical problems and treatment of

penguins at the Baltimore Zoo. Int. Zoo Yearb. 19:

202–209.

24. Wang, G., C. Ekstrand, and J. Svedberg. 1998.

Wet litter and perches as risk factors for development of

foot pad dermatitis in floor-housed hens. Br. Poult. Sci.

39: 191–197.

25. Weitzenburger, D., A. Vits, H. Hamann, M.

Hewicker-Trautwein, and O. Distl. 2006. Macroscopic

and histological alterations of foot pads of laying hens

kept in small group housing systems and furnished

cages. Br. Poult. Sci. 47: 533–543.

Received for publication 17 July 2009

NIELSEN ET AL.—FLAMINGO FOOT LESIONS 49