Abstract

Pododermatitis is considered a prevalent disease of captivity and is generally not found in wild birds. While most commonly described in captive raptors, pododermatitis can occur in any species of captive bird. This masterclass will cover the following topics, which will be illustrated using case studies from Jurong Bird Park, one of the largest bird parks in the world, with a collection of nearly 3500 birds across 400 species.

Classification of pododermatitis lesions include ulcerative, granulomatous, hyperkeratotic, fissural, nodular, papillomatous and differing degrees of severity.

Environmental and husbandry-related causes can include housing, climate, perches and substrate, diet and nutrition, activity. Development of pododermatitis can also be secondary to primary traumatic or medical conditions, or as a result of medical or surgical interventions, which must be considered when there is any defect of the appendicular skeleton.

There are differences in the presentation of acute versus chronic pododermatitis, and potential complications and consequences of both forms. Acute presentations are often associated with infectious repercussions, and chronic presentations are associated with inflammatory sequelae, such as amyloidosis. Differences in the management of acute versus chronic pododermatitis also include radical versus conservative treatment.

Treatment options include conventional surgical and medical interventions, as well as complementary procedures such as nerve blocks, intralesional and regional antibiotic therapy, and photodynamic therapy and there are advantages and disadvantages of each of these approaches.

Biomechanical treatment options include substrates and perching options, and pressure-relieving bandaging. Bandaging includes conventional bandage styles, donut-style disposable shoes, foam plantar shoes, padded reusable textile shoes, and molded silicone casting. A novel 3D printed option for silicone shoes will also be described.

Introduction

Pododermatitis, also referred to as foot pad dermatitis, or by the lay term bumblefoot, is a significant disease syndrome of the avian foot and one of the major diseases affecting the locomotory system. It is generally a chronic inflammatory or degenerative condition initiated by underlying abnormalities of pressure or trauma on the plantar surface of the foot, usually the metatarsal or digital pads. This results in plantar lesions associated with the development and progression of pressure sores; tissue swelling, calluses, abrasions, ulcerations, and fissures.

Hyperkeratosis, abrasion and avascular necrosis arising from initiating factors, if unnoticed or treated inappropriately, may progress to vascular damage, callus formation, inflammation, cellulitis, ulceration, and bacterial colonization of the skin and subcutaneous tissues of the plantar surfaces of the feet.

If left untreated, the disease becomes progressive, invasive, and eventually disabling, and chronic cases may develop deep bacterial infections, abscesses, osteomyelitis, synovitis, bacteremia and fatal septicemia. In non-fatal cases, lameness and loss of limb function may be caused by local infection or by osteotic changes attributed to persistent abnormalities in forces affecting the foot.

Pododermatitis can have significant welfare and implications for affected individuals and populations. While cases may range from mild, barely visible skin changes, to severely debilitated birds, most clinical signs of pododermatitis are considered painful or at least causing discomfort. Early stage hyperkeratotic lesions may result in mild lameness but may develop into more severe lesions which are associated with visible signs of pain and concurrent behavioural changes. Birds suffering from pododermatitis may be reluctant to stand, perch on certain surfaces, walk as much as usual, or may display other behaviours associated with pain, such as weight shifting, hock-sitting, recumbency, or displacement behaviours such as over preening or self trauma. Normal daily maintenance activities may also be adversely affected, with caregivers reporting reductions in self-preening, social engagement, and food and water consumption.

In commercial poultry production systems, the presence of pododermatitis lesions is used as an indicator of flock welfare throughout the industry and is important commercial consideration. Affected birds show reduced weight gain, and lesions can act as a portal of pathogen entry, with implications for food safety and carcass contamination. Pododermatitis also has negative economic impacts on other avian industries, including falconry, zoological collections and educational presentation programs.

As the etiology of pododermatitis generally involves abnormal bird-environment interactions, pododermatitis is usually considered a disease of captivity and is rarely found in wild birds, unless as a sequela to injury. There are very few reports of pododermatitis in free ranging wild birds, in contrast to their captive conspecifics.

Pododermatitis is also often reported in wild birds in temporary captivity undergoing rehabilitation. Along with fungal respiratory disease, it is one of the most frequent and important clinical complications in rehabilitation centers, particularly in seabirds. It is less frequently described in pet birds, but may be seen particularly in captive-reared, older, overweight pets, or those kept in suboptimal conditions. As in other groups, it is also reported as a consequence of other disorders affecting the pressure placed on the feet. Many early reports of pododermatitis come from captive birds of prey, and the disease remains commonly reported in falconry birds, those undergoing rehabilitation and in zoological collections. It is almost universally described in avian production systems (with a prevalence of between 20–98%), regardless of the species farmed, but more particularly in broiler breeds of chickens and ducks, and turkeys—where the condition has a direct effect on carcass quality—rather than in layer breeds.

Pododermatitis can become a significant issue in a large variety of avian taxa in large zoological collections, where shared environments can result in whole flocks being affected. There are several examples in the literature describing pododermatitis issues in populations of penguins, flamingos and other waterbirds.

At Jurong Bird Park, one of the largest bird parks in the world, with a collection of nearly 3500 birds across 400 species, pododermatitis cases have been reported in species representing most orders of birds. Examples and case studies from the Jurong Bird Park Veterinary Department will be used to illustrate the main concepts in this masterclass.

Classification of Pododermatitis Lesions

The classification of pododermatitis lesions is necessary to evaluate the type and severity of the condition and is used for many different reasons.

In production systems, lesion classification is used as part of carcass scoring and evaluation, and also to evaluate welfare. In wildlife rehabilitation, classification is used to evaluate both the rehabilitation process, techniques and protocols, and also as a prognostic indicator or successful rehabilitation and release. In collection and pet birds, lesion classification is used not only to evaluate enclosure suitability and substrate, but also to determine appropriate treatment and management techniques.

Multiple classification systems have been described and are in common use, but generally fall into two types; those that describe the severity of the lesion and those which describe the type of lesion. Some classification systems encompass both severity and lesion characteristic. However, both types of classification systems describe macroscopic pododermatitis lesions, and therefore a limitation of visual classification systems is that the condition is only detected once the lesions have formed and disease is well established, and generally does not distinguish between active and inactive (healed or fibrosed) lesions, nor do the classification systems take into account subclinical disease.

Identification of subclinical plantar disease would be beneficial, to allow early initiation of husbandry changes and treatment to prevent the development of clinical lesions. This has been attempted with thermal imaging and infrared thermography in flamingos and penguins but has not been shown to be a reliable diagnostic tool.

Classification systems describing the severity of lesions are generally based on the classic pododermatitis lesion. This is a nodular lesion with central ulceration, also known as the ulcerative form of pododermatitis. The first system, reported in the commercial poultry industry in 1984, is the most simplistic and assigns a score from 0 to 3, according to the following descriptions:

Pododermatitis lesions in poultry generally begin as plantar skin discolouration, developing to small scaly brown scabs on the metatarsal and digital pads (Score 1). These lesions develop and enlarge (Score 2) through mechanical erosion and inflammation, leading to hyperplasia and epidermal necrosis (Score 3). Necrotic debris is often associated with foreign material from the environment or substrate, and bacteria.

In captive collection or pet birds, classification systems are generally highly descriptive of the plantar lesions, as they are more often used for clinical assessment, prescription and evaluation of treatment. The systems used are based on those originally described for the description of pododermatitis in captive raptors, and also range in the number of categories of severity described.

A review article in JAMS by HF Burke et al. in 2002 compares four similar classification systems for pododermatitis in raptors, ranging in complexity from 3 to 7 stages of lesion severity. These systems are reproduced here:

While each study, report, clinic or institution may use a different classification system depending on the species examined, type of practice and need, this is unlikely to be problematic as long as the use of the selected classification system is consistent, and well defined. As in the commercial poultry industry, it is recommended that the classification system is well publicized or displayed within the clinic or institution, preferably with pictorial examples.

Classification systems describing the type of lesion are generally applied to flamingos, a species which appear to develop a variety of lesions. This classification system recognizes four pathoanatomical categories: the classic nodular lesion, hyperkeratosis, fissural, and papillomatous lesions. Lesions may also be identified as a combination of two or types, and multiple types may be present in the same individual, particularly in very chronic case. Within this classification system, severity can also be indicated in fairly truncated form; generally, only mild (Score 1) or advanced (Score 2) stages are indicated. As in previously described classification systems, Score 0 indicates the absence of macroscopic lesions.

While this classification system is generally only reported in the assessment of pododermatitis in flamingos, it can also be applied to other species in which non-classic or mixed-type lesions may be seen. To increase accuracy in lesion description, the plantar surface of each foot can also be divided into numbered weightbearing regions. In flamingos, there are seven such regions; the central metatarsal pad and two digital pads on each digit, one proximal and one distal. The number and pattern of these weightbearing regions varies based on the pedal anatomy of each species.

Figure 1

Classification of foot lesions in captive flamingos: a) hyperkeratosis, b) fissures, c) nodular lesions, and d) papillomatous growths. From: Nielsen AMW, Nielsen SS, King CE and Bertelsen MF (2010). Classification and prevalence of foot lesions in captive flamingos (Phoenicopteridae). J Zoo Wildlife Med. 41(1):44–49.

Causes of Pododermatitis

Environmental and Husbandry-Related Causes

As primarily a disease of captivity, the most common etiology of pododermatitis is directly due to the environment in which the bird is kept. Pododermatitis lesions are pressure sores caused by abnormalities of pressure or trauma on the plantar surface of the foot, and so the lesions are generally initiated in the regions in direct contact with the perches or substrate—the metatarsal or digital pads.

Like many aspects of avian anatomy, the pelvic limb has evolved to maximize efficiency in a particular environmental and behavioural niche. Basic examples of this include the placement of the pelvic limb on the body, which is dependent on whether the bird spends more time perching or standing and weight-bearing as opposed to swimming or flying (diving ducks have legs placed more caudally than dabbling ducks); the enormous variation in pedal morphology (aniso-, zygo-, hetero-, syn- and pamprodactyly, as well as variations in palmation and lobation); and the species variation in the number of digital actuator muscles (extensors and flexors), ranging from 11 to 18. Because of this variation and adaptation for particular niches, it is inevitable that there will be limitations in the extent to which the captive environment can permit normal free-ranging behavior. Even in the highest ideals of enclosure design, the very act of limiting the activity of the bird to a restricted space will lead to deviations in the normal forces acting on the feet. Whether or not these deviations are sufficient over time to cause clinical pododermatitis depends on the extent and chronicity of the imposed pressure abnormalities, as well as other confounding environmental factors.

The most obvious causes of pododermatitis lesions are the surfaces on which the bird stands or perches (weight-bearing substrates), and there are three main characteristics of substrates which may predispose to abnormal plantar pressures. The first is hardness. Hard, solid surfaces such as concrete, rock and tiles do not compress with the weight of the bird and therefore result in the highest pressure returned to the plantar surface. Natural surfaces such as wood produce lower pressures, and substrates such as earth and turf compress easily and therefore reduce the pressure on the foot, as do artificial compressible substrates such as foam and rubber matting. The second characteristic of substrates which can predispose to pododermatitis lesions is texture. A bird weight-bearing on a smooth solid substrate will experience pressure at the same points on the plantar surface regardless of where they stand; in pet birds this is most often seen where commercial dowel perches are used. A textured surface like a gnarly natural branch will change the pressure points on the plantar surface with each step, thus distributing the pressure on the foot over time. The third aspect of a substrate that impacts plantar pressure is the movement of the substrate itself. Movement of generally encourages the bird to change its stance and shift its weightbearing, thus actively changing the pressure points on the foot. Example of moveable substrates are dry sand and gravel, rope perches and dynamic branch perches. In summary, the harder, smoother and more rigid the substrate, the more likely it is to contribute to the formation of pressure sores and pododermatitis lesions.

However, there are a multitude of factors which also influence the likelihood of pressure sores and progression of pododermatitis. Being overweight or obese has been shown to increase the incidence or severity of pododermatitis lesions, likely simply by increasing the pressure borne by the feet in normal weightbearing. Excess bodyweight or over conditioning may also be associated with other risk factors typically found in captive birds. The sedentary lifestyle of captive birds when compared to their wild counterparts may firstly predispose the captive bird to overconditioning or obesity through reduced energy expenditure or increased caloric intake (or often a combination of both). In addition, the sedentary captive lifestyle results in increased time perching or standing, particularly in the same position or location, thus increasing the likelihood of plantar pressure sore formation. Reduced energy expenditure, increased caloric intake and limited perching positions may also result from housing in enclosures of insufficient size to allow appropriate activity. Enclosures may not only have perching substrates of inappropriate material and texture, but insufficient perching space or options. Food may be readily available without effort made on the bird’s part. Think of the stereotypical Victorian-era parrot in a cage; the food bowl is directly in front of a sedentary bird who has a single perch and no room to open its wings, let alone take more than two steps in either direction. While this is the extreme situation, there are elements of similar issues in many modern aviaries and enclosures.

As well as food availability, diet composition may also increase the risk of pododermatitis lesion development. While overall increased caloric and macronutrient intake lead to increased weight, deficiencies in other nutrients may reduce skin integrity, thus predisposing to lesion formation. In commercial poultry flocks, higher prevalence of pododermatitis has been reported in turkeys fed a diet deficient in methionine, and also in those with diets deficient in biotin. Zinc deficiency has also been hypothesized as having a role in the development of pododermatitis in flamingos, and it is possible that deficiencies in other vitamins and amino acids involved in skin formation and maintenance (such as vitamins A and E, pantothenic acid, lysine and riboflavin) may also play a role.

Another less obvious effect of diet on predisposition to pododermatitis is water and indigestible fat content, and the contribution to faecal composition. This is generally only applicable to individuals and species housed in enclosures where the substrate quality is directly affected by the composition of the droppings. The most common example is commercial poultry housed in deep litter systems, but might also apply to backyard or pet poultry, or handraised birds kept on organic litter. In commercial poultry operations, litter wetness is increased where birds are fed diets with higher indigestible fats. The fats passed in the faeces also causes both the faeces and litter to stick to the feet, increasing skin damage and increasing ammonia levels. The design and placement of water bowls and drinkers also directly impacts litter wetness through spillage. Wet litter not only leads to maceration and degradation of the plantar skin but increases the risk of infection of foot lesions. Pododermatitis may be a sequela of moist plantar dermatitis (contact dermatitis) and in large commercial poultry flocks, often most strongly associated with drinker type, litter depth and litter material.

There have also been some suggestions that climate may be a predisposing factor in the development of pododermatitis in certain captive species, though this is so far inconsistent. Humidity may increase in the incidence of moist plantar dermatitis in some species, though in a study of captive flamingos (a wetland species), temperature and humidity, as well as indoor versus outdoor housing, were found to correlate with the development of certain types of pododermatitis lesions. Conversely, an environment that is too dry may also predispose to the development of pododermatitis by causing desiccation of the plantar skin.

Secondary Pododermatitis

In addition to environmental and husbandry-related causes, pododermatitis may also develop secondary to any primary traumatic (including thermal and electrical burns, and frostbite) or medical conditions, or as a result of medical or surgical interventions in which plantar pressure is altered.

In the rare cases of pododermatitis reported in wild free-ranging birds, most appear to be unilateral cases which have developed due to injury of the contralateral pelvic limb, causing increased use and therefore pressure on the affected foot. A similar etiology occurs in captive birds, and pododermatitis lesion development has been reported in numerous cases after orthopaedic injury or surgery, as a consequence of asymmetric weight-bearing during recovery. Amputation of any part of the pelvic limb results in risk of pododermatitis occurrence on the contralateral foot.

Alterations in weight-bearing and distribution, and resultant pododermatitis, may also be caused by anatomical aberrations beyond the pelvic limb, in either the axial or appendicular skeleton or musculature. Lateral scoliosis of the spine may also lead to unilateral plantar pressure sores, as may any other asymmetry of the trunk that affects pelvic placement. Asymmetry of the wings or wing function may also cause mild alterations in weight-bearing, and lead to the development of pododermatitis over time. In the author’s observation, pinioning does not appear to increase the incidence of pododermatitis, though more severe asymmetries pectoral limb function do, such as amputation at the humerus, or ankylosis of the elbow, preventing limb extension. Both these abnormalities prevent the wing from being used for balance, and it is suspected that it is this that causes the asymmetry in weight bearing.

Pododermatitis may also be initiated or complicated by infection or inflammation to the foot. Moist dermatitis is mentioned previously, where infection is seeded via devitalized macerated plantar skin, though infection of the plantar skin and underlying structures may also occur through devitalization from bruising and pressure necrosis, or direct inoculation through skin puncture. The most common causes, particular in raptors and poultry, include progression of avipoxvirus lesions, and self-inflicted penetrating injuries from overgrown talons.

Though pododermatitis is not an infectious disease, a variety of viral, bacterial and fungal pathogens have been isolated from pododermatitis lesions in a range of species. Virus-like particles suggestive of Papovaviridae have been noted in a northern gannet with proliferative pododermatitis, and in multiple waterfowl species with verrucous hyperkeratotic lesions; herpesvirus-related proliferative lesions have been reported in macaws and cockatoos; herpesvirus has also been associated with ulcerative foot lesions in a duck. Mycotic (Candida spp.) pododermatitis is reported in turkey poults. Aerobic bacterial agents are commonly isolated from pododermatitis lesions and may play more of a causative role in younger birds. The most common bacterial isolate is the ubiquitous Staphylococcus aureus, often identified with Escherichia coli, Corynebacterium species, Enterococcus faecalis, Pseudomonas and Proteus species. Less commonly reported are Aerococcus viridans, Group D Enterococcus; Bacillus, Moraxella, Pasteurella, Klebsiella, Clostridium, Diplococcus, Nocardia, Actinobacillus, Actinomyces, Aeromonas and other Staphylococcus and Streptococcus species.

Bacterial invasion of the stratum corneum and exocytosis of heterophils into the epidermis are noted to be an early histologic signs of pododermatitis. In later, clinically visible stages, pressure necrosis and reduced vascular perfusion reduce the efficacy of local immune response, as well as antibiotic delivery to the affected area. A generalized failure to degrade phagocytosed pathogens then leads to chronic granulomatous disease.

Acute versus Chronic Pododermatitis

Presentation

Pododermatitis is considered a chronic disease, though cases may present with acute complications, and therefore require alterations in treatment and management strategies. In most instances, the authors consider any case presenting with recent trauma, active bleeding or active infection as an acute case, requiring immediate medical and potentially surgical management. Chronic cases, where infection is minimal and localized, and the lesions are granulomatous rather than purulent, can be managed through relief of pressure and through environmental changes.

Different presentations will also differ in disease considerations. For example, in acute cases, the immediate concerns are usually related to infection; local spread to pedal structures, osteomyelitis, systemic spread and bacteremia/septicemia. In chronic cases, concerns may be more centered around the consequences of ongoing and persistent inflammation, particularly amyloidosis, or other effects of chronic disease, such as immunosuppression and anemia.

However, as pododermatitis cases may present at any time on the disease timeline, they do not necessarily fall into easy categorizations of ‘acute’ or ‘chronic’ but are likely a combination of both. In individual cases, the bird should undergo thorough clinical examination and assessment to ascertain the general health and condition of the bird, as well as to identify the extent of any infection or inflammation. Earlier-stage or more acute cases may show inflammatory leukograms with elevations in CK; chronic cases may show mild anaemia and monocytosis. Pedal radiographs are always advised to ascertain bony involvement. Lesions should then be characterized and classified using whatever classification system is used within the particular clinic or institution. Culture of any open lesions is generally unrewarding; culture of deep samples, such as synovial fluid aspirates, may be more useful, though penetration of the plantar region by systemic antibiotics is limited, and are most effective in cases of osteomyelitis, or systemic infection. Ultrasonography or advanced imaging may be used to assess tendon integrity if required. It should be noted that though Clostridium tetani toxicosis is rarely reported in birds, it was been reported in gyrfalcon associated with chronic pododermatitis lesions.

Management

Apart from direct medical and surgical treatments, it is imperative that a thorough examination and evaluation be performed of the bird’s captive environment, to establish the (potentially numerous!) contributing factors. It is important to remember that while the clinical disease may be able to be resolved in the individual, unless the causative environmental factors are addressed, the condition will recur.

Treatment Options

As pododermatitis is a complex disease with a multifarious etiologies and contributing factors, the treatment of pododermatitis may require multiple approaches over a long period of time. No one treatment modality is likely to resolve the issue on its own. However, the main concept of pododermatitis treatment revolves around the relief of plantar pressure and allowing gradual healing of open wounds and lesions. Generally speaking, the more chronic the lesion, the longer the treatment time; in very chronic and severe cases, this may be up to a year. While historical literature on pododermatitis treatment tends to emphasis surgical exploration, debridement and primary closure, recent trends in treatment espouse healing by secondary intention, as tissue tension and recurrence rates are lower.

In addition to medical and surgical interventions, underlying causes must be addressed and rectified to avoid recurrence.

Medical Interventions

Medical intervention is almost always required in cases with acute complications: active infection or inflammation, tendon and bony involvement, purulent or caseous discharge or abscessation. Not all abscesses are associated with infection; one study of pododermatitis abscesses in penguins showed that around 10% were sterile.

Pododermatitis is always assumed to be a condition that causes pain, or at least discomfort. Depending on the species and the individual health of the bird, appropriate analgesics may range from non-steroidal anti-inflammatories to opioids, depending on the extent of the lesions, the involvement of pedal architecture and the behavior and response of the bird. Pain management is particularly important in unilateral pododermatitis, where pain in the affected limb may cause overreliance on the contralateral limb for weightbearing, thus leading to the development of pododermatitis lesions on the previously unaffected foot.

If surgical debridement or intervention is required, local and regional nerve blocks should be considered during the intra- and perioperative period, as nociceptors in tendons and joints (deep pain receptors) are often stimulated.

Antibiosis of some modality is often indicated, and may be a combination of topical (intralesional), systemic or regional through intravenous regional limb perfusion (IVRLP) or intraosseous regional limb perfusion (IORLP), depending on the type and severity of lesion, other treatment used, and patient (or owner) compliance or cooperation. Topical or intralesional antibiotics or antimicrobials are most often used after debridement and may also be used in conjunction with bandaging treatments following such a procedure. Antibiotic gels, creams and ointments are all described in the treatment of open lesions, and those with enzymatic debridement properties may also be useful, depending on the extent of tissue damage or penetration. Hydrocolloid gels are also useful in cases where there is significant tissue exposure and desiccation of underlying structures is on concern. Silver sulfadiazine cream is effective against a wide range of organisms and also promotes re-epithelialization, and so is more appropriate for more superficial lesions. Manuka honey has also been used with success, in conjunction with appropriate bandaging.

There are some reports of the use of intralesional antibiotic-impregnated polymethyl methacrylate (PMMA) beads after debridement, and antibiotic-impregnated poloxamer gels may also be used. Both these methods achieve ongoing high concentrations of antibiotic in a region where vasculature perfusion may be compromised.

Antibiotic therapy is best guided by culture of deep lesion swabs, and sensitivity testing. Pododermatitis lesions are often highly contaminated wounds and testing most often reveals environmental pathogens or organisms associated with faecal contamination. Systemic antibiotic therapy should be considered to prevent spread of local infection and ascending or systemic infection which may lead to sepsis. Broad spectrum antibiotics may be used initially, then changed according to results of culture and sensitivity testing as appropriate. Systemic antibiotic therapy may be continued for several weeks, depending on the extent of wound contamination. Topical treatments are often continued longer.

Antimicrobial photodynamic therapy (PDT) has been suggested as an alternative therapy to conventional antimicrobial treatments for pododermatitis. PDT is applied directly to the infected area, selectively destroying a large number of microorganisms without causing tissue destruction and may be useful in birds where the risk of wound contamination is high, such as penguins. It also has significant potential in infections with resistant microbes.

Low level laser therapy may be used as an adjunct treatment to assist in wound healing and pain relief. It is used in the treatment of human diabetic foot ulcers and is widely used in veterinary medicine in some places.

Surgical Interventions

Surgical treatment of pododermatitis is based around surgical debridement of the lesion and management of the open wound. Surgical closure is rarely recommended due to the scarcity of available skin for closure, significant tension and risk of dehiscence, and higher recurrence rates. Primary closure may not be possible due to the size of the lesion(s), and the use of purse string or tension-relieving sutures should only be used if absolutely necessary. Repeated attempts may result in exuberant granulation tissue or scar tissue formation at the lesion site. Use of skin flaps utilizing interdigital webbing is reported.

Healing by secondary intention, where there is no damage to the underlying bone and tendon structure of the foot, maintains the normal architecture of the foot and range of motion of the joints, and is generally preferred if possible. Cases in which there is osteomyelitis or damage to the bones, tendons or ligaments tend to have a poor prognostic outcome.

Debridement is performed under general anaesthesia. Local and regional nerve blocks are often useful at this stage. The foot should be cleaned of all debris and aseptically prepped as best as possible to avoid intraoperative contamination of deep tissues. All caseous purulent material should be removed, as well as all devitalized tissue and foreign debris. Flushing and irrigation are recommended to reduce antigen load. All wound edges should be freshened to encourage wound healing.

The wound healing process is a complex continuum of the inflammatory, proliferation, and remodeling phases of healing, and depends on the selection of appropriate topical antimicrobials or healing stimulants, dressings, and protective bandages.

Bandaging

Bandaging has two primary purposes. In the early stages of healing, the bandage must protect the open plantar wound after surgical debridement and should be changed regularly to allow monitoring of healing, cleaning or further debridement of the wound, and reapplication of topical treatments. The bandage or dressing must also alleviate direct pressure on lesions and redistribute the pressure on the plantar surface to prevent worsening of an existing lesion or recurrence of a debrided lesion. This becomes even more important in the chronic, remodeling phase of wound healing, which may take several months, as new tissue growth responds to pressure of weight-bearing.

Low-grade pododermatitis lesions without ulceration or contamination, particularly those involving flattening of the plantar papillae or hyperkeratosis, may respond to pressure-relieving bandaging only, which can be carried out while the underlying environmental causes are examined and rectified.

• Small lesions may be treated with commercially available corn pads, which redirect pressure to the immediate area surrounding the lesion.
• Interdigitating bandages are designed to provide padding to the central tarsal area. They allow relatively normal movement and use of the digits for perching. They are not suitable for birds with interdigital webbing or non-perching birds.
• Ball bandages are an extreme form of padding where all digits are closed around a central padded sphere. This provides padding to the central tarsal area and transfers pressure partially to the dorsal aspect of the digits, depending on the size of the ball.
• Donut bandages maintain the digits in full extension and relieve pressure on the tarsal area, by transferring weight-bearing to the digits. The donut may be made of rolled bandage material, but most commonly foam, which can be cut to size depending on the length of the digits and the size of the central lesion. A common method is to use slices of ‘pool noodle’ flotation devices, as these have an absent central core and are an ideal diameter for many hawks and falcons. Donut bandages are ideal for tarsal lesions, but not for digital lesions, and as weigh bearing pressure is transferred to the digits, care must be taken to ensure that secondary pressure sore do not develop.
• Foam shoes are comprised of a thick foam sole out of which holes are cut to accommodate the placement, size and shape of the lesion(s). These are therefore suitable for birds with webbed feet or those that usually stand on flat ground.
• ‘Íceflo’ shoes are a version of the foam shoe, using thick neoprene material instead of the foam sole, and a covering bootie—adapted from a wetsuit boot and fastened with Velcro—instead of the covering bandages. This style shoe was designed for penguins, as it can be worn both while swimming and on land. It is not suitable for other aquatic birds like Anseriformes, as paddling motions tend to dislodge the shoes, and the retention of moisture on land causes maceration and moist dermatitis of more delicate webbing.
• Silicone foot casts have been described for post-operative treatment and are designed to provide a soft but semirigid supportive cushion without creating pressure ischemia, by evenly distributing pressure over the whole surface.
• 3D-printed silicone shoes have been tested by the authors recently, based on the concept of the donut and foam shoe styles of bandaging. The silicone shoe is designed to be customizable, reusable, and comfortable, without the use of bandaging material. The benefit of this style is less wastage of disposable bandaging material, and the ability to get the shoe wet without the bandaging requiring replacement. Cutouts in the sole are created to accommodate the lesions.

Husbandry Considerations

Other pressure-relieving treatment options to consider, as well as bandaging, regard the substrate and perching options offered to the bird. Substrate modification may often be part of a conservative treatment option for low-grade pododermatitis lesions, or part of a larger environmental modification to rectify causes of lesion development.

As well as more permanent modifications to perches described earlier, during convalescence perches may be padded with bandage material, thin foam (such as yoga mats), rope, artificial turf, indoor-outdoor carpeting, neoprene or other soft material. For birds requiring extensive or prolonged bandaging, the replacement of perches with platforms may be necessary. Caged birds that use the cage mesh for climbing may benefit from a cage that uses a majority of vertically oriented bars, as there is far lesser plantar pressure when these are gripped.

For birds who do not, or are unable to perch, coarse-grain sand is an excellent substrate for recovery and to prevent recurrence. The shifting surface encourages muscle activity in the foot and pelvic limbs, and constantly changing pressure on the plantar surfaces. However, it must be dry, as wet sand quickly becomes hard and smooth, and very fine sand often compacts and hardens as well. For wading birds, sand or mud can also be used as an underwater substrate in the same way.

Rubber matting is also a good option for convalescent aviaries, either as a floor covering or pond lining. Saline foot baths have been used with success in several instances, either as a daily individual antimicrobial treatment, a walk-through as part of a pond system, or as a temporary water change for a period of time. This is an excellent option for treatment of larger flocks or wild birds undergoing rehabilitation, where regular restraint for treatment is challenging or not advised.

Activity is also important in the treatment of and prevention of pododermatitis. In birds that are able to fly or swim, these activities should be encouraged as much as possible, as it not only eliminates weight-bearing, but also increases blood flow. Resolution of lesions is much quicker in penguins that are encouraged to spend more times in the water and in hawks that spend more time in flight training. These birds are also less likely to become overweight, which also increases plantar pressure. For birds unable to do either, encouraging activity with enrichment items is recommended, particularly those which encourage whole body movement.

Conclusion

Pododermatitis is an important medical and welfare concern in captive birds of all species. It is a complex presentation with a multifactorial etiology and has many treatment and preventive challenges. Successful resolution and prevention of recurrence will always require a multimodal approach, as well as commitment to long-term treatment by the caregiver.

References

1.  Bailie CL, Baxter M, O’Connell NE. Exploring perch provision options for commercial broiler chickens. Appl Anim Behav Sci. 2018;200:114–122.

2.  Beaufrère H, Laniesse D, Stickings P, Tierney R, Sesardic T, et al. Generalized tetanus in a gyrfalcon (Falco rusticolus) with pododermatitis. Avian Dis. 2016;60:850–855.

3.  Bueno I, Anderson G, Willette M, Redig PT, Ponder J. Distraction osteogenesis in two wild raptors. J Avian Meg Surg. 2019;33:427–436.

4.  Burke HF, Swaim SF, Amalsadvala T. Review of wound management in raptors. J Avian Med Surg. 2002;16:180–191.

5.  d’Ovidio D, Noviello E, Adami C. Nerve stimulator-guided sciatic-femoral nerve block in raptors undergoing surgical treatment of pododermatitis. Vet Anaesth Analg. 2015;42:449–453.

6.  Daoust P-Y, Wadowska D, Kibenge F, Campagnoli RP, Latimer KS, et al. Proliferative pododermatitis associated with virus-like particles in a northern gannet. J Wildlife Dis. 2000;36:378–382.

7.  Doneley RJT, Smith BA, Gibson JS. Use of a vascular access port for antibiotic administration in the treatment of pododermatitis in a chicken. J Avian Meg Surg. 2015;29:130–135.

8.  Duncan AE, Torgerson-White LL, Allard SM, Schneider T. An evaluation of infrared thermography for detection of bumblefoot (pododermatitis) in penguins. J Zoo Wildlife Med. 2016;47:474–485.

9.  Erlacher-Reid C, Dunn JL, Camp T, Macha L, Mazzaro L, Tuttle AD. Evaluation of potential variables contributing to the development and duration of plantar lesions in a population of aquarium-maintained African penguins (Spheniscus demersus). Zoo Biol. 2012;31:291–305.

10.  Fiorello CV. Intravenous regional antibiotic perfusion therapy as an adjunctive treatment for digital lesions in seabirds. J Zoo Wildlife Med. 2017;48:189–195.

11.  Gartrell BD, Collen R, Dowding JE, Gummer H, Hunter S, et al. Captive husbandry and veterinary care of northern New Zealand dotterels (Charadrius obscurus aquilonius) during the CV Rena oil-spill response. Wildlife Res. 2013;40:624–632.

12.  Gebhardt-Henrich SG, Toscano MJ, Wurbel H. Perch use by broiler breeders and its implication on health and production. Poultry Sci. 2017;96:3539–3549.

13.  Jones MP. Vascular diseases in birds of prey. J Exotic Pet Med. 2013;22:348–357.

14.  Jones MP. Selected infectious diseases of birds of prey. J Exotic Pet Med. 2006;15:5–17.

15.  Kajagar BM, Godhi AS, Pandit A, Khatri S. Efficacy of low level laser therapy on wound healing in patients with chronic diabetic foot ulcers—a randomised control trial. Indian J Surg. 2012;74:359–363.

16.  Klambeck L, Stracke J, Spindler B, Klotz D, Wohlsein P, Schön H-G, Kaufmann F, Kemper N, Andersson R. First approach to validate a scoring system to assess footpad dermatitis in Pekin ducks. Europ Poult Sci. 2019;83.

17.  Knafo SE, Graham JE, Barton BA. Intravenous and intraosseous regional limb perfusion of ceftiofur sodium in an avian model. Am J Vet Res. 2019; 80:539–546.

18.  Li C, Lesuisse J, Schallier S, Clímaco W, Wang Y, Bautil A, Everaert N, Buyse J. The effects of a reduced balanced protein diet on litter moisture, pododermatitis and feather condition of female broiler breeders over three generations. Animal. 2018;12:1493–1500.

19.  Marques MVR, de Resende JS, Donatli RV, da Rocha Vilela DA, Ecco R, da Silva Martins NR. A bumblefoot outbreak and fatal septicemia in captive aquatic birds in Brazil. Cienc Rural. 2009;39:1905–1907.

20.  Mayne RK. A review of the aetiology and possible causative factors of foot pad dermatitis in growing turkeys and broilers. World Poultry Sci J. 2005;61:256–267.

21.  Nascimento CL, Ribeiro MS, Sellera FP, Dutra GHP, Simões A, Teixeira CR. Comparative study between photodynamic and antibiotic therapies for treatment of footpad dermatitis (bumblefoot) in Magellanic penguins (Spheniscus magellanicus). Photodiagn Photodyn. 2015;12:36–44.

22.  Nielsen AMW, Nielsen SS, King CE, Bertelsen MF. Classification and prevalence of foot lesions in captive flamingos (Phoenicopteridae). J Zoo Wildlife Med. 2010;41:44–49.

23.  Nielsen AMW, Nielsen SS, King CE, Bertelsen MF. Risk factors for development of foot lesions in captive flamingos (Phoenicopteridae). J Zoo Wildlife Med. 2012;43:744–749.

24.  Olsen RH, Christensen H, Kabell S, Bisgaard M. Characterization of prevalent bacterial pathogens associated with pododermatitis in table egg layers. Avian Pathol. 2018;47:281–285.

25.  Reidarson TH, McBain J, Burch L. A novel approach to the treatment of bumblefoot in penguins. J Avian Med Surg. 1999;13:124–127.

26.  Reisfeld L, Barbirato M, Ippolito L, Cardoso RC, Nichi M, Sgai MGFG, Pizzutto CS. Reducing bumblefoot lesions in a group of captive Magellanic penguins (Spheniscus magellanicus) with the use of environmental enrichment. Pesq Vet Bras. 2013;33:791–795.

27.  Reissig EC, Tompkins DM, Maloney RF, Sancha E, Wharton DA. Pododermatitis in captive-reared black stilts (Himantopus novaezelandiae). J Zoo Wildlife Med. 2011;42:408–413.

28.  Remple J. A multifaceted approach to the treatment of bumblefoot in raptors. J Exotic Pet Med. 2006;15:49–55.

29.  Sander S, Whittington JK, Bennett A, Burgdorf-Moisuk A, Mitchell MA. Advancement flap as a novel treatment for a pododermatitis lesion in a red-tailed hawk (Buteo jamaicensis). J Avian Med Surg. 2013;27:294–300.

30.  Scagnelli AM. Manuka honey. J Exotic Pet Med. 2016;25:168–171.

31.  Sellera FP, Sabino CP, Ribeiro MS, Fernandes LT, Pogliani FC, Teixeira CR, Dutra GHP, Nascimento CL. Photodynamic therapy for pododermatitis in penguins. Zoo Biol. 2014;33:353–356.

32.  Shepherd EM, Fairchild BD, Ritz CW. Alternative bedding materials and litter depth impact litter moisture and footpad dermatitis. J Appl Poult Res. 2017;26:518–528.

33.  Tolpinrud A, O’Brien MF, Justice WSM, Barrows M, Steele O, Gent S, Meredith AL. Infrared thermography as a diagnostic tool for pododermatitis in captive greater flamingos (Phoenicopterus roseus). J Zoo Aquarium Res. 2017;5:48–55.

34.  Webb JK, Keller KA, Welle K, Allender MC. Evaluation of the inter- and intraindividual agreement of a pododermatitis scoring model in greater flamingos (Phoenicopterus roseus). J Zoo Wildlife Med. 2020;51:379–384.

35.  Williams LK, Sait LC, Trantham EK, Cogan TA, Humphrey TJ. Campylobacter infection has different outcomes in fast- and slow-growing broiler chickens. Avian Dis. 2013; 57:238–241.

36.  Wyss F, Wenker C, Hoby S, von Houwald F, Schumacher V, Doherr MG, Robert N. The effect of fine granular sand on pododermatitis in captive greater flamingos (Phoenicopterus roseus). Anim Welfare. 2014;23:57–61.

37.  Wyss F, Wolf P, Wenker C, Hoby S, Schumacher V, Bechet A, Robert N, Liesegang A. Comparison of plasma vitamin A and E, copper and zinc levels in free-ranging and captive greater flamingos (Phoenicopterus roseus) and their relation to pododermatitis. J Anim Physiol Anim Nutr. 2014;98:1102–1109.

38.  Wyss F, Schumacher V, Wenker C, Hoby S, Gobeli S, Arnaud A, Engels M, Friess M, Lange CE, Stoffel MH, Robert N. Pododermatitis in captive and free-ranging greater flamingos (Phoenicopterus roseus). Vet Pathol. 2015;52:1235–1242.