Feather Loss and Feather Destructive Behavior in Pet Birds

REVIEW FEATHER LOSS AND FEATHER DESTRUCTIVE BEHAVIOR IN PET BIRDS

Jonathan Rubinstein, DVM, Dip. ABVP (Avian), and Teresa Lightfoot, DVM, Dip. ABVP (Avian)

Abstract Feather loss in psittacine birds is an extremely common and extremely frustrating clinical presentation. Causes include medical and non-medical causes of feather loss both with and without overt feather destructive behavior. Underlying causes are myriad and include inappropriate husbandry and housing; parasitic, viral and bacterial infections; metabolic and allergic diseases; and behavioral disorders. Prior to a diagnosis of a behavioral disorder, medical causes of feather loss must be excluded through a complete medical work-up including a comprehensive history, physical exam, and diagnostic testing as indicated by the history, signalment and clinical signs. This article focuses on some of the more common medical and non-medical causes of feather loss and feather destructive behavior as well as approaches to diagnosis and treatment. Copyright 2012 Published by Elsevier Inc. Key words: feather destructive behavior; psittacine; behavioral disorder; feather-picking; avian behavior

eather loss is one of the more common and frustrating reasons that avian patients are presented to veterinary hospitals. Several factors make the treatment of feather loss difﬁcult. The initial problem lies in the relative scarcity of controlled studies related to the underlying causes of feather loss in companion avian species and the paucity of current veterinary medical knowledge regarding feather loss and feather destructive behavior (FDB). Although many medical and environmental conditions haveF been associated with FDB, few have been proven to be causal. Wherever possible, this article references applicable controlled studies, although they are few. Elsewhere, review articles and conference proceedings are referenced, with personal observations referred to as necessary.

The initial clinical dilemma facing the practitio- psychogenic in origin, or, as is often the case, includes ner is determining if the feather loss is intrinsic a combination of factors. or due to FDB. Pet birds are often left unob- If environmental factors and medical conditions served for long periods of time, which limits the associated with feather loss and destruction can be owner’s ability to observe FDB. Additionally, reasonably ruled out, determining the underlying owners may be unable to distinguish normal triggers and reinforcing factors that may perpetuate preening behavior from overt feather destruction. psychogenic FDB can be complicated and time- Although definitions vary, for the purposes of this consuming. Limitations include the accuracy of the article, intrinsic feather loss will refer to feather loss owner’s observations and his or her willingness to that is either not self-inflicted or is the result of nor- learn and commit to behavioral enrichment and mal preening of abnormal feathers. FDB will be de- modification techniques. This article will discuss fined as self-inflicted feather loss, damage, or destruc- the more common causes and risk factors associ- tion, regardless of etiology. If it can be determined ated with feather loss, both with and without FDB, that the feather loss is self-induced, the next step is as well as treatment options. determining if this FDB has a primary medical etiol- Missing or damaged feathers warrant a com- ogy, involves husbandry and/or nutritional issues, is prehensive review of husbandry, as well as a

From Florida Veterinary Specialists, Tampa, FL USA. Address correspondence to: Jonathan Rubinstein, DVM, Dip. ABVP (Avian), BluePearl Veterinary Partners, 3000 Busch Lake Blvd, Tampa, FL 33614. E-mail: [email protected]. © 2012 Published by Elsevier Inc. 1557-5063/12/2103-$30.00 http://dx.doi.org/10.1053/j.jepm.2012.06.024

Journal of Exotic Pet Medicine 21 (2012), pp 219–234 219 Several excellent reviews are available that will help the practitioner in determining normalcy of companion avian species feather condition.2-4

INTRINSIC FEATHER LOSS

Non-medical Intrinsic Feather Loss A commonly encountered risk factor for feather loss in the absence of either an underlying medical problem or FDB is an inappropriate environment. A small cage or poor cage layout can damage the primary flight feathers or the rectrices (Fig. 2). The bird may be removing the damaged feathers at an inappropriate rate, but removal of damaged feathers is normal preening behavior. This will rarely affect the secondary or covert feathers. Toxins, both airborne (e.g., cigarette smoke, FIGURE 1. A common presentation of birds with FDB is a normally scented candles, perfume, air fresheners, hair- feathered head with a complete lack of feathers on the rest of the body. spray) and topical (e.g., hand lotion, hand creams), have been implicated in FDB, though the association remains anecdotal. Owners medical workup and behavioral assessment (Fig. should be encouraged to avoid the use of these 1). The first step is a thorough anamnesis. Be- products on or around their birds. cause of the need for extensive questioning re- Low humidity levels and abnormal photoperiods garding diet, husbandry, and behavior, a pre- can promote poor feather quality in pet birds; own- pared questionnaire can be e-mailed or faxed to ers and veterinarians may mistake the patient’s un- the owner before the office visit. By previewing a kempt feathers for FDB. In neonates, low humidity thought-provoking, problem-specific question- can lead to a failure of the feather sheath to soften, naire, the owner should be able to present more causing retention (Fig. 3).5 Adult birds housed in thoughtful and accurate responses, and allow the lower ambient humidity than required for that par- practitioner time to review the information. Ex- ticular species may develop dry, flaky skin and amples of these extensive questionnaires relating overall poor feather quality, which may be mis- to abnormal feather problems affecting compan- taken for FDB.6,7 Photoperiod is essential to the ion avian species have been published.1 regulation of circadian and circannual rhythms in The enclosure type (size, material), location (in- birds; therefore, the artificial and usually static pho- door, outdoor), and the presence or absence of cage mates or adjacently housed birds should be investigated. The current and previous diet, both what is offered and what is actually consumed, also should be determined by the attending clinician. Unless an obvious reason for feather damage can be ascertained when taking the patient history (e.g., excessively small cage damaging the rectrices) and signalment (e.g., the characteristic “bald spot” of Lu- tino cockatiels), or while performing the physical examination (e.g., an obese budgerigar with alopecia over the breast), a medical workup is indicated. Gen- erally, a complete blood count, plasma chemistry panel (including resting bile acids, cholesterol, and triglyceride levels), fecal cytology and wet mount examinations, and 2-view whole-body survey radio- graphs should be performed. On physical examination, the condition of the FIGURE 2. Damage to the primary flight feathers and skin, feathers, and feather shafts in areas with rectrices is common in birds kept in inappropriately and without feather loss should be examined. small cages.

220 Rubinstein and Lightfoot/Journal of Exotic Pet Medicine 21 (2012), pp 219–234 molting involves the staggered replacement of up to 30% of the lean, dry body mass of a bird, of which 90% is protein.11,12 The basal metabolic rate of avian species can double during molting periods.13 Given these physiological costs, it is not surprising that nutritional status has a significant impact on feather health, and deficiencies may manifest as feather disorders. Birds undergo- ing molt have increased need for energy, amino nitrogen, and amino acids, in particular cys- teine.10 Research studies have shown that food- deprived juvenile starlings have slower feather growth rates and sparrows fed diets deficient in sulfur-containing amino acids had delayed molts FIGURE 3. Retained feather shafts are commonly seen and a greater number of feather deformations in psittacine birds that are housed in low-humidity when compared with birds fed nutritionally ade- environments. quate diets.14,15 Deficiencies in certain sulfur-containing amino acids will create abnormalities of toperiod provided to pet birds may alter and often the rachis, abnormal persistence of the basal 8,9 delay molts. Retention of feathers due to the de- sheath, and misshapen vanes; lysine is essential lay in new feather formation can lead to a ragged, for overall feather strength; and methionine defi- unkempt appearance which may be mistaken for ciency has been associated with the formation of FDB. Providing a seasonally appropriate variation horizontal “stress lines” on feathers.10,16,17 How- in photoperiod, controlled access to the outdoors, ever, it is important to note that in experiments and bathing, showering, and/or misting birds af- where specific amino acid deficiencies were infected by this condition will often help to resolve duced, birds did not develop FDB.10 Whether the the problem. removal of these abnormal feathers explains the observed link between FDB and malnutrition or Medical Intrinsic Feather Loss a more direct link exists awaits further research. Many diseases can damage the feathers such that they are easily lost; these birds may be incor- Circovirus: Psittacine Beak and Feather Disease rectly labeled as “feather-pickers.” Chronic mal- Circoviruses are hardy, non-enveloped DNA viruses nutrition can result in a variety of feather dystro- that are responsible for psittacine beak and feather phies. Less often, viral infections and parasitic disease (PBFD).18 PBFD is somewhat of a misno- mite infestations damage the feather follicle and mer because the beak is rarely affected in non- shaft, weakening their attachment and allowing Cacatua spp. However, the name PBFD has re- the feather to be readily shed. mained in common usage. PBFD primarily affects young birds; in one study 92% of infected cocka- Malnutrition toos were under 3 years of age.18 Birds that mani- Nutritional feather disorders can be considered fest signs at a later age are suspected of having a to be both environmentally and medically in- latent infection.18 African species such as the Psitta- duced. Although malnutrition has long been as- cus spp. and lovebirds (Agapornis spp.) are consid- sociated with FDB, research into potential mech- ered highly susceptible to circovirus. Although rare, anisms is lacking. Birds in captivity, similar to PBFD has been reported in several New World par- those in the wild, do not self-select for dietary rots (e.g., macaws [Ara spp.] and Amazon parrots completeness.10 In addition, most captive birds [Amazona spp.]).19,20 The circovirus is shed in large are fed diets that are inherently nutritionally in- amounts in feather and skin dander; although the complete, and many of these diets further allow exact mode of transmission remains unclear, inha- the birds to select favored foods. Consequently, lation and/or oral ingestion is suspected. this creates a situation in which malnutrition is Feather dysplasia occurs via necrosis of the epi- endemic in captive psittacines both with and dermal collar, basal epidermis, and feather pulp, without FDB; clearly other factors are involved in and hemorrhage and necrosis within the feather the development of FDB. pulp. The type and extent of feather lesions de- The metabolic cost of growing, maintaining, pend on the species of bird and the stage of molt and replacing feathers can be high; the process of when the bird begins to develop abnormalities.

Rubinstein and Lightfoot/Journal of Exotic Pet Medicine 21 (2012), pp 219–234 221 unique manifestation occurs in budgerigars wherein the affected bird will exhibit normal feathering except for the presence of a “French molt” characterized by the absence of the primary and secondary wing feathers and often the rectrices as well. Breeders refer to these clinically affected budgerigars as “runners” or “creepers.” It is important to remember that a polyomavirus infection (or a combined polyomavirus/circovirus infection) can result in the similar clinical signs in budgerigars as described above. Diagnostic testing for PBFD is recommended for all susceptible birds before introduction to a collection regardless of the clinical condition of the bird during the initial examination. Polymerase chain reaction (PCR) analysis is considered the test of choice for avian circovirus.9,18,19 The most appropriate sample for testing is debatable, with some stud- FIGURE 4. Six-month-old lovebird with circoviral infection. Note the ies finding analysis of feather and cloacal samples diffuse feather loss and generally unthrifty appearance. more reliable than whole blood, especially in the case of subclinical birds, whereas other studies have Chicks affected during the initial stages of feather found PCR analysis of blood to be more sensitive development demonstrate the most severe pa- than that of feathers.19,24 If feather samples are sub- thology associated with PBFD.18 Initial signs may mitted, the practitioner must be careful to avoid include delayed molts or decreased powder-down environmental cross-contamination and false-posi- production with a small number of dysplastic tive results because other birds infected with circo- feathers; over time the number of affected feath- virus may be shedding copious amounts of virus. ers generally increases. Hemorrhage within or Laboratories have been shown to have different de- hyperkeratosis of the feather shaft, weak and eas- grees of accuracy in diagnosing circoviral infection via ily broken feathers, pinching off of the feather PCR, and the practitioner is encouraged to contact base, abnormally pigmented feathers (particularly their diagnostic laboratory to determine what internal reddening of normally gray feathers in Psittacus controls have been established to ensure accurate test spp.), or a combination of these feather dyspla- results.25 Veterinarians are also encouraged to remem- sias are commonly reported changes associated ber that in the case of circovirus, as in all viral infec- with this viral infection. In older juveniles, ab- tions, a positive PCR result does not necessarily equal normal clinical signs often begin with necrosis an active infection; positive circovirus PCR results and dystrophy of the powder-down and contour should be verified by retesting after 90 days, during feathers; the lesions then spread to other tracts of which quarantine is strongly recommended.26 Because contour feathers followed by similar lesions in circovirus is genetically diverse, PCR may not be able all other feather types. Eventually, feather folli- to detect all genotypes. Although there is much dis- cles become inactive and the bird will remain cussion regarding different “types” of avian circovi- largely featherless.18 ruses, it has been shown that many strains of circovi- Although the ban on importation of wild birds rus exist with new strains still being discovered.19,27-29 and the development of accurate testing has Although some degree of host specificity likely exists greatly decreased the incidence of circovirus in- it should be assumed that all susceptible psittacine fection in larger parrot species in the United species may be susceptible to any virus variant—an- States, lovebirds and budgerigars are still fre- other reason that owners should be encouraged to quently affected and diagnosed with this disease. test and quarantine any new birds they want to add Some studies have found infection rates as high to their established avian collection.19,27 as 30% in lovebirds; the number is likely lower in budgerigars.21,22 Many, if not most, infected Polyomavirus lovebirds will remain subclinical.23 Affected love- Avian polyomavirus, a DNA virus with a world- birds are usually older juvenile to young adult wide distribution in which there are a large num- birds; signs include an unthrifty appearance, de- ber of susceptible avian species, can, in budgeri- layed molts, and loss of feathers (Fig. 4). A gars, be a cause of feather dystrophy and feather

222 Rubinstein and Lightfoot/Journal of Exotic Pet Medicine 21 (2012), pp 219–234 loss in the absence of FDB. Polyomavirus infec- barring, hemorrhage, and fracture of feather tion is generally a disease of nestling birds. Nest- shafts with subsequent feather loss.33 Most lings and adult birds of most species are suscepti- feather mites can be visualized di- ble to infection; however, the vast majority of rectly or identified with tape prepa- infected adult birds will seroconvert and clear the rations or skin scrapes. Quill mites Although some infection without demonstratable illness. Particu- can be identified with cytology and degree of host lar disease syndromes, and if clinical disease even examination of feather shaft mate- develops at all, depend on multiple factors (e.g., rial from a growing feather. Mite specificity likely species, co-infection with other disease agents infestations can be treated with exists it should such as circovirus, age at exposure). Certain spe- fipronil, carbaryl, or avermectin cies, such as macaws, conures (Aratinga and drugs. be assumed that Pyrurrha spp.), Eclectus parrots (Eclectus rora- all susceptible tus), budgerigars, lovebirds, ring-necked para- FEATHER psittacine keets (Psittacula spp.), and caiques (Pionites DESTRUCTIVE BEHAVIOR spp.) seem to be most susceptible to polyoma- species may be virus infection.23 Feather lesions from polyo- Medical Associations mavirus are, in most cases, only clinically ob- susceptible to served in budgerigars.30 Although not defini- Numerous medical conditions, in- any virus tively proven, exposure to polyomavirus is cluding some that seem to have an suspected to occur primarily via inhalation.23 extremely spurious relationship to variant—another Disease in budgerigars is unique compared skin or feather health, have been reason that with that in other bird species and can take associated with FDB, though in many forms; although some budgies that survive most cases causality has not been owners should polyoma infection will never develop overt clini- proven. Despite this uncertainty, be encouraged cal signs, others will develop French molt as pre- should the history and/or physical viously discussed. English budgerigars are be- examination fail to provide a diag- to test and lieved to be more resistant to infection compared nosis, a comprehensive medical quarantine any with other lines of budgerigars. The development workup is indicated. Often, the pa- of feather lesions in surviving, infected nestling tient’s size and/or the financial lim- new birds they itations of the owner prevent the budgerigars follows a fairly predictable pattern: want to add to budgerigars under 2 weeks of age show a lack of extent of testing that would be ide- powder-down on the head and neck; those 2 al; in these circumstances the veter- their established inarian must choose those tests weeks to 1-month-old exhibit a lack of or incom- avian collection. pletely developed flight feathers; and, after 25 most likely to be informative given days of age, feathers will begin to develop, al- the signalment, history, and clinical though the tail and/or some flight feathers of signs. some birds remain underdeveloped or absent.31 PCR analysis of both whole blood and a com- Metabolic bined choanal/cloacal swab is recommended for Simply put, anything that produces pain or dis- birds during quarantine in order to identify vire- comfort may predispose that individual to mic and/or shedding birds.23 Because many birds feather destruction; this feather loss may be dif- survive and clear polyoma infections, positive fuse or occur directly over the site of irritation. results should be confirmed after 90 days. Renal disease has been associated with localized picking over the synsacrum.34,35 Septicemic alope- Mites cia is a condition of repeated rubbing and chew- Cnemidocoptes mite infestations are generally re- ing of a particular area, often over the breast, in stricted to the cere (budgerigars; “scaly face”) or response to generalized fungal or bacterial infec- feet (canaries; “tassel-foot”), although feather loss tion.7,36 Hepatic disease, long known to be re- in severe infestations involving the feather folli- sponsible for pigmentary changes and darkening cles have been reported.4,32 Feather mites can be of feathers, has often been associated with gener- found, nonpathogenically, in host-adapted spe- alized feather plucking.37,38 Recently, pruritis in cies, though feather loss can occur in immuno- people with cholestatic disease was linked to the compromised birds or in nonhost species.6 Quill increased expression of an enzyme that forms the mites (e.g., Syringophilus, Dermoglyphus) are gener- neuronal activator lysophosphatidic acid; the in- ally not pathogenic, but can cause horizontal creased lysophosphatidic acid then activates itch

Rubinstein and Lightfoot/Journal of Exotic Pet Medicine 21 (2012), pp 219–234 223 fibers.39 Whether similar mechanisms can produce pruritis in birds with hepatic disease, potentially contributing to FDB, is unknown. Hypothyroidism has also been linked to FDB, though in the single peer-reviewed case report that documented hypothyroidism through the use of a thyroid-stimulating hormone (TSH) as- say, the bird showed diffuse feather loss but not FDB.40-42 Chickens with primary hypothyroidism as well as thyroidectomized birds show abnormal molts and plumage patterns but not FDB.43 Stud- ies that investigated total T4 levels in birds exhibiting FDB have been inconclusive. TSH assays are considered superior to resting thyroid levels for diagnosis of avian hypothyroidism; this is especially true because birds have a resting total T4 level only one fifth to one tenth those reported in mammals.44,45 Although a TSH stimulation test has been validated for birds and normal val- ues established for certain species, this test is not currently commercially available because of a lack of availability of bovine TSH.46 Attempting to diagnose or treat FDB by observing response to treatment with thyroid supplementation is FIGURE 5. Malassezia dermatitis in a Psittacula parrot as 43 unreliable. Overall, the role of thyroid disorders confirmed by biopsy and histopathology. in FDB remains unclear. a possible cause of feather loss and FDB, though Allergic and Inflammatory Disease controlled studies are lacking (Fig. 5).51-56 Dermati- The roles of allergic and/or inflammatory diseases tis and feather damage were reported in chickens in FDB have also been investigated. A technique for from which C. albicans was identified and a fungus intradermal skin testing in birds has been de- suspected to be Malassezia spp. was associated with scribed, but was found by the authors to be unreli- pruritis and feather loss in a canary.52,53 In one able.47,48 One small, prospective study using a study examining acetate tape preparations from paired biopsy technique that compared samples birds with and without FDB, only 10% of the sam- from affected and unaffected areas of the same pa- ples contained any yeast at all. None of the identi- tient failed to find any inflammatory cells in sam- fied yeast were Malassezia spp. and only a very ples from either feather-picked or control birds, small percentage were identified as Candida spp. except in one sample from a nonpicked area of a The numbers of yeast identified microscopically did feather-picking bird.49 A larger, retrospective, case- not differ significantly between birds with and controlled study of feather-picking and self-mutilat- without FDB.51,54-56 Whether these findings indicate ing birds using this paired biopsy technique found the limitations of the tape preparation technique or inflammatory changes consistent with a cutaneous minimal involvement of fungal organisms in FDB delayed-type hypersensitivity reaction in both the required further scientific investigation. It is impor- affected and unaffected areas in slightly over half tant to note that bacterial or fungal dermatitis may the samples.50 The authors felt that the balance occur subsequent to self-mutilation. Treatment of of the samples represented “traumatic” skin disease the dermatitis is necessary, but addressing the un- that occurred in the absence of inflammation. In derlying factors that predispose the bird to self- the study, lories, macaws, and Amazon parrots mutilation is critical. were more likely to have inflammatory skin dis- Bacterial disease of the skin generally manifests ease, whereas cockatoos and African gray parrots as a folliculitis or a generalized dermatitis, both were more likely to exhibit traumatic skin disease of which can create local inflammation, pruritis, without inflammation. and feather destruction.51 Lesions associated with Fungal or yeast allergy and or/dermatitis, specifi- bacterial dermatitis are often reddened and exu- cally those cases involving Aspergillus spp., Malasse- dative with superficial crust formation and, in zia spp., and Candida spp., have been considered as severe cases, necrosis extending into the dermis

224 Rubinstein and Lightfoot/Journal of Exotic Pet Medicine 21 (2012), pp 219–234 cally, because ABV is a neurotropic virus shown to induce peripheral neuritis, a link between ABV, peripheral pain, and FDB or self-mutilation may exist, but remains speculative at this time.61 Theoretically, because ABV is Giardia Giardia psittaci are motile, flagellated a neurotropic protozoa with a worldwide distribu- virus shown to tion that are known to infect a wide variety of avian species, though they induce are most commonly documented in peripheral cockatiels. Although in most species clinical signs are limited to enteritis, neuritis, a link FIGURE 6. Bacterial dermatitis in the axillae of a peach- a unique, though unproven, mani- between ABV, faced lovebird. Note the feather loss and diffuse ery- festation of Giardia infection in cock- thema with crusting. atiels is pruritis and a predisposition peripheral pain, to feather plucking.62,63 Giardia is and FDB or (Fig. 6).51 Bacteria associated with these lesions only intermittently shed, so repeated are often Gram-positive cocci, commonly fecal examinations may be required self-mutilation Staphylococcus spp.32 In cases of suspected fungal for detection; fecal samples should may exist, but or bacterial dermatitis, an impression smear can be rapidly examined because the tro- assist in the interpretation of culture results; for phozoite form is very short lived remains example, should the cytology show a preponder- once excreted. The use of warm sa- speculative at ance of Gram-positive cocci, growth of Pseudomo- line solution and dilute Lugol’s solu- nas spp. on culture is unlikely to be clinically tion as a contrast agent may increase this time. significant. In both bacterial and fungal dermato- the success of identifying the organ- ses, definitive diagnosis is obtained via biopsy ism in infected bird feces.62 PCR analysis of feces and histology, because the presence of bacteria or and/or cloacal swabs is commercially available, yeast is not sufficient to prove causality; there- though sensitivity and specificity are not docu- fore, tissue invasion and an inflammatory reac- mented for avian species. Transmission is fecal-oral, tion must be confirmed through histopathologic and the treatments of choice for this disease are review of the affected tissue. In cases of suspected metronidazole, fenbendazole, or ronidazole. Cock- fungal infection, a portion of the biopsy sample atiels may be sensitive to fenbendazole and it can be frozen for culture and subsequently pro- should be used cautiously, if at all, in this species. cessed if indicated by the histopathology. Pend- ing culture results, the cytological results can be used to determine the initial antimicrobial MUTILATION SYNDROMES choice. Treatment involves long-term administra- Species-specific “syndromes” of self-trauma that tion of antibiotics and/or antifungals; often treat- may involve FDB have been reported. Although ment for 6 weeks or longer is required for suc- suspected links to infectious and/or metabolic con- cessful resolution of the case. ditions have been hypothesized, significant behav- Avian Bornavirus ioral components must be considered. Controlled Avian bornavirus (ABV), a single-stranded RNA studies of these “syndromes” are lacking, and fur- virus in the family Mononegavirales, is the putative ther identification of the unique disease entities agent of proventricular dilation disease, a common within this classification awaits further research. infectious disease of many bird species.57 The virus Cockatoos often present for severe self-mutila- has only recently been identified.58 In addition, a tion involving the feathers, skin, and muscles of subclinical carrier state has been documented in the breast or patagium. Chronic ulcerative der- cockatiels.59 Although a complete review of the matitis in lovebirds presents as severe self-trauma emerging research of this virus is beyond the scope to the feathers and skin of the patagium, neck, of this article, it is important to note that a link and/or back (Fig. 7). A severe and often fatal between ABV infection and FDB (as well as mutila- self-mutilation, Quaker/monk parakeet (Myiop- tion syndromes) has been postulated.60 Theoreti- sitta monachus) mutilation syndrome, has been

Rubinstein and Lightfoot/Journal of Exotic Pet Medicine 21 (2012), pp 219–234 225 anecdotally reported for many years, though no etiology has been identified (Fig. 8). Treatment of self-mutilation involves provision of a mechanical barrier via collaring or vesting, long-term antimicrobial therapy to treat and prevent secondary infections, and pain Treatment of control. In some individuals, most often reported in cockatoos, the use self-mutilation of psychotropic medications may be involves helpful (see below). Unfortunately, treatment is often unrewarding and provision of a many of these birds are euthanized mechanical because of recurrent self-mutilation. Further research, including the sub- barrier via mission of biopsy samples for histo- FIGURE 8. Severe self-mutilation in a Quaker parakeet. collaring or pathology by practitioners, may help elucidate the etiologies of these syn- to impulse control disorders such as trichotilloma- vesting, long- dromes. nia in humans.64-66 Stereotypies are defined as term those behaviors that are repetitive, performed out PSYCHOGENIC RISK FACTORS of their original context, and therefore serve no antimicrobial obvious purpose; these behaviors do nothing to therapy to treat If an environmental or medical basis reduce or ease the environmental situation on for feather loss or FDB cannot be which they depend, but are simply an expression of and prevent found, behavioral and/or psychologi- that environment.67 These abnormal behaviors are secondary cal factors must be considered. It is typically observed in situations of conflict and/or important to remember that behav- frustration. Stereotypical behaviors are often abnor- infections, and iorally induced feather destruction is mal expressions of normal behavior; the most com- pain control. a not a diagnosis, per se, but a reflec- mon stereotypies seen in avian patients can be tion of problems within the captive considered aberrations of typical behaviors: vocal- environment. For a list of specific ization and flock communication (screaming proposed etiologies or contributing factors for be- behavior), reproduction and mate interaction (ex- havioral FDB, and resources for client education, cessive masturbation and/or cockatoo prolapse syn- see Tables 1 and 2. drome), or grooming (FDB). Some veterinarians and behaviorists consider The fact that FDB is only observed in captive FDB to be a stereotypical behavior disorder, similar psittacines, and therefore is in some manner caused by captivity, indicates fundamental limitations in the environment of these animals.68 Frustratingly, many of the problems can be created by a “good” bird owner; for instance, the provision of a stable environment and abundant food, free from the normal costs and stressors that the bird would en- counter in the wild. This becomes obvious should one compare the daily activities of a wild-living parrot and a pet parrot. Captive orange-winged Amazon parrots (Amazona amazonica) fed a pelleted diet spend only 30 to 72 minutes a day in feeding behaviors, whereas free-ranging Amazon parrots spend up to 4 to 6 hours a day foraging for food.69,70 This is to say nothing of the distance the parrot would travel to find that food; the mental acumen required to locate and avoid predators; the challenge of observing and reacting to changing environmental and weather patterns; and the men- FIGURE 7. Chronic ulcerative dermatitis in a peach-faced lovebird tal flexibility required to navigate the myriad of exhibiting severe self-mutilation over the back and shoulders. interactions that occur in a flock of similarly intelli-

226 Rubinstein and Lightfoot/Journal of Exotic Pet Medicine 21 (2012), pp 219–234 TABLE 1. Factors associated with feather loss in psittacine birds Suspected Relative Prevalence in Etiology/Risk Feather Loss/ Classification Factor Damage Comments Intrinsic feather loss Environmental (Note: poor plumage more common than overt feather loss) Inappropriate caging ϩϩ Selected feathers affected Low humidity ϩϩ Retained feather shafts may be prominent Inappropriate ϩϩ Retained feather shafts may be prominent photoperiod Medical Malnutrition ϩϩϩ Can contribute to susceptibility to disease and subsequent feather destructive behavior Circoviral infection ϩ Mostly seen in Old-World species less than 3 years old Polyomaviral infection ϩ Budgerigars only Mite infestation ϩ Rarely causes feather signs Feather destructive behavior Medical feather destructive behavior Renal disease ϩ Usually localized to the area over the synsacrum Septicemic alopecia ϩ Usually localized to the breast Hepatic disease ϩϩ Diffuse; in humans hepatic pruritis is associated with increased expression of lysophosphatidic acid. Hypothyroidism ? Association not documented Allergic/inflammatory ϩϩϩ May be present in up to half of feather skin disease destructive behavior cases Bacterial dermatitis ϩϩ Biopsy needed to confirm infection—may be secondary to mutilation Fungal dermatitis ϩ As above Avian bornavirus ? Association is speculative Giardia psittaci ? Association suspected in cockatiels Nonmedical feather destructive behavior Psychogenic Multiple ϩϩϩϩ See Table 2 for specific risk factors and online resources Plus signs are meant to indicate the suspected relative prevalence of each of these etiologies as seen in clinical practice, although no controlled studies exist that determine the actual contribution or prevalence of these etiologies in feather loss.

gent individuals. Most pet parrots are housed in ronment. Given this situation, the similarity be- cages no larger than 5 to 10 times their own height tween the stereotypies seen in pet parrots and those and less than this in width. They are fed a bowl of observed in industrial farms and zoological institu- easily accessible food that requires no thought to tions is not surprising. select or prepare. Our generally poor understanding It has been estimated that 1 of every 10 birds has of avian social structure leads to the “human ﬂock” some degree of psychogenic feather-picking behav- sending confusing and inconsistent signals, espe- ior; FDB may be the most common disease presen- cially in terms of reproductive relationships. In ad- tation of companion psittacine species to veterinary dition, these birds are housed exclusively indoors hospitals.71 Counseling owners on the maintenance with no need to adapt to their highly static envi- of the psychological well-being of their bird is as

Rubinstein and Lightfoot/Journal of Exotic Pet Medicine 21 (2012), pp 219–234 227 TABLE 2. Psychogenic feather destructive behavior ronmental enrichments such as alternative perches, demonstrated improved feather condition.72 Forag- Specific Risk Factors Online Resources ing enrichment was shown to decrease psychogenic Deficiencies in social http://www.avianstudios.com feather-picking in African gray parrots.75 However, interaction and it should be noted that the 2 previous studies used mental stimulation poor plumage condition as an indirect measure of Lack of exercise http://www.goodbirdinc.com FDB, which has not been validated as an experi- Inadvertent http://www.parrotenrichment. reinforcement com mental model. Inappropriate bond http://www.behaviorworks. Providing enrichment through foraging can be as to owner org simple as the provision of relatively complicated Hormonal http://www.parrots.org/index. food items such as corn on the cob, pineapples, or stimulation php/referencelibrary/ pomegranates. Although a variety of complicated behaviourandenviroenrich/ foraging toys have become commercially available, Please note that these are a sampling of the available online these items can easily be constructed by the bird resources, with a significant and beneficial overlap in content. owner. Owners can try paper bags, cardboard These are provided for the practitioner’s convenience and are boxes, plastic water bottles, and other types of not exhaustive. “food toys,” while being cautioned to provide these items to their birds under supervision to ensure that only the food is being consumed. Owners essential as discussing basic nutritional and hus- should also be informed of the resources currently bandry requirements and should be an integral part available regarding captive foraging (see Table 2). of every “new bird” visit. Additional enrichment techniques (“jobs”) in- It is an accurate oversimplification to say that clude providing soft wooden perches for chew- most behavioral FDB is related to a reductive en- ing, as well as magazines, phone books, or other vironment over which the bird has little or no “destroyable” objects that the bird will be disin- control. Experimentally, it has been shown that clined to consume (Fig. 9). In addition to the certain behavioral disorders, including FDB, may destructive behaviors enjoyed by most parrots, potentially be prevented, and when established, cockatoos seem to enjoy unscrewing and solving can possibly be reversed with environmental items that are seen as “puzzles.” modification.65,72 Moreover, manipulation of the One simple way to provide the bird with a “job” physical and mental environment that creates is training. Many birds, despite their intelligence, situations in which the bird is given the ability are not asked to perform any action more compli- (and is required) to make decisions, is the first cated then stepping onto a hand or a finger. Own- step to improve the patient’s living condition. ers can begin by teaching the “come” and “stay” This is often easier than most owners realize. A commands they use with other pets.73 Providing first step may be changing the location and fur- food and verbal rewards for performing a task re- nishings of the cage, requiring the bird to accom- quires the bird to focus and think. This also allows modate to new surroundings. Weather permit- the bird and owner to bond in a way that does not ting, owners should be encouraged to allow their birds controlled, supervised access to the outdoors. Here the bird can observe and react to novel stimuli, such as cloud movement, baromet- ric pressure changes, traffic, wild birds, etc. Being outside also requires the bird to be vigilant for (hopefully nonexistent) predators, providing additional mental stimulation. It has been shown that providing mentally stimulating challenges and tasks can provide relief from psychogenic FDB. This has been referred to as a “compelling occupation” for the bird; or “giving the bird a job.”73 Well-fed starlings were shown to prefer foraging for their food rather than eating out of bowls.74 Young Amazon parrots that were intro- duced to a combination of foraging activities such FIGURE 9. One author’s bird spends hours per day as sifting through nonfood items, along with envi- chewing his perch symmetrically.

228 Rubinstein and Lightfoot/Journal of Exotic Pet Medicine 21 (2012), pp 219–234 FIGURE 10. Sedated Dusky Pionus (Pionus fuscus) after the application of an e-collar. “Playing dead” is a common sequelae of application. involve rubbing and petting, consequently this will FIGURE 12. The cardboard is cut to an appropriate height and not be perceived by the bird as reproductive behav- wrapped with cohesive bandaging. ior. collar, fluids and gavage feeding may be re- Other treatments that have been used for be- quired. Midazolam (Versed; Roche Labs, Basel, havioral FDB include avoidance devices such as Switzerland) dosed at 0.3 to 0.5 mg/kg is often Elizabethan collars and psychotropic medica- administered before collar placement to facilitate tions. Collaring of birds to prevent behavioral acclimation. Although radiograph film has com- FDB does nothing to change the underlying pa- monly been used to make collars, it is less dura- thology and should be avoided except in cases of ble than commercially available plastic collars.76 self-mutilation. Many birds do not readily toler- Available types of avian collars include molded ate collaring; commonly, initial responses by plastic spherical and straight extenders, the latter avian patients to collars include violent flailing, often with grooves for the addition of Elizabe- prolonged recumbency (“playing dead”), an- than-style collars (Fig. 11). Custom-made extend- orexia, and generalized anxiety (Fig. 10). In ers can be designed from the inner cardboard many veterinary hospitals, collaring an avian pa- support contained in rolls of flexible, cohesive ban- tient is an in-patient procedure. Owners are daging; the cardboard is cut circumferentially to the warned that multiple modifications may be required to find a functional, well-tolerated collar. If the bird does not immediately adapt to the

FIGURE 11. Types of commercially available avian collars include (from left to right) extenders, Elizabethan FIGURE 13. Note the padding goes beyond the edge of the cardboard collars, and spherical collars. to create tabs.

Rubinstein and Lightfoot/Journal of Exotic Pet Medicine 21 (2012), pp 219–234 229 FIGURE 16. Tabs are secured to one another (continued).

or “vests,” a spherical collar, or an extender alone may sufﬁce. Vests are fashioned from tubular FIGURE 14. Tabs are secured to one another. stretch-net bandaging material with holes cut out for the wings (Figs. 18 and 19). If an Elizabethan correct height, and then split vertically to allow it collar is required, attention must be paid to orien- to be applied around the neck (Figs. 12-17). Before tation. When placed with the opening directed cau- application, the cardboard is covered with layers of dally, mobility is compromised and the birds may the cohesive bandaging material for padding; the injure their wings on the collar edges. When placed bandaging material is left long, allowing overlap. with the opening directed cranially, the bird may These overlapping leaves are pressed together for be unable to eat and drink (Fig. 20). Note that the closure and secured with strips of fabric tape. use of collars without extenders can produce abra- Collars, regardless of type, must allow food to sions on the cervical skin. pass easily into the crop while still being snug Multiple pharmacological agents have been enough to prevent the bird from getting its lower advocated for use in behavioral disorders in beak underneath the collar. The speciﬁc type of birds, including FDB. Stereotypic and self-injuri- collaring used depends on the size of the bird, the ous behaviors have been shown to cause in- area requiring protection, and what the bird will creased activity at opioid receptors; it is suspected tolerate. A simple distraction may be enough to that the release of endogenous opioids activates prevent mutilation in some birds; fabric “ponchos” central dopaminergic systems, reinforcing the stereotypic behavior.73,77 Eventually, the behavior becomes gratifying in its own right, even when the initial stimulus is removed. Opioid blockade with receptor antagonists has been shown to be

FIGURE 15. Tabs are secured to one another (continued). FIGURE 17. Finally, the collar is secured with tape.

230 Rubinstein and Lightfoot/Journal of Exotic Pet Medicine 21 (2012), pp 219–234 FIGURE 18. Tubular stretch-net bandaging material with holes cut out for the wings. effective in treating self-injurious behavior in people, and as such has been advocated for treat- FIGURE 20. Collar placement must be tailored to the individual patient; ment of FDB.77,78 Although controlled, peer-re- downward-facing collars can cause immobility and wing trauma. viewed avian studies are lacking, in one small mutilating cockatoos, though side trial using the opioid antagonist naltrexone (pre- effects including sedation, depres- Although scribed at variable doses and durations), over sion, decreased appetite, and agita- three fourths of the birds appeared to respond to African gray tion were observed and considered treatment.79 A naltrexone dose of 1.5 mg/kg severe enough in some cases to dis- parrots and twice a day orally has been advocated, but phar- continue treatment. In addition, ex- macokinetic studies are lacking.80 Quaker tra-pyramidal side effects, often Antipsychotic drugs act as antagonists to dopa- noted in humans prescribed haloper- parakeets have minergic D receptors within the mesolimbic path- 2 idol, have been reported in birds.85,86 way causing a decrease in spontaneous movements, been Doses from 0.01 to 2.0 mg/kg have behavioral quieting, and, in people (and perhaps been published, including both oral documented to birds), a state of relative indifference to stressful situations termed ataraxia. Antipsychotics also have and injectable depot formulations, be at risk for but none of the doses are based on the ability to interrupt the endogenous opioid feed- disorientation back cycle; of these drugs haloperidol has received controlled studies and frequent dose the most attention in avian medicine.81-84 Haloperi- adjustments may be necessary. Al- and/or neuroses, dol is used most often for self-mutilation, as op- though African gray parrots and caution should posed to FDB. Several studies have documented a Quaker parakeets have been docu- decrease in injurious behaviors, especially in self- mented to be at risk for disorienta- be used when tion and/or neuroses, caution should be used when dosing haloperidol in dosing any species.87 haloperidol in Serotonergic agents used for the treatment of FDB are generally one any species. of two types; those having fairly spe- ciﬁc afﬁnity for presynaptic neurons, causing a selective blockade of the reuptake of serotonin in presynaptic neurons (selective serotonin reuptake inhibitors [SSRIs]), or the less selective tricyclic an- tidepressants (TCAs). TCAs inhibit the reuptake of not only serotonin but also, usually through the actions of their metabolites, norepinephrine, acetyl- choline, and histamine.88 Of the TCAs, clomipramine is the most commonly used in veterinary FIGURE 19. Proper application of a mesh vest. medicine. It is a serotonin-norepinephrine reuptake

Rubinstein and Lightfoot/Journal of Exotic Pet Medicine 21 (2012), pp 219–234 231 inhibitor and has been used extensively in small chogenic FDB is involved, a variety of enrichment animal medicine for behavioral disorders such as resources are available to create a more stimulating separation anxiety, urine marking, inappropriate environment. The owner should be counseled on barking, and destructive behavior. In psittacine basic behavioral modification techniques and pro- birds, a small, nonblinded prospective study vided with resources to continue gaining informa- showed that only 2 of 11 cockatoos exhibiting ei- tion. 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