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Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=cavp20 Avian Pathology ISSN: 0307-9457 (Print) 1465-3338 (Online) Journal homepage: http://www.tandfonline.com/loi/cavp20 The pathology of the avian integument: A review D.A. Pass To cite this article: D.A. Pass (1989) The pathology of the avian integument: A review, Avian Pathology, 18:1, 1-72, DOI: 10.1080/03079458908418580 To link to this article: https://doi.org/10.1080/03079458908418580 Published online: 12 Nov 2007. Submit your article to this journal Article views: 3531 View related articles Citing articles: 30 View citing articles

Transcript of ISSN: 0307-9457 (Print) 1465-3338 (Online) Journal homepage: …€¦ · View related articles...

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Full Terms & Conditions of access and use can be found athttp://www.tandfonline.com/action/journalInformation?journalCode=cavp20

Avian Pathology

ISSN: 0307-9457 (Print) 1465-3338 (Online) Journal homepage: http://www.tandfonline.com/loi/cavp20

The pathology of the avian integument: A review

D.A. Pass

To cite this article: D.A. Pass (1989) The pathology of the avian integument: A review, AvianPathology, 18:1, 1-72, DOI: 10.1080/03079458908418580

To link to this article: https://doi.org/10.1080/03079458908418580

Published online: 12 Nov 2007.

Submit your article to this journal

Article views: 3531

View related articles

Citing articles: 30 View citing articles

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Avian Pathology, 18: 1-72, 1989

THE PATHOLOGY OF THE AVIAN INTEGUMENT: A REVIEW

D.A. PASS

School of Veterinary Studies, Murdoch University,Murdoch, Western Australia, 6150

CONTENTSSummary 2

Introduction 2Structure of normal integument 3

Skin 3Feathers 5

Feather arrangements 5Feather structure 5Feather types 6Follicle and feather anatomy 7Feather development 8Colour of skin and feathers 9

Reactions of the skin to injury 9Definitions 9Inherited skin abnormalities 10

Avian ichthyosis 10Sclerodoma 10

Hyperplastic lesions 10Hyperplasia of foot-pad epidermis 10Pantothenic acid deficiency 11Zinc deficiency 11Avian poxvirus infection 12Cnemidocoptic mange 13Enlarged sternal bursa 13Miscellaneous hyperplastic conditions 13

Degeneration 14Inflammation of the skin 14

The inflammatory reaction 14Viral dermatitis 15Bacterial dermatitis 15

Received 18 February 1988Accepted 24 May 1988

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Mycotic dermatitis 17'Irritant' dermatitis 18Dermatitis due to ectoparasites 19Miscellaneous dermatitis 19

Parasitic skin disease 20Xanthomas and xanthomatosis . 20Neoplasia 21

Epithelial neoplasms 21Mesenchymal neoplasms 22Marek's disease 22

Diseases of feathers 24

Genetic or probable genetic feather disorders 24

Nutritional deficiencies 25

Clubbed down 25

Viral infections of feathers 26

Psittacine beak and feather disease (French m o u l t ) . . . . 27Reticuloendotheliosis virus infection 28Papovavirus infections 28

Toxins 29Feathering abnormalities associated with hormone deficiency. . . 30Abnormalities of unknown aetiology 30

Diseases of the beak 31

Acknowledgements 31

References 31

SUMMARYA review of the normal structure and the major pathological processesand disease entities of the avian integument is presented. The review hasbeen written primarily as a reference source for those involved in thepractice of veterinary pathology.

INTRODUCTION

Several excellent publications have been produced on the normal form and functionof the avian integument but there are few on the abnormal integument. To date,most reviews have been concerned primarily with the clinical presentation ofdisease (Altman, 1982; Harrison, 1984, 1986; Perry, 1987). This review has beenwritten with a bias towards the pathological appearance of conditions of theintegument. It is hoped that it will be an aid to those involved in the practice ofveterinary pathology.

Several entities that have been seen by the author but not described elsewhere, havebeen included. Comments on these entities would be welcome.

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Pathology of the integument 3

STRUCTURE OF NORMAL INTEGUMENT

SkinThe structure of the skin of birds has been described by Lucas and Stettenheim(1972), Hodges (1974), Spearman (1980) and Spearman and Hardy (1985) andsome physiological characteristics peculiar to avian skin have been reviewed bySpearman (1983).

The skin of birds has the same basic structure as that of mammals, namely an outerepidermis and inner dermis. Invaginations of the skin form feather follicles butthere are no glands associated with follicles as there are in mammals. The only trueglands of the skin are the uropygial or preen gland, glands of the ear canal andglands in the vent region.

Although there is a consistent structure to the dermis, the thickness of layers anddensity of connective tissue within layers varies considerably with site and species.For details the reader should consult Lucas and Stettenheim (1972). Essentially,the dermis is composed of superficial and deep layers, the deep layer being furtherdivided into an upper dense and lower looser layer. In the superficial layer collagenfibres are loosely arranged around numerous capillaries whereas in the deep layerscollagen fibres are arranged in interweaving bundles that run roughly at right anglesto each other and mostly horizontally to the skin surface. Adipose tissue, largerblood vessels, lymphatics, nerves, smooth muscle and the base of feather folliclesare found in the lower loose layer. Sensory nerve endings (Herbst corpuscles) occurthroughout the dermis, particularly associated with feather follicles. They are roundor ovoid lamellated structures with an outer capsule and a central nerve fibre.

The dermis is separated from the subcutis by a thin layer of elastic fibres. The sub-cutis is composed of haphazardly arranged collagen bundles and fat.

The basic structure of the epidermis is similar in all areas but the thickness variesconsiderably. Over most of the body it is extremely thin (Fig. 1), usually three tofive cells thick but it is much thicker over the naked parts of the legs (Fig. 2) andface. Two distinct layers of cells (keratinocytes) form the germinitive and cornifiedlayers of the epidermis. The germinitive layer is composed of basal, prickle-cell(stratum spinosum) and transitional layers but these are usually poorly defined insections. The transitional layer is equivalent to the stratum granulosum of mammalsbut keratohyalin granules are not obvious in sections stained with haematoxylinand eosin. Ultrastructurally, however, keratohyalin granules can be seen and failureto stain with haematoxylin is thought to be due to a lack of bound calcium(Spearman, 1983). The cornified layer is composed of sheets of keratinised, anuclear,flat cells that form lamellae separated by lipids. It is thickest in the skin of scales onthe legs and the plantar surface of the feet.

The dermo-epidermal junction is smooth in most areas of skin but is folded orforms distinct rete pegs in areas such as the base of the beak, cere, rictus and inparticular the digital pads (Lucas and Stettenheim, 1972). In all areas, basal cells siton a thin filamentous basal lamina that is anchored to the dermis by short pro-jecting fibrils that encircle collagen fibres of the dermis. The basal cells are an-chored to the basal lamina by hemidesmosomes.

During their upward migration from the basal layer to the outer cornified layer,keratinocytes undergo characteristic changes (Ackerman, 1978); they change shape

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from cuboidal to squamous, lose organelles, produce lipids and fibrous proteins(keratin), develop a thickened envelope beneath the cell membrane (Spearman andHardy, 1985), undergo cytolysis and dehydrate. In thin skin keratohyalin granulesare formed around the periphery of the cell (Matoltsy, 1969). They coalesce into afibrous-amorphous mass internal to the thickened envelope that forms concurrentlybeneath the cell membrane (Spearman and Hardy, 1985). It is not clear how theenvelope is formed but together with keratin it functions to give mechanical strengthto the cornified layer. In thick skin the process of keratin deposition differs (Hodges,1974). Keratin is formed on tonofibrils which coalesce into sheets that are arrangedparallel to the skin surface.

Avian keratinocytes are unique in that they produce lipids (Cane and Spearman,1967; Matoltsty, 1969; Lucas and Stettenheim, 1972; Freinkel, 1972; Lucas, 1980;Menon et al., 1981). Although there are few skin glands, the whole skin can-beconsidered to be an oil-producing holocrine gland and the term 'sebokeratocytes'(Wrench et al, 1980) has been applied to avian keratocytes. (Wrench et al. (1980)use 'keratocyte' synonymously with 'keratinocyte' and hence 'sebokeratocyte', not'sebokeratinocyte'. 'Keratinocyte' appears to be the accepted term for the keratin-producing epidermal cell (Ackerman, 1978). 'Keratocyte' or 'keratoblast' (Banks,1981) describes the specialised fibroblastic cells of the cornea.) More lipid is pro-duced in keratinocytes of thin skin than thick (Spearman and Hardy, 1985) andthere is also variation between areas of thin skin. In the chicken, for example,lipid production is greatest in areas that need to be kept supple such as the rictus ofthe beak, interdigital webs, comb and wattle (Lucas and Stettenheim, 1972). Thereis a progressive increase and coalescence of lipid droplets from the basal layerthrough to the cornified layer. Lipid is secreted through breaks in the cell mem-brane (Menon et al., 1981) as the cells cornify and as they flatten to form corneallaminae, lipid is sandwiched between the cells. The lipids are hydrophobic andtogether with sebum secreted from the uropygial gland form a thin film over thefeathers (Spearman and Hardy, 1985). This plays a role in waterproofing thefeathers, prevents feather keratin from drying out and becoming brittle and hasantifungal and antibacterial properties (Spearman and Hardy, 1985).

Scales, claws and beaks have a structure similar to that of the thick epidermis ofthe foot-pad but the keratin components are harder due to thicker layers of kera-tinised cells and the presence of free and keratin-bound calcium salts (Lucas andStettenheim, 1972). Scales are composed of curved plates of very compact epi-dermis. Sometimes the end of one scale overlaps the next (imbricated scales), butthe epidermis between the scales, the hinge epidermis, is thinner and softer toallow movement. The beak and claws have a very thickened stratum corneum com-posed largely of hard keratin. The hardness varies considerably with species and isexceptionally hard in large psittacine birds and softer in many waterbirds. Lucasand Stettenheim (1972) give details of the variations in birds.

Histologically (Fig. 3), the epidermis of the beak is typically arranged but theouter horny covering (rhamphotheca) is very thick and hard. The epidermis isthickest over the culmen (dorsal border) of the beak and the dermal-epidermaljunction is papillated so that dermal capillaries appear to penetrate the epidermisin sections. On the lateral surface, the epidermis is thinner and the dermal-epidermaljunction is smooth.

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Pathology of the integument 5

The structure of the comb (Fig. 4) and wattle are sufficiently similar to be con-sidered together. The epidermis of the comb is similar to thick skin. The dermis iscomposed of a superficial vascular layer, a wide intermediate layer and a deep colla-genous layer. Subcuticular fat separates the apposing dermal layers particularly at thebase. When the comb and wattle are red, the superficial dermis contains large sinuscapillaries immediately below the epidermis. Deeper in this layer, the size of capilla-ries decreases. The superficial layer merges into a wide intermediate or fibromucoidlayer composed of loose collagen and elastic fibres separated by a lightly stainingmucoid matrix. This layer ends rather abruptly on the deep collagenous layer.

The uropygial (preen) gland is bilobed, situated on the dorsal aspect of the baseof the tail and opens to the surface via a nipple. The gland is holocrine. Inter-nally, it is composed of long alveoli. The outer two thirds of an alveolus containsvacuolated cells, rich in lipid, in which nuclei degenerate and the cell ruptures torelease its contents. The cells in the inner third are more granular, contain moreglycogen but also release their secretion by cell breakdown (Hodges, 1974).

A sternal bursa is present in the subcutis on the ventral aspect of the keel of chic-kens and turkeys. The bursa develops with age. In the turkey (Miner etal, 1975a),it is first evident histologically from four to 12 weeks. The lining is composed of atypical synovial membrane thrown into folds at the edges, which is lined by cuboi-dal or squamous cells towards the edges. In the centre the lining may consist offibrous tissue and strands of connective tissue cross the lumen. With age, the wallthickens with connective tissue and by stratification of the mesothelium. Irritationenhances development of the bursa and stimulates hyperplasia of the lining andchronic inflammation in surrounding tissue.

FeathersThe arrangement, types, development, growth, structure and microscopic appearanceof feathers have been described by Lucas and Stettenheim (1972). The definitionsand descriptions of development and structure used here are taken from their text.

Feather arrangements. Lucas and Stettenheim (1972) describe four conditions:

Apterium: area of skin without feathers.

Pterylae: feather tracts.

Pterylosis: refers to the implantation point for each feather follicle inthe bird's skin.

Ptilosis: refers to the plumage in general, i.e. the size, shape andappearance of feathers.

Feather structure. The feather is composed basically of a shaft, vane and an after-feather.

Shaft or longitudinal axis of the feather composed of two parts, thescapus: calamus and rachis.

Calamus: short, tubular, unpigmented end of the mature feather thatis inserted in the feather follicle.

Rachis: long, solid portion, of the shaft above the skin. It is a thic-kened continuation of the mid-dorsal portion of the originalfeather tube distal to the calamus. The rachis contains pith

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which is composed of air-filled keratinised epithelial cellssurrounded by a solid keratinised outer cortex.

Vane or extended sides of the feather composed of individual barbs,vexillum: The vane is either described as plumulaceous (soft, downy)

or pennaceous (compact and closely knit).

Barbs: arise obliquely from the rachis and are composed of a ramus(shaft) and a vanule on each side. The vanule is a collectiveterm for all the barbules on one side of the ramus. The in-ternal structure of the ramus is the same as the rachis. Thebarbules are branches of the barb and are basically pro-jections of single cells. The barbules of plumulaceous barbsare variable in appearance but essentially have a nodal-internodal structure. The pennaceous barbules are morecomplex and differ in shape and complexity on the distaland proximal side of the ramus. Essentially, the cells of thedistal end of the distal barbules form hooks that lie over andhook onto the proximal barbules.

Afterfeather: a structure attached to the underside of a feather at thesuperior umbilicus. It may consist only of barbs or have ashaft (aftershaft or hyporachis) and plumulaceous barbs.

Pulp: mesodermal component of the growing feather consisting ofvascular connective tissue. The pulp regresses as the feathergrows and is absent in the mature feather.

Pulp caps: keratinising epidermis that covers the distal extremity of thepulp. As the pulp regresses the keratinised caps remain andare visible as horizontal bars crossing the lumen of thecalamus.

Feather types. Ten feather types are recognised.

Contour these are the predominant feathers covering the bird's body,feathers: They have a well-developed shaft, pennaceous and plumu-

laceous components of the vane and an afterfeather.

Coverts: refers mainly to rows of small contour feathers on the wings,tail and sometimes around the ears.

Remiges: large, stiff, well-developed flight feathers of the wings withan asymmetrical, entirely pennaceous vane and no aftershaftbut they do have an aftertuft of barbs. There are bothprimary and secondary remiges. Primaries (usually 10 andnumbered I-X from proximal to distal) arise from the skinover the manus (hand) and have an asymmetrical vane.Secondaries (usually 18 in the chicken and numbered 1-18distal to proximal) arise from the skin over the forearm andare more symmetrical.

Rectrices: large flight feathers of the tail with the same structure asremiges. In the chicken there are usually seven on each side.

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Pathology of the integum ent 7

Downs: small, fluffy wholly plumulaceous feathers with a very shortor absent rachis. There are two major types of downs, nataland definitive. Natal downs are present at or soon afterhatching (depending on the species) and in most species arereplaced by the first, or juvenal, contour feathers. Some birdshave semiplumes and a second set of downs before thejuvenal contour feathers. Definitive downs occur on variousparts of the body as part of the immature and adult plumage.Despite an apparent randomness, they are specifically arrangedin feather tracts and the pattern of distribution varies withspecies. For example they may be evenly distributed (e.g.parrots, waterbirds and hawks), sparsely or unevenly dis-tributed (e.g. gulls and shorebirds), confined to feathertracts, or confined to apteria (e.g. gallinaceous birds) orsparsely distributed in apteria or absent (e.g. pigeons andpasserines).

Powder specialised down feathers that disintegrate producing powderdowns: (keratin) that is spread through the feathers as a preening and

waterproofing agent. These feathers occur over the bodyamongst definitive down and contour feathers or in specificareas. They are not present in all birds.

Semiplumes: feathers with a long rachis and entirely plumulaceous vane.They occur in feather tracts of their own or along the marginsof contour feather tracts.

Bristles: stiff, tapered rachis with no barbs except at the proximalend. Usually found on the head, e.g. eyelashes.

Semibristles: feathers intermediate in structure between bristles and con-tour feathers.

Filoplumes: fine hair-like feathers with a long rachis and a tuft of barbson the tip. They are present in all feather tracts and generallyaccompany contour feathers in most species of birds.

Follicle and feather anatomy. Feather growth (anagen) occurs in cycles. During therest period (telogen) the feather remains anchored in the follicle and is held inplace by the tension exerted on the follicle by the feather muscles (Spearman andHardy, 1985), keratin bridges between the follicular and feather epidermis (Lucasand Stettenheim, 1973; Angel et al, 1982) and apposing concave and convexsurfaces of cells of the feather shaft and feather follicle respectively (Angel et al.,1982).

The regenerating feather grows upward from the dermal papilla pushing the oldfeather out (i.e. the process of moult) or replacing a feather that has been plucked.There are two basic components of the feather, the outer epidermis and the innerpulp (Figs. 5 and 6). The epidermis differentiates into the barb ridges (Fig. 7),rachis and hyporachis as it grows longitudinally. It also develops laterally from abasal layer to a keratinised layer which becomes the sheath. The follicle also deve-lops 'laterally' to form a stratified squamous keratinising epidermis but it develops

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towards the feather so that the two keratinised surfaces are apposed but eventuallyseparate towards the neck of the follicle.

The pulp also grows up with the epidermis and distally is covered by epidermis(pulp cap) (Fig. 8). As the rachis and barbs develop they are enclosed by thefeather sheath but as the tip of the feather fully keratinises and dries after emer-gence from the follicle the sheath starts to split distally allowing the rachis andbarbs to emerge and spread out. As this happens and the feather gows longitudi-nally the pulp regresses by degeneration and résorption of the connective tissues.The keratinised pulp cap remains, the new distal end of the pulp is re-epithelialisedand the process is repeated. Many distal pulp caps disintegrate as they are exposedbut others remain and are visible in the calamus. The calamus becomes completelykeratinised when longitudinal growth is completed. It sits on top of the dermalpapilla and does not contain pulp (Fig. 9).

Feather follicles lie obliquely or horizontally to the skin epidermis. Sections ofskin, therefore, cut across follicles and feathers in various planes and at differentlevels of feather development. The pathologist should appreciate, therefore, that insome follicles there may be a keratinised calamus and remnants of pulp caps,undifferentiated epidermal collar, barb ridges, barbule ridges, rachis and barbs, etc.

Degenerative changes in the pulp immediately below the pulp caps can be marked.Necrosis, oedema, haemorrhage and acute inflammation are common but largenumbers of lymphocytes, particularly deeper in the pulp or any form of inflam-mation deeper in the pulp is abnormal.

Feather development is complex and the order and timing of cell division andmigration is precise; factors that interrupt this development either by causing celldeath or decreased rate of replication or cell migration will produce changes inshape and colour or delay feather growth overall.

Feather development. Development of feathers in the chick embryo is first seen at5 days' incubation as condensations of mesenchyme and clusters of elongatedepidermal cells (placodes). The epidermal placode and condensation of dermal cellsbeneath it constitute the feather germ which ultimately form the feather follicleand feather. All of the follicles are formed in the embryo and persist throughoutlife.

The basal epithelial cells of the placode start to divide and form a new layer andvery early a stratum basale and stratum intermedium can be seen. Cell proliferationresults in the feather germ projecting upwards from the surface. Cell growth is morerapid on the anterior side so that the germ is bent caudally and the anterior sidebecomes dorsal. This is seen by the ninth day. By the 10th day, there is rapiddevelopment and cells of the intermediate layer begin to line up into barb ridges.By 11 days, the cells at the base of the germ move downwards into the dermisforming an invagination of epidermis. Differentiation in the invagination results inan outer follicular part and inner cylindrical feather tube. At the base of the feathergerm the epidermis thickens and forms a ring (epidermal collar) around the con-densed dermis (dermal papilla). The basement membrane of the outer featherfollicular epidermis is continuous with the inner surface of the feather tube. Thecylinder of pulp, encircled by the feather epidermis, resembles the dermis and has acentral (axial) artery.

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Pathology of the integument 9

A quotation from Lucas and Stettenheim (1972) is relevant to an understanding offeather development and interpretation of lesions in feathers: "Cell division occursmostly at the base of the feather germ and the parts differentiate as they moveupward. Accordingly, the distal and peripheral parts of a growing feather are morefully developed than the proximal and central parts. The tips of the barbs (and therachis, if any) are formed before the bases and, in feathers with a rachis, the barbsat the distal end are formed before those at the proximal end . . . Paradoxically,although the proximal and central parts of a growing feather are younger and lessfully developed than the parts beyond, they represent a later stage in the history ofthe feather as a whole. This sequence must be kept in mind for any study of factorsthat affect the appearance of the feather as a whole."

Colour of skin and feathers. Colour is due to pigments, structural conditions andcombinations of these (Lucas and Stettenheim, 1972). The pigments are melanins,carotenoids and prophyrins. Melanin is produced by melanocytes which migrateinto the epidermis during development. As in mammals, melanocyte processesbecome located between epidermal cells and melanin granules are taken up by theepidermal cells at a precise time in their development. Melanocytes are roughlytriangular eosinophilic cells and are obvious in the feathers and skin of darklypigmented birds because of their pigment but are also present in white birds thoughthey do not produce melanin. Melanins not only impart colour they also makefeathers denser and more resistant to wear and photochemical degredation.

Carotenoids (carotens and xanthophyll) are absorbed from the food and taken upby cells but uptake is genetically determined. Prophyrins are red and green pig-ments synthesised by the bird. Structural colours are produced by physical proper-ties of the surface of feathers that are capable of modifying or separating the com-ponents of white light. Iridescent colours change with the angle at which they areviewed.

REACTIONS OF THE SKIN TO INJURY

DefinitionsThe following definitions will be used in this review:

Acanthosis - hyperplasia of the cells of the stratum germinitivum.

Acantholysis - loss of cohesion between epidermal cells that leads to formation ofintraepidermal clefts, vesicles and bullae.

Ballooning degeneration - intracellular fluid accumulation.

Dyskeratosis - prematurely and therefore faultily cornified cells having eosinophiliccytoplasm and small, darkly staining nuclei.

Hyperkeratosis - increased thickness of the cornified layer.

Macule - flat discolouration of the skin.

Papule - solid, elevated lesion.

Parakeratosis - hyperkeratosis in which pyknotic nuclei are retained in the cells ofthe cornified layer.

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Spongiosis (intercellular oedema) - oedema between the prickle cells results inwidening of the intercellular spaces and a spongy appearance. Severespongiosis may lead to formation of intraepidermal bullae.

Inherited skin abnormalitiesAvian ichthyosis. This occurs as an autosomal recessive trait in chickens (Abbottand Sawyer, 1974; Renden and Abbott, 1980). The disease is characterised bythickened irregular patches of skin, stiff wiry down feathers and a greasy exudate athatching. Birds may lose digits, viability is reduced and sexual maturity is delayed.Histologically, the epidermis is up to four times normal thickness due to acanthosisand hyperkeratosis.

Scleroderma. Scleroderma has been reported as an inherited spontaneous auto-immune disease of a line of White Leghorn chickens (Gershwin et al, 1981 ; van deWater and Gershwin, 1985). The chicks are normal at hatching but from 1 to 2weeks of age 90% of birds develop erythema, oedema, necrosis and subsequent lossof the comb and joint swelling. From 4 to 6 weeks lesions appear on the skin of theback of the neck and in the oesophagus, small intestine, lung, kidney, heart andtestes. Grossly, the skin swells, loses feathers and becomes indurated. Histologically,mononuclear cells infiltrate all layers of the dermis, subcutis and underlying muscleand there is marked vascular proliferation and intense collagen deposition. Thicken-ing of the muscular wall and intimai proliferation occludes small arterioles and thisproduces ischaemia causing the comb and digits to slough. Antibodies to a numberof tissue components such as components of cytoplasmic skeleton, nuclei and type11 collagen can be detected in the blood.Hyperplastic lesionsHyperplasia of foot-pad epidermis. Proliferative lesions of the skin of the foot-pad(Fig. 10) in poultry are relatively common and often result in lameness. Outwardly,at least initially, lesions on the foot-pads are similar irrespective of the cause andconsist of horny proliferation of the epidermis accompanied by enlargement ofthe pad. Inflammation and ulcération are common in commercial situations andthis produces enlargement of the feet and at this stage the lesion is more correctlytermed pododermatitis.

This type of lesion has been associated with biotin deficiency (Patricke?al, 1942;Harms and Simpson, 1975; Harms et al, 1977; Frigg and Torhorst, 1980) and wetlitter (Harms and Simpson, 1975; Martland, 1984, 1985) in chickens and turkeys.Similar lesions are also associated with rough, or excessively smooth, perches andconcrete flooring (personal observations) and dietary factors other than biotin, inparticular methionine deficiency (Chavez and Kratzer, 1974; Murillo and Jensen,1976). Heavy birds, hence males, appear to develop more severe lesions thanlighter birds.

The skin lesions of biotin deficiency occur on the commissures of the beak and thefeet where they are most obvious on the weight bearing plantar foot-pads, particu-larly the metatarsal pad (Patrick et al, 1942; Harms and Simpson, 1975; Harms etal, 1977; Frigg and Torhorst, 1980). Minor lesions do occur, however, on the non-weight bearing surfaces. Hyperplasia of the epidermis is the major lesion. Histo-logically, there is acanthosis resulting in upward papillary growth and hyper-keratosis but minimal or absent parakeratosis (Frigg and Torhorst, 1980). Hyper-plasia of the germinitive layers is evident by enlarged nuclei and nucleoli, increased

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Pathology of the integument 11

cytoplasmic basophilia and more mitotic figures than normal. There is also anapparent increased vascularity and dermal vessels are engorged. The lesions areenhanced if birds are on litter (Harms and Simpson, 1975; Harms et al, 1977),particularly if it is damp. Erosion, ulcération, and inflammation ensue.

The pathogenesis of biotin-induced hyperplasia is not known but the relationshipbetween biotin, fatty acid synthesis and lipid production in keratinocytes may beworthy of investigation.

The pathogeneisis of the lesion induced by wet litter is not clear but appears to beassociated with irritants in the faeces or litter or both. Lesions are most prominenton the metatarsal pads but also occur on other pads, inter-pad epidermis, plantarsurface of the hocks and sternum. There seems to be no sex or weight relationshipin this condition. In the foot pads, the lesion starts as hyperplasia of the epidermisaround the periphery which is seen as horny papillary growths. The hyperplasiathen spreads across the pads but there is concommitant ulcération and inflam-mation around the ulcer. Histologically, the mildest lesions are inflammatory andconsist of infiltration of heterophils in the germinative layers and defective areas ofpoor keratinisation judged by poorly stained stratum corneum. As the lesionadvances, papillae form due to acanthosis and hyperkeratosis. At the tips of thepapillae, keratinisation is often defective and nuclear remnants may exist withinthe poorly stained areas. Heterophils accumulate in the transitional layer and bal-looning degeneration and necrosis of prickle cells results in microvesicle formation.Progressive necrosis, ulcération and defective keratinisation occur. Bacteria pro-liferate in the stratum corneum, the ulcerated areas fill up with cellular scabs anddermal inflammation, granulation tissue and ultimately fibrosis, accompany theepidermal changes.

Hyperkeratotic, wart-like lesions occur on the digital and metatarsal pads of cage-layers (Simonson et al., 1980; Burger arid Arscott, 1984). Histologically, there isaccentuation of the normal papillary pattern of the epidermis, acanthosis andhyperkeratosis (personal observation).Ulceration, splitting and secondary bacterialinfection may occur but the lesion is not as severe as that seen on wet litter.

Proliferative, warty lesions induced by poxvirus infection but similar in appearanceto those induced by irritation, have been described on the plantar surface of thefeet of a common golden eye (Bucephala clangulà) by Wobeser (1981).

Pantothenic acid deficiency. The lesions produced in experimental pantothenicacid deficiency have been described by Ram (1949). At levels of less than 5.5 jug/gof diet thickening and fissuring lesions occur on the skin of the rictus of the beak,eyelids, toes, web and distal tarsometatarsus. Histologically, hyperkeratosis andparakeratosis accompanied by heterophil infiltration and mild dermal oedema havebeen described. Parakeratosis is rarely described as a lesion in avian skin and onewonders whether the original interpretation was correct.

Zinc deficiency. Zinc deficiency has been reported in chickens (O'Dell et al,1958; Young et al, 1958), turkeys (Kratzer et al, 1958), pheasants (Scott et al,1959), Japanese quail (Spivey Fox and Harrison, 1964) and ducks (Wight andDewar, 1976). Most descriptions are based on experimental studies as naturallyoccurring deficiency is uncommon. Generally, affected birds have reduced growthrate, shortening and thickening of long bones, enlargement of the hocks, poor

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12 D.A.Pass

feathering and skin lesions. The feather lesions are discussed under Nutritionaldiseases of feathers. In chickens, skin lesions consist of hyperkeratosis and mildacanthosis of the feet and rictus of the beak (O'Dell et al., 1958). The epidermismay be seven to eight cells wide instead of the normal three to five cells but thereis no apparent increase in mitotic activity in the basal cell layer. Hyperkeratosisalso involves feather follicles and results in atrophy of follicles and feathers orfailure of feather development. Follicles are eventually replaced by fibrous tissue.

In ducks (Wight and Dewar, 1976), the gross changes consist of thick 'caseous'material attached to the posterior surface of the tongue and larynx, blockage ofnares by dried debris, caseous exudate in sinuses, mild ventral flexure of the beakand thickening, fissuring and inflammation of rictal skin. On the feet, there isexfoliation of keratin on the interdigital webs, and occasionally erythematousmacules and thickened patches covered by fissures and brown crusts. The plantarsurface of the digits becomes thickened, fissured and encrusted. Histological changesoccur in stratified squamous epithelia of the skin, mouth, oesophagus and larynx.In the skin, lesions occur in the epidermis although dermal inflammation, as a con-sequence of ulcération and bacterial infection, is not unknown. The basic lesionappears in the deep prickle cells adjacent to the basal layer. The epidermal lesionsconsist, in their mildest form, of atrophy of the germinative layers of cells and arelatively thickened stratum corneum. However, acanthosis and hyperkeratosis areprominent features. The basal cells enlarge and resemble prickle cells so that thebasic epidermal architecture is lost. Mitotic activity increases in the deep pricklecell layers rather than the basal layers. Spongiosis of the epidermis and ballooningdegeneration, dyskeratosis and acantholysis of individual keratinocytes occur.Degeneration of groups of prickle cells produce small bullae in which acantholyticcells and heterophils are seen. Heterophils are present diffusely through the epi-dermis and in addition to accumulating in bullae also accumulate between layers ofthe stratum corneum producing an overall increased cellularity. This leads to thethickened caseous crusty lesions seen grossly. In some cases hyperplasia of the basalcells produce long narrow rete pegs in the dermis.

Avian poxvirus infection. Avipoxvirus infections are common and the disease indomestic poultry (Tripathy and Cunningham, 1984), wild birds (Kirmse, 1969;Karstad, 1971; Wobeser, 1981) and caged and aviary birds (Clubb, 1986; Gerlach,1986) has been reviewed. Infection may result in lesions on the skin (Fig. 11) andmucous membranes but small passerines may die during the viraemic stage withoutevidence of typical lesions. Lesions on the skin occur most commonly on un-feathered areas but in severe infections they may be found over the entire body.The gross appearance varies with the age of the lesion and whether or not there issecondary infection with bacteria or fungi. Initially the lesions are small papuleswhich develop a crusty surface within a few days. Lesions commonly coalesce sothat large areas of skin are thickened and rough.

The basic change in the epidermis is hyperplasia and hypertrophy of prickle cells.The diagnostic feature is the presence of eosinophilic intracytoplasmic inclusionbodies which on HE sections often appear fragmented (Fig. 12). Necrosis of cells,particularly towards the centre of the lesion, and inflammation on the surface arecommon. Large crusts of necrotic cells, degenerate heterophils, bacteria and fungimay cover the lesion. Regression of the lesions occurs but there is considerable

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Pathology of the integument 13

variation in the time that they persist (Karstad, 1971). Both intracytoplasmic andintranuclear inclusion bodies have been described in avian pox virus infection of aslate-coloured junco (Junco hyemalis) (Goodpasture and Anderson, 1962). Theintranuclear inclusions were eosinophilic, smooth, compact, oval and surrounded bya clear halo. Electronmicroscopically, they were composed of branching, irregular,intertwining filaments but did not contain virions (Beaver and Cheatham, 1963).

Cnemidocoptic mange. Numerous species of Cnemidocoptes parasitise the skin ofbirds (Loomis, 1984). Those most commonly seen are C. mutans, the scaley-legmite of poultry, and C. pilae, the cause of scaley-face and scaley-leg of budgerigarsand 'tassle-foot' of canaries. These mites spend their entire life-cycle on the birdand apparently are transmitted directly from bird to bird. Lesions are normally seenon the featherless areas of the face (Fig. 13) and legs as scaley, hyperkeratoticencrustations that may encroach on the beak or claws. Minute pores are visible onthe surface. The mite burrows into the stratum corneum and stimulates hyperplasiaand hyperkeratosis (Yunker and Ishak, 1957). In some birds, inflammation in thedermis and accumulation of heterophils and vesiculation in the germinative layeraccompany the hyperplasia (Fig. 14). Atrophy of epidermis around mites mayoccur, giving an impression that the mite is in contact with the dermal tissues (Fig.15). This is seen when the normally thin skin of feathered areas becomes infectedafter feather loss as occurs, for example, in psittacine beak and feather disease (seeDiseases of feathers).

Enlarged sternal bursa. Enlargement of the sternal bursa (ESB) in chickens and tur-keys occurs primarily from continual irritation due to pressure or friction on theanterior keel (Miner and Smart, 1975). Development of ESB is, however, influencedby sex (males greater than females), strain of bird {e.g. lighter breeds develop fewerESBs), conformation, amount and completeness of feather cover over the bursa,growth rate and management practices, particularly those related to floor type andhardness (Miner and Smart, 1975). In chickens and turkeys, ESBs usually developfrom 9 to 12 weeks and 11 weeks onwards, respectively. The volume of serousfluid in the bursa increases and the wall thickens. This thickening is first evidenthistologically as focal increases in matrix and collagen fibres of the connectivetissue wall of the lateral folds (Miner et ah, 1975b). The connective tissue thicke-ning becomes more generalised as the bursa enlarges and lining cells round up andstratify. Inflammatory infiltrates and haemorrhage within the wall and free-floatinglumps of connective tissue covered by lining cells may also be seen. Infection ofthe bursa with staphylococci, Mycoplasma gallisepticum (Domermuth, 1962) andM. synoviae (Olson, 1984) may also occur.

Miscellaneous hyperplastic conditions. 'Brown hypertrophy' of the cere occurs, notuncommonly in budgerigars, particularly females. The lesion consists of hyper-keratosis of the cere epidermis. It is a benign condition of unknown aetiology.

Localised areas of hyperkeratosis, or 'cutaneous horns', have been described inDeshi fowl in India (Paikne and Dabre, 1981). The horns have a fibrovascular corewith a small cartilagenous plate at the base and are covered by acanthotic andhyperkeratotic epidermis. The aetiology is unknown.

Superficial fungal infection may also cause hyperkeratosis without significantinflammation (Fig. 16).

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14 DA. Pass

An unusual unreported hyperkeratotic skin disease occurred on two layer farms inWestern Australia in November and December, 1983. In both cases, the birds werefrom the same hatchery and had been reared to 18 weeks by the same pulletrearer. The birds had been vaccinated for fowl pox and infectious laryngotracheitis,were housed on slatted floored sheds and were supplied by feed from the same mill.Skin lesions were noted from about 24 weeks of age. The flocks were slow to comeinto lay and affected birds had small, pale combs and were not in lay. About 10%of birds in the flock were affected. Lesions were present only on the feathered partsof the skin. Feather loss was not noted. The lesions consisted of increased skinthickness and scurfiness (Fig. 17) and varied from mild, where the lesion was seenonly on close inspection to severe where the skin was thrown into thick, firm folds(Fig. 18). Microscopical changes included acanthosis, hyperkeratosis, acantholysis,spongiosis, necrosis of individual and groups of keratinocytes and bullous formationof the epidermis of skin and feather follicles (Fig. 19). Heterophil infiltration wasseen in association with epidermal cell necrosis and chronic inflammation anddermal oedema was prominent in some cases. The cause of the lesion and whether itwas primarily epidermal or dermal in nature was not determined. Superficially,fungal infection or zinc deficiency was suspected but neither was confirmed.Several birds had a high (20 to 35%) eosinophil count in peripheral blood, sug-gesting an allergic aetiology.

DegenerationDegenerative changes accompany hyperplastic and inflammatory lesions but purelydegenerative conditions occur rarely. Ballooning degeneration of prickle cells,acanthosis and hyperkeratosis of the skin epidermis occurs in budgerigar fledglingdisease. The disease is due to a papovavirus infection and is discussed further underDiseases of feathers.

Inflammation of the skinThe inflammatory reaction. Inflammation in the chicken skin has been studiedusing irritant {e.g. turpentine), infectious {e.g. staphylococci), non-infectious butimmunogenic {e.g. Freund's complete adjuvant) and particulate, relatively immuno-logically inert {e.g. talc) materials. The qualitative nature of the reaction is the sameirrespective of the stimulus. The following description has been assembled fromwork of Carlson and Allen (1969) and Nair (1973).

Within 30 min of stimulation, venules are dilated and contain large numbers ofheterophils, monocytes and basophils. In the first 3 hours, there is migration ofheterophils and monocytes which persist for some hours. Basophil migration alsooccurs. It is most noticeable between 3 and 6 hours, but the cells degranulate anddisappear after a few hours. From 6 hours, lymphocytes appear as eccentric cuffsaround vessels. The numbers gradually increase so that they are pronounced by24 hours and may dominate the reaction by 2 to 3 days. Morphological changesoccur within monocytes shortly after migration and they become recognisable asmacrophages, epithelioid and giant cells, if the stimulus is appropriate. Giant cellsand epithelioid cells are prominent in reactions due to agents normally associatedwith delayed hypersensitivity {e.g. Mycobacteria and Freund's complete adjuvant),and around areas of necrosis. Giant cells, which form from fusion of marcophages,and epithelioid cells may be recognisable by 12 hours and can be well developedand obvious as distinct granulomas by 24 to 28 hours. Some fibroplasia is evident

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Pathology of the integument 15

by 2 days around granulomas and gradually increases so that it is prominent by 7to 10 days.

Plasma cell development is seen in 2 to 3 days with immunogenic agents but isscanty in response to other agents. Eosinophils are not a feature of the acute in-flammatory reaction even in response to parasites. However, they are reported toaccount for 20 to 30% of the polymorphonuclear granulocytes in the exudate inresponse to 2,4-dinitrochlorobenzene (Awadhiya et al, 1982), an agent used tostimulate delayed hypersensitivity, and in response to injection of phytohaemag-glutinin(McCorklee?a/., 1980).

Experimentally induced type 3 hypersensitivity (Arthus reaction) has been de-scribed in chicken skin (Dhodapkar etal, 1983). Inflammation occurs as a result ofantigen-antibody complexes adhering to the endothelium which activates comple-ment and this attracts polymorphonuclear cells. The inflammatory reaction is thesame as that described above for acute inflammation except that haemorrhage,fibrinoid necrosis of venule walls and thrombosis accompany the cellular migration.In 6 to 8 hours, haemorrhage and necrosis are prominent and necrosis is progressiveover 2 to 3 days.Viral dermatitis. Acute, mild multifocal to severe, diffuse necrotising dermal infla-mmation (Fig. 20), oedema, haemorrhage, subepidermal bullae and focal epidermalvesicles in the wattles have been described in virulent avian influenza virus infection(Acland et al, 1984). Skin lesions have also been described in chickens infectedwith highly virulent, velogenic Newcastle disease virus (Cheville et al, 1972).Diffuse congestion and petechiation of the skin, oedema of the face and eyelidsand microvesicles, haemorrhagic ulcers and bullae on the combs occur. Histolo-gically, hydropic degeneration of epidermal cells, epidermal microvesicles andvasculitis are seen.

A coronavirus, in association with E. coli, is believed to be responsible for a facialcellulitis (swollen head syndrome) in broilers (Morley and Thompson, 1984). Thedisease is characterised by hyperaemia of conjunctivae and subcutaneous oedemaand a purulent exudate in the subcutis of the skin of the head. Histologically, thereis oedema, heterophil infiltration and lymphoid hyperplasia.

Nodular, granulomatous dermatitis occasionally accompanies feather lesions ofpsittacine beak and feather disease (PBFD) in lovebirds and galahs (Pass and Perry,1984, 1987). The nodules (Fig. 21) are comprised largely of macrophages andlymphocytes and are usually situated adjacent to feather follicles. Very occasionally,the cells surround a ruptured follicle. Aggregates of 20 nm virus-like particles,identical to those seen in feather epidermis of birds with PBFD, can be found incells of the nodules. It is presumed that these are the cause of the nodular lesions.

Bacterial dermatitis. Inflammation of the wattles with resultant swelling is a charac-teristic lesion in Pasteurella multocida (fowl cholera) infection but identical lesionsoccur with staphylococcal and E. coli infections. The source of infection in thelatter is often a wound. These lesions consist of a large area of caseous inflam-matory exudate surrounded by granulation tissue or multifocal granulomatousinflammation throughout the wattles.

Staphylococcal dermatitis occurs occasionally in birds and may involve featherfollicles in addition to the interfollicular skin. There is nothing characteristic about

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16 D .A. Pass

these lesions. In broiler chickens the incidence of infection has been shown to berelated to housing, for example, May et al. (1982) demonstrated a higher incidenceof disease in broilers reared on plastic mats compared with those kept on litterand Bayer et al. (1976) described a high incidence in broilers reared in cages withwooden slats.

Acute, exudative dermatitis, particularly of the head and neck, has been describedin broiler breeder chickens (Froyman et al, 1982). The subcutaneous tissues wereswollen with sero-sanguinous exudate from which pure cultures of Staphylococcusaureus were isolated. Birds died of septicaemia. Outbreaks of acute vesicular der-matitis of the comb, wattles, face, feet and shanks from which staphylococci wereisolated and which was experimentally reproducible using the bacteria isolated wasdescribed in White Leghorns by Hoffman (1939).

Caseous dermatitis and inflammation of the subcuticular fat (panniculitis) of theloose, fatty skin adjacent and ventral to the cloaca due to E. coli infection is seenoccasionally in association with E. coli septicaemia in broilers (personal observa-tions). The lesions consist of diffuse inflammation and large necrotic granulomassurrounded by macrophages and giant cells. Randall et al. (1984a) have describedtwo forms of dermatitis in broilers associated with infection with E. coli or P.multocida. The lesions have a unique feature in that they occur only on one side ofthe bird. In the mildest form, dermatitis occurs on the anterolateral aspect of thethigh below the femorotibial joint. The skin is faint, but bright yellow and purulentexudate is present in the subcutis. Histologically, there is acute inflammation of thedermis and subcutis and in more chronic cases, granulation tissue. Gram negativebacteria, which culturally are E. coli, are seen in the lesions. A more severe formalso occurs that generally affects the thigh but lesions also occur on the back orflank. The affected skin is raised and either dull yellow or reddish-brown due toscab formation. Histologically, the inflammation is more severe and walled off areasof necrotic debris may be present in the subcutis. The epidermis is not affected butareas of dermis covered by intact epidermis may be shed. E. coli or P. multocidahave been isolated from the more severe lesion.

Gangrenous dermatitis of chickens and turkeys is caused by infection with eitherQostridium septicum or S. aureus alone or in combination (Frazier et al, 1964;Saunders and Bickford, 1965). C. perfringens type A (Saunders and Bickford,1965) and E. coli, Proteus sp, Streptococcus fecalis and Bacillus sp (Frazier et al,1964) may also be isolated from the lesions. The disease occurs most commonly inbroiler chickens, particularly those that have no maternal antibody to infectiousbursal disease (IBD) virus (Rosenberger et al., 1975) and are subsequently chal-lenged by that virus. Wound infections may also occur. Lesions consist of black,purple or dark greenish discoloration of the skin and sero-sanguinous, sometimesgassy exudation into the subcutis of any area of skin but particularly the wing tips,thighs and abdomen. Feathers fall out or are removed easily. Histologically, there isnecrosis of the skin, accumulation of fluid and extravasated erythrocytes in thesubcutis and underlying muscle and myocyte necrosis. Bacteria are present in thelesion. Necrotic dermatitis has also been described in broiler chickens from whichE. coli, Proteus sp and S. aureus were isolated (Howell et al, 1982). Histologicalexamination revealed folliculitis and bacterial infection of the epidermis but clos-tridia were not seen in section. The birds had thymic atrophy and had serologicalevidence of reticuloendotheliosis virus infection but not IBD virus infection.

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Gangrenous dermatitis has also been described as a complication of a haemorrhagiccondition of chickens termed 'blue wing disease' (Engström and Luthman, 1984).This disease is an acute, fatal condition that is seen predominantly in 2- to 4-week-old broilers in which there are intracutaneous, subcutaneous and intramuscularhaemorrhages of the wing tips and occasionally the legs, toes, under the mandibleand breast. Randall et al (1984b) have also noted the occurrence of gangrenousdermatitis as part of a complex of multiple bacterial infection in broiler chickens.In this complex, they also described birds with severe conjunctivitis, subcutaneousoedema of the head from which Pseudomonas sp. were isolated and oedema of thefeet in which large numbers of Gram-negative bacteria were seen in section.

Severe subcutaneous oedema of the face, legs and feet of broiler breeder cockerels,from which pure culture of Pseudomonas aeruginosa have been isolated, has beenseen by the author. The skin of acutely affected birds was swollen and pale (Fig.22) but hyperaemia and induration occurred as the lesion aged. In many cases, theinfection was believed to be associated with a wound but in others no obvious siteof infection was seen. Microscopically, in acute cases, extreme oedema, necrosisof all components of the skin, including blood vessels, and myriads of Gram-negative bacteria are seen (Fig. 23). Inflammatory cells are noticeably absent. Thereaction in longer standing cases is similar to that seen in other bacterial infectionsof the skin. Some birds survived the acute infection but others died of septicaemia.

Mycotic dermatitis. Inflammation due to infection with dermatophytes, Candidaalbicans, yeasts of the genus Rhodotorula and Aspergillus have been described.Hyperkeratosis associated with fungal infection, which is often the main lesion, hasbeen mentioned under Hyperplasia.

Dermatitis of feathered skin due to infection with Rholotorula mucilaginosa(Beemer et al, 1970) and R. glutins (Page et al, 1976) has been reported in broi-lers. Affected skin is thickened and yellowish brown. Histologically, focal, multi-focal or diffuse areas of ulcération over acute inflammation of the dermis has beendescribed.

The skin in Aspergillus sp. or Mucor sp. infection is white, thickened and scaley(Fig. 24) although green discoloration of the surface has been described in Asper-gillus infection (Abour-Gabel and Malik, 1978). Histologically, there is acanthosisand hyperkeratosis with fungal hyphae present in the cornified layers (Fig. 25).Necrosis of the transitional and outer prickle cells may be apparent and infiltrationof the dermis with heterophils, intraepidermal vesicles that contain heterophilsand acute heterophilic dermatitis may be present. Hyphae will penetrate the epi-dermis and stimulate an intense inflammatory response. Similar reactions occur inthe feather follicle and feather epidermis.

The dermatophyte Microsporum (Trichophyton) gallinae, causes the clinical con-dition of Favus in birds (Chute, 1984; Fonseca and Mendoza, 1984). Lesions aremost prominent on the comb, wattles and skin of the head but they do occurelsewhere. The disease is uncommon. Histologie lesions consist of acanthosis andhyperkeratosis, the dermatophytes being visible in the hyperkeratotic layers. Ex-perimental infection of chickens with Trichophyton mentagrophytes (Christopher,1979) has revealed that infection can only be induced by inoculation of skin iffeathers have been removed. Nodular, hyperkeratotic lesions, associated with mild

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inflammation and lysis of keratin in feather follicles and destruction of featherfollicles, was reported.

Fungal infections of the feather and skin epidermis, which are believed to beDermatophytes have been seen by the author in Gouldian finches, {Erythruragouldiae) (Fig. 26) and Java sparrows (Padda oryzivora). Feather loss, the presenceof short hyperkeratotic feathers and mild hyperkeratosis of the epidermis are themajor signs. Microscopically, there is mild acanthosis and hyperkeratosis of the skinepidermis. Feathers are present in follicles but they appear to have stopped growingand consist predominantly of a very hyperkeratotic epidermis around a poorlydeveloped pulp. Spores (Fig. 27) or short, branching septate hyphae (Fig. 28) areseen within the keratinised layers. Inflammation of the skin is either not present orvery mild but in one case examined necrosis of cells in the outer layers of the stra-tum germinitivum of feathers and necrosis and infiltration of heterophils, plasmacells and lymphocytes in the pulp were seen. The fungi have not been identified.

Candida albicans has been described as a cause of dermatitis on the back of chic-kens (Kuttin et al., 1976). Microscopical changes consisted of epidermal necrosisand inflammation. Spores and pseudo-hyphae were visible in comified areas and innecrotic tissue. Combined C. albicans and A flavus infection has been associatedwith a nodular, granulomatous dermatitis in chickens (Mohammed etal, 1980).

Mycotic infection of the feathers has been incriminated in pruritis and feather lossin pigeons and psittacine birds (Tudor, 1983). Numerous species of fungi wereisolated from the calamus of feathers and birds responded to topical antifungaltherapy.

'Irritant' dermatitis. Contact dermatitis of broilers characterised by inflammation,erosions and ulcération of skin at points that come in contact with the ground inaddition to the foot-pads, has been described in broiler chickens (Green et al.,1985). The lesions occur in association with wet or sticky litter and the severity oflesions increases with the time the bird is in contact with the litter. Changes aresimilar to the hyperplastic, ulcerative lesions on foot-pads described under Hyper-plastic lesions but hyperplasia is not a constant feature. The pathogenesis is notclear but in both conditions it is probably similar. Lesions occur on the plantarsurface of the feet, posterior aspect of the hocks and the breast where in some casesthey are closely associated with feather follicles in the sternal feather tracts. Be-cause of their ulcerative nature, they have been referred to as 'breast burns'. Theearliest changes consist of basophilic debris in the keratin layers of epidermis,diffuse infiltration of the dermis with heterophils, localised sub-epidermal foci ofheterophils and a light infiltrate in the epidermis. As the lesion progresses, foci ofheterophils accumulate in vacuoles in the epidermis and epidermal cells mustdegenerate as erosion down to the basal cells occurs. Hyperplasia may or may notbe present. Ulcers are filled with inflammatory debris and inflammation in thedermis is severe.

Dermatitis of the hip and thigh of broilers (scabby-hip) has been described byHarris et al. (1978). This condition is directly related to stocking density andoccurs in birds housed in cages and on litter. The lesions occur on the featheredskin and consist of linear scab-covered scratches and circular dry scabs betweenfeather follicles and at the entrance of feather follicles. Histologically, some lesions

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consist of inflammatory debris within the cornified layers and minimal inflamma-tion. In others, ulcération and inflammation are present. Colonies of Gram-positivecocci are present in the overlying debris. The pathogenesis is believed to be asso-ciated with contact and trauma to the skin from other birds and secondary infec-tion.Dermatitis due to ectoparasites. Infection due to Cnemidocoptes sp. has been dis-cussed above under Hyperplastic lesions. Infection with the larvae of trombiculid(harvest, chigger) mites has been recognised in canaries (Pass and Jue Sue, 1983)and pigeons, budgerigars and other psittacine birds (Pass, unpublished). Clinicalsigns consist of non-pruritic, oedematous swellings of the skin of the legs dorsal tothe hocks and in some cases abdominal and thoracic skin (Fig. 29). The swellingspersist for weeks and become fibrotic during regression. The reaction microscopi-cally consists of massive subcutaneous oedema, areas of intense acute inflammationand perivascular accumulation of lymphocytes. The areas of acute inflammation areassociated with the attachment of larvae. At the point of attachment, there isnecrosis of epidermis, deposition of an amorphous eosinophilic material, infiltra-tion of heterophils and necrosis of blood vessel walls (Fig. 30). The mites areoften enclosed within the skin due to swelling of the skin around the mite, giving afalse impression that they are in feather follicles. Secondary bacterial infection ofthe affected skin may occur.

Miscellaneous dermatitis. Photodynamic dermatitis of the unfeathered skin ofchickens, turkeys, ducks and geese have been described as a result of ingestion ofseeds or leaves of members of the family Umbelliferae (Ammi mafus, A. visnaga,Cymopterus watsonii) (Trenchi, 1960; Williams and Binns, 1968; Van Kampen etal, 1969; Egyed et al, 1974; Schlosberg et al, 1974). The signs of acute inflam-mation are erythema, oedema, small vesicles that often coalesce, exudation ofserous fluid and in some cases haemorrhage and fissuring of the affected area. Thesuperficial epidermis sloughs and is replaced by dried scabby exudate. In chickensthe comb may slough. Chronic lesions consist of shortening and deformity of thebeak, contracture and deformities of the eyelids such as adhesions between thelids or eyeball, and deviation or loss of toes (Van Kampen et al, 1969; Egyed etal, 1975a, b; Egyed and Williams, 1977). The chronic effects are said to be due tovascular lesions induced during the acute phase (Van Kampen et al, 1969) andchronic fibrosis, and are more severe in soft-billed waterfowl than the hard-beakedgallinaceous birds. Photodynamic dermatitis in turkeys due to ingestion of buck-wheat (Faddoul and Fellows, 1958, cited by Peckham, 1984) and in pheasantsdue to phenothiazine toxicity (Clapham, 1950) have also been reported.

Facial oedema and thickening of the skin in association with eosinophilia has beenreported from caged chickens in an experimental flock (Maxwell et al, 1979).The cause is unknown.Dermatitis of the eyelids and conjunctivitis have been produced in experimentalinfection of chickens with Plasmodium gallinaceum (Al-Dabagh, 1961). Photo-phobia, serous ocular discharge, congestion and oedema of the eyelids followed byfocal then confluent necrosis of the skin of the eyelids are the predominant signs.Histologically, acute inflammation, haemorrhage, necrosis of epidermis and brownmalaria pigment in macrophages was described. It was suggested that the lesion wasdue to induced pantothenic acid deficiency as a result of competition for this

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vitamin between the parasite and host but the lesions described differ from thosedescribed in pantothenic acid deficiency (Ram, 1949).

Vesicular dermatitis of the comb, wattles, eyelids, shanks and toes have beendescribed in chickens that have consumed Lolium temulatum infected with thefungus Cladosporium herbarum (Perek, 1958). Initially, small vesicles, that oftencoalesced, formed in the epidermis which following rupture, were covered by agreenish scab. A similar lesion was produced by feeding 1% ergot alkaloid to chic-kens and it was assumed that the naturally occurring cases were due to ergot-like alkaloids produced by Cladosporium herbarum.

Focal areas of acute inflammation with epidermal necrosis of the skin of the backhave been seen commonly by the author in one-day-old broiler chickens (Fig. 31).These lesions are seen in birds removed from the incubator and have often beenpresent for a number of hours. They appear to resolve quickly and have no adverseeffect on the bird.

On several occasions, the author has examined skin from broiler breeders withswollen heads. The swelling has been over the top and sides of the head and face.On the cut surface, subcutaneous tissues are oedematous, and pale, dry or caseousfoci are present. Histologically, the foci are granulomas with a central vacuole(Fig. 32) which contains lipid surrounded by heterophils, macrophages and giantcells. The reaction seems to be in response to the lipid. These cases have alwaysoccurred after vaccination at the back of the head with infectious bursal diseasevirus vaccine which has an oily base. Occasionally, a few E. coli are isolated fromthese lesions.

Parasitic skin diseaseNumerous species of lice, mites and other ectoparasites parasitise the skin of birds(Loomis, 1984). Other than producing mild hyperkeratosis or feather damageassociated with the effects of irritation, most do not produce significant lesions.Cnemidocoptes mite and trombiculid mite infestations have already been dis-cussed. Quill mites, Syringophilus sp and Dermatoglyphus sp. are commonly seenwithin the calamus of feathers in sections but in most cases they have no effect onthe feather. Heavy infestations are said to cause breakage of the mature feather(Harrigan, 1981).

Subcutaneous mites {Laminosioptes sp and Hypodectes sp.) are sometimes found(Cassidy and Ketter, 1965; Harrigan, 1981). The dead mites induce white or cream-coloured caseo-calcareous nodules and minimal inflammation.

Numeous filaroids inhabit the subcutaneous connective tissue of birds (Ruff, 1984)but invoke little, if any, reaction. Avioserpens taiwana induces fibrous nodules insubmandibular skin and skin of the thighs in ducks in Asia (Ruff, 1984) and skinflukes of the family Collyriclidae induce fibrous cysts, particularly around thecloaca, in numerous speces of birds (Kingston, 1984).

Xanthomas and xanthomatosisXanthomas are skin lumps or diffuse thickenings, characterised microscopically byinfiltration of foamy, lipid-laden macrophages (Fig. 33) into the dermis and sub-cutis (Petrak and Gilmore, 1983). Focal or diffuse accumulation of giant cellssurrounding or containing cholesterol clefts are common in xanthomas. The lesions

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may be single, multiple, discrete lumps or more diffuse thickenings of the skin(Petrak and Gilmore, 1983). The overlying skin is featherless, yellow, friable andmay be ulcerated and trauma to, and haemorrhage from, xanthomas is common,particularly when they occur on the wings. They appear to occur most commonlyin captive psittacine birds and may overlie other skin tumours, particularly lipomas(Petrak and Gilmore, 1983). Multiple xanthomas, or xanthomatosis, were seencommonly in Leghorn chickens in USA in the 1950s when aromatic chlorinatedhydrocarbons were present in animal fats used in poultry feeds (Sänger and Lagace,1966). Lesions appeared as swollen wattles or swelling of the intermandibular spaceand as pendulous masses on the feathered skin of the breast and thighs. The inter-mandibular lesions were soft, yellow and oedematous. Lesions on the body werefirm, yellow to orange and adherent to underlying musculature. Microscopically,early lesions were composed of accumulations of foamy macrophages betweendermal collagen fibres and around vessels, serous exudate, giant cells and cholesterolclefts. As lesions aged, the proportion of giant cells and cholesterol clefts werereduced and fibrous tissue increased. In this situation, it was postulated that aro-matic chlorinated hydrocarbons accumulated in subcutaneous adipose tissue andacted as an irritant or foreign substance that initiated inflammation.

The aetiology and pathogenesis of xanthomas in other species is unknown. In theauthor's experience, some cases are nothing more than chronic steatitis in lipoma-tous fat, possibly induced by trauma. However, this does not account for thoselesions that occur on the wings where subcutaneous fat is minimal.

NeoplasiaThis subject has been reviewed by Campbell (1969), Petrak and Gilmore (1983)and Fredrickson and Helmboldt (1984). Neoplasms of the skin have been recordedfrom many species but are most common in psittacine birds, particularly budgeri-gars, and chickens. In psittacine birds, mesenchymal tumours, particularly lipomasand fibrosarcomas, are more common than epithelial tumours (Petrak and Gilmore,1983). In chickens, lymphoid tumours of Marek's disease (Calnek and Witter,1984) occur more commonly than other mesenchymal neoplasms and epithelialneoplasms are uncommon (Fredrickson and Helmboldt, 1984).

Epithelial neoplasms. Skin papillomas (Petrak and Gilmore, 1983; Jacobson et al,1983), uropygial gland adenoma and adenocarcinoma (Petrak and Gilmore, 1983),acanthomas (Campbell, 1969), keratoacanthomas (Petrak and Gilmore, 1983) andsquamous cell carcinomas (Turnquest, 1979; Riddell and Shettigara, 1980; Petrakand Gilmore, 1983) have been recorded in a number of species.

Papillomas, some of which are associated with the presence of papilloma virusparticles (Lina et al, 1973; Jacobson et al., 1983) or herpesvirus-like particles(Lowenstine et al, 1983) appear as single or multiple, projecting nodules or papillaethat may occur on any area of the skin. They are common on the feet of cockatoos{Cacatua sp.) in Australia (Fig. 34). Histologically, they are composed of upwardprojecting folds of acanthotic, hyperkeratotic or parakeratotic epidermis withcentral fibrovascular cores.

Multifocal, ulcerative squamous cell carcinomas have been reported in the skin ofbroiler chickens (Turnquest, 1979; Riddell and Shettigara, 1980). The neoplasmsare detected after birds have been slaughtered and plucked. Lesions occur most

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22 D.A. Pass

commonly in feather tracts on the back and sides and are usually less than 1 cm indiameter although coalescence of adjacent lesions occurs. Histologically, the base ofthe ulcer is comprised of proliferating epidermal cells that infiltrate the dermis(Fig. 35). Keratin pearl formation and areas of poorly differentiated epidermal cellsoccur. The proliferating cells may penetrate the subcutis but métastases have notbeen reported. Fibrosis, acute or chronic inflammation and foci of lymphocytesmay be present in the base of the tumour and it has been suggested (Riddell andShettigara, 1980) that this may indicate that the tumours may regress.

Mesenchymal neoplasms. Lipomas (Petrak and Gilmore, 1983), fibromas, fibro-sarcomas and myxosarcomas (Campbell, 1969; Purchase and Payne, 1984), haeman-giomas and haemangiosarcomas (Petrak and Gilmore, 1983; Purchase and Payne,1984) are the most well recognised neoplasms arising from mesenchymal com-ponents of skin.

Lipomas are common in caged psittacine birds, particularly budgerigars and galahs(Cacatua roseicapilla). Often they occur in the abdominal and sternal skin (Petrakand Gilmore, 1983) and may be multiple. The majority of affected birds are alsoobese and it is probable that the lipomas are hyperplastic areas of adipose tissuerather than true neoplasms. The tumours are composed of typical adipocytes andmay be encapsulated. Degenerative and inflammatory changes within the tumoursare common and large parts of the tumour may resemble a xanthoma. The skinoverlying the tumour is often xanthomatous.

In chickens, fibromas, fibrosarcomas, myxofibrosarcomas and haemangiomas canall be produced by strains of leukosis/sarcoma virus (Purchase and Payne, 1984)and it is assumed that naturally occurring cases are also due to these viruses. Fibro-mas may occur anywhere over the body including facial appendages (Campbell,1969). They are firm, white, composed of interweaving bundles of dense or looselyarranged fibroblasts and collagen fibres and may contain cartilage and bone. Fibro-sarcomas may also occur anywhere but are most common on the breast, featheredparts of the leg and under-surface of the wing (Campbell, 1969). These neoplasmsare locally infiltrative and may metastasise to the liver, kidney, heart, pancreas andintestine. The appearance varies depending on the amount of collagen or intercel-lular mucinous matrix produced and whether necrosis and haemorrhage are present.The histology also varies from plump, well differentiated fibroblasts, through mix-tures of less well differentiated pleomorphic cells and bizarre giant cells. The matrixmay be composed of collagen fibres, reticulin fibres or mucinous material in whichcase the term myxosarcoma or myxofibrosarcoma may be used. Fibrosarcomas arecommon in budgerigars (Petrak and Gilmore, 1983) but there is no known cause.

Haemangiomas (Fig. 36) occur as single or multiple nodules, several millimetres indiameter, in the skin (Purchase and Payne, 1984). They bleed easily and to such anextent that birds may exsanguinate. They may be composed of obvious, but thin-walled irregularly shaped blood vessels (Fig. 37) or less well-differentiated masses ofendothelial-like cells and thin irregular clefts. The overlying dermis may be oedema-tous and haemorrhagic. Spongiosis, vesiculation and necrosis of epidermis, probablydue to ischaemia, results in haemorrhage.

Marek's disease. Lesions in the skin due to infection with Marek's disease virus(MDV) occur predominantly in feather tracts (Lapen and Kenzy, 1972). MDV

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infects cells of the feather follicle epidermis, and viral antigen is sometimes demon-strable in feather epidermis but not in skin epidermis (Calnek and Hitchner, 1969).Lesions occur in the follicular epidermis (Lapen et al, 1970;Moriguchi and Izawa,1979), the dermis adjacent to affected epidermis (Lapen et al, 1970, 1971) andfeather pulp (Moriguchi et al, 1982). The mildest gross lesion consists of an ap-parent enlargement of feather follicles (Helfnboldt et al, 1963) that is best ob-served after the skin has been removed. Firm, fleshy, pale nodules up to severalcentimetres in diameter, between follicles or that replace follicles are common(Fig. 38). The surface is often ulcerated due to necrosis within the nodules.

The microscopic changes seen depend largely on the stage of infection. The earliestchange is the appearance of intranuclear inclusion bodies in cells of the transitionalzone and stratum corneum of the follicular epidermis (Lapen et al. 1970). Theinclusions are large, often filling the nucleus, eosinophilic or amphophilic and thenuclear chromatin is marginated (Fig. 39). The cytoplasm of affected cells mayundergo hydropic degeneration and in the most superficial layers the inclusionsmay persist in a keratin-cellular debris matrix (Lapen et al. 1970). The affectedepidermis is usually thicker than unaffected epidermis.

MDV antigen has been demonstrated in the nucleus and cytoplasm of cells withintranuclear inclusions (Lapen et al, 1970). Chickens that develop Marek's diseasehave persistent MDV antigen in feather follicle epidermis whereas the antigendisappears in birds that do not develop the disease (Steck and Haberstich, 1976).The presence and persistence of nuclear inclusions in feather follicle epidermis canbe used to predict the development of Marek's disease according to Moriguchi andIzawa (1979) and Moriguchi et al, (1984). Two patterns are described: pattern 1 inwhich there is transient inclusion formation 2 to 4 weeks after infection but de-clining by 9 weeks; pattern 2 in which there is persistent inclusion formation(Moriguchi and Izawa, 1979). The great majority of birds with pattern 1 do notdevelop Marek's disease whereas the majority of birds with pattern 2 do. Vaccina-tion with HVT vaccine leads to marked restriction of inclusion body formation(Moriguchi and Izawa, 1979) and incidence of Marek's disease. However, it ispossible that HVT as well as natural MDV infection is responsible for the early(2 to 4 weeks) development of inclusion bodies in field flocks (Moriguchi et al,1986),

The most obvious lesions in Marek's disease of the skin are those.that occur in thedermis. Aggregates of small lymphocytes first appear in the dermis adjacent toinfected feather follicle epidermis (Fig. 40) in response to the infection (Lapen etal, 1970, 1971). The number and size of aggregates increase with post-exposuretime and lymphocytes may be seen between the vessels of the follicular vascularbed, between and replacing feather follicle muscle fibres, in feather follicle epi-dermis and in interfollicular connective tissue, fat and nerves (Lapen etal, 1971).Neoplastic transformation occurs in some of these sites as the larger aggregatescontain more blastic medium and large lymphocytes, large mononuclear cells withvesicular nuclei containing prominent nucleoli and large cells (Marek's disease cells)with dark, basophilic pleomorphic nuclei and vacuolated basophilic cytoplasm(Lapen et al, 1971). The neoplastic lymphoid cells gradually replace dermal struc-tures and cause atrophy of feather follicles and skin epidermis.

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24 D.A. Pass

Microscopic examination of the neoplasms often reveals tumours within the featherpulp. These may be due to infiltration of neoplastic lymphoid cells from the dermisbut according to some reports both neoplastic and reactive changes occur spe-cifically in the feather pulp in experimentally infected (Moriguchi etal., 1982) andnaturally infected (Moriguchi et al, 1986) chickens. Pulp lesions have been classedas T-type (tumorous proliferation ) and R-type (non-tumorous response) (Moriguchiet al, 1982) based on the classification of lesions in peripheral nerves used byFujimoto et al. (1971). Because of the morphological diversity of the non-tumorous response, the R-type lesion has been divided into two sub-types, Rl andR2. The lesions are defined by Moriguchi et al. (1982, 1986) as follows: Rl-typeis morphologically a non-tumorous lymphoid lesion showing perivascular to diffuseinfiltration of small lymphocytes mixed with lymphoblasts, with activated mesen-chymal cells and endothelial hyperplasia of small blood vessels; R2-type is aninflammatory lesion with oedema, perivascular to diffuse infiltration of mature orimmature plasma cells, small lymphocytes and heterophils and occasional germinalcentre formation; T-type is a tumorous lymphoproliferative lesion consisting oflymphoblasts, blast-type cells and small lymphocytes that replace the pulp, andactivated mesenchymal cells. The earliest change following infection is a mild Rl-type lesion which may occur without the presence of inclusion bodies in the featherfollicle epidermis (Moriguchi et al., 1982, 1986). The Rl-type lesion may regress orpersist in which case it may convert to a T-type lesion. Birds with persistent Rl-type and T-type lesions tend to have persistent intranuclear inclusion bodies(pattern 2) and develop Marek's disease (Moriguchi et al, 1982, 1984). R2-typelesions tend to occur in older birds, 9 to 12 weeks of age, that have transient(pattern 1) intranuclear inclusion body formation in the follicle epidermis. Re-gressing Rl-type lesions may convert to R2-type and mixed Rl and R2-type lesionsoccur. The majority of birds with R2-type lesions do not develop Marek's disease(Moriguchi et al, 1982).

Diffuse swelling of the comb has also been reported as a lesion of Marek's diseaseof the skin (Ekperigin et al, 1983) in Leghorn layers. The comb is firm, swollenand in some cases ulcerated. Microscopically the dermal tissue is diffusely infil-trated by pleomorphic lymphocytes.

DISEASES OF FEATHERS

Genetic or probable genetic feather disordersThere are many genetically determined feather abnormalities. Many are cited bySomes (1984) under the groupings plumage distribution mutations (e.g. congenitalbaldness, naked, naked neck), plumage-developmental-rate mutations (e.g. slow,rapid, modified feather growth rates), feather-structure mutations (e.g. frizzing, henfeathering, silkiness), feather-length mutations (e.g. crest, non-moult, long filo-plumes), plumage colour mutations (e.g. blue, buff-red, albinism), plumage-patternmutations (e.g. extended black, dominant wheaten, buttercup), feather-patternmutations (e.g. autosomal barring, pencilling, pied). Others, not cited by Somes(1984) include fray feathering in chickens (Warren, 1938), hypoplasia of tail-feathers in Ingie fowl (Hashiguchi et al, 1978), 'snow-white' down in chicks (Hutt,1951a), 'woolly' chicks (Jones and Morgan, 1965), clubbed down associated withblack feathering (Hutt, 1951b) and rough-textured feathering in Japanese quail(Roberts and Fulton, 1979).

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Genetically determined feathering abnormalities undoubtedly occur in otherspecies and some are selected for by breeders of pigeons and canaries.

'Feather cysts'. These are most common in canaries, particularly those with complexfeathering such as the Norwich strain, and occasionally in other birds. In canariesthey are probably genetically determined but the mode of inheritance is not known.The cysts are either multiple or single and present as hard yellow lumps within, andprojecting from, the skin (Fig. 41). The hardness is due to accumulation of keratin.The cysts are formed by dysplastic feather follicle and feather growth. They arelined by stratified squamous epithelium which in places often has the characteristicsof developing feather epidermis (Fig. 42) in that barb ridges and even keratinisedstructures that resemble pulp caps are apparent. The lesions are benign.

'Feather duster'. This is also known as 'chrysanthemum feathering' and is a con-dition in budgerigars characterised by overly long feathers that do not 'sit down' inthe normal way (Fig. 43). In addition, birds are small and some have other defectssuch as microphthalmia. They lack viability and die within a year of hatching.Microscopic lesions in growing feathers have not been described.

Nutritional deficienciesNumerous amino acid deficiencies or imbalances have been linked to abnormalfeathering but histological lesions have not been described. Valine, leucine, isoleu-cine, glycine, phenylalanine and tyrosine deficiency produce concave feathers, thefeathers bending upwards from the body (Robel, 1977); lysine deficiency producesdepigmentation (Fritz et al, 1946; Sanders et al, 1950) of turkey feathers and lowarginine in the presence of normal lysine or methionine results in feathers with aretained sheath, loose barbules and thin rachis (Sanders et al, 1950). Lysine de-ficiency has been suggested as a cause of depigmentation of the feathers of psit-tacine birds (Harrison, 1984) but experimental work in cockatiels (Nymphicushollandicus) has failed to confirm this (Roudybush and Grau, 1985).

Selenium or vitamin E deficiency or both results in atrophy of the calamus ofprimary and secondary wing feathers, tail feathers and some contour feathers inturkeys (Supplée, 1966).

'Poor' feathering is reported in a number of deficiency states including biotin,folic acid, nicotinic acid, pantothenic acid (Ram, 1949; Taylor, 1967), calcium(Wallach and Flieg, 1969) zinc (Cook et al, 1984) and protein deficiency (personalobservation). In zinc deficiency, primary feathers are frayed and/or break andoccasionally have blood-filled blebs (Cook et al, 1984) in the rachis which mayrupture. Feathers lack barbules and barbule hooklets (Young et al, 1958) whichproduces a 'frizzled' appearance (O'Dell etal., 1958).

Clubbed down. Riboflavin deficiency is reported to produce short, abnormal nataldown feathers (clubbed down) in chickens (Austic and Scott, 1984) but this hasbeen questioned by Hawes and Fox (1962). Similar abnormalities have been linkedto the allele for extended black feathering in chickens (Hutt, 1951b), ducks(Hawes, 1965) and turkeys (Hawes and Buss, 1963). Clubbed-down has also beenreported as a lesion in dead-in-shell chickens infected with infectious bronchitisvirus (McFerran et al, 1971) and in chickens hatched from eggs subjected totemperatures of greater than 40°C at 16 days incubation (Thompson etal, 1976).

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It is not clear from the latter paper whether the feathers were 'clubbed' because inthe text the chickens were described as having "matted, coarse down."

In Australian broilers, clubbed down differs from that associated with factorsdescribed above. This disease is characterised by shortened and abnormal nataldown feathers with a specific bilaterally symmetrical feather tract distribution.Affected feathers fail to rupture the surrounding feather sheath or fluff out(Fig. 44). This syndrome has been investigated extensively by L. Denholm andothers, Department of Agriculture and Rural Affairs, Victoria, Australia (unpub-lished data). The following description is based on their work.

The major feather tracts involved are the sternal and abdominal tracts. Severelyaffected birds may lack feathers on sternal tracts and the affected feathers inseverely affected birds are deep yellow or orange compared with paler yellow ofnormal downs. Affected feathers may show the following abnormalities: shorteningby 50 to 75% and cigar-shaped; uneven, sometimes thickened barbs and short,uneven barbules; small cysts on the rachis that are continuous with the pulp andcovered by epidermis; terminal, discrete, hollow dilations surrounded by a thicksheath; non-terminal, discrete dilations. Juvenile feathering is poor and fault linesacross the vane and rachis are common. The lines are produced by poor develop-ment of barbules and barbule hooklets.

Histological lesions can be detected from 12 days of embryonic development. Inthe embryo a decrease in mitotic figures in the stratum intermedium compared withnormal and ballooning degeneration and necrosis of basilar cells and cells in thestratum intermedium occur. Cells with deeply basophilic inclusions may be seen inthese areas. The barb ridges appear disorganised as feathers develop. The feathersheath is thick, more eosinophilic than normal and contains ghost nuclei. At thetime of hatching the necrotic phase appears to have passed. The feathers containan abnormally large amount of pulp (Fig. 45). The axial artery and peripheral pulpcapillaries are congested and become dilated. Endothelial proliferation, endothelialdegeneration, perivascular oedema, haemorrhage and fibrosis may occur and mono-nuclear cells and heterophils may be seen in the pulp and perifollicular dermis. Inaddition to these changes the author has seen total necrosis of the epidermis of theneck of the follicle and cholesterol clefts in the pulp in a number of feathers(Fig. 45).

The aetiology and pathogenesis of clubbed down in Australian broilers are notknown. It has been shown by Denholm and his colleagues that the disease can notbe related to riboflavin deficiency or the presence of known viruses of chickensincluding reticuloendotheliosis virus. They have shown that the lesions are asso-ciated with a period of reduced alkaline phosphatase activity in feather epidermisduring embryogenesis and reduced serum alkaline phosphatase activity in plasmaof the newly hatched affected chicken compared with the normal chicken. Reducedalkaline phosphatase activity is believed in some outbreaks to be associated with aconditioned zinc and possibly manganese deficiency.

Viral infections of feathersIn this section, psittacine beak and feather disease, reticuloendotheliosis virusinfection and papovavirus infections are discussed. Marek's disease is discussedunder Neoplasia.

1

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Psittacine beak and feather disease (French moult). This is a major disease in manyspecies of psittacine bird (Figs 46 and 47). The list of affected species continues togrow and one could expect to diagnose it in any psittacine species. The disease iscaused by a 20 nm diameter virus (Wylie and Pass, 1987) which can be seen pri-marily in the epidermis of the feather and beak (Jacobson et al, 1986; Pass andPerry, 1984). The virus may also be less commonly found in feather follicle epi-dermis, macrophages in feather epidermis and feather pulp, in cells in the thymusand bursa of Fabricius, occasionally in hepatic reticuloendothelial cells and inoesophageal epithelial cells (Wylie and Pass - unpublished). The virus infection ispersistent and successive generations of feathers are infected and affected. Grossfeather abnormalities include slow growth, loss of down (Fig. 48) and powder downfeathers (Figs 49 and 50), loss of contour and flight feathers, retention of feathersheath, short feathers enclosed in a thick feather sheath, constrictions in the shaft,knob-like ends to short feathers (Fig. 48) and haemorrhage within the rachis(Perry, 1981 ; Pass and Perry, 1984,1985). Changes in feather colour, from green toyellow, may also be seen.

Microscopic changes occur in the epithelial collar and developing rachis and barbridges of growing feathers, the feather pulp and occasionally feather follicle epi-dermis and dermis (Pass and Perry, 1984). Lesions do not occur in the interfolli-cular epidermis of the skin. In the epidermal tissues the basic lesion is necrosis(Fig. 51) of epidermal cells in the germinative layers (Pass and Perry, 1984). Necrosisvaries from being focal and involving only a few cells to involvement of many cellsallowing cleft formation and separation of the epidermis from the pulp. The basallayer often appears disorderly due to apparent hyperplasia of cells. Epidermal cellnuclei may be enlarged and contain an enlarged nucleolus surrounded by mar-ginated chromatin or, the centre may be clear, or amorphous and amphophilic.Macrophages with conspicuous purple intracy toplasmic inclusion bodies of variablesize and number per cell may be present in the epidermis, sheath and pulp (Fig. 51).In the epidermis these cells are usually closely associated with necrotic cells and inthe pulp they commonly accumulate under the pulp cap (Fig. 52) and containmaterial other than inclusions, e.g. melanin. When sections are stained with Fuelgenthe intracytoplasmic inclusions stain positively and small inclusions which are notvisible on haematoxylin and eosin stained sections, may also be seen within thecytoplasm of feather epidermal cells. The amphophilic nuclei do not take up thestain. The sheath, of those feathers in which it is retained, is thickened and oftencontains macrophages with intracytoplasmic inclusions.

Changes within the pulp vary. There may be no lesions, a mild mononuclear cellinfiltrate, a heavy infiltrate of mononuclear cells or severe inflammation withheterophils. Inflammation is most marked and often chronic at the distal end ofshort feathers with a thick sheath. Necrosis of distal pulp and epithelium andhaemorrhage into the distal shaft is common. In some feathers, the distal kerati-nised rachis and barbs curl up within the feather sheath and in others large unstruc-tured masses of keratinised tissue are present within the sheath.

In some chronically affected birds very short contour feathers that just project outof the follicle may be all that are present other than a few primaries. Microscopi-cally these feathers appear to have stopped growing. They have a pulp surroundedby a thin epidermis and a very thick feather sheath. Necrosis and macrophages

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containing basophilic intracytoplasmic inclusions, typical of that seen in the activedisease, are demonstrable in these feathers.

Electronmicroscopy reveals necrosis of epidermal cells and engulfment of necroticdebris by macrophages. These cells contain numerous inclusions of variable size,shape and configuration. The majority lie free within the cytoplasm although someare membrane bound. They are composed of electron dense particles, on average20 nm in diameter, that form paracystalline arrays, whorls, semicircles and otherconfigurations. Cytoplasmic inclusions and also loose aggregates and single par-ticles of similar size occur in epidermal cells. Nuclear changes consist of eithernucleolar enlargement, nuclear enlargement, nucleolar segregation, chromatin mar-gination or electron lucency of the centre. Intranuclear viral particles have not beendemonstrated by the author, despite extensive examinations.

Reticuloendotheliosis virus infection. Reticuloendotheliosis virus (REV) is a retro-virus that produces lesions in turkeys, chickens, geese, ducks, quail and pheasants,very similar to lymphoid leukosis (Witter, 1984). The virus has been a contaminantof poultry vaccines and by this means has been responsible for a feathering abnor-mality ('nakanuke') of young chickens (Fig. 53) (Koyama et al, 1976; Jacksonet al, 1977).

Lesions occur in contour feathers of many feather tracts but are most conspicuousin primary and secondary flight feathers (Tajima et al., 1977). They consist ofincreased transparency of the calamus and rachis.loss of proximal barbs and sparse-ness of the vane. On close examination of areas in which the vane appears absent,the barbs can be seen running parallel to and closely associated with the rachis. Thislesion, however, is not specific for REV infection. It has been seen in associationwith runting and proventriculitis that has not been associated with REV (personalobservation) and in association with a degenerative lesion in developing feathers ofnewly hatched chickens in which there was also no evidence of REV infection.

In REV infection, the gross lesions are the result of destruction of epidermal cellsin the developing feather following infection with the virus. Lesions consist ofnecrosis of individual or clusters of cells in the germinative layers of epidermis ofthe rachis and barb ridges (Tajima et al., 1977). Cells in the barb ridges appeardisorderly. Mild inflammation occurs in the pulp. Electronmicroscopy reveals viralparticles, 92 nm in diameter between epidermal cells, within membrane-boundcytoplasmic vacuoles and budding from the cell membrane.

Papovavirus infections. Papovaviruses belonging to the polyoma subgroup (Lehnand Müller, 1986), produce generalised disease in budgerigars and other psittacinebirds (Bernier et al., 1981, 1984; Davis et al, 1981; Graham and Calnek, 1987).Morphologically similar viruses produce generalised disease in other species ofpsittacine birds (Jacobson et al, 1984; Pass, 1985; Pass et al, 1987) and finches(Johnston and Riddell, 1986; Forshaw et al, 1988). Lesions occur in skin, featherfollicle, feather and uropygial gland of fledgling budgerigars (Bernier et al, 1981;Davis et al, 1981; Dykstra and Bozeman, 1982) and other psittacine species(Jacobson et al, 1984; Graham and Calnek, 1987). In budgerigars the disease isknown as budgerigar fledgling disease (Davis et al, 1981). Clinical abnormalitiesinclude a lack of down feathers on the back and abdomen and lack of filoplumes onthe head and neck. Contour feathers grow slowly, are shorter than normal and lackbarbs.

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Pathology of the integument 29

The gross lesions are due to degeneration and necrosis of feather epidermis. Micro-scopically, the nuclei of affected epidermal cells of skin, feather follicles andfeathers are enlarged and basophilic (Fig. 54) or have a clear centre containingfaintly basophilic granules and marginated chromatin. Affected cells often undergocytoplasmic vacuolar (ballooning) degeneration and occasional dyskeratosis. Cyto-plasmic distension with basophilic globules has also been described (Graham andCalnek, 1987). Acanthosis and hyperkeratosis may be seen. Electronmicroscopicexamination of affected cells reveals round or cubic viral particles, 40 to 50 nmdiameter, and elongated tubular structures in the enlarged nuclei and in vacuolatedcytoplasm.

Papova-like virus infection may also result in feather loss in adult birds. A 4-year-old rainbow lorikeet (Trichoglossus haematodus) examined by the author had beenlosing primary wing feathers and tail feathers for 3 weeks before death which wasdue to acute hepatic necrosis. Lesions in feathers consisted of karyomegally in cellsof barb ridges (Fig. 55) and necrosis and degeneration (Fig. 56) of epidermal cells inthe epidermal collar and rachis. Degenerate cells were enlarged due to nuclearenlargement and vacuolation of the cytoplasm. The changes were very similar tothose seen in budgerigar fledgling disease. Round papovavirus-like particles about42 nm in diameter were seen in nuclei.

ToxinsIt is possible that many toxins, particularly those that interfere with cell division orcause necrosis, can produce lesions in feathers as a result of their action duringfeather growth. However, there are few reports on the mechanism of action andhistological lesions.

Monensin sodium in the diet has been reported to delay maturation of growingfeathers in chickens (Kingston, 1977). The mycotoxins (T-2 toxin and diacetoxy-scirpenol) of Fusarium sp. have a radiomimetic effect and will produce lesions infeathers as well as other organs (Wyatt et al, 1975; Hoerr et al, 1981, 1982).Lesions consist of necrosis of cells in the epidermal collar, rachis and barb ridges ofthe feather. Necrosis of cells of the stratum germinativum of the neck of the featherfollicle have also been reported.

Cyclophosphamide, an immunosuppressant, has been reported to interfere withfeather growth and barb development in chickens (Ratnamohan, 1981). Theabnormality in the feathers resembles 'nakanuke' feathering.

Degenerative changes in growing feather quills followed by haemorrhage into thefeather pulp, similar to that seen in vitamin E, pantothenic acid, folic acid, biotinand nicotinic acid deficiency, has been reported to occur in chickens and Japanesequail fed on diets containing excess vitamin A (Taylor, 1967) but microscopicchanges have not been described.

Toxins would appear to have maximum effect on embryonic feather growth whenthe embryo is exposed between days 9 to 12 of incubation, the period in whichfeather growth is very rapid (Lucas and Stettenheim, 1972). Experimental injectionof chick embryos with retinoic acid between days 10 to 12 of incubation has beenshown to induce feather formation on the scales of the dorsal and ventral surfacesof the feet (Hardy and Dhouailly, 1979). Feather malformations have also beeninduced by exposure of 10 to 12 day chick embryos to cadmium chloride (Narbaitz

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30 D.A. Pass

et al, 1983). When injected into the yolk sac of 10- and 11-day-old chick embryos,feather growth was retarded and feathers in all tracts were curled; when given onday 12, haemorrhage and atrophy of the distal end of the feathers occurred. Simul-taneous administration of zinc sulphate was protective, suggesting cadmium inter-feres with zinc metabolism, as zinc is necessary for feather differentiation. It is ofinterest that chicks with naturally occurring clubbed down in Australia have lowerconcentration of liver zinc and alkaline phosphatase, a zinc-dependent enzyme,than normal birds (Schuster and Hindmarsh, 1980) but whether cadmium or anyother compound that can replace zinc is involved in the genesis of this lesions isunknown.

Feathering abnormalities associated with hormone deficiencyIt has been stated that the hallmark of endocrine related feather loss is a lack offeathers on the head and back of the neck (Lothrop et al, 1983) but evidence tosupport this statement is lacking. It has been established that thyroxine plays arole in feather growth (Ringer, 1965) and that one of the features of hypothy-roidism is abnormal feather structure. The feathers are fringed and elongated withloss of barbules such that they have a 'lacy' or 'silky' appearance (Ringer, 1965;Cole, 1966). Pigmented feathers also lose their colour (Ringer, 1965).

Progesterone has been shown to stimulate feather growth (Schaffner, 1954) andbaldness of the back of the head and neck in psittacine birds that responded toprogesterone therapy has been reported (Rad, 1976). Adrenal insufficiency has alsobeen incriminated as a cause of feather loss (Rosskopf et al, 1979; Onderka andClaffey, 1987) but this remains unproven.

Abnormalities of unknown aetiologyUnerupted primary and secondary flight feathers at hatching in broilers hasbeen seen by the author. The abnormality was seen in association with a flockexperiencing clubbed down but the birds in question did not necessarily haveclubbed down. Affected wing-tips were thicker than normal because the feathershad not emerged from the follicles. When they did emerge, they grew slowly andunevenly and had a ragged appearance (Fig. 57). In the second and third weeks,fault lines and adhesion of the barbs to the rachis as seen in 'nakanuke' type fea-thering (Fig. 53) were common. Rectrices were also slow to develop. Contourfeathers developed normally. The birds were smaller than normal in the first fewdays of life but the growth rate of affected birds during the life of the affectedflocks was not determined. There was no serological evidence of reticuloendothe-liosis virus infection. Microscopic examination of primary feathers at 1 day of agerevealed necrosis of epidermal cells of the feather and follicle. Individual necroticcells were evident in basal layers but necrosis was most severe in the stratum inter-medium and corneum (Fig. 58). Many nuclei in the outer layers of cells containedenlarged nucleoli and nuclei were retained within the cornifying layers. In someareas, cells in the stratum intermedium were ballooned and large fluid filled cleftsformed. A few heterophils had infiltrated these areas. The pulp of affected featherswas more vascular than normal and was occasionally infiltrated by heterophils.

Another apparently dysplastic condition occurs in budgerigars which is charac-terised by short feathers, particularly at the base of the tail. Affected feathers areshort and multiple feathers emerge from the same follicle. The feather shafts are

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Pathology of the integument 31

separated by a thin layer of keratinised epithelium and the feathers often appearthicker than normal. There are no cellular abnormalities apparent within theepidermis or pulp to explain the defect.

DISEASES OF THE BEAK

Difficulties in cutting sections of beaks, particularly of psittacine birds, probablyinhibits pathological investigation in many cases of beak disease. Even after pro-longed décalcification cutting is difficult and many sections are poor. Embeddingin polymerised resins improves the quality of sections.

Other than the changes described in psittacine beak and feather disease, specifichistological descriptions of beak abnormalities are lacking. However, as the beak is aliving epidermal structure, abnormalities such as inflammation, degeneration orneoplasia should be suspected if the ramphotheca is abnormal. Pathological changesresult in changes in colour, eveness of the surface and change in shape. The lesionsmay primarily affect the beak epidermis and/or the underlying bone. Examples ofchronic inflammatory and neoplastic processes that involve the beak are presentedin Figs 59, 60 and 61.

Lesions of the beak in psittacine beak and feather disease occur predominantly inthe cockatoos. They are uncommon in the smaller parrots. Changes consist ofprogressive elongation (Fig. 62), development of fault lines, lifting of layers ofcornified epidermis, longitudinal splitting, breakage and underrunning of the outer,and particularly the oral surfaces. Similar changes may occur in the claws. Themicroscopic lesions in the beak are basically the same as those in feathers (Pass andPerry, 1984), namely, necrosis of epidermal cells and accumulation of macrophageswith purple intracytoplasmic granules in and below the epidermis. Necrosis resultsin separation of the cornified layers, fluid accumulation and often infiltration byinflammatory cells (Fig. 63). The splits that develop in the epidermis lift the outerlayers away from the basal layers exposing these structures to secondary infection.Chronic inflammation is common.

AcknowledgementsI wish to acknowledge R. Perry for the stimulus he provides by his enthusiasm forthe study of disease in birds and G. Griffiths for his photographic expertise.

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Mohammed, M.A., Sokkar, S.M., Batrawi, A., Refaie, M.K. and Ahmed, A.A.S. (1980). Naturaland experimental nodular dermatomycosis in chickens. Avian Pathology, 9: 185-192.

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36 D.A. Pass

Moriguchi, R., Fujimoto, Y., Mori, F. and Izawa, H. (1986). Chronological observations ofMarek's disease-associated feather-pulp lesions in field chickens. Avian Diseases, 30:282-296.

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Patrick, H., Boucher, R.V., Dutcher, R.A. and Knandel, H.C. (1942). The nutritional sig-nificance of biotin in chick and poult nutrition. Poultry Science, 21: 476.

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Perek, M. (1958). Ergot and ergot-like fungi as the cause of vesicular dermatitis (sod disease) inchickens. Journal of the American Veterinary Medical Association, 132: 529-533.

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Purchase, H.G. and Payne, L.N. (1984). Neoplastic diseases, leucosis/sarcoma group. In:Diseases of Poultry, 8th Edition. Edited by Hofstad, M.S. Ames, Iowa: State UniversityPress.

Rad, M.A. (1976). Treatment of moulting in psittacines with medroxyprogesterone acetate.Avian Pathology, 5: 155.

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Randall, C.J., Siller, W.G., Wallis, A.S. and Kirkpatrick, K.S. (1984b). Multiple infections inyoung broilers. Veterinary Record, 114: 270-271.

Ratnamohan, N. (1981). Feather lesions in cyclophosphamide-treated chickens. Avian Diseases,25: 534-537.

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Renden, J.A. and Abbott, U.K. (1980). Developmental studies with avian ichthyosis. PoultryScience, 59: 1654.

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Thompson, J.B., Wilson, H.R. and Voitle, R.A. (1976). Influence of high temperature stress of16-day embryos on subsequent hatchability. Poultry Science, 55: 892-894.

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with mammalian comparisons. In: Skin of Vertebrates. Edited by Spearman, R.I.C. andRiley, P.A. London: Academic Press.

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Yunker, C.W. and Ishak, K.C. (1957). Histopathological observations on the sequence ofinfection in knemidocoptic mange of budgerigars (Melopsittacus undulatus). Journal ofParasitology, 43: 664-672.

RESUME

Pathologie du tégument des oiseaux: une revue

Une revue concernant la structure normale et les processus pathologiques majeursainsi que les entités morbides du tégument aviaire est présentée. Cette revue a étéfaite principalement pour servir de source de référence à ceux qui sont impliquésdans la pratique de la pathologie aviaire.

ZUSAMMENFASSUNG

Die Pathologie des Vogelinteguments: ein Übersichtsreferat

Es wird eine Übersicht über den normalen Aufbau und über die wichtigsten patho-logischen Prozesse und Krankheiten des aviären Integuments vorgelegt. Das Referatwurde primär als Nachschlagwerk für praktisch tätige Veterinärpathologen konzi-piert

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Pathology of the integument

RESUMEN

39

Patológia del integumento aviar: una revisión

Se realiza una revisión de la estructura normal y de los principales procesos pato-lógicos y enfermedades del integumento aviar. Esta revisión se ha escrito inicial-mente como fuente de referenda para aquéllos interesados en la prâctica de lapatología veterinaria.

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Pathology of the integument 41

1. Normal thin skin of an apterium. HE. Bar 50 ßm.

Fig. 2. Normal thick skin of the featherless shank of a chicken. HE. Bar 50 ßm.

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42 D.A. Pass

N

A • '

-S"A" - \

V

Fig. 3. Normal epidermis of the beak of a psittacine bird. Note sensory nerveendings (Herbst corpuscles) in the dermis. HE. Bar 50 urn.

iFig. 4. Normal red comb of a chicken. HE. Bar 200 am.

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Pathology of the integument43

-r

I

Av-Ï,

g-. 5. Normal structure of a growing plumulaceous feather. A - dermal papilla,B - pulp, C - epidermal collar. HE. Bar 500 [im.

g-. 5. Normal structure of growing pennacious feather cut lateral to the dermalpapilla. A - pulp, B — epidermal collar. Barb ridges (arrows). HE. Bar500 ßm.

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44 DA. Pass

4

Fig. 7. Normal developing vane. Barb ridges differentiating into barbule ridges.Feather sheath (arrow). HE. Bar 50 ym.

Fig 8 Tip of growing feather. The barbs are still retained within the sheath. Pulp

caps (arrows). HE. Bar 500 y.m.

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Pathology of the integument 45

Normal mature feather infeather follicle. Keratinisedpulp caps are visible cros-sing the calamus. HE.Bar 50 /im.

Fig. 10Plantar surface of chickenfeet with hyperplastic ul-cerative lesions on the foot-pads.

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46 D J V . Pass

S >> *'' ~ß^v€^$a:\*&."•.••.y*

fe»ir--. •> » " S O T " ' ' ' 7 _~ x . " >-

^g. 2i. Avian pox virus infection. Pigeon.

ZV/"*"- ''

ig. 12. Avian pox virus infection. Note hyperplasia and intracytoplasmic inclusionbodies (arrows). HE. Bar 50 jum.

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Pathology of the integument 47

.V

i i . Cnemidocoptic mange (scaley-face) in a budgerigar. The hyperkeratotic,pitted lesion above the eye is characteristic.

v h

v

Fig. 14. Cnemidocoptic mange. Budgerigar cere. Note acanthosis, hyperkeratosis,mites in the hyperkeratotic epidermis and mild inflammation. HE. Bar200 ßm.

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48 D.A. Pass

Fig. 15. Cnemidocoptic mange. Abdominal skin of Agapornis sp. The mite hascaused atrophy of the epidermis and appears to be in direct contact withdermal connective tissue. HE. Bar 200 \xm.

Fig. 16. Superficial fungal infection of the skin of a crow. Note acanthosis andextreme hyperkeratosis. Clear, slightly refractile hyphae (arrows) arepresent in the hyperkeratotic layers. HE. Bar 50 \un.

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Pathology of the integument 49

Fig. 17Hyperkeratosis of the fea-therless skin of the face ofa chicken. Cause unknown.Fig. 18Extreme hyperkeratosis ofchicken skin. The skin wasplucked to reveal the dis-tribution of the lesionwhich is restricted to ptery-lae.

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50 D.A. Pass

Fig. 19. Acanthosis, spongiosis and bullous formation in the epidermis of a chickenwith severe hyperkeratosis shown in Fig. 18. HE. Bar 50 urn.

ig. 20. 5fcj« o/ the comb of a chicken infected with avian influenza virusNote the extreme necrotising inflammatory reaction that involves all layersof the skin and subcutis. (Slide provided by Australian Animal HealthLaboratory, Geelong, Victoria, Australia). HE. Bar 200 [xm.

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Pathology of the integument 51

Fig. 21. Granulomatous dermatitis associated with psittacine beak and featherdisease. HE. Bar 500 fxm.

Fig. 22. Pseudomonas aeruginosa infection. The swelling is due to severe dermaland subcutaneous oedema.

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?. 23. Pseudomonas aeruginosa infection. All tissues are ischaemic and oede-matous. Blood vessels are thrombosed and bacteria are visible in therconnective tissue. HE. Bar 50 ßm.

Fig. 24. Mycotic dermatitis. Note the similarity to Fig. 17.

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Pathology of the integument 53

25. Mycotic dermatitis. Note fungal hyphae, acanthosis, early spongiosis anddermal oedema. HE. Bar 50 \im.

• • • • - ,

\

Fig. 26. Gouldian finch with suspected dermatophyte infection. Feather lossoccurred only on the head.

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54 D.A. Pass

Fig. 27. Skin from Gouldian finch. Hyperkeratotic feather with fungal spores inthe superficial layers. Suspected dermatophyte. HE. Bar 50 yon.

Fig. 28. Skin from Gouldian finch stained with PAS. Thin fungal hyphae in hyper-keratotic skin and feather epidermis. Suspected dermatophyte. PAS.Bar 50 ytm.

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Pathology of the integument 55

Fig. 29Canary with subcutaneousoedema of the abdomenand legs proximal to thehock due to trombiculidmite infection. (Reprintedfrom the Australian Vete-rinary Journal by permis-sion of the Editor). HE.Bar 50 iim.Fig. 30Trombiculid larva surroun-ded by amorphous cement.At the point of attach-ment, there is necrosis ofepidermis and acute infla-mmation. Oedema of thedermis causes the skin tosurround the mite. (Re-printed from the Austra-lain Veterinary Journal bypermission of the Editor).HE. Bar 50 jim.

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56 DA. Pass

fs'. J i . Sfcin o/ f/ie bacfc of a day-old broiler chicken with focal epidermal necrosisand acute dermatitis. HE. Bar 50 [im.

Fig. 32. Granulomatous inflammation of the subcutis associated with depositionof exogenous oil. The vacuoles contained lipid material prior to embeddingin paraffin. HE. Bar 200 y.m.

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Pathology of the integument 57

Fig. 33. Subcutaneous xanthoma composed of foamy macrophages and cholesterolclefts. HE. Bar 50/im.

. *.;:.-«J^!*

?. 34. Papilloma on galah /'Cacatua roseicapilla,/ foot.

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58 D.A. Pass

ig. J5. Squamous cell carcinoma. Chicken skin. Cords of epidermal cells pene-trating the dermis. HE. Bar 50 \im.

ig. 56. Haemangioma on chicken skin. The lesion is circumscribed, raised andhaemorrhagic.

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Pathology of the integument 59

Fig. 37. Haemangioma composed of thin-walled irregular vascular spaces. HE.Bar 50 [im.

Fig. 38. Marek's disease. Tumour nodules centred on feather follicles.

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60 DA. Pass

.or-:/:-

r:"^ar- V» /V' l j V

- - « * . : T > . ' . ^

;g. 59. Marek's disease. Feather follicle epidermis. Numerous cells in the outerlayers contain nuclei with amorphous amphophilic inclusion bodies. (Slidekindly provided by C. Riddell). HE. Bar 25 fim.

Fig. 40. Marek's disease. Perifollicular aggregation of lymphoid cells. Note degene-ration of cells in the epidermis. HE. Bar 50 ytm.

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Pathology of the integument 61

a£»a

mtefflm**.

^ . 41Multiple 'feather cysts' ina canary. The bird hasbeen plucked to reveal thelesions.

Fig. 42'Feather cyst'. Note thedifferentiation of the epi-dermal lining towards fea-ther components, e.g. barbs(arrow). HE. Bar 500 ytm.

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62 D.A. Pass

Fig. 43Chrysanthemum or featherduster budgerigar.

j Fig. 44Clubbed down. Abnormaldown feathers.

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Pathology of the integument 63

, ; , • - - ; ; ; , %

Fig. 45Clubbed down. Longitu-dinal section of affectedfeather. The pulp is in-creased in amount, appearsoedematous and containscholestrol clefts. The fea-ther sheath is thickenedand there is a zone ofnecrosis of epidermis inthe neck of the follicle(arrow). HE. Bar 50 urn.

Fig. 46Galah (C. roseicapillaj se-verely affected with psit-tacome beak and featherdisease. (Reprinted fromthe Australian VeterinaryPractitioner by permissionof the Editor.

S ^MW.A,» k, "w -

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64 D.A. Pass

Fig. 47Budgerigar with psittacinebeak and feather disease(French moult) in whichrectrices and primary re-miges are missing. Contourfeathers are normal. (Re-printed from the AustralianVeterinary Practitioner bypermission of the Editor).Fig. 48Skin from sulphur-crestedcockatoo (C. galeritaj withPBFD. Note total absenceof down feathers and short,clubbed contour feathers.

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Pathology of the integument 65

Fig. 49. Hip region of a galah showing normal powder down feathers.

;̂ . 50. //;'p region of a galah with PBFD. Note that the powder down feathers areshort and almost devoid of plumulaceous barbs.

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Fig. 51. PBFD. Barb ridges of growing feather. Note necrotic epidermal cells,macrophages with dark cytoplasmic inclusions (arrows) and disorderlinessof the basal and intermediate layers. (Reprinted from the AustralianVeterinary Journal by permission of the Editor). HE. Bar 50 yjn.

^. 52. PBFD. Transverse section of regenerating feather. There is hyperkeratosisof the feather sheath and accumulation of inclusion body laden macro-phages in the pulp. Similar cells are present in the sheath. Necrotic cells arepresent in the follicular epidermis. (Reprinted from the Australian Veteri-nary Journal by permission of the Editor). HE. Bar 50 jum.

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Pathology of the integument 67

Fig. 53. Adhesion of barbs to the rachis as seen here has been referred to as 'nake-nuke'feathering. The lesion is not specific for reticuloendotheliosis virus in-fection. There was no evidence of REV infection in the case pictured here.

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Fig'. 54. Budgerigar fledgling disease. Note cytomegally, karyomegally and intra-nuclear inclusion bodies of epidermal cells in epidermal collar of growingfeather. (Slide kindly provided by C. Riddell). HE. Bar 50 [im.

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68 DA. Pass

Fig. 55. Papovavirus infection. Adult rainbow lorikeet fTrichoglossus haematodusj.Karyomegally in cells of barb ridges (arrows). HE. Bar 50 \im.

Fig. 56. Papovavirus infection. Adult rainbow lorikeet. Note ballooning degenera-tion and necrosis of epidermal cells in the epidermal collar of growingfeather. HE. Bar 50 \im.

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Pathology of the integument 69

Fig. 57. Poorly developed primary and secondary remiges in a 4-day-old broiler(right) compared to normal (left). This lesion was associated with degene-ration and necrosis of feather epidermis present at hatching (Fig. 58).

Necrosis, spongiosis and bullous formation in the epithelium of developingprimary feather. HE. Bar 50 (xm.

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Fig. 59. Owl. Erosion of the rhamphotheca of the beak due to chronic inflam-mation of the underlying dermis.

Fig. 60. Gang gang cockatoo fCallocephalon fimbriatumy. Enlargement of the upperbeak due to infection of the nasal cavity, premaxilla and integumentarystructures with Cryptococcus neoformans. The rhamphotheca was soft andflakey. Soft tumorous masses projected from the tomial edge on the left side.

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Pathology of the integument 71

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6i. Budgerigars. The bird on the right has chronic infection of the cere andbeak with Cnemidocoptes pilae. The bird on the left has a haemangio-sarcoma of the deep tissues of the upper beak.

62. Sulphur-crested cockatoo (C. galeritaj with chronic psittacine beak andfeather disease. The top and bottom beaks are elongated.

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Fig. 63. Beak. Psittacine beak and feather disease. Degeneration of epidermal cellshas resulted in splitting of the cornifying epidermis and fluid accumu-lation. (Reprinted from the Australian Veterinary Journal by permissionof the Editor). HE. Bar 500 (im.