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Avian Pathology
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Disorders of the avian female reproductive system


I. F. Keymer a a Ministry of Agriculture, Fisheries and Food, Veterinary Investigation Centre, Norwich, Norfolk, United Kingdom Online Publication Date: 01 July 1980

To cite this Article Keymer, I. F.(1980)'Disorders of the avian female reproductive system',Avian Pathology,9:3,405 419 To link to this Article: DOI: 10.1080/03079458008418424 URL: http://dx.doi.org/10.1080/03079458008418424

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Avian Pathology, 9: 405-419, 1980

DISORDERS OF THE AVIAN FEMALE REPRODUCTIVE SYSTEM1

I.F. KEYMER Ministry of Agriculture, Fisheries and Food, Veterinary Investigation Centre, Norwich, Norfolk, United Kingdom SUMMARY An analysis is provided of reproductive disorders encountered at necropsy of 1666 adult, female birds excluding poultry. The results are compared with other accounts of these disorders in non-domesticated species and poultry. At least 650 different species were examined, belonging to 24 of the 27 avian orders. All were non-domesticated birds, with the exception of 133 budgerigars, 48 canaries and 4 pigeons. Reproductive disorders were found in 148 (8.9%) representing 88 different species in six orders. There was no conclusive evidence of species susceptibility. Some individuals were affected with more than one type of disorder, the most prevalent being obstruction of the oviduct and ectopic ovulation; in each case 28.6% of 161 disorders. Less common disorders were oophoropathies (16.8%), salpingitis without apparent obstruction (10.6%), neoplasia (4.3%), ruptured oviduct (3.1%) and miscellaneous disorders (8.0%). Domestic poultry bred for egg production are probably more susceptible to reproductive disorders than non-domesticated species. In the latter birds predisposing causes include senility and bacterial infections, but many more are probably involved. INTRODUCTION Disorders of the mature female reproductive system are common in domestic poultry in which they can be of considerable economic importance by causing mortality and loss of egg production. These disorders also occur in domesticated cage birds such as budgerigars (Melopsittacus undulatus) and canaries (Serinus canaria)as well as in non-domesticated species of cage and aviary birds, hindering breeding and often resulting in death. It is remarkable that comparatively little attention has been paid to these abnormalities. It was therefore decided that an analysis of female reproductive disorders found post mortem in a wide variety of birds at the London Zoo during the course of a 10-year period
Received 30 November 1979 Accepted 28 January 1980 1 Paper presented at a Symposium "Tagung Krankheiten der Vgel", Munich, 7th and 8th March 1979, based mainly on work carried out at the Zoological Society of London. A German summary of this paper has been published in Deutsche Veterinrmedizinische Gesellschaft e V. 10-23.

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might help to clarify the causes and prevalence of the various types that occur. The emphasis in this survey is on the types of disorders rather than the species affected. The anatomy of the reproductive tract is similar in all species and closely resembles that of the domestic fowl (King and McLelland, 1975). It is not surprising, therefore, that the results of this survey show little variation between birds in different species or even between different orders. Most text books dealing with avian diseases have only small sections or chapters devoted to the subject, for example, those by Blount (1947), Altara (1957), Hilbrich (1963), Biester and Schwarte (1965), Lesbouyries (1965), Hungerford (1969), Petrak (1969), Hofstad et al. (1978), Kronberger (1973) and Arnall and Keymer (1975). Most accounts are of a general nature, and unlike the present investigation, not based on surveys. Some notable exceptions, however, are the monograph on salpingitis and salpingo-peritonitis in the domestic fowl by Lindgren (1964), the clinical study in pet psittacine and passerine birds by Hasholt (1966) and surveys in domestic fowls by Valsala and Sivadas (1971) and Singh et al. (1977). Blackmore (1969) also gave a good account of reproductive disorders in non-domesticated species, based mainly on the pathological aspects. The general opinion is that reproductive disorders are most likely to occur in heavylaying poultry or in cage birds such as budgerigars and zebra finches (Poephila (= Taeniopygia) guttata), which for commercial purposes are encouraged to lay excessive numbers of eggs. The present survey, however, suggests that the aetiology is complex and that malfunction may be related to a variety of causes. MATERIALS AND METHODS The survey is based on 4287 necropsies on non-domesticated species of birds, 1666 of which were considered to be adult (i.e. sexually mature) female birds. Some of these birds were old. A bird was considered to be old when it had lived for a longer period than would normally be expected for that or a closely related species, bearing in mind the average life expectancy in captivity and in the free state when this was known or could be assessed. For example, small species such as passerines usually have a shorter life expectancy than larger birds. The term "senility" is used here as in a previous survey (Keymer, 1977) for "old" and debilitated birds showing signs such as poor quality plumage, hyperkeratosis of the scaly parts of the feet and legs, distortion of the beak, atrophy of the gonads or arteriosclerosis. The examinations were carried out at London Zoo during the period 1 January 1966 to 31 December 1975. Approximately three quarters of the birds were the property of the Zoological Society of London. The remainder were birds from other collections, pets submitted by practising veterinary surgeons, or free-living wild birds. The 1666 adult females examined included at least 650 different species. They belonged to 24 of the 27 orders in the class Aves (Table 1), the missing orders being the Casuariiformes (Cassowaries and emus), Apterygiformes (kiwis) and Caprimulgiformes (nightjars). The adult female birds (Table 1) were mostly non-domesticated species, none of which was represented by more than 10 individuals. However, 133 domestic budgerigars, 48 canaries and four pigeons (Columba livid) are included, but no breeds or species of domestic poultry. All carcases were examined for macroscopic lesions. Routine histological examinations

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were carried out when indicated, unless impractical because of decomposition. Heart blood smears and various organs were examined for parasites when possible. Bacteriological and mycological examinations, using routine cultural methods, were carried out on a high proportion of specimens. Tissues were submitted for virus isolation when this was thought necessary, although no attempts were made to isolate the viruses of infectious bronchitis and epidemic tremor (avian encephalomyelitis) or adenoviruses. Table 1. Types of mature female birds examined and affected with reproductive disorders. Orders Rheiformes Struthioniformes Tinamiformes Sphenisciformes Galliformes Columbiformes Anseriformes Gruiformes Strigiformes Pelecaniformes Psittaciformes Ciconiiformes Cuculiformes Falconiformes Passeriformes Examples of species Rheas Ostriches Tinamous Penguins Quails, pheasants, partridges, pea-fowls, jungle fowl and capercaillies Pigeons and doves Ducks, geese and swans Rails, waterhens, crakes and cranes Owls Pelicans Budgerigars, cockatiels, lovebirds, cockatoos, lorys, parakeets and parrots Herons, egrets, storks and spoonbills Touracos Eagles, hawks, falcons, harriers and secretary birds Canaries, zebra and other finches, weavers, mynahs, starlings, bulbuls, cardinals, pittas, magpies, mesias, whydahs, etc. Gulls, thicknees, lapwings Kingfishers, bee-eaters, rollers, hoopoes and hornbills Barbets, woodpeckers Hummingbirds Shearwaters Diver Grebe Mousebird or colie Trogon All species TOTAL: Numbers of mature females examined
3 2 2 33

Numbers affected
2 1 1 8

Percentage affected 66.7 50.0 50.0 24.2 20.0 15.4 14.9 12.5 10.5
9.1

120 91 161 32 38 11

24 14 24 4 4 1

365 61 13 41

31 5 1 2

8.5 8.2 7.7 4.9

504 95 40 38 12 2 1 1 1 1

Charadriiformes Coraciiformes Piciformes Apodiformes Procellariifortnes Gaviiformes Podicipediformes Coliiformes Trogoniformes

23 3 0 0 0 0 0 0 0 0 148

4.6 3.2 _ 8.9

1666

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I.F. Keymer

RESULTS It can be seen from Table 1 that reproductive disorders of various types were encountered in 148 (8.9%) of 1666 different individuals, representing 16 different orders. No reproductive disorders were found in representatives of eight orders but this is not surprising because relatively few birds were examined in these orders. When less than 50 representatives of an order were examined it is probably unreliable to draw conclusions from the percentages except perhaps when these are very high or very low. Eighty eight different species (not listed for the sake of brevity) were affected, the most common being budgerigars with 13 out of 133 (9.8%). Numbers of other species were much smaller. With the possible exception of budgerigars, there was no evidence that any particular species was especially susceptible. The unusually high percentage of affected penguins (representing three different species) is probably due to the fact that a high proportion were old birds (see later). Also, during a part of the period of this survey there was evidence of hypovitaminosis A in some of the penguins (Keymer, 1972, 1974, 1976) and this may have been a contributory factor. The numbers of individuals examined in the orders Coraciiformes and Piciformes were not very high (40 and 38 respectively), but it is interesting to note that no disorders were encountered in these birds. This is in contrast to 12.5% of 32 birds in the Gruiformes and 10.5% of 38 in the Strigiformes. The reason for these discrepancies is again probably not connected with host susceptibility, but due to the fact that comparatively few species of Coraciiformes and Piciformes were being bred at the zoo at the time, especially in contrast to members of the Strigiformes. The relatively high percentages of affected birds in the Galliformes (20%), Columbiformes (15.4%) and Anseriformes (14.9%) can probably be explained by the fact that many species in these orders were breeding and included numerous older birds (see later). The Psittaciformes and Ciconiiformes with 8.5% and 8.2% affected respectively were nearer the overall average (8.9%) for this survey. The comparatively low figure of 4.6% of 504 passerine birds is unlikely to denote a low susceptibility in these birds but is probably due to the fact that although some were breeding birds many were not. The two most common and widespread disorders were obstruction of the oviduct and ectopic ovulation (Table 2). Oophoropathies of various types were also relatively common. Some individuals were affected with more than one type of disorder, there being 161 disorders (Table 2) in 148 birds (Table 1). Obstruction of the oviduct The 46 cases occurred in a wide variety of birds representing 11 orders (Table 2). An analysis of the cases of obstructed oviducts (Table 3) revealed that this occurred most frequently (21.2%) in old birds. It was nearly always associated with an obvious salpingitis. Obstructions appeared to be due mainly to the presence of necrotic egg material (20%), a broken-shelled egg (12.9%), normal soft-shelled egg (12.9%) (usually in the posterior half of the oviduct) or to a localised infection with Escherichia coli (12.9%). However, as discussed later there was undoubtedly a variety of predisposing causes, in addition to senility already mentioned. Taking into consideration the numbers of breeding birds examined and excluding possible predisposing causes such as senility and hypovitaminosis A in the order Sphenisciformes, it will be seen from Table 2 that pigeons and doves (Columbiformes) and Galliformes, to which the domestic fowl and game birds belong, appeared to be the most susceptible to obstruction of the oviduct; 7.7 and 5.0% respectively. However,

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Table 2. Types of disorders and birds affected.


Numbers of Numbers of Percentages birds of birds Avian orders affected adult female birds affected affected examined 1 Obstruction of oviduct or Tinamiformes 2 50.0 cloaca (with or without Gruiformes 9.4 32 3 Salpingitis and/or egg 7 7.7 Columbiformes 91 peritonitis) Number: 46, representing Sphenisciformes 2 33 6.1 28.6% of 161 disorders Galliformes 6 5.0 120 Falconiformes 41 2 4.9 Psittaciformes 12 3.3 365 1 Strigiformes 38 2.6 Anseriformes 4 161 2.5 1 Ciconiiformes 61 1.6 Passeriformes 504 7 1.4 1 Ectopic ovulation (with or Rheiformes 3 33.3 without egg peritonitis and Galliformes 9 7.5 120 with or without salpingitis) 2 Sphenisciformes 33 6.1 Number: 46, representing 28.6% of 161 disorders Anseriformes 9 5.6 161 2 3.3 Ciconiiformes 61 2.7 Psittaciformes 365 10 Columbiformes 2 2.2 91 2 2.1 Charadriiformes 95 504 1.8 Passeriformes 9 Struthioniformes 2 1 Oophoropathies, including 50.0 oophoritis, oophorrhagia and Pelecaniformes 11 1 9.1 degenerative ova (with or 1 13 7.7 Cuculiformes without salpingitis) Number: 27, representing Sphenisciformes 2 6.1 33 16.8% of 161 disorders 2 Strigiformes 38 5.3 Galliformes 5 4.2 120 Anseriformes 161 6 3.7 Columbiformes 2 2.2 91 1 Ciconiiformes 61 1.6 504 5 Passeriformes 0.9 1 Psittaciformes 365 0.3 Type of disorder and number of cases

continued..

410 Table 2 continued Type of disorder and number of cases Salpingitis without obstruction. Number: 17, representing 10.6% of 161 disorders

L.F. Reymer

Neoplasia Number: 7, representing 4.3% of 161 disorders

Ruptured oviduct. Number: 5, representing 3.1% of 161 disorders Miscellaneous disorders Number: 13, representing 8.0% of 161 disorders. Ruptured egg in oviduct Prolapse of oviduct

Numbers of Numbers of Percentages Avian orders affected adult female birds of birds birds affected affected examined 2 Rheiformes 3 66.7 5 Galliformes 120 4.2 Anseriformes 161 3.7 6 Gruiformes 1 32 3.1 1 Sphenisciformes 33 3.0 2 Psittaciformes 365 0.6 Columbiformes 1 91 1.1 Charadriiformes 95 1 1.0 1 Galliformes 120 0.8 1 Anseriformes 161 0.6 2 504 0.4 Passeriformes 1 Psittaciformes 365 0.3 32 1 Gruiformes 3.1 Anseriformes 161 3 1.9 1 Columbiformes 1.1 91 Galliformes Psittaciformes Anseriformes Galliformes Columbiformes Psittaciformes Sphenisciformes Psittaciformes Psittaciformes Strigiformes Galliformes Ciconiiformes
120 365 161 120 91 365 33 365 365 38 120 61 1 2 1 1 1 1 1 1 1 1 1 1 0.8 0.6 0.6 0.8 1.1 0.3 3.0 0.3 0.3 2.6 0.8 1.6

Two oviducts Presence of a functional right ovary Oophorocystosis Impaction of cloaca and cloacitis

a Right ovaries were observed in 10 birds (24.3%) representing nine species and eight genera of diurnal birds of prey. The anomaly can therefore probably be regarded as a normal finding in the Falconiformes. as already pointed out, both orders contained a relatively high proportion of older birds, so little importance can be attached to these figures. Ectopic ovulation Of the total of 46 cases affecting nine orders (Table 2), egg peritonitis was also present in at least 40, being manifested by the presence of turbid yolky fluid or "cheesy", yellowish masses of yolk material in the peritoneal cavity. Peritoneal adhesions were usually present, but not always obvious. Egg peritonitis was associated with coliforms in the fresh carcases of at least 19 birds. E. coli may have been a significant pathogen in many cases, but owing to autolysis bacteriological examination was not always carried out. There was also one case each

Disorders of female reproductive system

411

Table 3. Possible causes of obstruction of the oviduct. Contributory causes Senility Presence of necrotic egg material Presence of broken-shelled egg Presence of normal soft-shelled egg Localised bacterial infection, Escherichia coli E. coli and Streptococci Generalised infection. Tuberculosis (Mycobacterium avium infection) Presence of over-sized soft-shelled egg Presence of over-sized hard-shelled egg Presence of normal egg Presence of egg with two shells Presence of intact shelled egg containing necrotic egg material Presence of incompletely calcified shelled egg Intestinal strangulation with normal egg present Presence of urate encrusted egg in cloaca Generalised infection. Erysipelas (Erysipelothrix rhusiopathiae infection) Obesity Number of birds affected 18 17 11 11
%of

birds affected 21.2


20

io\
H 3 3 2 2 1 1 1 1 1 1 1

12.9 12.9 12.9


3.5 3.5 2.3 2.3 1.2 1.2

1.2 1.2 1.2 1.2 1.2

of egg peritonitis associated with pseudotuberculosis (Yersinia pseudotuberculosis infection), Staphylococcus and Proteus spp. In the former two cases the affected bird was a cockatiel (Nymphicus hollandicus). In this group of disorders, taking into account the complicating factors mentioned in the last paragraph, the Galliformes were once again amongst the most affected groups with a prevalence of 7.5%. Similarly the Anseriformes, with a relatively high proportion of older birds, had 5.6% of adult females affected. Oophoropathies Ovarian inactivity was excluded from the analysis because without histological examination of all ovaries it was impossible to know if this was physiological or pathological. However, in the majority it was probably the former. The majority of the 27 diagnoses of oophoropathy (Table 2) were based on the naked eye appearance of the developing yolks in the ovary and included angulated, inspissated, pedunculated and haemorrhagic ova. Eleven avian orders were affected. Doubtful lesions were excluded in the absence of histological examination. Relatively few yolks were cultured for bacteria, and Salmonella spp. were not recovered. However, various Salmonella spp. (although excluding S. pullorum which can infect the ovary of the domestic fowl), were isolated on approximately 30 occasions from females during this 10-year period. In one bird, namely a Knysna touraco (Tauraco corythaix) which died from S. typhimurium infection, oophoritis was present, but unfortunately the ovary was not cultured. However, Mycobacterium (sp. not identified, but probably M. avium) was cultured and found associated with oophoritis in a collared turtle dove {Streptopelia decaocto) and similarly E. coli associated with oophoritis in a night heron (Nycticorax

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I.F. Keymer

nycticorax) and a Californian crested quail (Lophortyx californica). Once again it is the Galliformes and Anseriformes with 4.2% and 3.7% respectively that stand out as being the most significantly affected orders. In spite of the large numbers of birds examined in the Passeriformes and Psittaciformes very few adult hens showed oophoropathies. This may have been because the majority of these species are small birds and lesions were overlooked in the absence of routine histological examinations on all ovaries. Salpingitis A simple salpingitis without apparent obstruction of the oviduct was appreciably less common than the previous disorders and occurred in only six orders (Table 2). It was sometimes associated with ectopic ovulation and egg peritonitis, being an extension of the inflammatory reaction from the abdomen. On other occasions, had the bird lived, the salpingitis might well have resulted in obstruction of the oviduct as it was usually associated with necrotic egg material or eggs in some other form. A few cases were shown to be associated with.fi1. coli. As with internal laying and oophoropathies, the most significantly affected orders were again the Galliformes (4.2%) and Anseriformes (3.7%), probably reflecting the association of salpingitis with the other two disorders. Table 4. Neoplasia of the reproductive tract and species affected.
Species Age Anseriformes Chilean teal (Anas 5 years flavirostris) Galliformes Jungle fowl (Gallus Unknown gallus) Charadriiformes Over Australian thicknee 24 years (Burhinus magnirostris) Columbiformes At least Barred shouldered dove 6 years (Geopelia humeralis) Psittaciformes . At least Pennant's parakeet 4 years (Platycercus elegans) Passeriformes Rufous-necked weaver (Ploceus cucullatus) Green singing finch (Serinus morzambicus) At least 8 years At least 1 year Type of Neoplasia Suspected leukosis with ovarian involvement. Lesions impossible to differentiate with certainty from Marek's disease (Appleby and Keymer, 1968). Marek's disease involving ovary (Appleby and Keymer, 1973). Diffuse papillary adenocarcinoma of ovary and serous surfaces of abdominal viscera (Appleby and Keymer, 1971). Luteinising granulosa cell tumour of ovary.

Papillary cystadenoma probably arising from the oviduct (Appleby and Keymer, 1968). Leukosis with ovarian involvement.

Luteoma of ovary (Appleby and Keymer, 1973).

Neoplasia Seven cases of neoplasia were encountered (Tables 2 and 4) and, with one exception, all involved the ovary. There was no evidence of order or species susceptibility. Although in most birds the exact age was unknown, it is likely that all were old birds. Ruptured oviduct The fact that three of the five cases were in members of the Anseriformes (Table 2)

Disorders of female reproductive system

413

is probably of little significance, except that, as already shown, birds in this order were quite frequently affected with other reproductive disorders. The causes of this uncommon disorder were not clear. The cases were associated with soft-shelled eggs or necrotic egg material: the rupture occurred at various sites. Miscellaneous disorders These comprised six rare disorders affecting birds in seven orders. Ruptured eggs. Ruptured soft-shelled eggs were found in the oviduct of a budgerigar, cockatiel and Californian crested quail and a broken-shelled egg in a common pochard (Aythyaferina). In each case there was no convincing evidence of any lesions, probably because the eggs had either ruptured shortly before or after death. Prolapse of the oviduct. This occurred associated with the presence of a yolk in a diamond dove (Geopelia cuneatd) with a soft-shelled egg in a Chinese painted quail (Excalfactoria chinensis) and with the remains of a partly dehydrated hard-shelled egg in a budgerigar. In the latter bird a soft-shelled egg was also present in the anterior part of the oviduct. In the quail and the budgerigar only the posterior part of the oviduct had prolapsed, but in the dove most of the organ had done so. In each bird the actual cause of the prolapse was obscure and except in the quail, the prolapse appeared to be recent. Two oviducts. An unusual finding was the presence of two oviducts in a budgerigar and a Humboldt's penguin (Spheniscus humboldti). The anomaly in the budgerigar has been illustrated by Keymer and Dennett (1975). In both cases only the left ovary could be detected, although it is possible that the right gonad was rudimentary and therefore overlooked. Presence of right ovary. Both left and right ovaries were observed in nine different species of diurnal birds of prey representing three of the five families of the Falconiformes. Members of the families Cathartidae and Pandionidae were not examined. As 24.3% of the birds had two normal ovaries this phenomenon can probably be regarded as normal. Two ovaries were also found in three other birds, namely a funereal cockatoo (Calyptorhynchus funereus), an Aharoni's eagle owl (Bubo bubo interpositus) and a Fraser's eagle owl (B. poensis). However, in hen Psittacines and owls the presence of a right gonad can probably be regarded as an abnormality, because in each bird the ovary appeared to be vestigial. In the Fraser's eagle owl it was inflamed and undergoing some necrosis. Oophorocystosis or cystic ovary was seen only in a pheasant (Phasianus colchicus) that was at least 8 years old. A pedunculated cyst was present measuring approximately 4 cm in diameter. Impaction of the cloaca and cloacitis. It is surprising that although obstruction of the oviduct was a common finding, impaction confined to the lower part of the tract i.e. the cloaca, was encountered only once. The affected bird was an 8-year-old African cattle egret (Bubulcus ibis). A severe cloacitis ("vent gleet") was present, with many adhesions between the intestinal wall and the lower part of the oviduct. The cloaca was grossly distended and impacted with a normal-shelled egg. The wall of the organ was intensely congested and in places ulcerated, and it had numerous adhesions to the egg shell. On bacteriological examination E. coli and Proteus spp. were isolated from the cloacal epithelium. The small numbers of miscellaneous disorders diagnosed preclude any conclusions regarding species, family or order susceptibility.

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I.F. Keymer DISCUSSION

There are undoubtedly many predisposing causes of reproductive disorders in birds and these will be discussed first. When dealing with non-domesticated species it is necessary to consider the possibility of species susceptibility, that might be linked with such factors as normal egg shape, egg surface texture or clutch size. As outlined and illustrated by Pitman (1964) and also illustrated by Keymer and Dennett (1975), these vary considerably within different orders and even species and the present survey provides no evidence that any of the variations are related to malfunctioning of the female reproductive system. This is not surprising, because different species have evolved so that these variations are beneficial and not the reverse. Both in captivity and in the wild it is inevitable that unfavourable conditions may sometimes occur which adversely affect the functioning of the reproductive system. Although no disorders in free-living species were encountered in this survey, they have been reported (Jennings, 1959; Keymer, 1958; Macdonald, 1962). The possible adverse effects in captive birds of excessive egg laying, breeding out of season, dietary deficiencies, fright and stress, poor general health, violence, obesity, chilling, hormonal imbalance, moulting, increasing age and even enteritis have all been discussed to a varying extent by Arnall (1975), Blackmore (1969), Hasholt (1966) and Wailly (1976 and 1977). It is important therefore, for the clinician to consider all these possibilities when diagnosing and treating reproductive disorders in the live bird and also to remember that they can occur in non-breeders (Blackmore, 1969), although less frequently. In the present pathological survey, no records of these predisposing causes were made, with the exception of noting senility and obesity as possible causes of obstruction of the oviduct (Table 3). Most authorities do not mention increasing age, but in this survey senility was found to be the most common factor associated with obstruction of the oviduct. This is probably because most references are to domestic poultry which are killed before old age is reached. Some workers (e.g. Arnall, 1975; Wailly, 1977) have considered obesity to be a predisposing cause of obstruction of the oviduct. In the domestic fowl many cases of salpingitis have been associated with excessive deposits of abdominal fat (Vasala and Sivadas, 1971), but in this survey obesity did not appear to play an important role in non-domesticated species (Table 3). Obstruction of the oviduct and ectopic ovulation (both with and without salpingitis or egg peritonitis) were of equal importance and the most common abnormalities (Table 2), each accounting for 28.6% of all disorders. Indeed, Lindgren (1964) considered these disorders to represent one type of syndrome. Both he and Valsala and Sivadas (1971) found these disorders in the domestic fowl to be less common than oophoritis. This is in contrast to the findings of the present survey and to those of Randall etal. (1977) who found that egg peritonitis was the most important reproductive disorder resulting in death of caged laying hens. Lindgren (1964) and Valsala and Sivadas (1971) did not differentiate between salpingitis associated with obstruction of the oviduct and uncomplicated salpingitis. In this survey the latter was less prevalent than oophoritis. It must be emphasised that sometimes more than one of the abnormalities listed in Tables 2 and 3 were present in the same bird. For example some individuals had oophoritis, egg peritonitis, salpingitis and obstruction of the oviduct with necrotic egg material, hence the reason why 85 abnormalities (Table 3) occurred in only 46 cases of obstructed oviduct (Table 2). There is little doubt that salpingitis was present

Disorders of female reproductive system

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in most if not all cases of obstruction of the oviduct, but it is not listed in Table 3 because in many cases no histological examination was carried out to confirm its presence. It was found that necrotic egg material often caused obstruction of the oviduct (20% of cases). Bacterial infections can also be relatively important. E. coli infection not infrequently caused salpingitis (12.9%). Indeed it is quite likely that this infection was more common than the figure suggests, as on many occasions the oviduct was not examined bacteriologically. The importance of E. coli as a probable cause of salpingitis and salpingoperitonitis (egg peritonitis) in the domestic fowl was emphasised by Lindgren (1964) and Sharma and Singh (1968). Also Valsala and Sivadas (1971) demonstrated experimentally that E. intermedia and Pradhan and Nayak (1973) that E. coli could produce salpingitis and oophoritis respectively in chickens. Bisgaard (1975) isolated an organism resembling Actinobacillus lignieresii from the ovary and oviduct of domestic white Pekin ducks affected with salpingitis, but also from the ovary of ducks showing no lesions in the reproductive tract. He also attributed Pasteurella multocida and E. coli infections as causes of salpingitis in ducks. Domermuth et a/. (1967) demonstrated that Mycoplasma gallisepticum could cause salpingitis in the domestic fowl. Unfortunately, special cultures for the isolation of Mycoplasma spp. were not used in this survey, although salpingo-peritonitis was found associated with pseudotuberculosis and other bacterial infections and obstructions of the oviduct with tuberculosis and erysipelas (Table 3). Bacterial infections therefore clearly play a significant role and it is important to carry out bacteriological and histological examinations in all cases of suspected salpingitis. The presence of large or misshapen eggs in the oviduct, especially at the beginning or end of the laying period, have been recorded by some workers (Arnall, 1975;Wailly, 1976 and 1977) as causes of egg retention or oviduct obstruction. The results of the present survey, support this opinion although such egg abnormalities were not common (Table 3). It is perhaps surprising that neoplasia accounted for as much as 4.3% of all reproductive disorders and that only one psittacine bird was affected, especially as 133 of the 365 psittacines were budgerigars. Petrak and Gilmore (1969) found neoplasms involving the reproductive tract to be common in this species. They also recorded numerous examples found by others. For example Blackmore (1969) listed 24 ovarian tumours in the budgerigar and said that neoplasia of the oviduct was apparently confined to budgerigars. More recently, however, Nath and Singh (1971) have recorded a leiomyoma of the oviduct in a domestic fowl. Regarding miscellaneous disorders (Table 2), Blackmore (1969) suggested that rupture of the oviduct was secondary to egg peritonitis and not the cause. He also stated that prolapse of the oviduct occurs in all species, especially in budgerigars and canaries and was always associated with egg production and physiological hyperplasia of the oviduct. In this survey, however, it was not encountered in canaries and only once in a budgerigar. Cystic hyperplasia of the oviduct was mentioned by Blackmore (1969), Lesbouyries (1965) and Arnall (1975), but this abnormality was not recognised in the present survey. Oophorocystosis was seen only once and this agreed with Blackmore's opinion that primary cystic ovaries are infrequently seen in cage birds. Hasholt (1966) and Wailly

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(1976), however, recorded them in budgerigars and in canaries. The frequent presence of two functional ovaries in the Falconiformes (Table 2) is worthy of special mention because this might be regarded as an abnormality by those not experienced with diurnal birds of prey. The findings corresponded with the statement by Matthews (1964) that in various species of Falconiformes both ovaries may persist, although the right oviduct remains vestigial. He stated that the right ovary was most highly developed in the Accipitridae and that it is present, but progressively smaller, in the Falconidae and Cathartidae. According to King and McLelland (1975) in kiwis (Apteryx spp.) both ovaries are regularly present, but these birds were not examined in this survey. Trematodes may occasionally infest the oviduct of certain species of gallinaceous birds such as the domestic fowl and also waterfowl i.e. Anseriformes (Byrd, 1972) but no parasites of any kind were found in this survey in the reproductive tract. The role of viruses in reproductive disorders is almost unknown. However, in the domestic fowl, infectious bronchitis can be associated with disorders of the reproductive tract, but the disease appears to be confined to that species. The virus causing epidemic tremor in the domestic fowl also naturally infects three other species of gallinaceous birds (Hofstad etai, 1978). Although little is known of the host range of adenoviruses it seems likely that it may be wide because McFerran et al. (1976) referred to several susceptible species representing the Galliformes, Columbiformes, Anseriformes and Psittaciformes. There appears to be no evidence that adenoviruses cause reproductive disorders, although in common with the viruses of epidemic tremor and infectious bronchitis they can be associated with decreased egg production in the domestic fowl (Hofstad etal, 1978). The overall incidence of reproductive disorders in non-domesticated species in this survey was found to be only 8.9% although in the budgerigar it was 9.8%. When compared with similar surveys in domestic poultry, such as that carried out by Singh et al (1977) and others quoted by them, these figures are low. They obtained a figure of 27.5% and quoted others of 40%, 25%, 16% and 8%. Randall et al. (1977) recording 15.1% in caged, laying, domestic hens. This suggests that domestic poultry bred for egg production are more susceptible to reproductive disorders than non-domesticated species of birds. In conclusion, non-domesticated species appear to be less susceptible to reproductive disorders than domestic poultry. There is no evidence of order, family or even species susceptibility. Disorders can occur in non-breeders, i.e. hens that have not been mated, but they are more common in breeding birds. The most common disorders are obstruction of the oviduct and ectopic ovulation, the latter often resulting in egg peritonitis. Oophoropathies are apparently a little less common. Egg peritonitis and obstruction of the oviduct appear to be equally important and often occur together. They should therefore probably be regarded as one syndrome as suggested by Iindgren (1964). There appear to be many predisposing causes of reproductive disorders, especially for obstruction of the oviduct. Senility is an important factor but obesity does not appear to play a significant role in non-domesticated species. E. coli and other bacterial infections are sometimes associated with reproductive disorders, but the role - of M. gallisepticum and viruses are unknown in non-domesticated birds and need investigation. The presence of a right ovary in diurnal birds of prey (Falconiformes) is common, but in other species should probably be regarded as an abnormality.

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Acknowledgements Over the years I was greatly indebted to the technical staff of the Pathology Department, Zoological Society of London for assistance in many ways, especially Miss D. Ridealgh, Miss C. Carroll and Messrs. H. Corbett, R. Cinderey, J. Burlison and S. Pugsley. Mr. P. Olney, The Curator of Birds, gave me helpful suggestions regarding analysis and interpretation of the records. REFERENCES
Altara, I. (1957). Patologia aviaria igiene degli allevamenti avicoli. Veterinaria Italiana: 264-289. Appleby, E.C. and Keymer, I.F. (1968). Some tumours in captive wild mammals and birds. A brief report. Erkrankungen der Zootiere. Verhandlungsbericht des X. Internationalen Symposiums ber die Erkrankungen der Zootiere. Salzburg, pp. 199-200. Appleby, E.C. and Keymer, I.F. (1971). More tumours in captive wild mammals and birds. A second brief report Erkrankungen der Zootiere. Verhandlungsbericht des XIII. Internationalen Symposiums ber die Erkrankungen der Zootiere. Helsinki, pp.241-244. Appleby, E.C. and Keymer, I.F. (1973). More tumours in captive wild animals: A third brief report. Erkrankungen der Zootiere. Verhandlungsbericht des XV. Internationalen Symposiums ber die Erkrankungen der Zootiere. Kolmarden. pp.347-351. Arnall, L. (1975). The Reproductive or Genital System. In: Bird Diseases, pp.26 7-276. Arnall, L. and Keymer, I.F., London: Baillire Tindall Arnall, L. and Keymer, I.F. (1975). An Introduction to clinical diagnosis and treatment of diseases in birds other than poultry. In: Bird diseases, London: Baillire Tindall. Biester, H.E. and Schwarte, L.H. (1965). Diseases of Poultry, 5th Edition. Ames, Iowa: Iowa State University Press. Bisgaard, M. (1975). Characterisation of typical Actinobacillus lignieresii isolated from ducks with salpinigitis and peritonitis. Nordisk Veterinaermedicin, 27: 378-383. Blackmore, D.K. (1969). Diseases of the Reproductive System. In: Diseases of Cage and Aviary Birds, pp.321-329. Edited by Petrak, M.L., Philadelphia: Lea and Febiger. Blount, W.P. (1947). Diseases of Poultry. London: Baillire, Tindall and Cox. Byrd, E.E. (1972). Trematodes. In: Diseases of Poultry, pp.935-936. Edited by Hofstad, M.S., Calnek, B. W., Helmboldt, C.F., Reid, W.M. and Yoder, Jr., H. W., 6th Edition, Ames, Iowa: Iowa State University Press. Domermuth, C.H., Cross, W.B. and du Bose, R.T. (1967). Mycoplasmal salpingitis of chickens and turkeys. Avian Diseases, 11: 393-398. Hasholt, J. (1966). Diseases of the Female Reproductive Organs in Pet Birds. Journal of Small Animal Practice, 7: 313-320. Hilbrich, P. (1963). Krankheiten des Geflgels, unter besonderer Bercksichtigung der Haltung und Ftterung. Verlag Hermann Kuhn K.G. Schwenningen am Neckar. Hofstad, M.S., Calnek, B.W., Helmboldt, C.F., Reid, W.M. and Yoder, Jr. H.W. (1978). Diseases of Poultry, 7th Edition. Ames, Iowa: Iowa State University Press. Hungerford, T.G. (1969). Diseases of Poultry including Cage Birds and Pigeons, 4th Edition. Sydney: Angus and Robertson Ltd. Jennings, A.R. (1959). Diseases of wild birds, Fifth report. Bird Study, 6: 19-22. Keymer, I.F. (1958). A Survey and Review of the Causes of Mortality in British Birds and the Significance of Wild Birds as Disseminators of Disease. Part I. Veterinary Record, 70: 713-720. Keymer, I.F. (1972). Report of the Pathologist. 1969 and 1970. The Zoological Society of London. Scientific Report 1969-1971. Journal of Zoology, London. 166: pp.524 and 533. Keymer, I.F. (1974). Report of the Pathologist. 1971 and 1972. The Zoological Society of London. Scientific Report 1971-1973. Journal of Zoology, London. 173: pp.56 and 72. Keymer, I.F. (1976). Report of the Pathologist, 1973 and 1974. The Zoological Society of London, Scientific Report 1973-1975. Journal of Zoology, London. 178: p.463. Keymer, I.F. (1977). Cataracts in birds. Avian Pathology, 6: 335-341. Keymer, I.F. and Dennett, T.C. (1975). In: Bird Diseases, p.384. Edited by Arnall, L. and Keymer, I.F., London: Baillire Tindall. King, A.S. and McLelland, J. (1975). Outlines of Avian Anatomy, London: Baillire Tindall. Kronberger, H. (1973). Haltung von Vgeln. Krankheiten der Vgel. V.E.B. Gustav Fischer Verlag Jena.

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Lesbouyries, G. (1965). Pathologie des Oiseaux de Basse-Cour. Paris: Vigot Frres. Lindgren, N.O. (1964). On the aetiology of salpingitis and salpingo-peritonitis of the domestic fowl. A statistical and experimental investigation. Stockholm. AkademiskAvhandling. Macdonald, J. W. (1962). Mortality in wild birds with some observations on weights. Bird Study, 9: 147-167. McFerran, J.B., Connor, T.J. and McCracken, R.M.M. (1976). Isolation of Adenoviruses and Reoviruses from Avian Species other than Domestic Fowl. A vian Diseases, 20: 519-524. Matthews, L.H. (1964). Reproductive System. In: A new Dictionary of Birds, pp.691-692. Edited by Sir A. Landsborough Thomson, London: Nelson. Nath, R. and Singh, CM. (1971). Studies on pathology of uro-genital tract of poultry. 1. Pathology of genital tract Haryana Agricultural University Journal of Research, 1: 106-111. Petrak, M.L. (1969). Diseases of Cage and Aviary Birds. Philadelphia: Lea and Febiger. Petrak, M.L. and Gilmore, C.E. (1969). Neoplasms. In: Diseases of Cage and Aviary Birds, pp.459-489. Edited by Petrak, M.L., Philadelphia: Lea and Febiger. Pitman, C.R.S. (1964). In: A New Dictionary of Birds, pp.238-242. Edited by Sir A. Landsborough Thomson. London: Nelson. Pradhan, H.K. and Nayak, B.C. (1973). Studies on Pathology of the Female Reproductive Tract of Domestic Fowls. II. Experimentally Induced Oophoritis and Egg Peritonitis with E. coli organisms. Indian Journal of Poultry Science, 8: 81-86. Randall, C.J., Blandford, T.B., Borland, E.D., Brooksbank, N.H. and Hall, S.A. (1977). A Survey of Mortality in 51 Caged Laying Flocks. A vian Pathology, 6: 149-170. Sharma, D.N. and Singh, C.M. (1968). Studies on Pathology of Female Genital Tract of Poultry with special reference to Egg Peritonitis incidence, Patho-Anatomy and Experimental Study. Indian Journal of Veterinary Science and Animal Husbandry, 38: 737-746. Singh, M.P., Mehrotra, R.L., Prasad, C.B. and Prasad, L.N. (1977). Studies on the incidence of egg-peritontiis, salpingitis and oophoritis in laying hens. Indian Veterinary Medical Journal, 1: 38-42. Valsala, K.U. and Sivadas, C.G. (1971). Salpingitis in the hen. Kerala Journal of Veterinary Science, 2: 105-108. Wailly, Ph. de. (1976). Les dominantes pathologiques des oiseaux de cage. Mdicine Vtrinaire, 152: 754-755. Wailly, Ph. de (1977). Troubles de la reproduction et anomalies du plumage chez les oiseaux de cage et de volire. Le Point Vtrinaire, 6: 53-59. RESUME Troubles de l'appareil gnital femelle des oiseaux Une analyse est faite des troubles de l'appareil gnital observs l'autopsie de 1666 oiseaux femelles adultes, l'exclusion des volailles. Les rsultats sont compars d'autres informations concernant ces dsordres chez les espces non domestiques et chez les volailles: Au moins 650 espces diffrentes ont t examines, appartenant 24 des 27 ordres de la classe des oiseaux. Tous taient des oiseaux non domestiques exception faite de 133 perruches onduls, 48 canaris et 4 pigeons. Des troubles de l'appareil reproducteur ont t trouvs chez 148 d'entre eux (8,9%) reprsentant 88 espces diffrentes appartenant 6 ordres. Il n'y avait pas apparemment de sensibilit d'espce. Quelques individus taient affects par plus d'un type de trouble, le plus frquent tant l'obstruction de l'oviducte et l'ovulation ectopique; dans chaque cas 28,6% des 161 troubles. Les troubles les moins frquent ont t les ovariopathies (16,8%), les salpingites sand obstruction apparente (10,6%), les noplasies (4,3%), les ruptures d'oviducte (3,1%) et les troubles divers (8%). Les volailles domestiques destines la production de l'oeuf sont probablement plus sensibles aux troubles de l'appareil reproducteur que les espces non domestiques. Chez ces dernires les causes prdisposantes telles que la snilit, les infections bactriennes et bien d'autres sont probablement impliques.

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ZUSAMMENFASSUNG Erkrankungen des weiblichen Geschlechtsapparates der Vgel Es wird eine Analyse der bei der Zerlegung von 1666 erwachsenen weiblichen Vgel ohne Wirtschaftsgeflgel festgestellten Vernderungen des Geschlechtsapparates vorgelegt. Die Ergebnisse werden mit anderen Zusammenstellungen solcher krankhaften Vernderungen bei nichtdomestizierten Vgeln und beim Wirtschaftsgeflgel verglichen. Es wurden mindestens 650 verschiedene Spezies untersucht, die zu 24 von 27 aviren Ordnungen gehren. Es handelt sich stets um nichtdomestizierte Vgel mit Ausnahme von 133 Wellensittichen, 48 Kanaries und 4 Tauben. Erkrankungen des Geschlechtsapparates wurden bei 148 (8,9%) Vgeln, die zu 88 verschiedenen Spezies aus 6 Ordnungen gehren, festgestellt. Es besteht kein schlssiger Hinweis fr eine besondere Speziesempfindlichkeit. Einige Tiere zeigten mehr als eine Vernderung, am hufigsten waren Obstruktionen des Eileiters und Ovulationen in die Leibeshhle; immerhin waren das 28,6% der 161 Flle. Weniger hufig waren Eierstockserkrankungen (16,8%), Eileiterentzndung ohne offensichtliche Verstopfung (10,6%), Neoplasmen (4,3%), Eileiterrupturen (3,1%) und andere Strungen (8.0%). Das auf Legeleistung gezchtete Hausgeflgel ist wahrscheinlich empfindlicher gegenber Strungen des Geschlechtsapparates als nichtdomestizierte Arten. Bei den zuletzt genannten Tieren sind neben Senilitt und bakteriellen Infektionen wahrscheinlich auch noch manche andere praedisponierende Faktoren beteiligt.