29th of December 2003

French Moult in Budgerigars - A Review

[Melopsittacus undulatus]

By: Inte Onsman, Research coordinator
Research & Advice Group

As long as people breed Budgerigars, French Moult has been the subject of many publications and discussions. One of the first important publications about this feather disease, was presented in Diseases of Budgerigars published in august 1951, Wisconsin USA. At that time French Moult was believed to be caused by faulty diet, overbreeding, and other factors and even a hereditary form was presumed. The term "French Moult" was coined in Europe in the last century where the disease was very prevalent in the 1870's. It had, however been known before that time. The disease has been called French Moult because budgerigars which were shipped all over Europe from the large breeding establishments in southern France, either had the disease in its obvious form or carried it in its hidden form. These birds when bred, would frequently produce a certain percentage of youngsters suffering from French Moult. Two manifestations of F.M. were reported then. The severest form is when young budgerigars in the nest never grow normal feathers. They have been called runners, creepers, crawlers, or bullets. The second, milder form of F.M. includes birds which may eventually grow a normal coat of feathers and become good flyers.


As early as 1888 Dr. Karl Russ made a summary of statements by breeders on the subject of F.M. as they had appeared in early bird journals. Dr. Russ, who was familiar with microscopic work, did not ascribe the cause of F.M. to feather parasites, but to faulty feeding, overbreeding, and breeding in rooms which are too warm. But the most comprehensive study on F.M. has been done in 1932 by Dr. Hans Steiner from the University of Zurich in Switzerland. By continuously inbreeding victims of F.M. he was able to establish a strain in which this disease was carried on in the "hereditary" form from generation to generation according to the Mendelian Law. Dr. Steiner concluded from his experiments that F.M. is the result of degeneration. The view that mites may cause F.M. has been mentioned many times during the last 50 years or more, but has been abandoned each time.

In 1950 scientific work on young Budgerigars suffering from F.M. was done by the Armed Forces Institute of Pathology, Registry of Vetrinary Pathology, Washington, D.C. The report published in All-Pets Magazine in May 1950, was very clear. F.M. is not caused by parasites (including mites) nor by any other "bugs". To find an answer to the question what really causes this unpredictable disease, more scientific work was necessary. However, it was not until 1969 that T.G.Taylor published some experimental investigations on F.M. in Diseases of Cage and Aviary Birds. He came up with a definition and a describtion of the symptoms and stated that the latter vary considerably and depend a great deal on the severety of the attack. He also stated that these variable symptoms have led some people to suggest that F.M. is not a single disease but that it includes several distinct, though related, feather diseases. One of the most interesting findings during these investigations was that a striking difference was found between bone marrow smears obtained from healthy birds and birds suffering from F.M. Red blood cells of diseased birds were abnormally fragile and the life span of the erythrocytes (white blood cells) is unusually short. Taylor concluded, after testing most theories, that the possibility that F.M. may be due to a virus or a virus-like agent, should be taken seriously. However, it was not before 1981 the first serious case report was published in Avian Diseases by Davis and coworkers [5]. They reported high rates of mortality amongst fledgeling budgerigars from aviaries in Georgia and Texas. Affected birds died acutely and exhibited abdomal distention and reddening of the skin. Post mortem they found enlarged heart and liver with areas of necrosis, and swollen, congested kidneys. They examined a variety of tissues and found cells with enlarged nuclei containing inclusions. Electron micrographs revealed the presence of viral particles in the nuclei in the kidneys, feather follicles, liver, heart, bone marrow, spleen and brain. Later on in a separate publication also in Avian Diseases (1981), Bozeman and coworkers isolated a virus that belongs to the Papovaviridae family [4]. They found characteristics that suggest the virus belongs to this family, e.g. the presence of DNA, the side of viral replication appearing to be in the nucleus, and the size of the virus particles ranging from 42 to 49 nm in diameter. (The name Papovavirus was chosen to denote papilloma (PA), polyoma (PO) and vacuolating (VA) viruses). However, they referred to the condition of affected birds as budgerigar fledgling disease (BFD) and characterized a virus (BFDV) isolated from diseased birds.

Again in 1981 another research note was published in Avian Diseases by Bernier, Morin and Marsolais from Canada [2]. They also reported high mortality rates in Budgerigars between one and 15 days of age in 19 aviaries in the Province of Quebec. Signs in adult birds were similar to those described as French Moult. They considered F.M. to be a milder form of the infection described. Surviving birds exhibited a retarded growth of flight and tail feathers. Results of their investigations suggest that this disease of budgerigars is caused by a papova-like agent that can replicate in many tissues of the body, causing widespread lesions responsible for the high mortality rate in very young birds.

In 1982 Dykstra and Bozeman published the results of a light and electron microscopic examination of a "newly" described avian virus in Budgerigars [8]. They found that the virus particles are of the same size and symmetry as members of the polyoma subgroup of the Papovaviridae. The means of transmission of the virus within an aviary population is less clear, though their studies have implicated several possible routes. Adults may pass the virus by feeding their young by regurgitation. Air currents circulating inside affected aviaries may also be responsible for transmission. They also suggest a possible respiratory route of transmission since virions within cells of lung tissue were found.

In 1984 Prof.Dr.Kaleta from Germany and coworkers, published some results obtained by their investigations on young budgerigars showing signs of F.M. [13]. The birds were purchased from five different sources. Infected cells were isolated and examined electronmicroscopically. During this investigation intranuclear virus particles were found with a diameter of 35-45nm.

In the American Journal of Veterinary Research Dykstra and coworkers published a report to characterize a virus linked to Budgerigar Fledgling Disease (BFD) which previously had been identified as a papovavirus [9]. The purpose of this investigation was to prepare further genetic investigations to develop a possible vaccine as has been done for e.g. foot-and-mouth disease of cattle. Their results showed little similarity to simian virus 40 (SV40) or polyomavirus DNA. During the same year Bernier, Morin and Marsolais published an article in The Canadian Veterinary Journal involving clinical and pathological findings in budgerigars suffering from a papovavirus infection [3]. They described one to 15 day old birds displaying a lack of nestling down feathers and filoplumes on the head and neck. Microscopic lesions in the feather follicles of the affected birds less than 15 days of age, were characterized by focal, multifocal or diffuse ballooning degeneration in the plate cells of the barb ridges. Again microscopic examination of these cells showed virus particles similar to those already described by earlier investigators. Results of this investigation suggested that a papovavirus can cause temporary absence, retarded growth and the incomplete development of feathers in young budgerigars. The infection was also suspected to be egg transmitted. The fact that eggs from pairs producing affected young will also give diseased birds when fostered by pairs whose own youngsters are normal, supports the hypothesis of egg-transmission. It was suggested that F.M. is a nonfatal form of the papovavirus infections described in budgerigars.

Lynch and coworkers from the Veterinary Laboratory Services Branch, Ontario, Canada, also published their results in Avian Diseases (1984) [18]. They examined birds from three unrelated outbreaks of disease occurring in Ontario in 1981,1983, and 1984. Egg-inoculation experiments suggested that the disease may be egg-transmitted and that significant virus replication must occur before the budgerigar's immune system matures sufficiently to mount a response.

In the year 1984 many research was carried out on this unpredictable disease. Jacobson and coworkers reported 45 fledling psittacine birds being raised in an avian nursery of which 14 died over a 6-week period [12]. Birds died acutely with full crops, abdominal distention, and hemorrhagic skin. Feather abnormalities were seen in birds older than 15 days. In this report, a die-off of fledgling conures and macaws was described. Electron microscopy demonstrated a virus similar in size and conformation to BFDV (Budgerigar Fledgling Disease Virus). They concluded that the psittacine papovavirus present in affected birds, appeared to be related to the polyomavirus subgroup of the papovaviruses. They also concluded that fledglings from seronegative parents should not be introduced into a nursery with chicks from seropositive parents. Also in the same year Pass and Perry from the School of Veterinary Studies, Murdoch University, Murdoch, Western Australia, described a disease called Psittacine beak and feather disease [21]. The disease is characterized by loss of feathers, abnormally shaped feathers and overgrowth and irregularity of the surface of the beak. The disease was seen in Sulphur-crested Cockatoos, Lovebirds, Budgerigars and Galahs. During their investigations they found viral particles 17 to 22 nm in diameter who could be identified in a later state as the picorna virus which is not a member of the Papova virus family.

In 1985 Pass published a papova-like virus infection of Lovebirds [22]. The article was published in the Australian Veterinary Journal and contained information about similarities to papovavirus infections of psittacine birds described elswhere.

Krautwald and Kaleta (1984) investigated 250 budgerigars obtained from 45 different breeders. Approximately 50 birds came from breeders who never had F.M. in their aviaries [14]. It was observed that birds who never had any problems with F.M. were very easy to infect for lack of sufficient antibodies. In the German Cancer Research Center of the University of Giessen, Lehn and Müller (1986) cloned and characterized for the first time a virus isolated from fledgling budgerigars, designated BFDV [16]. A relationship to the polyomavirus subgroup was already recognized and suggested by previous investigators, but it was now confirmed by this investigation. Their experiments showed that BFDV is related to but not identical to the other polyomaviruses. Until now, polyomaviruses had been isolated only from a variety of mammalian species including man; in contrast, BFDV represents the first avian member of this subgroup. Lehn and Müller found strong evidence that BFDV is associated with French Moult.

In 1986 Müller and Nitschke from the Institute for Virology, University of Giessen, Germany, investigated a virus isolated from fledgling budgerigars suffering from F.M. Results obtained by their investigation led to the conclusion that the virus isolated warrant the classification as a polyoma-like virus [20].

David Graham and Bruce Calnek reported in Avian Diseases (1987), a papovavirus infection in 44 parrots of at least 18 species exclusive of the budgerigar [10]. They compared this infection to a generalized virus infection of young budgerigars which had been recognized in the United States, Canada, Italy, Hungary, Japan, and the Federal Republic of Germany. A papovavirus infection was confirmed in 27 of the birds by using antibody tests.

In the Journal of Veterinary Medicine (1989), Krautwald, Müller and Kaleta from the Institute of Poultry Diseases and Institute of Virology, University of Giessen, Germany, examined 298 budgerigars from 49 different flocks in order to obtain some insight into the aetiology of FM and BFD [15]. The difference between birds infected with FM and birds infected with BFD is that FM birds mostly survive and BFD infected birds die when 2-to-3-weeks old. Mortality rates even reached up to 100% in several flocks. However, surviving budgerigars showed disorders of feathers, similar to those of birds with FM; these birds remained less developed, and many of them were unable to fly (runners). The structural and physicochemical properties of viruses isolated from budgerigars with BFD and from several budgerigars with FM described by Krautwald and coworkers and their results published in a previous paper (1984) confirm the recently published classification of BFDV as a member of the polyomavirus group (Lehn and Müller,1986; Müller and Nitzschke,1986). They proposed to place this virus into a distinct subgroup within the polyomavirus family.

Regine Stoll and coworkers (1993) studied molecular and biological characteristics of avian polyomaviruses from different species of birds including chickens and a parrot [24]. The chicken polyomavirus is called BFDV-2 and the parrot polyomavirus is called BFDV-3. The non-mammalian polyomavirus isolated from Budgerigars is now called BFDV-1 virus. They consider Budgerigar Fledgeling Disease virus (BFDV) to represent the first avian virus being recognized as a member of the polyomavirus genus in the family papovaviridae (Müller & Nitschke, 1986;Lehn & Müller,1986). They also consider French moult of Budgerigars to be a milder and more protracted form of a BFDV infection resulting in chronic feathering disorders (Krautwald,1989). It is proposed that the avian polyomaviruses should be placed in a distinct subgroup within the polyomavirus genus of the family Papovaviridae and the designation Avipolyomavirus is suggested (Stoll,1993).

The aetiology of French Moult has been very well investigated throughout the years. It appeared to be a contageous viral disease caused by a member of the papovaviridae family and is designated now as the avipolyomavirus. This mammalian virus was obviously able to adapt, replicate and survive in psittacine birds because of its unique properties (Griffin,1983) [11]. Two forms of the disease have been recognized in Budgerigars; the most severe form (BFD) causing mortality rates up to 100% in budgerigar fledgelings and a mild form called French Moult causing feather disturbances resulting in birds called "runners". If an outbreak of the disease occurs, precausions should be taken to prevent the virus from spreading throughout the aviary (Baker,1990) [1]. Adult birds probably spread the disease through feather dust and droppings. Runners spread the virus through feather dander, feather dust and droppings. The infection is egg-transmitted for eggs from pairs producing affected young will also give diseased birds when fostered by pairs whose own youngsters are normal. The use of an effective disinfectant such as Vircon S is recommanded. If the disease is present in your aviary, do not sell or exhibit birds because if you do so, you will spread the disease to other fanciers.

Consulted and cited Literature:
[1] Baker J.R., (1990)
    Preventing the Spread of Budgerigar Fledgling Disease
    Cage & Aviary Birds nr.9

[2] Bernier G., Morin M., Marsolais G., (1981)
    A Generalized Inclusion Body Disease in the	Budgerigar Caused by 
    a Papovavirus-like Agent
    Avian Diseases vol.25 no.4; p.p.1083-1092

[3] Bernier G., Morin M., Marsolais G., (1984)
    Papovavirus Induced Feather Abnormalities and Skin Lesions in the Budgerigar:
    Clinical and Pathological Findings
    The Canadian Vet. Journ.; p.p.307-310

[4] Bozeman L.H., Davis R.B., Gaudry D., (1981)
    Characterization of a Papovavirus Isolated from Fledgling Budgerigars
    Avian Diseases vol.25 no.4; p.p.972-980

[5] Davis R.B., Bozeman L.H., Gaudry D., (1981)
    A Viral Disease of Fledgling Budgerigars
    Avian Diseases vol.25 no.1; p.p.179-183

[6] Dulbecco R., (1966)
    Mechanism of Cell Transformation by Polyoma	Virus
    Persp.in Biology and Medicine; p.p.298-305

[7] Dulbecco R., (1969)
    Cell Transformation by Viruses
    Science vol.166; p.p.962-968

[8] Dykstra M.J., Bozeman L.H., (1982)
    A Light and Electron Microscopic Examination of Budgerigar 
    Fledgling Disease Virus in Tissue and in Cell Culture
    Avian Pathology 11; p.p.11-28

[9] Dykstra M.J., Dykstra C.C., Lukert P.D., (1984)
    Investigations of Budgerigar Fledgling Disease Virus
    Am.Journ.Vet.Res.; p.p.1883-1887

[10]Graham L., Calnek B.W., (1987)
    Papovavirus Infection in Hand-fed Parrots: Virus Isolation and Pathology
    Avian Diseases Vol.31, no. 2; p.p.398-410

[11]Griffin B.E., Dilworth S.M., (1983)
    Polyomavirus: An Overview of its Unique Properties
    Adv. in Cancer Research vol.39; p.p.183-269

[12]Jacobson E.R.,Hines S.A.,Qesenberry K., (1984)
    Epornitic of Papova-like Virus-associated disease in a Psittacine nursery
    JAVMA, vol. 185, no 11; p.p.1337-1341

[13]Kaleta E.F.von, Herbst W., Kaup F.J., (1984)
    Untersuchungen zur Virusatiologie einer mit
    Hepatitis und Befiederungsstorungen einhergehender Krankheit bei
    Wellensittich-Nestlingen [Melopsittacus undulatus]
    Zbl.Vet.Med.B., vol 31; p.p.219-224

[14]Krautwald M.E., Kaleta E.F., (1984)
    Untersuchungen zur Atiologie der "Franzosischen Mauser" des Wellensittichs
    sowie einer mit Hepatitis und Befiederungsstorungen	einhergehenden
    Erkrankung junger Wellensittichnestlinge
    Prakt.Tierart. vol.66; p.p.5-6

[15]Krautwald M.E., Muller H., Kaleta E.F., (1989)
    Polyomavirus Infection in Budgerigars
    (Melopsittacus Undulatus): Clinical and Aetiological Studies
    Journ.Vet.Med. Vol.B 36; p.p.459-467

[16]Lehn H., Muller H., (1986)
    Cloning and Characterization of Budgerigar Fledgling Disease Virus,
    an Avian Polyomavirus
    Virology 151; p.p.362-370

[17]Levine A.J., (1974)
    The Replication of Papovavirus DNA
    Progr.med Virol.,vol.17; p.p.1-37

[18]Lynch J., Swinton J., Key D., (1984)
    Isolation and Experimental Chicken-Embryo-Inoculation Studies with
    Budgerigar Papovavirus
    Avian Diseases vol.28 no.4; p.p.1135-1139

[19]Melnick J.L., Allison A.C., Butel J.S., (1974)
    Intervirology; p.p.106-120

[20]Muller H., Nitschke R., (1986)
    A Polyoma-like Virus associated with an Acute
    Disease of Fledgling Budgerigars
    Med.Microbiol. Immunol. Vol.175; p.p.1-13

[21]Pass D.A., Perry R.A., (1984)
    The Pathology of Psittacine Beak and Feather
    Austr.Vet.Journ. vol.61,no 3; p.p.69-74

[22]Pass D.A., (1985)
    A Papova-like Virus Infection of Lovebirds
    Austr.Vet.Journ. Vol.67., no.9; p.p.318-319

[23]Pass D., (1989)
    The Latest News on French Moult
    Budgerigar World Issue 82; p.p.21-22

[24]Stoll R., Luo D., Kouwenhoven B., (1993)
    Molecular and Biological Characteristics of Avian Polyomaviruses: Isolates
    from Different Species of Birds Indicate that Avian Polyoma Viruses 
    form a Distinct Subgenus within the Polyomavirus Genus
    Journal of General Virology Vol.74; p.p.229-237

[25]Taylor T.G., (1969)
    French Moult
    Dis.of Cage and Aviary Birds; p.p.237-242

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