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Fowlpox (FP) is a common epitheliotropic disease in chickens that is usually controlled by live attenuated vaccines. However, there have been some reports of outbreaks of FP in recent years, even in vaccinated flocks, presenting as atypical lesions and feathering abnormalities in chickens. These findings can be associated with fowlpox virus (FPV) with the reticuloendotheliosis virus (REV) integrated into its genome. In the present study, outbreaks of atypical FP were explored in vaccinated commercial laying hen flocks to determine the nature of the causative agent by histopathologic and molecular approaches. FPV and REV were detected and classified into subclade A1 of the genus Avipoxvirus and subtype 3 of REV (REV3), respectively. Additionally, heterogeneous populations of FPV with partial (containing only a remnant long terminal repeat-LTR) or total (all functional genes) integration of REV were identified by heterologous PCRs and detected considering reference integration sites. These results indicate the mechanism of chimeric genome FPV-REV associated with outbreaks and atypical clinicopathological manifestations in commercial laying hens for the first time in Brazil and in South America. In addition, this study demonstrates the emergence of REV integrated in the FPV genome in Brazilian chicken flocks., (© 2020 Blackwell Verlag GmbH.)

Fowlpox virus is the type species of an extensive and poorly-defined group of viruses isolated from more than 200 species of birds, together comprising the avipoxvirus genus of the poxvirus family. Long known as a significant poultry pathogen, vaccines developed in the early and middle years of the twentieth century led to its effective eradication as a problem to commercial production in temperate climes in developed western countries (such that vaccination there is now far less common). Transmitted mechanically by biting insects, it remains problematic, causing significant losses to all forms of production (from backyard, through extensive to intensive commercial flocks), in tropical climes where control of biting insects is difficult. In these regions, vaccination (via intradermal or subcutaneous, and increasingly in ovo, routes) remains necessary. Although there is no evidence that more than a single serotype exists, there are poorly-described reports of outbreaks in vaccinated flocks. Whether this is due to inadequate vaccination or penetrance of novel variants remains unclear. Some such outbreaks have been associated with strains carrying endogenous, infectious proviral copies of the retrovirus reticuloendotheliosis virus (REV), which might represent a pathotypic (if not newly emerging) variant in the field. Until more is known about the phylogenetic structure of the avipoxvirus genus (by more widespread genome sequencing of isolates from different species of birds) it remains difficult to ascertain the risk of novel avipoxviruses emerging from wild birds (and/or by recombination/mutation) to infect farmed poultry.

Fowlpox virus (FWPV), the type species of the genus Avipoxvirus family Poxviridae, is a large double-stranded DNA virus that causes fowlpox in chickens and turkeys. Notably, sequences of the avian retrovirus reticuloendotheliosis virus (REV) are frequently found integrated into the genome of FWPV. While some FWPV strains carry remnants of the REV long terminal repeats (LTRs), other strains have been shown to contain insertions of nearly the full-length REV provirus in their genome. In the present study we detected heterogeneous FWPV populations carrying the REV LTR or the near full-length REV provirus genome in a Merriam's wild turkey (Meleagris gallopavo merriami). The bird presented papules distributed throughout the non-feathered areas of the head. Avipoxvirus-like virions were observed in the lesions by transmission electron microscopy and the presence of FWPV was confirmed by DNA sequencing. Metagenomic sequencing performed on nucleic acid extracted from the skin lesions revealed two FWPV genome populations carrying either a 197-nt remnant of the REV LTR or a 7939-nt long fragment corresponding to the full-length REV provirus. Notably, PCR amplification using primers targeting FWPV sequences flanking the REV insertion site, confirmed the natural occurrence of the heterogeneous FWPV genome populations in one additional clinical sample from another turkey affected by fowlpox. Additionally, sequencing of a historical FWPV isolate obtained from chickens in the US in 2000 also revealed the presence of the two FWPV-REV genome populations. Results here demonstrate distinct FWPV populations containing variable segments of REV genome integrated into their genome. These distinct genome populations are likely a result of homologous recombination events that take place during FWPV replication., (Copyright © 2018 Elsevier B.V. All rights reserved.)

The present report documents the occurrence of a poxvirus infection in commercial meat turkeys. The affected farm had six flocks, with a total of 11,680 birds at different ages; birds from two of these flocks were affected. The clinical picture was characterized by severe epithelial lesions and proliferations on the head and neck regions as reported for the cutaneous form of poxvirus infection. Except for these lesions, no adverse clinical signs or gross pathologic lesions were observed. Only a low number of birds was affected (n = 20) and no increase of mortality could be seen. Bacteriologic investigations from the lesions revealed multiresistant Staphylococcus aureus. Eosinophilic inclusions (Bollinger bodies) in histologic examinations in the cytoplasm of keratinocytes were noticeable. Typical pox virions were demonstrated by electron microscopy, and poxvirus was isolated on the chorioallantoic membrane of specific-pathogen-free chicken eggs. Further identification of the poxvirus species was carried out by PCR and sequencing, revealing an infection with the species fowlpox. Layers in vicinity of the turkey farm that also were affected by fowlpox were considered as potential source of infection. Although it is assumed that avian poxviruses are strongly species specific, the present case report reinforces the changing picture of poxvirus infections in turkeys. Furthermore, it supports the assumption of previous data that fowlpox virus has to be seen as recently emerging pathogen in turkeys.

An unusual cutaneous fowl pox outbreak occurred in 8-wk-old broilers in California. Rounded and longitudinal, proliferative scratch-associated lesions were found only in feathered areas of the body. Both sides of the hip, the lower abdomen, pericloacal area, and lateral lower neck area were involved. The head, legs, feet, and toes did not have lesions. Birds in only one section of one of five houses were affected. Fifteen percent condemnations occurred in birds from the affected house due to the skin lesions. A diagnosis of fowl pox was achieved by histopathology, viral isolation, and direct electron microscopy. The unusual distribution of pox lesions was assumed to be associated with skin scratches. There was no evidence that mosquitoes or other types of insects were involved in this outbreak. To the knowledge of the authors, this is the first report of this kind of unusual fowl pox in the United States.

Cutaneous fowlpox occurring in vaccinated layer hens was investigated pathologically and microbiologically. Anorexia, decrease of egg production, increased mortality, yellow scabs on faces, and alopecia of feathered skins with yellow scabs were observed in affected hens. Histologically, proliferative and necrotic dermatitis with eosinophilic ring-shaped cytoplasmic inclusions (Bollinger bodies) and clumps of gram-positive cocci (Staphylococcus hyicus) were noted in the affected birds. Fowlpox lesions were primarily observed in the feathered skins. Proliferation of feather follicle epidermal cells, with cytoplasmic inclusions and degeneration of the feather, and bacterial clumps in the feather follicles were noted in the affected skins. Ultrastructurally, characteristic fowlpox viral particles were observed in the cytoplasmic inclusions of hyperplastic epidermal cells. Amyloid deposition was observed in the Disse space of the liver, splenic sinus, and lamina propria of the bronchiolar, bronchial, and tracheal areas. Amyloidosis could be one factor inducing the fowlpox infection in vaccinated chickens.

The finding of closely associated squamous cell carcinoma (SCC)-like lesions and pox lesions in chorioallantoic membranes (CAMs) inoculated with skin and palate samples taken from broilers is described. The samples were obtained from two broilers coming from different flocks that were not vaccinated against fowl pox. Both birds presented skin lesions, which were diagnosed in one bird as fowl pox, and in the other as SCC. After inoculation of CAMs with fresh tissues from both birds, histologic examination revealed, in all CAMs, lesions that were characteristic of fowl pox together with lesions consistent with those seen in the skin of broilers affected with SCC. This finding was unexpected and may shed some light on the etiology of SCC.

A case of cutaneous avian pox infection in a Hodgson's grandala (Grandala coelicolor) is described. The bird was emaciated and had nodules on the eyelids, bill, neck, legs, and toes. Eosinophilic intracytoplasmic inclusion bodies were visualized by light microscopy in epithelial cells of the cutaneous nodules. Electron microscopy revealed numerous pox virions in the inclusion bodies. This is the first report of cutaneous poxvirus infection in a Hodgson's grandala.

The polymerase chain reaction (PCR) was used to amplify a 578-bp fragment of the fowl poxvirus (FPV) genome and with a set of primers framed a region within the gene coding for 4b core protein. An amplified product was detected with six strains of FPV, whereas none was obtained from uninfected cell cultures, skin tissue or four unrelated avian pathogens. The sensitivity of PCR was tested with nucleic acids from the FPV-infected cell cultures. The detection limit was 10(-1) TCID50 in an ethidium bromide-stained gel. In addition, this assay system was used to detect FPV in tissue specimens of skin and respiratory swabs collected from commercially reared chickens. The identity of the amplification products from the tissue specimen preparations was determined further by using a simple, rapid procedure in which an internally nested, end-labeled probe was used.

Poxvirus was isolated from cutaneous nodules on two young Houbara bustards (Chlamydotis undulata) bred in captivity in Saudi Arabia. Birds were emaciated and presented nodules on tibiotarso-tarsometatarsal joints, toes, and the carpal joint. Diagnosis was confirmed by histopathology, virus isolation on inoculated chorioallantoic membranes of embryonated chicken's eggs, and electron microscopy. Progressive leg lesions were extensive and interfered with walking, significantly debilitating the birds. Successful excisions of these lesions were performed.

An unusual fowl pox outbreak occurred in two integrated broiler operations. The uncommon characteristic of this outbreak was that the pox lesions were manifested in the feathered parts of the body, mainly in the posterior dorsal area and external part of the thigh. Diagnosis was made by means of histopathology and virus isolation. Severe losses were incurred at the processing plant as a consequence of condemnation due to dermatitis. Vaccination of day-old chicks with mild fowl pox vaccine combined with Marek's disease (HVT) vaccine in the area of the outbreak appeared to be important in controlling the disease.

Avian pox is an important disease in birds of prey in Bahrain. A live pigeon pox vaccine was administered to hunting falcons (Falco species) together with other therapeutic methods to arrest the development of primary stage pox lesions and for the treatment of well established secondary stage pox lesions. Quarantine and general hygiene procedures were also used as an integral part of the management and control of the disease.

Poxvirus was isolated from nodules on four immature grackles (Quiscalus sp.) collected in two residential areas of Victoria, Texas. All of the birds were emaciated and had nodules on the eyelids, bill, legs, toes, and areas of the skin on the wings, neck, and ventral abdomen. These pox nodules were extensive and probably interfered with both sight and flight. The preliminary diagnosis was confirmed by virus isolation, histopathology, and electron microscopy. Poxvirus was isolated on the chorioallantoic membrane of embryonated hen's eggs and in Muscovy duck embryo fibroblast cell culture. Phaenicia calliphoridae (blowfly) larvae were found in one of the pox nodules, raising the possibility of mechanical transmission of the virus by contaminated adult blowflies.

During a 1-month period at a quarantine station, an epornitic of avian pox occurred in blue-fronted Amazon parrots (Amazona aestiva). Clinical signs included conjunctivitis, blepharitis, and varying degrees of anorexia and respiratory distress. Lesions included periocular ulcerations and scabs and necrotic plaques in the oral cavity. Histologically, the lesions consisted of epithelial hyperplasia, secondary inflammatory changes, and eosinophilic inclusions which, by electron microscopy, were shown to contain poxvirus. When chicken embryos were inoculated with material from eyelid scabs and pharyngeal plaques, lesions of avian pox developed on the chorioallantoic membrane. The death rate of infected birds was high because of secondary bacterial and fungal infections, but uncomplicated cases were usually self-limiting. Periocular lesions also developed in 2 other species of psittacine birds housed in the same facility.

Poxvirus infection was diagnosed on the basis of gross and microscopic appearance plus the presence of typical inclusion bodies in a juvenile American green-winged teal (Anas crecca carolinensis) in Alaska. This constitutes the first known report of avian pox in migratory ducks and the first report of poxvirus infection in wild birds in Alaska.

Twelve turkeys from a flock of 2,500 had cutaneous lesions somewhat resembling fowl pox. Lymphoid-like tumors were evident in livers and spleens. Closer examination of cutaneous lesions, and histopathological examinations indicated skin lesions were also infiltrative and not unlike reticuloendotheliosis. Electron micrographs revealed the presence of C-type virus particles.

An outbreak of avian pox, with an estimated 12-fold increase in the incidence of infection, occurred among wild bobwhites (Colinus virginianus) in the southwestern Georgia/northcentral Florida region. The outbreak was first detected in July, 1978, and continued at least until March, 1979. During this period, 26 separate clinical case accessions involving 43 bobwhites from 8 counties in Florida and Georgia were diagnosed as avian pox. A survey of 2,586 bobwhites from 6 southeastern states revealed avian pox infections in 312 bobwhites from Florida, Georgia, North Carolina, and Tennessee. Seventy-seven percent of the infected birds in the survey had only mild lesions on the legs and feet; however, 23% had more extensive lesions on the head. Severely affected birds had lesions around the eyes, nares, and in the mouth which impaired vision, respiration, and/or feeding. Infection rates were not related to age or sex of the birds but varied greatly among locales, even on adjoining properties. A morbidity rate of approximately 2% and a mortality rate between 0.6 and 1.2% were estimated for a 13,000 km2 region in Georgia and Florida.

A virulent fowlpox virus was isolated from a natural outbreak of the disease in the Sudan. The virus was used for experimental transmission of the disease to susceptible chickens. Scarification and intravenous methods were used to infect one-month-old chickens. Scarification induced typical pox lesions at 5-7 days postinoculation, whereas intravenous injection induced only swelling of combs or wattles, at 10-11 days postinoculation, although neutralizing antibodies against fowlpox virus were detected 2, 3, and 4 weeks postinoculation. The histopathological features of the pox lesions obtained in both natural and experimental infection were described.

Poxvirus infection and aspergillosis were diagnosed in a Royal tern (Thalasseus maximus) based on gross and microscopic lesions. This represents the first known report of avian pox in a tern. Renal trematodiasis, caused by a species of Renicola also is described.

An isolate of fowl pox (FP) virus from a case of "wet" pox in commercial white leghorn (WL) pullets was used to expose WL cockerels via the comb-scratch (CS), eye-drop (ED), or laryngeal-swab (LS) route. Seven days postinoculation (PI), the groups challenged via CS had scabby proliferative pox lesions at the challenge site, the groups challenged via LS had slight dyspnea and rales, and 20% of the cockerels challenged via ED had mild conjunctivitis and lacrimation. By termination of the trial on day 21 PI, the CS-challenged groups had developed pronounced pox lesions. The LS-challenged groups showed severe dyspnea and rales with pronounced raised plaque-like lesions at the opening to the trachea and extending into the upper quarter of the trachea with heavy yellowish caseous exudate partly occluding the glottis. The ED-challenged groups had severe lacrimation and conjunctivitis and small pox lesions on the face, comb, and wattles; 12 of 18 had proliferative lesions on the oral mucosa in the area of the larynx. Forty-five percent of the LS-challenged groups died of suffocation. Pox virus was re-isolated from tissues in all treatment groups. Wet pox transmission appears to be possible via the LS and ED routes.

Twenty chickens were inoculated intravenously with fowlpox (FP) virus, and clinical and pathological examinations were carried out chronologically. Upon gross examination, miliary nodules scattered in the kidneys were observed from 10 to 18 days postinoculation (PI), as were papules on the skin and diphtheritic lesions on the mucous membrane of the upper respiratory tract. Microscopically, characteristic FP lesions, composed of swelling and proliferation of cells with formation of Bollinger bodies, were observed in the epithelial cells of renal tubules from 4 to 14 days PI and in the epithelial reticular cells of the thymic medulla from 4 to 10 days PI, as well as in the skin and mucous membrane. Immunofluorescent and electron microscopic observations confirmed the presence of viral antigen and virus particles in the characteristic lesions of FP.

Five-week-old chickens were inoculated with fowl pox (FP) virus and killed on various days through day 30 postinoculation (PI). The trachea was examined with a scanning electron microscope (SEM), a transmission electron microscope (TEM), and a light microscope (LM). From day 3 PI, small focal lesions of the mucosa were detected. On day 7 PI, upon formation of cytoplasmic inclusion bodies, epithelial cells proliferated profusely, enlarged, and formed clusters like papillomata. The disease proceeded to the gradual disruption of the lesions owing to the collapse of individual degenerating epithelial cells. Total desquamation of the lesions was observed. Ultrastructural examination revealed that the surface degenerating epithelial cells of the lesions ruptured and had virus particles inside. These changes were accompanied by severe inflammatory reaction. Thereafter, epithelial cells regenerated actively and the mucosa recovered by day 27 PI.

California quail (Lophortyx californicus) from several locations in Oregon were examined seasonally between fall 1975 and summer 1978 for avian pox. Pox lesions were present on 66 of 256 (26%) birds from the E.E. Wilson Wildlife Area. None of the remaining 41 birds from other areas was infected. Rates of infection of males and females were equal; juveniles had a slightly, but not significantly, higher prevalence of pox than did adults.

Avian pox was determined to be the cause of death of a spectacled Amazon parrot (Amazona albifrons). Intracytoplasmic inclusion bodies were visualized by light microscopy in esophageal and bronchial epithelial lesions. Electron microscopy revealed pox-virus virions in the inclusions.

During a 6-week period at the San Diego Zoo, avian pox occurred in 9 pheasants representing 5 species. Lesions were limited to facial skin and consisted of epithelial cell hyperplasia, secondary inflammatory changes, and intracytoplasmic eosinophilic inclusion bodies which, by electron microscopy, were shown to contain pox virus. The disease was self-limiting in 7 pheasants, but 2 pheasants died. Free-ranging Indian red junglefowl were implicated as the source of the infection.

Lesions caused by an avian poxvirus were identified on the face and nares of fledgling white-tailed tropicbirds (Phaethon lepturus catesbyi) in the natural environment on Bermuda. Between 1958 and 1978, 6 of 81 fledglings found off the nest and unable to fly at departure time had lesions suggestive of poxvirus infection. More detailed nest-site surveys from 1974 to 1978 indicated an overall prevalence of less than 0.5%, involving the fledgling population only.

Several wild species of birds, including starlings (Sturnus vulgaris), house sparrows (Passer domesticus) and pigeons (Columba livia) gained access to an aviary housing Rothchild's mynahs (Leucospar rothchildii) and over 100 additional birds representing a variety of species. Six of approximately 15 mynahs became infected with avian pox and all of them died. None of the other birds in the aviary developed lesions. Pox virus was isolated from mynah facial lesions on chicken chorioallantoic membrane and in duck embryo fibroblast cell culture. It did not produce lesions in white Leghorn chickens, but did produce lesions in 4 of 11 wild starlings captured outside the aviary. Results indicated the agent was an indigenous starling pox capable of infecting and producing disease in mynah birds. Destruction of the captive starlings and isolation of the remaining mynahs immediately stopped the mortality.

Erysipelothrix rhusiopathiae was isolated from the spleen, liver, lung, heart, kidney, and skin of a red-tailed hawk (Buteo jamaicensis) which had a concurrent avian pox virus infection. The hawk had been housed on a farm with domestic turkeys, providing a possible source of the E. rhusiopathiae.

Atypical fowlpox occurred in several poultry farms in Kenya. On two occasions layers had their eyes closed and egg production dropped. Fowlpox virus was isolated from lesions on the inner surfaces of the closed eyelids. Other chickens had lesions covered by yellow caseous necrotic material in the mouth, around the epiglottis, and in the trachea and choanae. Typical proliferative cutaneous lesions were observed in birds of all ages in other flocks examined. Fowlpox virus was recovered from both cutaneous and diphtheritic lesions. The infected chorioallantoic membranes had focal hyperplastic lesions containing pink-staining intracytoplasmic inclusion bodies in most cells. Transmission studies showed that the virus was highly virulent to susceptible chickens.

Egg production dropped after hens were inoculated with fowlpox virus originally isolated from a natural mild infection. The drop started from the 2nd week and continued to the 5th week after inoculation. All birds developed focal lesions at the site of inoculation, and some developed secondary lesions. The drop in individual birds was related to the severity of lesions. Birds challenged with fowlpox virus fifteen months after vaccination with pigeon pox vaccine were susceptible.

Red-stained elementary bodies of fowlpox virus were detected in smears from lesions of infected chorioallantoic membrane and from skin of infected birds stained by the Giménez method.

An outbreak of avian pox in a bird research colony was reported. Although 10 species of passerine birds were housed within the facility, clinical signs and mortality were restricted to canaries and house sparrows. Post-mortem lesions initially occurred in the upper and lower respiratory tracts and were characterized by proliferative rhinitis, proliferative bronchopneumonia, and proliferative airsacculitis, and diphtheritic lesions occurring in the esophagus were characterized by proliferative granulomatous esophagitis. Cutaneous lesions occurred subsequently in some birds, and a diagnosis was made by histopathology, electron microscopy, and virus isolation. The occurrence of diphtheritic lesions in pox infections of wild birds has been rare, and a sparrow showed an unusual combination of both diphtheritic and acute systemic lesions previously undescribed.

Lesions suggestive of Avian Pox were found on a debilitated Canada goose (Branta canadensis). These were demonstrated histologically to be characteristic poxvirus lesions and poxvirus particles were seen using electron microscopy. The virus was successfully transmitted to domestic geese but not to leghorn chickens or to domestic ducks.

Natural pox infection occurred in a free-living, immature common murre (Uria aalge) in northern California. Cutaneous and diphtheritic lesions were present. Death of the bird was attributed to respiratory insufficiency and starvation resulting from impairment of breathing and feeding, respectively.