Lymphoproliferative Disease Virus in Wild Turkeys (Meleagris gallopavo) from Manitoba and Quebec, Canada Authors: MacDonald, Amanda M., Barta, John R., McKay, Michelle, Lair, Stéphane, Le Net, Rozenn, et al. Source: Avian Diseases, 63(3) : 506-510 Published By: American Association of Avian Pathologists URL: https://doi.org/10.1637/aviandiseases-D-19-00102 The BioOne Digital Library ( https://bioone.org/) provides worldwide distribution for more than 580 journals and eBooks from BioOne’s community of over 150 nonprofit societies, research institutions, and university presses in the biological, ecological, and environmental sciences. The BioOne Digital Library encompasses the flagship aggregation BioOne Complete ( https://bioone.org/subscribe), the BioOne Complete Archive ( https://bioone.org/archive), and the BioOne eBooks program offerings ESA eBook Collection ( https://bioone.org/esa-ebooks) and CSIRO Publishing BioSelect Collection ( https://bioone.org/csiro- ebooks). Your use of this PDF, the BioOne Digital Library, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/terms-of-use. Usage of BioOne Digital Library content is strictly limited to personal, educational, and non-commmercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne is an innovative nonprofit that sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Downloaded From: https://bioone.org/journals/Avian-Diseases on 01 May 2026 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Florida Lymphoproliferative Disease Virus in Wild Turkeys ( Meleagris gallopavo ) from Manitoba and Quebec, Canada Amanda M. MacDonald, ABH John R. Barta, A Michelle McKay, C St ́ ephane Lair, D Rozenn Le Net, D Frank Baldwin, E Neil Pople, F and Nicole M. Nemeth G A Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada NIG 2W1 B Canadian Wildlife Health Cooperative, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada NIG 2W1 C Department of Biology and Environmental & Life Sciences, Trent University, Peterborough, Ontario, Canada K9J 7B8 D Canadian Wildlife Health Cooperative, Facult ́ e de m ́ edecine v ́ et ́ erinaire, Universit ́ e de Montr ́ eal, St. Hyacinthe, Quebec, Canada J2S 2M2 E Wildlife Branch, Manitoba Sustainable Development, Winnipeg, Manitoba, Canada R3J 3W3 F Veterinary Diagnostic Services, Manitoba Agriculture, Winnipeg, Manitoba, Canada R3T 5S6 G Southeastern Cooperative Wildlife Disease Study, University of Georgia, Athens, GA 30602 Received 16 April 2019; Accepted 11 June 2019; Published ahead of print 11 June 2019 SUMMARY. This study describes the first recognized clinical case of lymphoproliferative disease virus (LPDV) in Canada and extends the range of LPDV in Canada through its detection in Manitoba and Quebec. We assessed the prevalence of LPDV in eastern wild turkeys ( Meleagris gallopavo silvestris ) with the use of whole, clotted blood from live birds in Manitoba ( n ¼ 65) and tissue samples collected postmortem in Quebec ( n ¼ 4). We tested for LPDV proviral DNA through PCR amplification and sequencing of a portion of the gag (p31) gene. Samples were also tested for reticuloendotheliosis virus (REV) by PCR. Twenty-four birds (34.8%) were positive for LPDV, including all diagnostic cases. One bird (1.4%) from Quebec had gross and microscopic lesions consistent with LPDV. Two turkeys (2.9%) were REV positive, one (1.4%) of which was co-infected with LPDV. Phylogenetic analysis of LPDV strains from Quebec and Manitoba grouped with previously sequenced samples from Ontario and publicly available sequences from a North American lineage. This study contributes valuable information toward ongoing surveillance and monitoring of LPDV in North America. RESUMEN. Virus de la enfermedad linfoproliferativa en pavos silvestres ( Meleagris gallopavo ) de Manitoba y Quebec, en Canada ́. Este estudio describe el primer caso cl ́ ınico reconocido del virus de la enfermedad linfoproliferativa (LPDV) en Canada ́ y extiende el rango de detecci ́ on de este virus a trav ́ es de su detecci ́ on en Manitoba y Quebec. Se evalu ́ o la prevalencia del virus de la enfermedad linfoproliferativa en pavos silvestres ( Meleagris gallopavo silvestris ) de la parte oriental, mediante el uso de sangre coagulada de aves vivas en Manitoba ( n ¼ 65) y de muestras de tejidos recolectadas postmortem en Quebec ( n ¼ 4). Se analiz ́ o el ADN proviral del virus de la enfermedad linfoproliferativa del pavo a trav ́ es de la amplificaci ́ on por PCR y la secuenciaci ́ on de una parte del gene gag (p31). Las muestras tambi ́ en se analizaron para detectar el virus de la reticuloendoteliosis (REV) mediante PCR. Veinticuatro aves (34.8%) resultaron positivas para la presencia del virus de la enfermedad linfoproliferativa, incluyendo todos los casos diagn ́ osticos. Un ave (1.4%) de Quebec ten ́ ıa lesiones macrosc ́ opicas y microsc ́ opicas compatibles con este virus. Dos pavos (2.9%) fueron positivos a la presencia del virus de la reticuloendoteliosis, uno (1.4%) de los cuales se co-infect ́ o con el virus de la enfermedad linfoproliferativa. El ana ́lisis filogen ́ etico de cepas del virus de la enfermedad linfoproliferativa de Quebec y Manitoba agrup ́ o a estos virus con muestras previamente secuenciadas de Ontario y secuencias disponibles p ́ ublicamente de un linaje de Am ́ erica del Norte. Este estudio aporta informaci ́ on valiosa para la vigilancia y el monitoreo continuos del virus de la enfermedad linfoproliferativa en Am ́ erica del Norte. Key words: Canada, clade, lymphoproliferative disease virus, Manitoba, phylogenetics, Quebec, surveillance, wild turkey Abbreviations: CWHC ¼ Canadian Wildlife Health Cooperative, LPD ¼ lymphoproliferative disease, LPDV ¼ lymphoproliferative disease virus, REV ¼ reticuloendotheliosis virus In Canada, the eastern wild turkey ( Meleagris gallopavo silvestris ) historically occupied a range that included the southernmost parts of Ontario and Quebec; however, in the early 1900s it was extirpated because of overhunting and habitat loss (1,2,3). Wild turkeys were successfully reintroduced to Ontario by means of trap and transfer programs beginning in 1984 (3), and their subsequent re- establishment in Quebec arose from the expansion and dispersal of Ontario and U.S. populations and through relocation programs (1,2,4). Wild turkeys are not native to Manitoba, but were introduced with the use of game-farmed birds from North Dakota in 1958, whose stock originated in Pennsylvania (5). Since then, ongoing trap and transfer programs and species dispersal have led to the establishment of spring and fall hunts in areas across southern Manitoba (5,6,7,8). There are now an estimated 4.8–5.0 million eastern wild turkeys across North America, with populations robust enough to support hunting seasons in several Canadian provinces, as well as the continental United States, making them a valued and economically important game species (9,10). Information pertaining to the health status of these birds in Canada, in particular the potential disease-causing agents that may circulate within populations, is lacking. Lymphoproliferative disease virus (LPDV), a relatively recently detected virus in North America, is increasingly reported in wild turkeys in the United States and, more recently, in Ontario, Canada (11,12,13). This disease has been detected in wild turkeys across a broad geographic range that extends from Ontario to Florida and as far west as Colorado (11,12,13). Lymphoproliferative disease virus is an oncogenic avian retrovirus that can induce neoplastic disease in wild and domestic turkeys; H Corresponding author. E-mail: amacdo21@uoguelph.ca AVIAN DISEASES 63:506–510, 2019 506 Downloaded From: https://bioone.org/journals/Avian-Diseases on 01 May 2026 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Florida Table 1. Demographic data and summary of results for 69 wild turkeys ( Meleagris gallopavo ) from Manitoba and Quebec, Canada. Results include presence of lesions, type and location of lesions, PCR findings for LPDV and REV, and accession numbers for sequenced samples. Accession Province Year Age, A/J Sex, M/F Lesions LPDV REV Y/N Type Location – MB 2018 A M N – – – MB 2018 A M N – – – MB 2018 A M N – – – MB 2018 A F N – – – MB 2018 J F N – – MK548370 MB 2018 A F N – – þ – MB 2018 J F N – – MK548371 MB 2018 A F N – – þ – MB 2018 J F N – – – MB 2018 J F N – – – MB 2018 J F N – – – MB 2018 A F N – – þ MK548372 MB 2018 A M N – – þ MK548373 MB 2018 A M N – – þ – MB 2018 A M N – – – MB 2018 A M N – – – MB 2018 A F N – – – MB 2018 J F N – – MK548374 MB 2018 J M N – – þ – MB 2018 A F N – – – MB 2018 J F N – – – MB 2018 A F N – – – MB 2018 J F N – – – MB 2018 J M N – – – MB 2018 A F N – – þ – MB 2018 J F N – – – MB 2018 A F N – – þ – MB 2018 J M N – – – MB 2018 A F N – – – MB 2018 A M N – – – MB 2018 J F N – – – MB 2018 A F N – – – MB 2018 A M N – – – MB 2018 A F N – – MK548375 MB 2018 A F N – – þ MK548376 MB 2018 A F N – – þ MK548377 MB 2018 A F N – – þ – MB 2018 J F N – – MK548378 MB 2018 A F N – – þ – MB 2018 A F N – – – MB 2018 J F N – – – MB 2018 A F N – – – MB 2018 A F N – – þ – MB 2018 J F N – – þ MK548379 MB 2018 A F N – – þ – MB 2018 J M N – – – MB 2018 A F N – – – MB 2018 A F N – – – MB 2018 A M N – – – MB 2018 J F N – – – MB 2018 J F N – – – MB 2018 J F N – – – MB 2018 A F N – – – MB 2018 J M N – – – MB 2018 J F N – – – MB 2018 A F N – – MK548380 MB 2018 A F N – – þ – MB 2018 A F N – – þ – MB 2018 A F N – – þ – MB 2018 J F N – – þ – MB 2018 A F N – – þ – MB 2018 A M N – – Lymphoproliferative disease virus in wild turkeys in Manitoba and Quebec 507 Downloaded From: https://bioone.org/journals/Avian-Diseases on 01 May 2026 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Florida however, most detections represent infections with no apparent clinical impact (11,12,14). Knowledge gaps exist concerning how and when the virus arrived in North America, where it originated, and how widespread it is among wild turkey populations. The purpose of this study was to gain a better understanding of the distribution and phylogenetic structure of LPDV in Canada (1) by surveying wild turkeys from trap and transfer programs in Manitoba and diagnostic (postmortem) cases in Quebec, and (2) by performing a phylogenetic analysis including a subset of LPDV sequences from Manitoba and Quebec, including comparison with available LPDV sequences from turkeys in Ontario, the United States, and Israel. MATERIALS AND METHODS Sample origin and submission data. Between 2017 and 2018, samples from 69 wild turkeys were submitted to the University of Guelph for LPDV testing. Most of these samples ( n ¼ 65) consisted of whole, clotted blood obtained from live birds during trap and transfer programs in Manitoba. All live birds appeared to be in good general health. In addition, routine postmortem evaluation (gross and histopathology) was performed on four wild turkey carcasses at the Quebec node of the Canadian Wildlife Health Cooperative from which select tissue samples (i.e., lesions suggestive of LPDV or avian pox; Table 1) were tested for LPDV. Date, location, age, and sex were recorded for each bird. DNA extraction and PCR. For DNA extraction, all samples were treated as tissue using QIAGEN t DNeasy t Blood & Tissue Kit (Qiagen, Toronto, Ontario, Canada) per manufacturer’s guidelines. For LPDV, proviral DNA was tested for by PCR with the use of the primer set LPDV-F (5 0 -ATGAGGACTTGTTAGATTGGTTAC-3 0 ) and LPDV-R (5 0 -TGATGGCGTCAGGGCTATTTG-3 0 ) that targeted a 431 base-pair (bp) fragment of the gag polyprotein (partial p31/partial capsid; 2). Reactions were carried out in 50- l l volumes consisting of 1x PCR buffer, 0.5 l M of each primer, 200 l M dNTPs, and 0.025 units Taq DNA polymerase (New England Biolabs, Whitby, Ontario, Canada). Thermal parameters included initial denaturation for 2 min at 94 C, followed by 40 cycles at 94 C for 30 sec, 50 C for 1 min, 72 C for 1 min, and a final 10-min extension at 72 C. Lymphoproliferative disease virus–positive controls, originating from known-positive wild turkeys in Ontario, and negative template controls of distilled water were used. Sequencing and phylogenetic analysis. Sequencing was performed (Advanced Analysis Centre, Genomics Facility, University of Guelph) on a subset of 14 LPDV-positive wild turkeys (Manitoba, n ¼ 10; Quebec, n ¼ 4) from this study and were deposited in GenBank as accessions MK548370–MK548385. A phylogenetic analysis (Fig. 1) to infer evolutionary relationships among the virus isolates was performed on 86 partial p31/capsid sequences that included 14 new sequences from this study and 69 previously published sequences (10 Ontario-derived sequences, 58 sequences from the United States, and the Israeli prototype strain (11,12,13). Sequences were aligned and subjected to Bayesian inference with the use of MrBayes 3.2.4 (15,16) and Geneious software (17), with the general time-reversible model (18). This model accounted for a proportion of invariant sites with gamma-distributed rate variation among sites, and gaps were treated as missing in all data sets. The codon nucleotide model (i.e., lset nucmodel ¼ codon rates ¼ gamma ngammacat ¼ 6) was used to analyze the aligned LPDV sequences. RESULTS Demographic data and postmortem assessment. Among the 69 wild turkeys tested, the sex ratio was 52 females to 17 males. The age ratio was 45 adults to 24 juveniles. Of the four turkey carcasses submitted to the CWHC, one had gross and microscopic lesions consistent with lymphoproliferative disease (LPD; 2), and the other three had lesions on the head, neck, and/or oral cavity that were suggestive of poxvirus (which was later confirmed by histopathology and/or PCR, Table 1). Gross lesions in the LPD-suspect turkey consisted of multiple, variably sized, yellow masses covering the unfeathered skin of the eyelids, the head, and the neck (Fig. 2). These masses were histologically characterized by multinodular accumulations of highly pleomorphic lymphocytes that expanded the dermis (Fig. 3). Lymphoid infiltrates were often centered on hyperplastic and hyperkeratotic feather follicles. Multinucleated giant cells were scattered among the lymphoid nodules. The overlying epidermis was hyperplastic, hyperkeratotic, and multi- focally ulcerated. Similar nodular lymphoid infiltrations were also within the conjunctiva, nictitating membranes, and sclera. PCR results. Of all wild turkeys tested, 34.8% (24/69) were LPDV-positive (30.8%, 20/65 from Manitoba; 100%, 4/4 from Quebec). In terms of age, adult turkeys accounted for 87.5% (21/ 24) of LPDV-positive birds, and juveniles 12.5% (3/24). For sex, 83.3% (20/24) of LPDV-positive wild turkeys were female, and 16.7% (4/24) were male. Phylogenetic results. The phylogenetic analysis of 85 North American LPDV sequences, combined with the prototype Israeli strain, revealed two distinct clades (Fig. 1). Clade 1 contained the majority of sequences from North America, including sequences from Manitoba and Quebec. Sequences from Manitoba clustered more closely with sequences from southern states, such as South Carolina, North Carolina, and Missouri, whereas Quebec sequences grouped most closely with those from Ontario, Canada and northeastern states such as New Hampshire and Maine. Clade 2 was comprised of the prototype Israeli strain (GenBank accession U09568 [19]) that clustered with four sequences from South Carolina. Table 1. Continued. Accession Province Year Age, A/J Sex, M/F Lesions LPDV REV Y/N Type Location MK548381 MB 2018 A F N – – þ – MB 2018 A F N – – – MB 2018 J F N – – MK548382 QC 2017 A M Y Pox-like Head/neck/diphtheretic þ MK548383 QC 2017 A F Y Tumor Head/neck þ MK548384 QC 2017 A F Y Pox-like Head/diphtheretic þ MK548385 QC 2017 A F Y Pox-like Head/neck/diphtheretic þ þ 508 A. M. MacDonald et al Downloaded From: https://bioone.org/journals/Avian-Diseases on 01 May 2026 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Florida DISCUSSION This study reports the detection of LPDV in wild turkeys from Manitoba and Quebec, Canada. This follows a recent report that LPDV was commonly detected among apparently healthy, hunter- harvested wild turkeys in Ontario (12). Approximately one-third of wild turkeys in Manitoba tested positive for LPDV by PCR, none of which had clinical signs suggestive of LPD. All diagnostic cases from Quebec tested PCR-positive for the virus, with one wild turkey exhibiting neoplastic disease associated with LPDV. Additionally, one LPDV-positive adult female was co-infected with REV, and another adult female was infected with REV alone. As both LPDV and REV can have similar clinical manifestations and can occur concurrently in turkeys, samples were tested for both agents (11,12,14). The high prevalence of LPDV in wild turkeys lacking overt signs of disease is consistent with previous observations in Canada and the United States (11,12,20). A small percentage (15.4%; 6/39) of wild turkey cases received for diagnostic evaluation at the Southeastern Cooperative Wildlife Disease Study in Georgia, United States, that tested positive for LPDV had lymphoid neoplasia in a variety of tissues (11). The LPDV-infected wild turkey with lymphoid neoplasia in Quebec is the first such report in Canada. Wild turkey samples Fig. 3. Histological section of the skin of the wild turkey with lymphoproliferative disease. There are multinodular accumulations of lymphocytic cells expanding the dermis. These cellular infiltrates are often centered on feather follicles (A). Hematoxylin, phloxine, and saffronstains. Bar ¼ 300 l m. Fig. 2. Wild turkey ( Meleagris gallopavo ) with clinical lymphopro- liferative disease. Multiple variably sized and often ulcerated masses are scattered in the skin over the head and neck. Bar ¼ 1 cm. Fig. 1. Phylogenetic tree of p31/capsid sequences from lympho- proliferative disease virus strains isolated from 10 live trap and transfer eastern wild turkeys ( Meleagris gallopavo silvestris ) from Manitoba, four diagnostic (postmortem) cases from Quebec, and 69 previously published sequences (the prototype Israeli strain, 10 Ontario-derived sequences, and 58 virus strains from the United States). The tree was generated with the use of Bayesian inference with a codon-based nucleotide substitution model. New sequences obtained from this study are shown in bold. Lymphoproliferative disease virus in wild turkeys in Manitoba and Quebec 509 Downloaded From: https://bioone.org/journals/Avian-Diseases on 01 May 2026 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Florida were collected through opportunistic blood collection during the trap and transfer of wild turkeys in Manitoba, and from diagnostic cases in Quebec; therefore, results may be influenced by lack of temporal and spatial range. Wild turkeys that were LPDV positive in the present study were predominantly adult females. This likely reflects the demographics of the majority of birds sampled (i.e., sampling bias). However, these results are consistent with those of a previous study, in which age and sex (i.e., adult, female birds) were strong predictors of LPDV infection in wild turkeys from New York (20). The phylogenetic analysis in this study compared nucleotide sequences of LPDV strains from wild turkeys in Manitoba and Quebec with those from Ontario, the United States (11), and Israel (i.e., the prototype strain [19]). Strains from Manitoba and Quebec clustered with the majority of sequences from North American in a clade distinct from a second clade that included the prototype Israeli strain. Although all individuals from Quebec and Manitoba were infected with the North American LPDV strain, at a finer scale, virus strains from Quebec clustered more closely with strains found in Ontario, Indiana, Pennsylvania, New York, New Hampshire, and Maine; whereas virus strains from Manitoba clustered more closely with those from the southern states of South Carolina, North Carolina, and Missouri. This could suggest that birds introduced to Manitoba originally came from more southern populations of turkeys in which LPDV was already present, as opposed to subsequent disease transmission from neighboring populations from northern midwestern states. Following the extirpation of wild turkeys from Quebec, popula- tions were reestablished through range expansion from Ontario and northern U.S. states, as well as translocations from Ontario and established populations within Quebec (1,4). Manitoba wild turkeys were initially introduced from North Dakota, and subsequently trapped and transferred to other regions of the province, augmented by natural expansion of U.S. populations (7). Infected birds may have been released into these provinces through restoration efforts or through natural dispersal. Quebec shares borders with Ontario and several U.S. states with detected infections with LPDV, including New York, Vermont, New Hampshire, and Maine. 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Genome organization of a biologically active molecular clone of the lymphoproliferative disease virus of turkeys. Virology 204:680–691; 1994. 20. Alger K, Bunting E, Schuler K, Whipps CM. Risk factors for and spatial distribution of lymphoproliferative disease virus (LPDV) in wild turkeys in New York State, USA. J Wildl Dis . 53:499–508; 2017. ACKNOWLEDGMENTS This research was funded by the Ontario Ministry of Agriculture, Food, and Rural Affairs–University of Guelph Research Program (UofG2013-1530). We thank Kathleen Brown (Universit ́ e de Montr ́ eal) for logistical and technical support, Amanda Salo for assisting in sample collection, volunteers with Wild Gobblers Unlimited for trapping birds in Manitoba, and in-kind support from Manitoba Department of Sustainable Development. 510 A. M. MacDonald et al Downloaded From: https://bioone.org/journals/Avian-Diseases on 01 May 2026 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Florida