Bagaza virus emerged in Spain in 2010 and was not reported in other countries in Europe until 2021, when the virus was detected by molecular methods in a corn bunting and several red-legged partridges in Portugal. Sequencing revealed high similarity between the 2021 strains from Portugal and the 2010 strains from Spain.Peer reviewe

Abade dos Santos, Fábio

Alves, Paulo C.

Barros, Sílvia C.

Cardona, Teresa

Duarte, Margarida D.

Fagulha, Teresa

Fernández de Mera, Isabel G.

Fontoura-Gonçalves, Catarina

Gonçalves, David

Gortázar, Christian

Henriques, Ana Margarida

Höfle, Ursula

Queirós, João

Rodrigues, Marisa

Sánchez Cano, Alberto

Emerging Infectious Diseases

PubMed

Bagaza virus emerged in Spain in 2010 and was not reported in other countries in Europe until 2021, when the virus was detected by molecular methods in a corn bunting and several red-legged partridges in Portugal. Sequencing revealed high similarity between the 2021 strains from Portugal and the 2010 strains from Spain

Sánchez-Cano, Alberto

dos Santos, Fábio Abade

Cabrera, Teresa Cardona

de Mera, Isabel G. Fernández

Gortazar, Christian

Alves, Paulo Célio

PubMed Central

Bagaza Virus in Wild Birds, Portugal, 2021

Cardona-Cabrera, Teresa

Digital.CSIC

Bagaza Virus in Wild Birds, Portugal, 2021João Queirós, Sílvia C. Barros, Alberto Sánchez-Cano, Ana Margarida Henriques, Teresa Fagulha, Fábio Abade dos Santos, Margarida D. Duarte, Catarina Fontoura-Gonçalves, David Gonçalves, Marisa Rodrigues, Teresa Cardona Cabrera,  Isabel G. Fernández de Mera, Christian Gortazar, Ursula Höfle, Paulo Célio AlvesAuthor affiliations: Universidade do Porto Centro de Investigação em Biodiversidade e Recursos Genéticos, Vairão, Portugal (J. Queirós, C. Fontoura-Gonçalves, D. Gonçalves, M. Rodrigues, P.C. Alves); Estação Biológica de Mértola, Mértola, Portugal  (J. Queirós, D. Gonçalves, M. Rodrigues, P.C. Alves);  Universidade do Porto, Porto, Portugal (J. Queirós, D. Gonçalves, P.C. Alves); Instituto Nacional de Investigação Agrária e  Veterinária, Oeiras, Portugal (S.C. Barros, A.M. Henriques,  T. Fagulha, F.A. Abade dos Santos, M.D. Duarte); Instituto de Investigación en Recursos Cinegéticos, Ciudad Real, Spain  (A. Sánchez-Cano, T.C. Cabrera, I.G. Fernández de Mera,  C. Gortazar, U. Höfle)DOI: http://doi.org/10.3201/eid2807.212408Bagaza virus (BAGV) is a single-stranded, pos-itive-sense RNA virus. The virus belongs to the mosquitoborne cluster of the genus Flavivirus, fam-ily Flaviviridae, which includes such other emerging pathogens as West Nile, Japanese encephalitis, den-gue, Zika, and yellow fever viruses, all of which are associated with neurologic disease in animals and hu-mans and have zoonotic potential (1). BAGV was first isolated in 1966 from a pool of Culex species mosqui-toes in the Bagaza District of Central African Republic and was detected subsequently in several species of mosquitoes. The first BAGV-associated deaths in ver-tebrates were detected in Spain, in 2010, in red-legged partridges (Alectoris rufa) and ring-necked pheasants (Phasianus colchicus) (2) and then, in 2016, in Hima-layan monal pheasants (Lophophorus impejanus) in South Africa (3). BAGV infection causes neurologic disease in red-legged partridges, gray partridges (Perdix per-dix), ring-necked pheasants, and, to a lesser degree, in common wood pigeons (Columba palumbus) (1–6). Estimated mortality rates range from 23% to 30% in naturally and experimentally infected red-legged partridges (5,7); rates are higher (up to 40%) in experi-mentally infected gray partridges (6) and lower rates in pheasants and columbiformes (4,7). We describe a BAGV outbreak in Portugal in autumn 2021, associ-ated with abnormal fatalities in red-legged partridges and 1 corn bunting (Emberiza calandra).On September 1, 2021, three red-legged par-tridges were found dead in Serpa, southern Portugal. From September through mid-October, 9 partridges and 1 corn bunting were found dead in the same area (Appendix Table, https://wwwnc.cdc.gov/EID/article/28/7/21-2408-App1.pdf). Local reports emerged of partridges displaying neurologic signs compatible with potential viral infection, such as dis-orientation and motor incoordination. Twelve of the 13 birds were necropsied. Laboratory examinations and preliminary diagnoses were conducted at the Re-search Institute in Hunting Resources (Ciudad Real, Spain) and at the Center for Research on Biodiversity and Genetic Resources (InBIO Laboratório Associado, Vairão, Portugal). Official diagnosis was determined at the National Institute of Agrarian and Veterinary Research, I.P. (Lisbon, Portugal). Growing feathers were collected from 30 partridges live-trapped in the same area on October 3.Researchers conducted molecular detection by using RNA extracted from various sampling points (feather pulp, brain, heart, kidney, spleen, and intestine) and followed 2 strategies targeting different regions of the BAGV genome (nonstructural 2b, nonstructural 5 [NS5], and 3′ nontranslated region) (Appendix Table); first, a duplex quantitative reverse transcription PCR (RT-PCR) for the simultaneous and differential detec-tion of Japanese encephalitis and Ntaya flavivirus sero-complexes (8), and second, a uniplex quantitative RT-PCR specific for the NS5 coding region of BAGV (9). The researchers used conventional nested RT-PCR for sequencing to target part of the NS5 gene (10) and an in-house RT-PCR (developed at the National Institute of Agrarian and Veterinary Research) to target part of the NS2b gene (Appendix Table).Out of the 12 necropsied birds, 8 red-legged par-tridges and 1 corn bunting (75%) tested positive for BAGV, as did 4 of 30 live-captured red-legged par-tridges (13.3%) (Appendix Table). The 108 bp sequenc-es obtained from duplex quantitative RT-PCR from partridge 9 and the corn bunting showed 100% simi-larity with the 3′ nontranslated region of the BAGV reference strain (GenBank accession no. HQ644143) detected in the 2010 outbreak in Spain (Appendix 1504 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 27, No. 7, July 2022RESEARCH LETTERSBagaza virus emerged in Spain in 2010 and was not re-ported in other countries in Europe until 2021, when the vi-rus was detected by molecular methods in a corn bunting and several red-legged partridges in Portugal. Sequenc-ing revealed high similarity between the 2021 strains from Portugal and the 2010 strains from Spain.Table). In comparing the NS5 regions, researchers found very high similarities with HQ644143 in the 110 base pair sequences obtained from 6 partridges by nested RT-PCR (99.1%) and in the 171 base pair se-quences taken from 2 partridges by RT-PCR (98.8%).Upon necropsy, all birds were in good body con-dition, suggesting an acute disease course. Histopa-thology, albeit hampered by autolysis and freezing artifacts, revealed lymphoid depletion in the spleen and severe congestion, moderate to abundant diffuse mononuclear inflammatory infiltrates, and focal ne-crosis in all tissues. The heart, brain, kidney, and liver were the most affected organs (Figure).This work confirms BAGV emergence in Portu-gal, in autumn 2021, associated with abnormal fa-talities in red-legged partridges. Active circulation of BAGV was also evidenced in the studied region, where 13.3% of live-captured red-legged partridges testing positive for BAGV, even though ecologic and demographic studies are required to determine the extent and magnitude of the outbreak. Substantial population decline in the red-legged partridge can be anticipated in this region of Portugal on the ba-sis of the mortality rate previously estimated for this species (4,7). The fatal case in a songbird, the corn bunting, suggests that BAGV might have a broad-er spectrum and effect in wild bird species. This finding, combined with the small size of the analyzed sequences, suggests the need for further research to identify the vectors for BAGV in Portugal and their role in the epidemiology of the disease, and eluci-date the phylogenetic relationships between the 2021 strains in Portugal and 2010 strains in Spain against known BAGV strains. No conclusions can be made from this research regarding the origin of this infection. However, the introduction of the virus in Portugal might be linked to persistence of the disease and migration of infected wild birds from North Africa or Spain.AcknowledgmentsWe thank the personnel from the hunting sector for their help during field work (sampling and capturing) and Fernanda Simões for the sex determination of partridges 7 and 8 by molecular methods.About the AuthorMr. Queirós is a junior researcher at CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, BIOPOLIS Program in Genomics, Biodiversity and Land Planning, University of Porto. His research interests include the epidemiology of emerging infectious diseases in wildlife species and their interface with livestock and humans, as well as population genetics and phylogeography. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 28, No. 7, July 2022 1505RESEARCH LETTERSFigure. Microscopic lesions caused by Bagaza virus infection in liver, heart, kidney, and brain tissue of red-legged partridges (Alectoris rufa), Portugal, 2021. A) In liver, congestion, hemozoin presence in Kupffer cells, focal hepatocyte necrosis, and a moderate mononuclear infiltrate are visible despite some freezing artifacts. B) In heart, congestion, hemorrhage, edema, degeneration of myofibers of the myocardium, and endothelial swelling and moderate to abundant diffuse mononuclear infiltrates are visible. C) In kidney, tubulointerstitial nephritis characterized by congestion, hemorrhage necrosis of proximal convoluted tubular epithelium, and diffuse moderate to abundant mononuclear inflammatory infiltrate are visible. D) In brain, mild nonpurulent encephalitis with congestion, mononuclear cell extravasation, and endothelial cell swelling are visible. Hematoxilin eosin staining; original magnification ×400.References  1. Benzarti E, Linden A, Desmecht D, Garigliany M.  Mosquito-borne epornitic flaviviruses: an update and  review. J Gen Virol. 2019;100:119–32. https://doi.org/ 10.1099/jgv.0.001203  2. Agüero M, Fernández-Pinero J, Buitrago D, Sánchez A, Elizalde M, San Miguel E, et al. Bagaza virus in partridges and pheasants, Spain, 2010. Emerg Infect Dis. 2011;17:1498–501. https://doi.org/10.3201/eid1708.110077  3. Steyn J, Botha EM, Lourens C, Coetzer JAW, Venter M. Bagaza virus in Himalayan monal pheasants, South  Africa, 2016–2017. Emerg Infect Dis. 2019;25:2299–302. https://doi.org/10.3201/eid2512.190756  4. Gamino V, Gutiérrez-Guzmán AV, Fernández-de-Mera IG, Ortíz JA, Durán-Martín M, de la Fuente J, et al. Natural Bagaza virus infection in game birds in southern Spain.  Vet Res (Faisalabad). 2012;43:65. https://doi.org/ 10.1186/1297-9716-43-65  5. Llorente F, Pérez-Ramírez E, Fernández-Pinero J,  Elizalde M, Figuerola J, Soriguer RC, et al. Bagaza virus is pathogenic and transmitted by direct contact in  experimentally infected partridges, but is not infectious in house sparrows and adult mice. Vet Res (Faisalabad). 2015;46:93. https://doi.org/10.1186/s13567-015-0233-9  6. Cano-Gómez C, Llorente F, Pérez-Ramírez E, Soriguer RC, Sarasa M, Jiménez-Clavero MÁ. Experimental infection of grey partridges with Bagaza virus: pathogenicity evaluation and potential role as a competent host. Vet Res (Faisalabad). 2018;49:44. https://doi.org/10.1186/s13567-018-0536-8  7. García-Bocanegra I, Zorrilla I, Rodríguez E, Rayas E,  Camacho L, Redondo I, et al. Monitoring of the Bagaza  virus epidemic in wild bird species in Spain, 2010.  Transbound Emerg Dis. 2013;60:120–6. https://doi.org/ 10.1111/j.1865-1682.2012.01324.x  8. Elizalde M, Cano-Gómez C, Llorente F, Pérez-Ramírez E, Casades-Martí L, Aguilera-Sepúlveda P, et al. A duplex quantitative real-time reverse transcription-PCR for  simultaneous detection and differentiation of flaviviruses of the Japanese encephalitis and Ntaya serocomplexes in birds. Front Vet Sci. 2020;7:203. https://doi.org/10.3389/fvets.2020.00203  9. Buitrago D, Rocha A, Tena-Tomás C, Vigo M, Agüero M, Jiménez-Clavero MA. Real-time fluorogenic reverse  transcription polymerase chain reaction assay for the specific detection of Bagaza virus. J Vet Diagn Invest. 2012;24:959–63. https://doi.org/10.1177/104063871245272310. Sánchez-Seco MP, Rosario D, Domingo C, Hernández L,  Valdés K, Guzmán MG, et al. Generic RT-nested-PCR for  detection of flaviviruses using degenerated primers and internal control followed by sequencing for specific  identification. J Virol Methods. 2005;126:101–9.  https://doi.org/10.1016/j.jviromet.2005.01.025Address for correspondence: João Queirós, CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, BIOPOLIS Program in Genomics, Biodiversity and Land Planning, Campus de Vairão,  Universidade do Porto, 4485-661 Vairão, Portugal; email:  joao.queiros@cibio.up.ptHodgkin Lymphoma after  Disseminated Mycobacterium genavense Infection,  GermanyJanina Trauth, Thomas Discher,  Moritz Fritzenwanker, Can Imirzalioglu,  Tobias Arnold, Dagmar Steiner, Elvira Richter,  Laura Crisponi, Bodo Grimbacher, Susanne HeroldAuthor affiliations: Justus Liebig University, Giessen, Germany  (J. Trauth, T. Discher, M. Frizenwanker, C. Imirzalioglu, S. Herold); University Hospital Gießen, Gießen (T. Arnold, D. Steiner);  MVZ Labor Doctor Limbach and Kollegen, Heidelberg, Germany (E. Richter); Medical Center–University of Freiburg, Freiburg, Germany (L. Crisponi, B. Grimbacher)DOI: http://doi.org/10.3201/eid2807.220425Mycobacterium genavense was first described in 1992 in HIV-positive patients with low CD4 counts and disseminated mycobacterial disease (1). Since the 2000s, additional risk factors for this bacterial infec-tion became known (e.g., solid organ transplantation, hematopoietic stem cell transplantation, Epstein-Barr virus–associated lymphoproliferative disorder, neu-tralizing anti–interferon γ autoantibodies, adenosine deaminase deficiency, nuclear factor κB1 deficiency) (2,3). Clinical manifestations of M. genavense common-ly involve blood and lymph nodes but can include the gastrointestinal tract, spleen, liver, and bone marrow; pneumonia, prosthetic joint infection, endobronchial mass, and brain mass have also been described.A previously healthy 23-year-old woman sought medical treatment at University Hospital Gießen (Gießen, Germany) for progressive cervical lymph-adenopathy (Figure, panel A) and fever originating 4 months prior. A professional animal keeper, she had no history of previous infections or autoimmune dis-ease, an unremarkable family history, and no travel outside of Europe; her tattoos showed no signs of ir-ritation. She experienced gender dysphoria and used masculinizing hormone therapy (testosterone). We 1506 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 28, No. 7, July 2022RESEARCH LETTERSMycobacterium genavense infection, a rare nontuber-culous mycobacteria infection, occurs in heavily immu-nocompromised patients (i.e., those with advanced HIV disease, genetic disorders, or acquired immunologic dis-orders and those undergoing immunosuppressive thera-py). We report a case of disseminated M. genavense in-fection preceding Hodgkin lymphoma in a patient without obvious risk factors for this infection.

Bagaza virus in wild birds, Portugal, 2021

Bagaza virus in wild birds, Portugal, 2021

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