The The first case of Co-infection of Sacbr ood virus and Varroa destructor virus-1 in honey bees (Apis mellifera L., 1758)
Περίληψη
Viral infections can occur at all developmental stages of honey bees and are of great concern for the beekeeping industry as they cause significant economic losses in beehives. The aim of this study is to investigate sudden bee mortalities and colony losses in a beekeeping facility. In 2022, high levels of bee mortality were observed in an apiculture facility in Kırıkhan district of Hatay province. In order to determine the cause of bee mortality, adult worker bee samples (n = 50) with clinical symptoms were collected from hives within the facility. Collected bee samples were processed for RNA extraction. One step real time RT-PCR methods were applied for the detection of Sacbrood virus (SBV) and Varroa destructor virus-1 (VDV-1). The one step real time RT-PCR analysis revealed the presence of mixed infection with SBV and VDV-1 viruses in the facility. As far as we know, this study is the first report of a mixed infection of SBV and VDV-1 in honey bees. Additional comprehensive studies are needed to better understand the epidemiology of mixed infections caused by viruses in honey bees.
Λεπτομέρειες άρθρου
- Πώς να δημιουργήσετε Αναφορές
-
Zerek, A., Şevik, M., Erdem, I., & Yaman, M. (2025). The The first case of Co-infection of Sacbr ood virus and Varroa destructor virus-1 in honey bees (Apis mellifera L., 1758). Περιοδικό της Ελληνικής Κτηνιατρικής Εταιρείας, 76(2), 9385–9390. https://doi.org/10.12681/jhvms.36354
- Τεύχος
- Τόμ. 76 Αρ. 2 (2025)
- Ενότητα
- Case Report
Αυτή η εργασία είναι αδειοδοτημένη υπό το CC Αναφορά Δημιουργού – Μη Εμπορική Χρήση 4.0.
Οι συγγραφείς των άρθρων που δημοσιεύονται στο περιοδικό διατηρούν τα δικαιώματα πνευματικής ιδιοκτησίας επί των άρθρων τους, δίνοντας στο περιοδικό το δικαίωμα της πρώτης δημοσίευσης.
Άρθρα που δημοσιεύονται στο περιοδικό διατίθενται με άδεια Creative Commons 4.0 Non Commercial και σύμφωνα με την άδεια μπορούν να χρησιμοποιούνται ελεύθερα, με αναφορά στο/στη συγγραφέα και στην πρώτη δημοσίευση για μη κερδοσκοπικούς σκοπούς.
Οι συγγραφείς μπορούν να καταθέσουν το άρθρο σε ιδρυματικό ή άλλο αποθετήριο ή/και να το δημοσιεύσουν σε άλλη έκδοση, με υποχρεωτική την αναφορά πρώτης δημοσίευσης στο J Hellenic Vet Med Soc
Οι συγγραφείς ενθαρρύνονται να καταθέσουν σε αποθετήριο ή να δημοσιεύσουν την εργασία τους στο διαδίκτυο πριν ή κατά τη διαδικασία υποβολής και αξιολόγησής της.
Λήψεις
Τα δεδομένα λήψης δεν είναι ακόμη διαθέσιμα.
Αναφορές
Aizen MA, Harder LD (2009) The global stock of domesticated
honey bees is growing slower than agricultural demand for
pollination. Curr biol, 19 (11): 915–918. DOI: 10.1016/j.
cub.2009.03.071
Ball BV, Bailey L (1997) Viruses. In, Morse RA, Flottum K. (Eds.),
Honey Bee Pest, Predators, & Diseases. The A. I. Root Co.,
Medina, OH, pp. 11–31.
Benaets K, Van Geystelen A, Cardoen D, De Smet L, de Graaf DC,
Schoofs L, Larmuseau MH, Brettell LE, Martin SJ, Wenseleers
T (2017) Covert deformed wing virus infections have long-term
deleterious effects on honeybee foraging and survival. Proc Biol
Sci. 284: 20162149. DOI: 10.1098/rspb.2016.2149.
Berényi O, Bakonyi T, Derakhshifar I, Köglberger H, Nowotny N
(2006) Occurrence of six honeybee virus in diseased Austrian
apiaries. Appl Environ Microbiol, 72 (4):2414-2420. DOI:
1128/AEM.72.4.2414-2420.2006
Blanchard P, Guillot S, Antùnez K, Köglberger H, Kryger P, de
Miranda JR, Franco S, Chauzat MP, Thiéry R, Ribière M (2014)
Development and validation of a real-time two-step RT-qPCR
TaqMan® assay for quantitation of Sacbrood virus (SBV)
and its application to a field survey of symptomatic honey bee
colonies. J Virol Methods, 197: 7-13. DOI: 10.1016/j.jviromet.
09.012
Brasesco C, Quintana S, Di Gerónimo V, Genchi García ML, Sguazza
G, Bravi ME, Fargnoli L, Reynaldi FJ, Eguaras M, Maggi M
(2021) Deformed wing virus type a and b in managed honeybee
colonies of Argentina. Bull Entomol Res, 1-11. DOI: 10.1017/
S000748532000036X.
Brettell LE, Mordecai GJ, Schroeder DC, Jones IM, da Silva JR,
Vicente-Rubiano M, Martin SJ (2017) A Comparison of Deformed
Wing Virus in Deformed and Asymptomatic Honey
Bees. Insects. 8 (1): 28. DOI: 10.3390/insects8010028.
Cagirgan AA, Yazici Z (2021) The prevalence of seven crucial
honeybee viruses using multiplex RT-PCR and their phylogenetic
analysis, Turk J Vet Anim Sci, 45: 44-55. DOI: 10.3906/
vet-2004-139
Cavigli I, Daughenbaugh KF, Martin M, Lerch M, Banner K, Garcia
E, Brutscher LM, Flenniken ML (2016) Pathogen prevalence
and abundance in honey bee colonies involved in almond pollination.
Apidologie. 47(2):251-266. DOI: 10.1007/s13592-
-0395-5.
Chen Y, Evans J, Feldlaufer M (2006) Horizontal and vertical transmission
of viruses in the honey bee, Apis mellifera. J Invertebr
Pathol, 92: 152-159. DOI: 10.1016/j.jip.2006.03.010
Chen Y, Zhao Y, Hammond J, Hsu HT, Evans J, Feldlaufer M (2004)
Multiple virus infections in the honey bee and genome divergence of honey bee viruses. J Invertebr Pathol, 87: 84-93. DOI:
1016/j.jip.2004.07.005.
Choe SE, Nguyen TTD, Hyun BH, Noh JH, Lee HS, Lee CH, Kang
SW (2012) Genetic and phylogenetic analysis of South Korean
sacbrood virus isolates from infected honey bees (Apis cerana).
Vet Microbiol, 157: 32-40. DOI: 10.1016/j.vetmic.2011.12.007
Daughenbaugh KF, Martin M, Brutscher LM, Cavigli I, Garcia
E, Lavin M, Flenniken ML (2015) Honey Bee Infecting Lake
Sinai Viruses. Viruses. 7(6): 3285-309. DOI: 10.3390/v7062772.
de Miranda JR (2008) Diagnostic techniques for virus detection in
honey bees. In, Aubert MFA, Ball BV, Fries I, Morritz RFA,
Milani N, Bernardinelli I (Eds.): Virology and the Honey Bee.
Luxembourg: EEC Publications, pp. 121-232.
de Miranda JR, Bailey L, Ball BV, Blanchard P, Budge GE, Chejanovsky
N, Chen YP, Gauthier L, Genersch E, de Graaf DC,
Ribière M, Ryabov E, De Smet J, Van Der Steen JJM (2013)
Standard methods for virus research in Apis mellifera. J Apic
Res, 52(4): 1-56. DOI: 10.3896/IBRA.1.52.4.22.
Genersch E (2010) Honey bee pathology: current threats to honey
bees and beekeeping. Appl Microbiol Biotechnol, 87: 87–97.
DOI: 10.1007/s00253-010-2573-8
Haddad N, Brake M, Migdadi H, de Miranda JR (2008) First detection
of honey bee viruses in Jordan by RT-PCR. Jordan Journal
of Agricultural Sciences, 4 (3): 242-247.
Kalayci G, Cagirgan AA, Kaplan M, Pekmez K, Beyazit A, Ozkan
B, Yesiloz B, Arslan F (2020) The role of viral and parasitic
pathogens affected by colony losses in Turkish apiaries. Kafkas
Univ Vet Fak Derg. DOI: 10.9775/kvfd.2020. 24154.
Kevill JL, Highfield A, Mordecai GJ, Martin SJ, Schroeder DC
(2017) ABC Assay: Method Development and Application to
Quantify the Role of Three DWV Master Variants in Overwinter
Colony Losses of European Honey Bees. Viruses, 9 (11): 314.
DOI: 10.3390/v9110314.
Kızıltepe Ş, Akpınar R, Akman A, Kaya S, Çelik S (2023) Iğdır
İlinde Görülen Arı Kolonisi Kayıplarında Viral ve Paraziter
Etkenlerin Rolü. Journal of the Institute of Science and Technology,
(2): 858-871. DOI: 10.21597/jist.1184308.
Lanzi G, de Miranda JR, Boniotti MB, Cameron CE, Lavazza A,
Capucci L, Camazine SM, Rossi C (2006) Molecular and biological
characterization of deformed wing virus of honeybees
(Apis mellifera L.). J Virol. 80(10): 4998-5009. DOI: 10.1128/
jvi.80.10.4998-5009.2006.
Li J, Wang T, Evans JD, Rose R, Zhao Y, Li Z, Li J, Huang S, Heerman
M, Rodríguez-García C, Banmekea O, Brister JR, Hatcher
EL, Cao L, Hamilton M, Chen Y (2019) The Phylogeny and
Pathogenesis of Sacbrood Virus (SBV) Infection in European
Honey Bees, Apis mellifera. Viruses, 11(1):61. DOI: 10.3390/
v11010061.
Lu C, Hung YT, Cheng Q (2020) A review of sub-lethal neonicotinoid
insecticides exposure and effects on pollinators. Curr Pollution
Rep, 6(2): 137-151. DOI: 10.1007/s40726-020-00142-8
Martin SJ (2001) The role of Varroa and viral pathogens in the
collapse of honeybee colonies: a modeling approach. J Appl
Ecol, 38: 1082–1093. DOI: 10.1046/j.1365-2664.2001.00662.x
McMenamin AJ, Flenniken ML (2018) Recently identified bee viruses
and their impact on bee pollinators. Curr Opin Insect Sci,
: 120-129. DOI: 10.1016/j.cois.2018.02.009
Moharrami M, Modirrousta H (2018) Molecular identification of
six honeybee viruses in Iranian apiaries. Arch Razi Inst, 73 (4):
-318. DOI: 10.22092/ARI.2017.107481.1068
Morawetz L, Koglberger H, Griesbacher A, Derakhshifa I, Crailsheim
K, Brodschneide R, Moosbeckhofe R (2019) Health status
of honey bee colonies (Apis mellifera) and disease-related
risk factors for colony losses in Austria. PLoS ONE 14 (7):
e0219293. DOI: 10.1371/journal.pone.0219293
Muz D, Muz MN (2023a) Israel acute bee paralysis virus and its
prevalence in apiaries with colony loss in Türkiye. U. Bee J,
(1): 105-114. DOI: 10.31467/uluaricilik.1265816.
Muz D, Muz MN (2023b) Acute bee paralysis virus field isolates
from apiaries suffering colony losses in Türkiye. J Apic Res,
(5): 1169-1175. DOI: 10.1080/00218839.2023.2242123.
Nielsen SL, Nicolaisen M, Kryger P (2008) Incidence of acute bee
paralysis virus, black queen cell virus, chronic bee paralysis
virus, deformed wing virus, Kashmir bee virus and sacbrood
virus in honey bees (Apis mellifera) in Denmark. Apidologie,
: 310-314. DOI: 10.1051/apido:2008007.
Ongus JR, Peters D, Bonmatin JM, Bengsch E, Vlak JM, van Oers
MM (2004) Complete sequence of a picorna-like virus of the
genus Iflavirus replicating in the mite Varroa destructor. J Gen
Virol. 85 (12):3747-3755. DOI: 10.1099/vir.0.80470-0.
Oz ME, Avci O, Dogan M (2023) Impact of deformed wing virus
master variants (DWV-A, DWV-B, and DWV-C) in managed
honey bee colonies of Türkiye. Eurasian J Vet Sci, 39 (3): 124-
DOI: 10.15312/EurasianJVetSci.2023.407.
Parveen N, Miglani R, Kumar A, Dewali S, Kumar K, Sharma N,
Bisht SS (2022) Honey bee pathogenesis posing threat to its
global population: A short review. Proc Indian Natl Sci Acad,
(1): 11-32. DOI: 10.1007/s43538-022-00062-9
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O,
Kunin WE (2010) Global pollinator declines: Trends, impacts
and drivers. Trends Ecol Evol, 25: 345–353. DOI: 10.1016/j.
tree.2010.01.007
Remnant EJ, Shi M, Buchmann G, Blacquière T, Holmes EC, Beekman
M, Ashe A (2017) A diverse range of novel RNA viruses
in geographically distinct honey bee populations. J Virol,
:e00158-17. DOI: 10.1128/jvi.00158-17.
Rüstemoğlu M, Sipahioğlu HM (2019) Occurrence and prevalence
of six honey bee viruses in Hakkari (Türkiye) and their genomic
divergence. Mun Ent Zool, 14(2): 574-583.
Ryabov EV, Childers AK, Chen Y, Madella S, Nessa A, vanEngelsdorp
D, Evans JD (2017) Recent spread of Varroa destructor
virus-1, a honey bee pathogen, in the United States. Sci Rep,
: 17447. DOI:10.1038/s41598-017-17802-3.
Schurr F, Tison A, Militano L, Cheviron N, Sircoulomb F, Riviere
MP, Chabert MR, Thiery R, Dubois E (2019) Validation
of Quantitative Real-Time RT-PCR Assays for the Detection
of Six Honeybee Viruses. J Virol Methods, 270: 70-78. DOI:
1016/j.jviromet.2019.04.020
Sguazza GH, Reynaldi FJ, Galosi CM, Pecoraro MR (2013) Simultaneous
detection of bee viruses by multiplex PCR. J Virol
Methods, 194:102-106. DOI: 10.1016/j.jviromet.2013.08.003.
Tantillo G, Bottaro M, Di Pinto A, Martella V, Di Pinto P, Terio V
(2015) Virus infections of honeybees Apis mellifera. Ital J Food
Saf, 30: 4 (3): 5364. DOI: 10.4081/ijfs.2015.5364
Tentcheva D, Gauthier L, Zappulla N, Dainat B, Cousserans F, Colin
ME, Bergoin M (2004) Prevalence and seasonal variations of
six bee viruses in Apis mellifera L. and Varroa destructor mite
populations in France. Appl Environ Microbiol, 70 (12):7185-
DOI: 10.1128/AEM.70.12.7185-7191.2004.
Tlak Gajger I, Kolodziejek J, Bakonyi T, Nowotny N (2014) Prevalence
and distribution patterns of seven different honeybee
viruses in diseased colonies: a case study from Croatia. Apidologie,
:701-706. DOI: 10.1007/s13592-014-0287-0.
Tozkar CÖ, Kence M, Kence A, Huang Q, Evans JD (2015) Metatranscriptomic
analyses of honey bee colonies. Front Genet,
:100. DOI: 10.3389/fgene.2015.00100.
Ullah A, Gajger IT, Majoros A, Dar SA, Khan S, Shah AH, Khabir
MN, Hussain R, Khan HU, Hameed M, Anjum SI (2021) Viral
impacts on honey bee populations: A review. Saudi J Biol Sci,
(1): 523-530. DOI: 10.1016/j.sjbs.2020.10.037
Valles SM, Chen Y, Firth AE, Guérin DMA, Hashimoto Y, Herrero
S, de Miranda JR, Ryabov E (2017) ICTV Report Consortium.
ICTV Virus Taxonomy Profile: Iflaviridae. J Gen Virol,
(4):527-528. DOI: 10.1099/jgv.0.000757.
Wei R, Cao L, Feng Y, Chen Y, Chen G, Zheng H (2022) Sacbrood
virus: a growing threat to honeybees and wild pollinators. Viruses,
(9): 1871. DOI: 10.3390/v14091871
Wyszkowska J, Grodzicki P, Szczygieł M (2019) Electromagnetic
fields and colony collapse disorder of the Honey bee. Przegląd
Elektrotechniczny, 95(1): 137-40.
