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BACTERIAL DISEASES OF HONEY BEES and CURRENT METHODS FOR THE DIAGNOSIS OF DISEASES

Year 2023, Volume: 14 Issue: 3, 149 - 161, 30.12.2023
https://doi.org/10.38137/VFTD.1392294

Abstract

Unlike other animals, honey bees are considered a super-organism consisting of thousands of individuals, including queen, worker and drones. Bacterial diseases such as foulbrood, spiroplasmosis and septicemia are observed in honey bees. In honey bees Among the bacterial diseases of honey bees, foulbroods caused by Paenibacillus larvae and Melissococcus plutonius, which affect the larvae, are more economically important than others. Diagnosis and control of these diseases is critical for the sustainability of the beekeeping sector, as honey bees contribute to the easy spread of infections due to their proximity and foraging habits within the hive. In this context, researchers have been driven to develop new and reliable diagnostic methods for accurate and rapid detection of bee diseases. This review focuses on the diagnosis of bacterial bee diseases of importance for the beekeeping industry and current developments in diagnostics.

References

  • Adjlane, N., Haddad, N. & Kechih, S. (2014). Comparative study between techniques for the diagnosis of American foulbrood (Paenibacillus larvae) in honeybee colony. Journal of Animal and Veterinary Advances, 13, 970-973.
  • Applegate, J. R. Jr. & Petritz, O. A. (2020). Common and emerging infectious diseases of honeybees (Apis mellifera). Veterinary Clinics: Exotic Animal Practice, 23, 285-297.
  • Arafah, K., Voisin, S. N., Masson, V., Alaux, C., Le Conte, Y., Bocquet, M. & Bulet, P. (2019). MALDI–MS profiling to address honey bee health status under bacterial challenge through computational modeling. Proteomics, 19, 1900268.
  • Arai, R., Miyoshi-Akiyama, T., Okumura, K., Morinaga, Y., Wu, M., Sugimura, Y., Yoshiyama, M., Okura, M., Kirikae, T. & Takamatsu, D. (2014). Development of duplex pcr assay for detection and differentiation of typical and atypical Melissococcus plutonius strains. Journal of Veterinary Medical Science, 76, 491-498.
  • Arai, R., Tominaga, K., Wu, M., Okura, M., Ito, K., Okamura, N., Onishi, H., Osaki, M., Sugimura, Y., Yoshiyama, M. & Takamatsu, D. (2012). Diversity of Melissococcus plutonius from honeybee larvae in japan and experimental reproduction of European foulbrood with cultured atypical isolates. Plos One, 7, e33708.
  • Arculeo, P., Carpana, E., Di Noto, A. M. & Ferro, A. (2005). Melissococcus plutonius isolation from honeybee brood samples with European foulbrood in some Italian regions. Paper presented at the Apimondia 2005, Dublin.
  • Bailey, L. (1957). The isolation and cultural characteristics of Streptococcus pluton and further observations on Bacterium eurydice. Microbiology, 17, 39-48.
  • Bailey, L. & Ball, B. V. (1991). Bacteria. In, L. Bailey & B. V. Ball Eds. Honey Bee Pathology (Second Edition). London: Academic Press; 1991. pp. 35-52.
  • Bailey, L. & Collins, M. D. (1982). Reclassification of ‘Streptococcus pluton’ (White) in a new genus Melissococcus, as Melissococcus pluton nom. rev.; comb. nov. Journal of Applied Bacteriology, 53, 215-217.
  • Bamrick, J. F. (1967). Resistance to American foulbrood in honey bees: VI. Spore germination in larvae of different ages. Journal of Invertebrate Pathology, 9, 30-34.
  • Beims, H., Janke, M., Von der Ohe, W. & Steinert, M. (2020). Rapid identification and genotyping of the honeybee pathogen Paenibacillus larvae by combining culturing and multiplex quantitative PCR. Open Veterinary Journal, 10, 53–58-53–58.
  • Bikaun, J. M., Bates, T., Bollen, M., Flematti, G. R., Melonek, J., Praveen, P. & Grassl, J. (2022). Volatile biomarkers for non-invasive detection of American foulbrood, a threat to honey bee pollination services. Science of The Total Environment, 845, 157123.
  • Borum, E. (2014). Arıların yavru çürüklüğü infeksiyonlarinda doğru teşhis, mücadele ve korunma yöntemleri. Uludağ Arıcılık Dergisi, 14, 44-55.
  • Burritt, N. L., Foss, N. J., Neeno-Eckwall, E. C., Church, J. O., Hilger, A. M., Hildebrand, J. A., Warshauer, D. M., Perna, N. T. & Burritt, J. B. (2016). Sepsis and hemocyte loss in honey bees (Apis mellifera) infected with Serratia marcescens strain sicaria. Plos One, 11, e0167752.
  • Clark, T. B., Whitcomb, R. F., Tully, J. G., Mouches, C., Saillard, C., Bové, J. M., Wróblewski, H., Carle, P., Rose, D. L., Henegar, R. B. & Williamson, D. L. (1985). Spiroplasma melliferum, a new species from the honeybee (Apis mellifera). International Journal of Systematic and Evolutionary Microbiology, 35, 296-308.
  • Cremer, S., Armitage, S. A. & Schmid-Hempel, P. (2007). Social immunity. Current Biology, 17, R693-R702.
  • Dainat, B., Grossar, D., Ecoffey, B. & Haldemann, C. (2018). Triplex real-time PCR method for the qualitative detection of European and American foulbrood in honeybee. Journal of Microbiological Methods, 146, 61-63.
  • Daniels, M. (1983). Mechanisms of Spiroplasma pathogenicity. Annual Review of Phytopathology, 21, 29-43.
  • De Graaf, D. C., Alippi, A. M., Brown, M., Evans, J. D., Feldlaufer, M., Gregorc, A., Hornitzky, M., Pernal, S. F., Schuch, D. M. T., Titĕra, D., Tomkies, V. & Ritter, W. (2006). Diagnosis of American foulbrood in honey bees: a synthesis and proposed analytical protocols. Letters in Applied Microbiology, 43, 583-590.
  • Djordjevic, S. P., Noone, K., Smith, L. & Hornitzky, M. A. Z. (1998). Development of a hemi-nested PCR assay for the specific detection of Melissococcus pluton. Journal of Apicultural Research, 37, 165-174.
  • Dobbelaere, W., C. de Graaf, D. & E. Peeters, J. (2001). Development of a fast and reliable diagnostic method for American foulbrood disease (Paenibacillus larvae subsp. larvae) using a 16S rRNA gene based PCR. Apidologie, 32, 363-370.
  • Ehrenberg, S. (2022). Establishment of an ELISA and a lateral flow device for detection of European and American foulbrood including genotype-differentiation of the American foulbrood causing agent (ERIC I & ERIC II) in honey bees. Greifswald, Germany. Thesis of PhD, UG.
  • El Sanousi, S. M., El Sarag, M. S. A. & Mohamed, S. E. (1987). Properties of Serratia marcescens isolated from diseased honeybee (Apis mellifera) larvae. Microbiology, 133, 215-219.
  • Erban, T., Ledvinka, O., Kamler, M., Nesvorna, M., Hortova, B., Tyl, J., Titera, D., Markovic, M. & Hubert, J. (2017). Honeybee (Apis mellifera)-associated bacterial community affected by American foulbrood: detection of Paenibacillus larvae via microbiome analysis. Scientific Reports, 7, 5084.
  • Forsgren, E. (2010). European foulbrood in honey bees. Journal of Invertebrate Pathology, 103, S5-S9.
  • Forsgren, E., Budge, G. E., Charrière, J.-D. & Hornitzky, M. A. Z. (2013). Standard methods for European foulbrood research. Journal of Apicultural Research, 52, 1-14.
  • Forsgren, E. & Laugen, A. T. (2014). Prognostic value of using bee and hive debris samples for the detection of American foulbrood disease in honey bee colonies. Apidologie, 45, 10-20.
  • Forsgren, E., Locke, B., Sircoulomb, F. & Schäfer, M. O. (2018). Bacterial diseases in honeybees. Current Clinical Microbiology Reports, 5, 18-25.
  • Forsgren, E., Stevanovic, J. & Fries, I. (2008). Variability in germination and in temperature and storage resistance among Paenibacillus larvae genotypes. Veterinary Microbiology, 129, 342-349.
  • Fünfhaus, A., Ebeling, J. & Genersch, E. (2018). Bacterial pathogens of bees. Current Opinion in Insect Science, 26, 89-96.
  • Garrido-Bailón, E., Higes, M., Martínez-Salvador, A., Antúnez, K., Botías, C., Meana, A., Prieto, L. & Martín-Hernández, R. (2013). The prevalence of the honeybee brood pathogens Ascosphaera apis, Paenibacillus larvae and Melissococcus plutonius in Spanish apiaries determined with a new multiplex PCR assay. Microbial Biotechnology, 6, 731-739.
  • Genersch, E. (2008). Paenibacillus larvae and American foulbrood – long since known and still surprising. Journal für Verbraucherschutz und Lebensmittelsicherheit, 3, 429-434.
  • Genersch, E. (2010). American Foulbrood in honeybees and its causative agent, Paenibacillus larvae. Journal of Invertebrate Pathology, 103, S10-S19.
  • Govan, V. A., Allsopp, M. H. & Davison, S. (1999). A PCR detection method for rapid identification of Paenibacillus larvae. Applied and Environmental Microbiology, 65, 2243-2245.
  • Govan, V. A., Brözel, V., Allsopp, M. H. & Davison, S. (1998). A PCR detection method for rapid identification of Melissococcus pluton in honeybee larvae. Applied and Environmental Microbiology, 64, 1983-1985.
  • Grimont, F. & Grimont, P. A. D. (2006). The Genus Serratia. In, M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, & E. Stackebrandt Eds. The Prokaryotes: A Handbook on the Biology of Bacteria Volume 6: Proteobacteria: Gamma Subclass. New York, NY: Springer New York; 2006. pp. 219-244.
  • Grimont, P. A. & Grimont, F. (1978). The genus Serratia. Annual Reviews in Microbiology, 32, 221-248.
  • Hoage, T. R. & Rothenbuhler, W. C. (1966). Larval honey bee response to various doses of Bacillus larvae spores1. Journal of Economic Entomology, 59, 42-45.
  • Hornitzky, M. A. & Smith, L. (1998). Procedures for the culture of Melissococcus pluton from diseased brood and bulk honey samples. Journal of Apicultural Research, 37, 293-294.
  • Ingemar, F. & Scott, C. (2001). Implications of horizontal and vertical pathogen transmission for honey bee epidemiology. Apidologie, 32, 199-214.
  • Kušar, D., Papić, B., Zajc, U., Zdovc, I., Golob, M., Žvokelj, L., Knific, T., Avberšek, J., Ocepek, M. & Pislak Ocepek, M. (2021). Novel TaqMan PCR assay for the quantification of Paenibacillus larvae spores in bee-related samples. Insects, 12.
  • Lannutti, L., Gonzales, F. N., Dus Santos, M. J., Florin-Christensen, M. & Schnittger, L. (2022). Molecular detection and differentiation of arthropod, fungal, protozoan, bacterial and viral pathogens of honeybees. Veterinary Sciences, 9, 221.
  • Lauro, F. M., Favaretto, M., Covolo, L., Rassu, M. & Bertoloni, G. (2003). Rapid detection of Paenibacillus larvae from honey and hive samples with a novel nested PCR protocol. International Journal of Food Microbiology, 81, 195-201.
  • Lee, S., Lim, S., Choi, Y.-S., Lee, M.-l. & Kwon, H. W. (2020). Volatile disease markers of American foulbrood-infected larvae in Apis mellifera. Journal of Insect Physiology, 122, 104040.
  • Lim, S.-J., Min, S.-H., Wang, J.-H. & Yoon, B.-S. (2016). The development of ultra-rapid multiplex detection method for 6 species major pathogens of honeybee. Proceedings of the Korean society of apiculture conference, 102-102.
  • Lim, S., Kim, J., Lee, C. & Yoon, B. (2017). Development of ultra-rapid multiplex PCR detection against 6 major pathogens in honeybee. Korean Journal of Apiculture.
  • López-Uribe, M. & Robyn, U. (2022). Honey bee diseases: American foulbrood Retrieved 19.10.2023 https://extension.psu.edu/honey-bee-diseases-american-foulbrood.
  • Meeus, I., Vercruysse, V. & Smagghe, G. (2012). Molecular detection of Spiroplasma apis and Spiroplasma melliferum in bees. Journal of Invertebrate Pathology, 109, 172-174.
  • Mikušová, Z., Farka, Z., Pastucha, M., Poláchová, V., Obořilová, R. & Skládal, P. (2019). Amperometric immunosensor for rapid detection of honeybee pathogen Melissococcus plutonius. Electroanalysis, 31, 1969-1976.
  • Milbrath, M. O. G., Fowler, P. D., Abban, S. K., Lopez, D. & Evans, J. D. (2021). Validation of diagnostic methods for European foulbrood on commercial honey bee colonies in the united states. Journal of Insect Science, 21, 6.
  • Mouches, C., Bové, J. M. & Albisetti, J. (1984). Pathogenicity of Spiroplasma apis and other spiroplasmas for honey-bees in Southwestern France. Annales de l'Institut Pasteur / Microbiologie, 135, 151-155.
  • Mouches, C., Bové, J. M., Tully, J. G., Rose, D. L., McCoy, R. E., Carle-Junca, P., Garnier, M. & Saillard, C. (1983). Spiroplasma apis, a new species from the honey-bee Apis mellifera. Annales de l'Institut Pasteur / Microbiologie, 134, 383-397.
  • Okamoto, M., Furuya, H., Sugimoto, I., Kusumoto, M. & Takamatsu, D. (2022). A novel multiplex PCR assay to detect and distinguish between different types of Paenibacillus larvae and Melissococcus plutonius, and a survey of foulbrood pathogen contamination in Japanese honey. Journal of Veterinary Medical Science, 84, 390-399.
  • Pastucha, M., Odstrčilíková, E., Hlaváček, A., Brandmeier, J. C., Vykoukal, V., Weisová, J., Gorris, H. H., Skládal, P. & Farka, Z. (2021). Upconversion-linked immunoassay for the diagnosis of honeybee disease American foulbrood. iEEE Journal of Selected Topics in Quantum Electronics, 27, 1-11.
  • Peters, M., Kilwinski, J., Beringhoff, A., Reckling, D. & Genersch, E. (2006). American foulbrood of the honey bee: Occurrence and distribution of different genotypes of Paenibacillus larvae in the administrative district of Arnsberg (North Rhine-Westphalia). Journal of Veterinary Medicine Series B, 53, 100-104.
  • Poláchová, V., Pastucha, M., Mikušová, Z., Mickert, M. J., Hlaváček, A., Gorris, H. H., Skládal, P. & Farka, Z. (2019). Click-conjugated photon-upconversion nanoparticles in an immunoassay for honeybee pathogen Melissococcus plutonius. Nanoscale, 11, 8343-8351.
  • Raymann, K., Coon Kerri, L., Shaffer, Z., Salisbury, S. & Moran Nancy, A. (2018). Pathogenicity of Serratia marcescens strains in honey bees. mBio, 9.
  • Raymann, K., Shaffer, Z. & Moran, N. A. (2017). Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. Plos Biology, 15, e2001861.
  • Regassa, L. B. & Gasparich, G. E. (2006). Spiroplasmas: Evolutionary relationships and biodiversity. Frontiers in Bioscience-Landmark, 11, 2983-3002.
  • Rieg, S., Bauer, T. M., Peyerl-Hoffmann, G., Held, J., Ritter, W., Wagner, D., Kern, W. V. & Serr, A. (2010). Paenibacillus larvae bacteremia in injection drug users. Emerging Infectious Disease Journal, 16, 487.
  • Roetschi, A., Berthoud, H., Kuhn, R. & Imdorf, A. (2008). Infection rate based on quantitative real-time PCR of Melissococcus plutonius, the causal agent of European foulbrood, in honeybee colonies before and after apiary sanitation. Apidologie, 39, 362-371.
  • Schuch, D. M. T., Madden, R. H. & Sattler, A. (2001). An improved method for the detection and presumptive identification of Paenibacillus larvae subsp. larvae spores in honey. Journal of Apicultural Research, 40, 59-64.
  • Schwarz, R. S., Teixeira, É. W., Tauber, J. P., Birke, J. M., Martins, M. F., Fonseca, I. & Evans, J. D. (2014). Honey bee colonies act as reservoirs for two Spiroplasma facultative symbionts and incur complex, multiyear infection dynamics. Microbiology Open, 3, 341-355.
  • Stahly, D. P., Alippi, A. M., Bakhiet, N., Campana, C. F., Novak, C. C. & Cox, R. (1999). PPL1C, a virulent mutant bacteriophage useful for identification of Paenibacillus larvae subspecies larvae. Journal of Invertebrate Pathology, 74, 295-296.
  • Stamereilers, C., Fajardo, C. P., Walker, J. K., Mendez, K. N., Castro-Nallar, E., Grose, J. H., Hope, S. & Tsourkas, P. K. (2018). Genomic analysis of 48 Paenibacillus larvae bacteriophages. Viruses, 10, 377.
  • Thompson, H. M. & Brown, M. A. (2001). Is contact colony treatment with antibiotics an effective control for European foulbrood? Bee World, 82, 130-138.
  • Tomkies, V., Flint, J., Johnson, G., Waite, R., Wilkins, S., Danks, C., Watkins, M., Cuthbertson, A. G. S., Carpana, E., Marris, G., Budge, G. & Brown, M. A. (2009). Development and validation of a novel field test kit for European foulbrood. Apidologie, 40, 63-72.
  • Uygur, Ş. Ö. & Girişgin, A. O. (2008). Bal arısı hastalık ve zararlıları. Uludağ Arıcılık Dergisi, 8, 130-142.
  • Vita Bee Health (2023a). AFB Diagnostic Test Kit. Retrieved 19.10.2023. https://www.vita-europe.com/beehealth/products/afb-diagnostic-test-kit/.
  • Vita Bee Health (2023b). EFB Diagnostic Test Kit. Retrieved 25.10.2023. https://www.vita-europe.com/beehealth/products/efb-diagnostic-test-kit/. Whitcomb R.F. (1983). Culture Media for Spiroplasmos. In, S. Razin, Tully, J.G., Ed. Methods in Mycoplasmology: Mycoplasma. New York: Academic Press; 1983. pp. 147-158.
  • WOAH (2023a). Chapter 1.3. Diseases, infections and infestations listed by WOAH. Retrieved 16.10.2023. https://www.woah.org/en/what-we-do/standards/codes-and-manuals/terrestrial-code-online-access/?id=169&L=1&htmfile=chapitre_oie_listed_disease.htm.
  • WOAH. (2023b). Chapter 3.2.2. American foulbrood of honey bees (Infection of honey bees with Paenibacillus larvae). Retrieved 18.10.2023 https://www.woah.org/fileadmin/Home/eng/Health_standards/tahm/3.02.02_AMERICAN_FOULBROOD.pdf
  • WOAH. (2023c). Chapter 3.2.3. European foulbrood of honey bees (Infection of honey bees with Melissococcus plutonius). Retrieved 24.10.2023 https://www.woah.org/fileadmin/Home/fr/Health_standards/tahm/3.02.03_EUROPEAN_FOULBROOD.pdf
  • Yue, D., Nordhoff, M., Wieler, L. H., & Genersch, E. (2008). Fluorescence in situ hybridization (FISH) analysis of the interactions between honeybee larvae and Paenibacillus larvae, the causative agent of American foulbrood of honeybees (Apis mellifera). Environmental microbiology, 10, 1612-1620.
  • Zheng, H.-Q., & Chen, Y. P. (2014). Detection of Spiroplasma melliferum in honey bee colonies in the US. Journal of invertebrate pathology, 119, 47-49.

BAL ARILARININ BAKTERİYEL HASTALIKLARI ve HASTALIKLARIN TEŞHİSİNE YÖNELİK GÜNCEL METOTLAR

Year 2023, Volume: 14 Issue: 3, 149 - 161, 30.12.2023
https://doi.org/10.38137/VFTD.1392294

Abstract

Bal arıları, diğer hayvanlardan farklı olarak binlerce bireyden oluşan bir süper-organizma olarak kabul edilir ve içinde kraliçe, işçi ve erkek arılar bulunur. Bal arılarında yavru çürüklükleri, spiroplazmoz ve septisemi gibi bakteriyel hastalıklar görülmektedir. Bu hastalıklar arasında larvaları etkileyen Paenibacillus larvae ve Melissococcus plutonius’un neden olduğu yavru çürüklükleri ekonomik açıdan diğer bakteriyel hastalık etkenlerine kıyasla daha fazla öneme sahiptir. Bal arıları, kovan içindeki yakınlıkları ve yiyecek arama alışkanlıkları nedeniyle infeksiyonların kolayca yayılmasına katkıda bulunduklarından bu hastalıkların teşhisi ve kontrolü, arıcılık sektörünün sürdürülebilirliği için kritik bir öneme sahiptir. Bu bağlamda, arı hastalıklarının doğru ve hızlı bir şekilde tespiti için araştırmacılar yeni ve güvenilir teşhis yöntemleri geliştirmeye yönelmişlerdir. Bu derlemede, arıcılık sektörü için önem taşıyan bakteriyel arı hastalıklarının teşhisi ve teşhiste güncel gelişmeler üzerine odaklanılmıştır.

References

  • Adjlane, N., Haddad, N. & Kechih, S. (2014). Comparative study between techniques for the diagnosis of American foulbrood (Paenibacillus larvae) in honeybee colony. Journal of Animal and Veterinary Advances, 13, 970-973.
  • Applegate, J. R. Jr. & Petritz, O. A. (2020). Common and emerging infectious diseases of honeybees (Apis mellifera). Veterinary Clinics: Exotic Animal Practice, 23, 285-297.
  • Arafah, K., Voisin, S. N., Masson, V., Alaux, C., Le Conte, Y., Bocquet, M. & Bulet, P. (2019). MALDI–MS profiling to address honey bee health status under bacterial challenge through computational modeling. Proteomics, 19, 1900268.
  • Arai, R., Miyoshi-Akiyama, T., Okumura, K., Morinaga, Y., Wu, M., Sugimura, Y., Yoshiyama, M., Okura, M., Kirikae, T. & Takamatsu, D. (2014). Development of duplex pcr assay for detection and differentiation of typical and atypical Melissococcus plutonius strains. Journal of Veterinary Medical Science, 76, 491-498.
  • Arai, R., Tominaga, K., Wu, M., Okura, M., Ito, K., Okamura, N., Onishi, H., Osaki, M., Sugimura, Y., Yoshiyama, M. & Takamatsu, D. (2012). Diversity of Melissococcus plutonius from honeybee larvae in japan and experimental reproduction of European foulbrood with cultured atypical isolates. Plos One, 7, e33708.
  • Arculeo, P., Carpana, E., Di Noto, A. M. & Ferro, A. (2005). Melissococcus plutonius isolation from honeybee brood samples with European foulbrood in some Italian regions. Paper presented at the Apimondia 2005, Dublin.
  • Bailey, L. (1957). The isolation and cultural characteristics of Streptococcus pluton and further observations on Bacterium eurydice. Microbiology, 17, 39-48.
  • Bailey, L. & Ball, B. V. (1991). Bacteria. In, L. Bailey & B. V. Ball Eds. Honey Bee Pathology (Second Edition). London: Academic Press; 1991. pp. 35-52.
  • Bailey, L. & Collins, M. D. (1982). Reclassification of ‘Streptococcus pluton’ (White) in a new genus Melissococcus, as Melissococcus pluton nom. rev.; comb. nov. Journal of Applied Bacteriology, 53, 215-217.
  • Bamrick, J. F. (1967). Resistance to American foulbrood in honey bees: VI. Spore germination in larvae of different ages. Journal of Invertebrate Pathology, 9, 30-34.
  • Beims, H., Janke, M., Von der Ohe, W. & Steinert, M. (2020). Rapid identification and genotyping of the honeybee pathogen Paenibacillus larvae by combining culturing and multiplex quantitative PCR. Open Veterinary Journal, 10, 53–58-53–58.
  • Bikaun, J. M., Bates, T., Bollen, M., Flematti, G. R., Melonek, J., Praveen, P. & Grassl, J. (2022). Volatile biomarkers for non-invasive detection of American foulbrood, a threat to honey bee pollination services. Science of The Total Environment, 845, 157123.
  • Borum, E. (2014). Arıların yavru çürüklüğü infeksiyonlarinda doğru teşhis, mücadele ve korunma yöntemleri. Uludağ Arıcılık Dergisi, 14, 44-55.
  • Burritt, N. L., Foss, N. J., Neeno-Eckwall, E. C., Church, J. O., Hilger, A. M., Hildebrand, J. A., Warshauer, D. M., Perna, N. T. & Burritt, J. B. (2016). Sepsis and hemocyte loss in honey bees (Apis mellifera) infected with Serratia marcescens strain sicaria. Plos One, 11, e0167752.
  • Clark, T. B., Whitcomb, R. F., Tully, J. G., Mouches, C., Saillard, C., Bové, J. M., Wróblewski, H., Carle, P., Rose, D. L., Henegar, R. B. & Williamson, D. L. (1985). Spiroplasma melliferum, a new species from the honeybee (Apis mellifera). International Journal of Systematic and Evolutionary Microbiology, 35, 296-308.
  • Cremer, S., Armitage, S. A. & Schmid-Hempel, P. (2007). Social immunity. Current Biology, 17, R693-R702.
  • Dainat, B., Grossar, D., Ecoffey, B. & Haldemann, C. (2018). Triplex real-time PCR method for the qualitative detection of European and American foulbrood in honeybee. Journal of Microbiological Methods, 146, 61-63.
  • Daniels, M. (1983). Mechanisms of Spiroplasma pathogenicity. Annual Review of Phytopathology, 21, 29-43.
  • De Graaf, D. C., Alippi, A. M., Brown, M., Evans, J. D., Feldlaufer, M., Gregorc, A., Hornitzky, M., Pernal, S. F., Schuch, D. M. T., Titĕra, D., Tomkies, V. & Ritter, W. (2006). Diagnosis of American foulbrood in honey bees: a synthesis and proposed analytical protocols. Letters in Applied Microbiology, 43, 583-590.
  • Djordjevic, S. P., Noone, K., Smith, L. & Hornitzky, M. A. Z. (1998). Development of a hemi-nested PCR assay for the specific detection of Melissococcus pluton. Journal of Apicultural Research, 37, 165-174.
  • Dobbelaere, W., C. de Graaf, D. & E. Peeters, J. (2001). Development of a fast and reliable diagnostic method for American foulbrood disease (Paenibacillus larvae subsp. larvae) using a 16S rRNA gene based PCR. Apidologie, 32, 363-370.
  • Ehrenberg, S. (2022). Establishment of an ELISA and a lateral flow device for detection of European and American foulbrood including genotype-differentiation of the American foulbrood causing agent (ERIC I & ERIC II) in honey bees. Greifswald, Germany. Thesis of PhD, UG.
  • El Sanousi, S. M., El Sarag, M. S. A. & Mohamed, S. E. (1987). Properties of Serratia marcescens isolated from diseased honeybee (Apis mellifera) larvae. Microbiology, 133, 215-219.
  • Erban, T., Ledvinka, O., Kamler, M., Nesvorna, M., Hortova, B., Tyl, J., Titera, D., Markovic, M. & Hubert, J. (2017). Honeybee (Apis mellifera)-associated bacterial community affected by American foulbrood: detection of Paenibacillus larvae via microbiome analysis. Scientific Reports, 7, 5084.
  • Forsgren, E. (2010). European foulbrood in honey bees. Journal of Invertebrate Pathology, 103, S5-S9.
  • Forsgren, E., Budge, G. E., Charrière, J.-D. & Hornitzky, M. A. Z. (2013). Standard methods for European foulbrood research. Journal of Apicultural Research, 52, 1-14.
  • Forsgren, E. & Laugen, A. T. (2014). Prognostic value of using bee and hive debris samples for the detection of American foulbrood disease in honey bee colonies. Apidologie, 45, 10-20.
  • Forsgren, E., Locke, B., Sircoulomb, F. & Schäfer, M. O. (2018). Bacterial diseases in honeybees. Current Clinical Microbiology Reports, 5, 18-25.
  • Forsgren, E., Stevanovic, J. & Fries, I. (2008). Variability in germination and in temperature and storage resistance among Paenibacillus larvae genotypes. Veterinary Microbiology, 129, 342-349.
  • Fünfhaus, A., Ebeling, J. & Genersch, E. (2018). Bacterial pathogens of bees. Current Opinion in Insect Science, 26, 89-96.
  • Garrido-Bailón, E., Higes, M., Martínez-Salvador, A., Antúnez, K., Botías, C., Meana, A., Prieto, L. & Martín-Hernández, R. (2013). The prevalence of the honeybee brood pathogens Ascosphaera apis, Paenibacillus larvae and Melissococcus plutonius in Spanish apiaries determined with a new multiplex PCR assay. Microbial Biotechnology, 6, 731-739.
  • Genersch, E. (2008). Paenibacillus larvae and American foulbrood – long since known and still surprising. Journal für Verbraucherschutz und Lebensmittelsicherheit, 3, 429-434.
  • Genersch, E. (2010). American Foulbrood in honeybees and its causative agent, Paenibacillus larvae. Journal of Invertebrate Pathology, 103, S10-S19.
  • Govan, V. A., Allsopp, M. H. & Davison, S. (1999). A PCR detection method for rapid identification of Paenibacillus larvae. Applied and Environmental Microbiology, 65, 2243-2245.
  • Govan, V. A., Brözel, V., Allsopp, M. H. & Davison, S. (1998). A PCR detection method for rapid identification of Melissococcus pluton in honeybee larvae. Applied and Environmental Microbiology, 64, 1983-1985.
  • Grimont, F. & Grimont, P. A. D. (2006). The Genus Serratia. In, M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, & E. Stackebrandt Eds. The Prokaryotes: A Handbook on the Biology of Bacteria Volume 6: Proteobacteria: Gamma Subclass. New York, NY: Springer New York; 2006. pp. 219-244.
  • Grimont, P. A. & Grimont, F. (1978). The genus Serratia. Annual Reviews in Microbiology, 32, 221-248.
  • Hoage, T. R. & Rothenbuhler, W. C. (1966). Larval honey bee response to various doses of Bacillus larvae spores1. Journal of Economic Entomology, 59, 42-45.
  • Hornitzky, M. A. & Smith, L. (1998). Procedures for the culture of Melissococcus pluton from diseased brood and bulk honey samples. Journal of Apicultural Research, 37, 293-294.
  • Ingemar, F. & Scott, C. (2001). Implications of horizontal and vertical pathogen transmission for honey bee epidemiology. Apidologie, 32, 199-214.
  • Kušar, D., Papić, B., Zajc, U., Zdovc, I., Golob, M., Žvokelj, L., Knific, T., Avberšek, J., Ocepek, M. & Pislak Ocepek, M. (2021). Novel TaqMan PCR assay for the quantification of Paenibacillus larvae spores in bee-related samples. Insects, 12.
  • Lannutti, L., Gonzales, F. N., Dus Santos, M. J., Florin-Christensen, M. & Schnittger, L. (2022). Molecular detection and differentiation of arthropod, fungal, protozoan, bacterial and viral pathogens of honeybees. Veterinary Sciences, 9, 221.
  • Lauro, F. M., Favaretto, M., Covolo, L., Rassu, M. & Bertoloni, G. (2003). Rapid detection of Paenibacillus larvae from honey and hive samples with a novel nested PCR protocol. International Journal of Food Microbiology, 81, 195-201.
  • Lee, S., Lim, S., Choi, Y.-S., Lee, M.-l. & Kwon, H. W. (2020). Volatile disease markers of American foulbrood-infected larvae in Apis mellifera. Journal of Insect Physiology, 122, 104040.
  • Lim, S.-J., Min, S.-H., Wang, J.-H. & Yoon, B.-S. (2016). The development of ultra-rapid multiplex detection method for 6 species major pathogens of honeybee. Proceedings of the Korean society of apiculture conference, 102-102.
  • Lim, S., Kim, J., Lee, C. & Yoon, B. (2017). Development of ultra-rapid multiplex PCR detection against 6 major pathogens in honeybee. Korean Journal of Apiculture.
  • López-Uribe, M. & Robyn, U. (2022). Honey bee diseases: American foulbrood Retrieved 19.10.2023 https://extension.psu.edu/honey-bee-diseases-american-foulbrood.
  • Meeus, I., Vercruysse, V. & Smagghe, G. (2012). Molecular detection of Spiroplasma apis and Spiroplasma melliferum in bees. Journal of Invertebrate Pathology, 109, 172-174.
  • Mikušová, Z., Farka, Z., Pastucha, M., Poláchová, V., Obořilová, R. & Skládal, P. (2019). Amperometric immunosensor for rapid detection of honeybee pathogen Melissococcus plutonius. Electroanalysis, 31, 1969-1976.
  • Milbrath, M. O. G., Fowler, P. D., Abban, S. K., Lopez, D. & Evans, J. D. (2021). Validation of diagnostic methods for European foulbrood on commercial honey bee colonies in the united states. Journal of Insect Science, 21, 6.
  • Mouches, C., Bové, J. M. & Albisetti, J. (1984). Pathogenicity of Spiroplasma apis and other spiroplasmas for honey-bees in Southwestern France. Annales de l'Institut Pasteur / Microbiologie, 135, 151-155.
  • Mouches, C., Bové, J. M., Tully, J. G., Rose, D. L., McCoy, R. E., Carle-Junca, P., Garnier, M. & Saillard, C. (1983). Spiroplasma apis, a new species from the honey-bee Apis mellifera. Annales de l'Institut Pasteur / Microbiologie, 134, 383-397.
  • Okamoto, M., Furuya, H., Sugimoto, I., Kusumoto, M. & Takamatsu, D. (2022). A novel multiplex PCR assay to detect and distinguish between different types of Paenibacillus larvae and Melissococcus plutonius, and a survey of foulbrood pathogen contamination in Japanese honey. Journal of Veterinary Medical Science, 84, 390-399.
  • Pastucha, M., Odstrčilíková, E., Hlaváček, A., Brandmeier, J. C., Vykoukal, V., Weisová, J., Gorris, H. H., Skládal, P. & Farka, Z. (2021). Upconversion-linked immunoassay for the diagnosis of honeybee disease American foulbrood. iEEE Journal of Selected Topics in Quantum Electronics, 27, 1-11.
  • Peters, M., Kilwinski, J., Beringhoff, A., Reckling, D. & Genersch, E. (2006). American foulbrood of the honey bee: Occurrence and distribution of different genotypes of Paenibacillus larvae in the administrative district of Arnsberg (North Rhine-Westphalia). Journal of Veterinary Medicine Series B, 53, 100-104.
  • Poláchová, V., Pastucha, M., Mikušová, Z., Mickert, M. J., Hlaváček, A., Gorris, H. H., Skládal, P. & Farka, Z. (2019). Click-conjugated photon-upconversion nanoparticles in an immunoassay for honeybee pathogen Melissococcus plutonius. Nanoscale, 11, 8343-8351.
  • Raymann, K., Coon Kerri, L., Shaffer, Z., Salisbury, S. & Moran Nancy, A. (2018). Pathogenicity of Serratia marcescens strains in honey bees. mBio, 9.
  • Raymann, K., Shaffer, Z. & Moran, N. A. (2017). Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. Plos Biology, 15, e2001861.
  • Regassa, L. B. & Gasparich, G. E. (2006). Spiroplasmas: Evolutionary relationships and biodiversity. Frontiers in Bioscience-Landmark, 11, 2983-3002.
  • Rieg, S., Bauer, T. M., Peyerl-Hoffmann, G., Held, J., Ritter, W., Wagner, D., Kern, W. V. & Serr, A. (2010). Paenibacillus larvae bacteremia in injection drug users. Emerging Infectious Disease Journal, 16, 487.
  • Roetschi, A., Berthoud, H., Kuhn, R. & Imdorf, A. (2008). Infection rate based on quantitative real-time PCR of Melissococcus plutonius, the causal agent of European foulbrood, in honeybee colonies before and after apiary sanitation. Apidologie, 39, 362-371.
  • Schuch, D. M. T., Madden, R. H. & Sattler, A. (2001). An improved method for the detection and presumptive identification of Paenibacillus larvae subsp. larvae spores in honey. Journal of Apicultural Research, 40, 59-64.
  • Schwarz, R. S., Teixeira, É. W., Tauber, J. P., Birke, J. M., Martins, M. F., Fonseca, I. & Evans, J. D. (2014). Honey bee colonies act as reservoirs for two Spiroplasma facultative symbionts and incur complex, multiyear infection dynamics. Microbiology Open, 3, 341-355.
  • Stahly, D. P., Alippi, A. M., Bakhiet, N., Campana, C. F., Novak, C. C. & Cox, R. (1999). PPL1C, a virulent mutant bacteriophage useful for identification of Paenibacillus larvae subspecies larvae. Journal of Invertebrate Pathology, 74, 295-296.
  • Stamereilers, C., Fajardo, C. P., Walker, J. K., Mendez, K. N., Castro-Nallar, E., Grose, J. H., Hope, S. & Tsourkas, P. K. (2018). Genomic analysis of 48 Paenibacillus larvae bacteriophages. Viruses, 10, 377.
  • Thompson, H. M. & Brown, M. A. (2001). Is contact colony treatment with antibiotics an effective control for European foulbrood? Bee World, 82, 130-138.
  • Tomkies, V., Flint, J., Johnson, G., Waite, R., Wilkins, S., Danks, C., Watkins, M., Cuthbertson, A. G. S., Carpana, E., Marris, G., Budge, G. & Brown, M. A. (2009). Development and validation of a novel field test kit for European foulbrood. Apidologie, 40, 63-72.
  • Uygur, Ş. Ö. & Girişgin, A. O. (2008). Bal arısı hastalık ve zararlıları. Uludağ Arıcılık Dergisi, 8, 130-142.
  • Vita Bee Health (2023a). AFB Diagnostic Test Kit. Retrieved 19.10.2023. https://www.vita-europe.com/beehealth/products/afb-diagnostic-test-kit/.
  • Vita Bee Health (2023b). EFB Diagnostic Test Kit. Retrieved 25.10.2023. https://www.vita-europe.com/beehealth/products/efb-diagnostic-test-kit/. Whitcomb R.F. (1983). Culture Media for Spiroplasmos. In, S. Razin, Tully, J.G., Ed. Methods in Mycoplasmology: Mycoplasma. New York: Academic Press; 1983. pp. 147-158.
  • WOAH (2023a). Chapter 1.3. Diseases, infections and infestations listed by WOAH. Retrieved 16.10.2023. https://www.woah.org/en/what-we-do/standards/codes-and-manuals/terrestrial-code-online-access/?id=169&L=1&htmfile=chapitre_oie_listed_disease.htm.
  • WOAH. (2023b). Chapter 3.2.2. American foulbrood of honey bees (Infection of honey bees with Paenibacillus larvae). Retrieved 18.10.2023 https://www.woah.org/fileadmin/Home/eng/Health_standards/tahm/3.02.02_AMERICAN_FOULBROOD.pdf
  • WOAH. (2023c). Chapter 3.2.3. European foulbrood of honey bees (Infection of honey bees with Melissococcus plutonius). Retrieved 24.10.2023 https://www.woah.org/fileadmin/Home/fr/Health_standards/tahm/3.02.03_EUROPEAN_FOULBROOD.pdf
  • Yue, D., Nordhoff, M., Wieler, L. H., & Genersch, E. (2008). Fluorescence in situ hybridization (FISH) analysis of the interactions between honeybee larvae and Paenibacillus larvae, the causative agent of American foulbrood of honeybees (Apis mellifera). Environmental microbiology, 10, 1612-1620.
  • Zheng, H.-Q., & Chen, Y. P. (2014). Detection of Spiroplasma melliferum in honey bee colonies in the US. Journal of invertebrate pathology, 119, 47-49.
There are 75 citations in total.

Details

Primary Language Turkish
Subjects Veterinary Microbiology
Journal Section Review
Authors

Saliha Bediz Şahin 0000-0002-1963-8958

Barış Sareyyüpoğlu 0000-0002-2212-2610

Publication Date December 30, 2023
Submission Date November 17, 2023
Acceptance Date December 26, 2023
Published in Issue Year 2023 Volume: 14 Issue: 3

Cite

APA Bediz Şahin, S., & Sareyyüpoğlu, B. (2023). BAL ARILARININ BAKTERİYEL HASTALIKLARI ve HASTALIKLARIN TEŞHİSİNE YÖNELİK GÜNCEL METOTLAR. Veteriner Farmakoloji Ve Toksikoloji Derneği Bülteni, 14(3), 149-161. https://doi.org/10.38137/VFTD.1392294