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Journals / Anadolu Bil Meslek Yüksekokulu Dergisi / 2026 / Cilt: 21 Sayı: 73

Use of bacteriophages in american foulbrood

Amerikan yavru çürüklüğünde bakteriyofaj kullanımı

Alper Mete(İSTANBUL ÜNİVERSİTESİ-CERRAHPAŞA, VETERİNER FAKÜLTESİ, KLİNİK ÖNCESİ BİLİMLERİ BÖLÜMÜ, VETERİNERLİK MİKROBİYOLOJİSİ ANABİLİM DALI)0009-0005-5039-433X
Deniz Kesen(İSTANBUL ÜNİVERSİTESİ-CERRAHPAŞA, VETERİNER FAKÜLTESİ, KLİNİK ÖNCESİ BİLİMLERİ BÖLÜMÜ, VETERİNERLİK MİKROBİYOLOJİSİ ANABİLİM DALI)0009-0006-8104-8138
Kemal Metiner(İSTANBUL ÜNİVERSİTESİ-CERRAHPAŞA, VETERİNER FAKÜLTESİ, KLİNİK ÖNCESİ BİLİMLERİ BÖLÜMÜ, VETERİNERLİK MİKROBİYOLOJİSİ ANABİLİM DALI)0000-0003-4105-5852
Pages
37–60
Publication Date
2026-07-20
DOI
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AI Summary & Key Takeaways

AI Insight
⚡ TL;DR(Too Long; Didn't Read)

Although control methods using bacteriophages against AFB are not yet widely implemented, research demonstrates the potential of this method.

📌 3 Key Takeaways

🎯
Objective & Hypothesis:The honey bee (Apis mellifera L.) is the world's most important pollinator of plant-based agricultural products in terms of economics.
📊
Key Findings & Data:AFB is a serious infection that can cause up to 100% mortality, especially in the larval stage, leading to significant economic losses in the global beekeeping industry.
💡
Conclusion & Impact:Although control methods using bacteriophages against AFB are not yet widely implemented, research demonstrates the potential of this method.
🔬Design:Review & Systematic Survey
📍Scope:Comprehensive Sample
⚙️Variables:Apis mellifera L. · Amerikan yavru çürüklüğü · Bal arısı

Abstract

The honey bee (Apis mellifera L.) is the world's most important pollinator of plant-based agricultural products in terms of economics. Factors that negatively affect honey bees can reduce their vitality and productivity. One of these threats, American Foulbrood (AFB), is a globally widespread, high-mortality, spore-forming, epizootic bacterial infection caused by the Gram-positive bacterium Paenibacillus larvae. AFB is a serious infection that can cause up to 100% mortality, especially in the larval stage, leading to significant economic losses in the global beekeeping industry. Specifically, ERIC I strain cause 100% mortality in infected larvae within 12 days, while ERIC II strain kills infected larvae in about 7 days. The contemporary ban on antibiotic use has increased the demand for alternative approaches in the treatment of AFB. In this context, bacteriophages (phages) stand out as promising biological agents due to their specific effects; environmental safety profiles, and minimal impact on the honey bee microbiota. This review examines the biology, spread, current diagnostic methods, and bacteriophage-based biocontrol approaches for P. larvae, the causative agent of AFB, in light of current literature. Although control methods using bacteriophages against AFB are not yet widely implemented, research demonstrates the potential of this method.

Özet

Bal arısı (Apis mellifera L.), ekonomik açıdan bitkisel tarım ürünlerinin dünyadaki en önemli tozlaştırıcısıdır. Bal arılarını olumsuz etkileyen etkenler, onların yaşama gücünü ve verimini düşürebilmektedir. Bu tehditlerden biri de Paenibacillus larvae’nın neden olduğu Amerikan Yavru Çürüklüğü (AYÇ) enfeksiyonudur. P. larvae Gram pozitif, sporlu, mortalite oranı yüksek, dünya genelinde yayılmış olan epizootik nitelikte enfeksiyona neden olmaktadır. AYÇ, özellikle larva döneminde %100'e varan ölümlere neden olarak küresel arıcılık sektöründe önemli ekonomik kayıplara yol açan ciddi bir enfeksiyondur. Özellikle ERIC I suşu ile enfekte larvaların 12 gün içinde %100 öldüğü, ERIC II suşu ile enfekte larvaların ise yaklaşık 7 gün içinde öldüğü görülmüştür. Günümüzde antibiyotik kullanımının yasaklanması, AYÇ tedavisinde alternatif yaklaşımlara olan ihtiyacı artırmıştır. Bu kapsamda bakteriyofajlar, özgül etkileri, çevresel güvenlik profilleri ve bal arılarının mikrobiyotasına minimal etkileri sayesinde umut vadeden biyolojik ajanlar olarak ön plana çıkmaktadır. Bu derlemede, AYÇ’nin etkeni olan P. larvae’nın biyolojisi, yayılımı, mevcut teşhis yöntemleri ve bakteriyofaj temelli biyokontrol yaklaşımları güncel literatür ışığında ele alınmıştır. AYÇ’nün kontrolünde bakteriyofajlarla yapılan mücadele yöntemleri henüz yaygın olarak uygulanmamasına rağmen, yapılan araştırmalar bakteriyofajların bal arılarını bu enfeksiyondan koruma ve tedavide potansiyelinin yüksek düzeyde olduğunu göstermektedir.

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Cite This Article

Mete, A., Kesen, D., Metiner, K. (2026). Use of bacteriophages in american foulbrood. Anadolu Bil Meslek Yüksekokulu Dergisi, Cilt: 21 Sayı: 73, 37–60. https://ajindex.com/articles/1579889

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References (52)

  1. Akpınar, R., Bozdeveci, A. & Çelik, S. (2023). Orta ve Doğu Karadeniz Bölgesindeki bal arılarında ve temel petekte Amerikan yavru çürüklüğünün teşhisi. Arıcılık Araştırma Dergisi, 15(1), 1–10.
  2. Ashiralieva, A. & Genersch, E. (2006). Reclassification, genotypes and virulence of Paenibacillus larvae, the etiological agent of American foulbrood in honeybees—A review. Apidologie, 37(4), 411–420. https://doi.org/10.1051/apido:2006025
  3. Atterbury, R. J. (2009). Bacteriophage biocontrol in animals and meat products. Microbial Biotechnology, 2(6), 601–612. https://doi. org/10.1111/j.1751-7915.2009.00114.x
  4. Beims, H., Bunk, B., Erler, S., Mohr, K. I., Spröer, C., Pradella, S., Günther, G. et al. (2020). Discovery of Paenibacillus larvae ERIC V: Phenotypic and genomic comparison to genotypes ERIC I-IV reveal different inventories of virulence factors which correlate with epidemiological prevalences of American foulbrood. International Journal of Medical Microbiology, 310(2), Article 151394. https://doi. org/10.1016/j.ijmm.2020.151394
  5. Beims, H., Wittmann, J., Bunk, B., Overmann, J., Rohde, C., Rohde, M., Günther, G., Hölzle, L. E., von der Ohe, W., & Steinert, M. (2020). Paenibacillus larvae virulence and spore production: A comparative study of European-American foulbrood genotypes. Frontiers in Microbiology, 11, 1460. https://doi.org/10.3389/fmicb.2020.01460
  6. Beims, H., Wittmann, J., Bunk, B., Spröer, C., Rohde, C., Günther, G., Rohde, M. et al. (2015). Paenibacillus larvae-directed bacteriophage HB10c2 and its application in American foulbrood-affected honey bee larvae. Applied and Environmental Microbiology, 81(16), 5411–5419. https://doi.org/10.1128/AEM.01457-15
  7. Bonilla-Rosso, G., Steiner, T., Wichmann, F., Bexkens, E. & Engel, P. (2020). Honey bees harbor a diverse gut virome engaging in nested strain-level interactions with the microbiota. Proceedings of the National Academy of Sciences, 117(13), 7355–7362. https://doi. org/10.1073/pnas.1914655117
  8. Bozdeveci, A. (2021). Paenibacillus larvae bakteriyofajlarının izolasyonu, moleküler karakterizasyonu ve farklı suşlarına karşı etkinliğin belirlenmesi (Tez No. 691713) [Doktora tezi, Recep Tayyip Erdoğan Üniversitesi]. YÖK Ulusal Tez Merkezi.
  9. Brady, T. S., Fajardo, C. P., Merrill, B. D., Hilton, J. A., Graves, K. A., Eggett, D. L. & Hope, S. (2018). Bystander phage therapy: Inducing host-associated bacteria to produce antimicrobial toxins against the pathogen using phages. Antibiotics, 7(4), Article 105. https://doi. org/10.3390/antibiotics7040105
  10. Brady, T. S., Merrill, B. D., Hilton, J. A., Payne, A. M., Stephenson, M. B. & Hope, S. (2017). Bacteriophages as an alternative to conventional antibiotic use for the prevention or treatment of Paenibacillus larvae in honeybee hives. Journal of Invertebrate Pathology, 150, 94–100. https://doi.org/10.1016/j.jip.2017.09.010
  11. Brady, T. S., Roll, C. R., Walker, J. K., Fajardo, C. P., Breakwell, D. P., Eggett, D. L. & Hope, S. (2021). Phages bind to vegetative and spore forms of Paenibacillus larvae and to vegetative Brevibacillus laterosporus. Frontiers in Microbiology, 12, Article 588035. https:// doi.org/10.3389/fmicb.2021.588035
  12. Cieplak, T., Soffer, N., Sulakvelidze, A. & Nielsen, D. S. (2018). A bacteriophage cocktail targeting Escherichia coli reduces E. coli in simulated gut conditions, while preserving a non-targeted representative commensal normal microbiota. Gut Microbes, 9(5), 391–399. https://doi.org/10.1080/19490976.2018.1447293
  13. Clokie, M. R., Millard, A. D., Letarov, A. V. & Heaphy, S. (2011). Phages in nature. Bacteriophage, 1(1), 31–45. https://doi.org/10.4161/ bact.1.1.14942
  14. De Graaf, D. C., Alippi, A. M., Antúnez, K., Aronstein, K. A., Budge, G., De Koker, D., De Smet, L. et al. (2013). Standard methods for American foulbrood research. Journal of Apicultural Research, 52(1), 1–28. https://doi.org/10.3896/IBRA.1.52.1.14
  15. Dingman, D. W. & Stahly, D. P. (1983). Medium promoting sporulation of Bacillus larvae and metabolism of medium components. Applied and Environmental Microbiology, 46(4), 860–869. https://doi. org/10.1128/aem.46.4.860-869.1983
  16. Djukic, M., Becker, D., Fünfhaus, A., Papadometrio, C., Pauli, E. B., Hierlmeier, T., Genersch, E., & Daniel, R. (2014). Genomic analysis of Paenibacillus larvae and survey of its virulence factors. PLOS ONE, 9(7), e103022. https://doi.org/10.1371/journal.pone.0103022
  17. El-Meihy, R. M., Hassan, E. O., Alamoudi, S. A., Negm, S., Al- Hoshani, N., Al-Ghamdi, M. S. & Nowar, E. E. (2024). Probing the interaction of Paenibacillus larvae bacteriophage as a biological agent to control the American foulbrood disease in honeybee. Saudi Journal of Biological Sciences, 31(6), Article 104002. https://doi.org/10.1016/j. sjbs.2024.104002
  18. Food and Agriculture Organization. (2022, December). Tarım ve hayvancılık ürünleri, 2022. https://www.fao.org/faostat/en/#data
  19. Fünfhaus, A., Ebeling, J., & Genersch, E. (2017). Bacterial toxins relevant for pathogenesis of American Foulbrood of honey bees (Apis mellifera). Toxins, 9(12), 397. https://doi.org/10.3390/toxins9120397
  20. Garcia-Gonzalez, E., & Genersch, E. (2020). Paenibacillus larvae and American Foulbrood: A review of a deadly core pathogen of honey bees. Environmental Microbiology, 22(11), 4501-4513. https://doi. org/10.1111/1462-2920.15166
  21. Genç, F., & Dodoloğlu, A. (2002). Arıcılığın temel esasları. Atatürk Üniversitesi Ziraat Fakültesi Ders Yayınları.
  22. Genersch, E. (2010). American foulbrood in honeybees and its causative agent, Paenibacillus larvae. Journal of Invertebrate Pathology, 103(Supplement 1), S10–S19. https://doi.org/10.1016/j. jip.2009.06.015
  23. Genersch, E. & Otten, C. (2003). The use of repetitive element PCR fingerprinting (rep-PCR) for genetic subtyping of German field isolates of Paenibacillus larvae subsp. larvae. Apidologie, 34(3), 195– 206. https://doi.org/10.1051/apido:2003010
  24. Gregorc, A. & Bowen, I. D. (1998). Histopathological and histochemical changes in honeybee larvae (Apis mellifera L.) after infection with Bacillus larvae, the causative agent of American foulbrood disease. Cell Biology International, 22(2), 137–144. https:// doi.org/10.1006/cbir.1997.0232
  25. Gülpınar, V. (2005). Bal arısı hastalık ve zararlıları. Teknik Arıcılık, 87, 2–7.
  26. Hansen, H. & Brødsgaard, C. J. (1999). American foulbrood: A review of its biology, diagnosis and control. Bee World, 80(1), 5–23. https://doi.org/10.1080/0005772X.1999.11099415
  27. Heyndrickx, M., Vandemeulebroecke, K., Hoste, B., Janssen, P., Kersters, K., De Vos, P., Logan, N. A. et al. (1996). Reclassification of Paenibacillus (formerly Bacillus) pulvifaciens (Nakamura 1984) Ash et al. 1994, a later subjective synonym of Paenibacillus (formerly Bacillus) larvae (White 1906) Ash et al. 1994, as a subspecies of P. larvae, with emended descriptions of P. larvae as P. larvae subsp. larvae and P. larvae subsp. pulvifaciens. International Journal of Systematic and Evolutionary Microbiology, 46(1), 270–279. https:// doi.org/10.1099/00207713-46-1-270
  28. Hornitzky, M. & Karlovskis, S. (1989). A culture technique for the detection of Bacillus larvae in honeybees. Journal of Apicultural Research, 28(2), 118–120. https://doi.org/10.1080/00218839.1989.11 100832
  29. Jończyk-Matysiak, E., Popiela, E., Owczarek, B., Hodyra- Stefaniak, K., Świtała-Jeleń, K., Łodej, N., Orwat, F. et al. (2020). Phages in therapy and prophylaxis of American foulbrood—Recent implications from practical applications. Frontiers in Microbiology, 11, Article 1913. https://doi.org/10.3389/fmicb.2020.01913
  30. Karali, M., Akpınar, R., Sevim, E., Bozdeveci, A. & Alpay Karaoğlu, Ş. (2022). Amerikan Yavru Çürüklüğü etkeni P. larvae suşlarında bakteriyofaj izolasyon ve karakterizasyonu [BAP Araştırma Projesi Sonuç Raporu]. Recep Tayyip Erdoğan Üniversitesi.
  31. Kekeçoğlu, M., Rasgele, P. G., Acar, F. & Kaya, S. T. (2013). Düzce ilinde bulunan arıcılık işletmelerinde görülen koloni kayıplarının, bal arısı hastalık ve zararlılarının ve mücadele yöntemlerinin araştırılması. Düzce Üniversitesi Bilim ve Teknoloji Dergisi, 3(3), 620–633.
  32. Kok, D. N., Gosselin, S. P., Howard, B., Cresawn, S. G., Tsourkas, P. K. & Hendrickson, H. L. (2025). Genomic analysis of 96 Paenibacillus larvae bacteriophages including 26 from Aotearoa, New Zealand. Viruses, 17(2), Article 137. https://doi.org/10.3390/v17020137
  33. Kok, D. N., Zhou, D., Tsourkas, P. K. & Hendrickson, H. L. (2023). Paenibacillus larvae and their phages; a community science approach to discovery and initial testing of prophylactic phage cocktails against American foulbrood in New Zealand. Microbiome Research Reports, 2(4), Article 32. https://doi.org/10.20517/mrr.2023.36
  34. Pasupuleti, V. R., Sammugam, L., Ramesh, N. & Gan, S. H. (2017). Honey, propolis, and royal jelly: A comprehensive review of their biological actions and health benefits. Oxidative Medicine and Cellular Longevity, 2017, Article 1259510. https://doi. org/10.1155/2017/1259510
  35. Paull, K., Spencer, E., Miller, C. R. & Van Leuven, J. T. (2024). Viral adaptations to alternative hosts in the honey bee pathogen Paenibacillus larvae. bioRxiv. https://doi.org/10.1101/2024.01.22.576711
  36. Ribeiro, H. G., Correia, R., Moreira, T., Vilas Boas, D., Azeredo, J. & Oliveira, A. (2019). Bacteriophage biodistribution and infectivity from honeybee to bee larvae using a T7 phage model. Scientific Reports, 9(1), Article 620. https://doi.org/10.1038/s41598-018-37034-w
  37. Sancak, K., Zan Sancak, A. & Aygören, E. (2013). Dünya ve Türkiye’de arıcılık. Arıcılık Araştırma Dergisi, 5(10), 7–13.
  38. 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(2), 59–64. https://doi.org/10.1080/00218839.2001.11101052
  39. Sillankorva, S. M., Oliveira, H. & Azeredo, J. (2012). Bacteriophages and their role in food safety. International Journal of Microbiology, 2012, Article 863958. https://doi.org/10.1155/2012/863958
  40. Simsek, H. & Kalender, H. (2001). Elazığ’daki arı işletmelerinde Amerikan Yavru Çürüklüğü Hastalığının araştırılması. Pendik Veteriner Mikrobiyoloji Dergisi, 33(1-2), 27–32.
  41. Stamereilers, C., Fajardo, C. P., Walker, J. K., Mendez, K. N., Castro-Nallar, E., Grose, J. H., Hope, S. et al. (2018). Genomic analysis of 48 Paenibacillus larvae bacteriophages. Viruses, 10(7), Article 377. https://doi.org/10.3390/v10070377
  42. Şahinler, N. & Gül, A. (2005). Hatay yöresinde bulunan arıcılık işletmelerinde arı hastalıklarının araştırılması. Uludağ Arıcılık Dergisi, 5, 27–31.
  43. T.C. Resmî Gazete. (2011, 21 Aralık). Bal arılarının Amerikan yavru çürüklüğü hastalığına karşı korunma ve mücadele yönetmeliği (Sayı: 28149). https://www.resmigazete.gov.tr/eskiler/2011/12/20111221-5. htm
  44. Tsourkas, P. K. (2020). Paenibacillus larvae bacteriophages: Obscure past, promising future. Microbial Genomics, 6(2), Article e000330. https://doi.org/10.1099/mgen.0.000330
  45. Tutkun, E. & Boşgelmez, A. (2003). Bal arısı zararlıları ve hastalıkları teşhis ve tedavi yöntemleri. Bizim Büro Basımevi.
  46. Türkiye İstatistik Kurumu. (2024). Hayvansal üretim istatistikleri, 2023. https://data.tuik.gov.tr
  47. Van Leuven, J., Miller, C., Peters, T., Spencer, E., Eline, Y., Paull, K. & Linzan, K. (2024). Bacteriophage resistance evolution in a honey bee pathogen. bioRxiv. https://doi.org/10.1101/2024.07.15.603584
  48. Woodrow, A. W. (1942). Susceptibility of honeybee larvae to individual inoculations with spores of Bacillus larvae. Journal of Economic Entomology, 35(6), 892–895. https://doi.org/10.1093/ jee/35.6.892
  49. World Organisation for Animal Health. (2023). American foulbrood of honey bees (infection of honey bees with Paenibacillus larvae). In Manual of diagnostic tests and vaccines for terrestrial animals 2023 (12th ed., Vol. 1, pp. 888–903). https://www.woah.org/fileadmin/Home/eng/Health_standards/tahm/3.02.02_AMERICAN_FOULBROOD.pdf
  50. Yost, D. G., Tsourkas, P. & Amy, P. S. (2016). Experimental bacteriophage treatment of honeybees (Apis mellifera) infected with Paenibacillus larvae, the causative agent of American foulbrood disease. Bacteriophage, 6(1), Article e1122698. https://doi.org/10.10 80/21597081.2015.1122698
  51. Zeybek, H. (1991). Arı hastalıkları ve zararlıları. Tarım ve Köyişleri Bakanlığı Hayvan Hastalıkları Araştırma Enstitüsü Müdürlüğü.
  52. Van Leuven, J., Miller, C., Peters, T., Spencer, E., Eline, Y., Paull, K. & Linzan, K. (2024). Bacteriophage resistance evolution in a honey bee pathogen. bioRxiv. https://doi.org/10.1101/2024.07.15.603584