American Foulbrood well known and still unknown
Yordan Hristov
Abstract: American Foulbrood is one of the most distributed and deadly diseases of honeybee colonies. Despite being known for centuries some aspects of the disease are still not well understood. In the present review the current knowledge about etiology, pathogenesis, prophylactics and control of American Foulbrood are systemized and generalized. Attention is also drawn to the resistance mechanisms of honeybees to the disease. The new scientific discoveries which are changing our understanding about this dangerous disease are also highlighted.
Keywords: American Foulbrood; Paenibacillus larvae; pathogenesis; prophylactics
Citation: Hristov, Y. (2024). American Foulbrood – well known and still unknown. Bulgarian Journal of Animal Husbandry, 61(1), 31-40. (Bg).
| References: (click to open/close) | Abouda, Z., Zerdani, I., Kalalou, I., Faid, M. & Ahami, M. T. (2011). The Antibacterial Activity of Moroccan Bee Bread and Bee-Pollen (Fresh and Dried) against Pathogenic Bacteria. Res. J. Microbiol., 6, 376–384.
Antúnez, K., Harriet, J., Gende, L. B., Maggi, M. D., Eguaras, M. J. & Zunino, P. (2008). Efficacy of natural propolis extract in the control of American foulbrood. Vet. Microbiol., 131(3–4), 324–331.
Ash, C., Farrow, J. A. E., Wallbanks, S. & Collins, M. D. (1991). Phylogenetic heterogeneity of the genus Bacillus revealed by comparative analysis of small subunit-ribosomal RNA sequences. Lett. Appl. Microbiol., 13, 202 –206.
Ash, C., Priest, F. G. & Collins, M. D. (1993). Molecular identification of rRNA group 3 bacilli (Ash, Farrow, Wallbanks and Collins) using a PCR probe test. Anton. Leeuw., 64, 253 – 260.
Bailey, L. & Ball, B. V. (1991). Honey bee pathology. Academic Press, New York, London.
Bastos, E. M. A. F., Simone, M., Jorge, D. M., Soares, A. E. E. & Spivak, M. (2008). In vitro study of the antimicrobial activity of Brazilian propolis against Paenibacillus larvae. J. Invertebr. Pathol., 97(3), 273–281.
Beims, H., Wittmann, J., Bunk, B., Spröer, C., Rohde, C., Günther, G., Rohde, M., von der Ohe, W. & Steinert, M. (2015). Paenibacillus larvae-Directed Bacteriophage HB10c2 and Its Application in American Foulbrood-Affected Honey Bee Larvae. Appl. Environ. Microbiol., 81(16), 5411-5419.
Beims, H., Bunk, B., Erler, S., Mohr, K. I., Spröer, C., Pradella, S., Günther, G., Rohde, M., von der Ohe, W. & Steinert, M. (2020). Discovery of Paenibacillus larvae ERIC V: Phenotypic and genomic comparison to ERIC I-IV reveal different inventories of virulence factors which correlate with epidemiological prevalences of American foulbrood. Int J Med Microbiol., 310(2), 151394.
Bíliková, K., Wu, G. & Šimúth, J. (2001). Isolation of a peptide fraction from honeybee royal jelly as a potential antifoulbrood factor. Apidologie, 32(3), 275–283.
Bíliková, K., Popova, M., Trusheva, B. & Bankova, V. (2013). New anti-Paenibacillus larvae substances purified from propolis. Apidologie, 44(3), 278–285.
Boonsai, P., Phuwapraisirisan, P. & Chanchao, C. (2014). Antibacterial activity of a cardanol from Thai Apis mellifera propolis. Int. J. Med. Sci., 11(4), 327–336.
Borba, R. S. & Spivak, M. (2017). Propolis envelope in Apis mellifera colonies supports honey bees against the pathogen, Paenibacillus larvae. Sci. Rep., 7, 11429.
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. J. Invertebr. Pathol., 150, 94–100.
Brødsgaard, C. J., Hansen, H. & Ritter, W. (2000). Progress of Paenibacillus larvae larvae infection in individually inoculated honey bee larvae reared single in vitro, in micro colonies, or in full-size colonies. J. Apic. Res., 39, 19–27.
Cerenius, L. & Soderhall, K. (2004). The prophenoloxidase-activating system in invertebrates. Immunol. Rev., 198, 116–126.
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., Titera, D., Tomkies, V. & Ritter, W. (2006a). Diagnosis of American foulbrood in honey bees: a synthesis and proposed analytical methods. Lett. Appl. Microbiol., 43, 583–590.
De Graaf, D. C., De Vos, P., Heyndrickx, M., Van Trappen, S., Peiren, N. & Jacobs, F. J. (2006b). Identification of Paenibacillus larvae to the subspecies level: An obstacle for AFB diagnosis. J. Invertebr. Pathol., 91, 115 – 123.
Dickel, F., Bos, N. M. P., Hughes, H., Martín-Hernández, R., Higes, M., Kleiser, A. & Freitak, D. (2022). The oral vaccination with Paenibacillus larvae bacterin can decrease susceptibility to American Foulbrood infection in honey bees—A safety and efficacy study. Front Vet Sci., 9, 946237.
Ebeling, J., Knispel, H., Hertlein, G., Fünfhaus, A. & Genersch, E. (2016). Biology of Paenibacillus larvae, a deadly pathogen of honey bee larvae. Appl. Microbiol. Biotechnol., 100, 7387–7395.
Evans, J. D. (2003). Diverse origins of tetracycline resistance in the honey bee bacterial pathogen Paenibacillus larvae. J. Invertebr. Pathol., 83, 46–50.
Evans, J. D., Aronstein, K., Chen, Y. P., Hetru, C., Imler, J. L., Jiang, H., Kanost, M., Thompson, G. J., Zou, Z. & Hultmark, D. (2006). Immune pathways and defense mechanisms in honey bees Apis mellifera. Insect Mol. Biol., 15, 645–656.
Forsgren, E., Olofsson, T. C., Vásquez, A. & Fries, I. (2010). Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie, 41, 99 –108.
Fries, I. & Camazine, S. (2001). Implications of horizontal and vertical pathogen transmission for honeybee epidemiology. Apidologie, 32, 199–214.
Fries, I. & Raina, S. (2003). American Foulbrood and African honey bees (Hymenoptera: Apidae). J. Econ. Entomol., 96, 1641-1646.
Fries, I., Lindstrom, A. & Korpela, S. (2006). Vertical transmission of American foulbrood (Paenibacillus larvae) in honey bees (Apis mellifera). Vet. Microbiol., 114, 269–274.
Garcia, M. C., Finola, M. S. & Marioli, J. M. (2013). Bioassay Directed Identification of Royal Jelly’s Active Compounds against the Growth of Bacteria Capable of Infecting Cutaneous Wounds. Adv. Microbiol., 3(2), 138-144.
Garcia-Gonzalez, E., Genersch, E. (2013). Peritrophic matrix degradation through P. larvae. Environ. Microbiol., 15, 2894-2901.
Genersch, E. (2008). Paenibacillus larvae and American Foulbrood – long since known and still surprising. J. Verbr. Lebensm., 3, 429–434.
Genersch, E. (2010). American Foulbrood in honeybees and its causative agent, Paenibacillus larvae. J. Invertebr. Pathol., 103, 10–19.
Genersch, E., Ashiralieva, A. & Fries, I. (2005). Strain- and genotype-specific differences in virulence of Paenibacillus larvae subsp. larvae, the causative agent of American foulbrood disease in honey bees. Appl. Environ. Microb., 71, 7551–7555.
Genersch, E., Forsgren, E., Pentikainen, J., Ashiralieva, A., Rauch, S., Kilwinski, J. & Fries, I. (2006). Reclassification of Paenibacillus larvae subsp. pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies differentiation. Int. J. Syst. Evol. Micr., 56, 501–511.
Ghorbani-Nezami, S., LeBlanc, L., Yost, D. G. & Amy, P. S. (2015). Phage therapy is effective in protecting Honeybee Larvae from American Foulbrood disease. J. Insect Sci., 15, 84.
Goodwin, R. M., Perry, J. H. & Ten-Houten, A. (1994). The effect of drifting honey bees on the spread of American foulbrood infections. J. Apic. Res., 33, 209–212.
Hansen, H. & Brødsgaard, C. J. (1999). American foulbrood: a review of its biology, diagnosis and control. Bee World, 80, 5–23.
Hernandez-Lopez, J., Schuehly, W., Crailsheim, K. & Riessberger-Galle, U. (2014). Trans-generational immune priming in honeybees. Proc. R. Soc. B, 281, 20140454.
Heyndrickx, M., Vandemeulebroecke, K., Hoste, B., Janssen, P., Kersters, K., de Vos, P. Logan, N., Ali, N. & Berkeley, R. (1996). Reclassification of Paenibacillus (formerly Bacillus) pulvifaciens (Nakamura 1984) Ash et al. 1994, a later 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. Int. J. Syst. Bacteriol., 46, 270 – 279.
Hoffmann, J. A. & Reichhart, J. M. (2006). Drosophila innate immunity: an evolutionary perspective. Nat. Immunol., 3, 121–126.
Hornitzky, M. A. Z. (1998). The spread of Paenibacillus larvae subsp. Larvae infections in an apiary. J. Apic. Res., 37, 261–265.
Hornitzky, M. A. Z. & White, B. (2001). Controlling American foulbrood : assessing effectiveness of shaking bees and antibiotic therapy strategies: a report for the Rural Industries Research and Development Corporation. RIRDC publication No. 01/048.
Katznelson, H. (1950). Bacillus pulvifaciens (n. Sp.), an organism associated with powdery scale of honeybee larvae. J. Bacteriol., 59, 153–155.
Lamei, S., Stephan, J. G., Riesbeck, K., Vasquez, A., Olofsson, T., Nilson, B., de Miranda, J. R. & Forsgren, E. (2019). The secretome of honeybee-specific lactic acid bacteria inhibits Paenibacillus larvae growth. J. Apic. Res., 58, 405– 412.
Lavine, M. & Strand, M. (2002). Insect hemocytes and their role in immunity. Insect Biochem. Mol., 32, 1295–1309.
Le Blanc, L., Nezami, S., Yost, D., Tsourkas, P. & Amy, P. S. (2015). Isolation and characterization of a novel phage lysin active against Paenibacillus larvae, a honeybee pathogen. Bacteriophage, 5(4), e1080787.
Lindstrom, A., Korpela, S. & Fries, I. (2008). Horizontal transmission of Paenibacillus larvae spores between honey bee (Apis mellifera) colonies through robbing. Apidologie, 39, 1–8.
Lodesani, M., Costa, M. (2005). Limits of chemotherapy in beekeeping: development of resistance and the problem of residues. Bee World, 86, 102–109.
Mandal M. D. & Mandal, S. (2011). Honey: Its medicinal property and antibacterial activity. Asian Pacific Journal of Tropical Biomedecine, 1, 154–160.
Miyagi, T., Peng, C. Y. S., Chuang, R. Y., Mussen, E. C., Spivak, M. S. & Doi, R. H. (2000). Verification of oxytetracycline-resistant American foulbrood pathogen Paenibacillus larvae in the United States. J. Invertebr. Pathol., 75, 95–96.
Molan, P.C. (1992). The antibacterial activity of honey: 1. The nature of the antibacterial activity. Bee World, 73, 5–28.
Morais, M., Moreira, L., Feás, X. & Estevinho, L. M. (2011). Honeybee-collected pollen from five Portuguese Natural Parks: Palynological origin, phenolic content, antioxidant properties and antimicrobial activity. Food Chem. Toxicol., 49, 1096–1101.
Mussen, E. C. (2000). Antibiotic-resistant American foulbrood. Am. Bee J., 140, 300–301.
OIE (2023). OIE-Listed diseases, infections and infestations in force in 2023 (Chapter Bee diseases, infections and infestations). OIE; Paris, France.
OIE (2023). Chapter 3.2.2. American foulbrood of honey bees (infection of honey bees with Paenibacillus larvae). In OIE Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, 2023. OIE; Paris, France.
Oliveira, A., Leite, M., Kluskens, L. D., Santos, S. B., Melo, L. D. R. & Azeredo, J. (2015). The first Paenibacillus larvae bacteriophage endolysin (PlyPl23) with high potential to control American Foulbrood. PLoS One, 10, e0132095.
Palacio, M. A., Figini, E. E., Ruffinengo, S. R., Rodriguez, E. M., Hoyo, M. L. & Bedascarrasbure, E. L. (2000). Changes in a population of Apis mellifera L. selected for hygienic behaviour and its relation to brood disease tolerance. Apidologie, 31, 471–478.
Pettis, J. S. & Feldlaufer, M. F. (2005). Efficacy of lincomycin and tylosin in controlling American foulbrood in honey bee colonies. J. Apic. Res., 44, 106–108.
Piccini, C. & Zunino, P. (2001). American foulbrood in Uruguay: isolation of Paenibacillus larvae larvae from larvae with clinical symptoms and adult honeybees and susceptibility to oxytretracycline. J. Invertebr. Pathol., 78, 176–177.
Rauch, S., Ashiralieva, A., Hedtke, K. & Genersch, E. (2009). Negative correlation between individual-insect-level virulence and colony-level virulence of Paenibacillus larvae, the etiological agent of American foulbrood of honeybees. Appl. Environ. Microb., 75, 3344–3347.
Reybroeck, W., Daeseleire, E., De Brabander, H. F. & Herman, L. (2012). Antimicrobials in beekeeping. Vet. Microbiol., 158, 1–11.
Rusenova, N., Parvanov, P. & Stanilova, S. (2013). Molecular typing of Paenibacillus larvae strains isolated from Bulgarian apiaries based on repetitive element polymerase chain reaction (Rep-PCR). Curr. Microbiol., 66, 573-577.
Sadd, B. M. & Schmid-Hempel, P. (2006). Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr. Biol., 16, 1206–1210.
Salmela, H., Amdam, G. V. & Freitak, D. (2015). Transfer of immunity from mother to offspring is mediated via egg-yolk protein vitellogenin. PLoS Pathog, 11(7), e1005015.
Schmid, M. R., Brockmann, A., Pirk, C. W. W., Stanley, D. W. & Tautz, J. (2008). Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase-based immunity. J. Insect Physiol., 54, 439–444.
Shimanuki, H. (1997). Bacteria. In: Honey Bee Pests, Predators, and Diseases (Morse R. A., Flottum K., eds). A.I. Root Company, Medina, Ohio, USA, 35-54.
Spivak, M. & Gilliam, M. (1998a). Hygienic behaviour of honey bees and its application for control of brood diseases and varroa. Part I. Hygienic behaviour and resistance to American foulbrood. Bee World, 79, 124–134.
Spivak, M. & Gilliam, M. (1998b). Hygienic behaviour of honey bees and its application for control of brood diseases and varroa. Part II. Studies on hygienic behaviour since the Rothenbuhler era. Bee World, 79, 169–186.
Spivak, M. S. & Reuter, G. S. (2001). Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behaviour. Apidologie, 32, 555–565.
Stephan, J. G., Lamei, S., Pettis, J. S., Riesbeck, K., de Miranda, J. R. & Forsgren, E. (2019). Honeybee-specific lactic acid bacterium supplements have no effect on American foulbrood-infected honeybee colonies. Appl. Environ. Microb., 85(13), e00606-19.
Sturtevant, A. P. & Revell, I. L. (1953). Reduction of Bacillus larvae spores in liquid food of honey bees by action of the honey stopper, and its relation to the development of American foulbrood. J. Econ. Entomol., 46, 855-860.
Turcatto, A. P., Lourenco, A. P. & De Jong, D. (2018). Propolis consumption ramps up the immune response in honey bees infected with bacteria. Apidologie, 49(3), 287-296.
White, G. F. (1906). The bacteria of the apiary with special reference to bee disease. USDA, Bureau of Entomology, Technical Series. 14, 1–50.
Waite, R., Brown, M., Thompson, H. & Bew, M. (2003). Control of American foulbrood by eradication of infected colonies. Apiacta, 38, 134-136.
Wilson-Rich, N., Dres, S. T. & Starks, P. T. (2008). The ontogeny of immunity: development of innate immune strength in the honey bee (Apis mellifera). J. Insect Physiol., 54, 1392–1399.
Wilson, M. B., Brinkman, D., Spivak, M., Gardner, G., Cohen, J. D. (2015). Regional variation in composition and antimicrobial activity of US propolis against Paenibacillus larvae and Ascosphaera apis. J. Invertebr. Pathol., 124, 44–50.
Woodrow, A. W. & States, H. J. (1943). Removal of diseased brood in colonies infected with AFB. Am. Bee J., 81, 22-26.
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, e1122698.
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). Environ. Microbiol., 10, 1612–1620.
USDA Licenses Honeybee Vaccine to Dalan Animal Health. (2023). Highlights/Fed Lab News https://federallabs.org/flc-highlights/federal-lab-news/usda-licenses-honeybee-vaccine-to-dalan-animal-health.
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| Date published: 2024-02-26
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