American foul brood
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IdentityTop of page
Preferred Scientific Name
- American foul brood
International Common Names
- English: AFB; American foulbrood; American foulbrood of honey bees; Infection of honey bees with Paenibacillus larvae
OverviewTop of page
This datasheet is about American foul brood of honeybees as defined by the OIE (OIE, 2013a), i.e. a disease of the larval and pupal stages of honey bee, Apis mellifera and other Apis spp., which occurs in most countries where such bees are kept. It is on the list of diseases notifiable to the OIE.
The causative organism is a bacterium, Paenibacillus larvae, which can produce over 1 billion spores per infected larva. The spores are very long-lived and resistant to heat and chemical agents. Only the spores are capable of inducing the disease (OIE, 2013a).
Paenibacillus is a genus of Gram-positive, facultative anaerobic, endospore-forming bacteria. Members of this genus were originally included in Bacillus, until reclassification separated them into a distinct genus in 1993 (Ash et al., 1993). Previously, American foul brood and powdery scale disease were considered distinct (Graaf et al., 2006), but this is no longer valid and the pathogenic agents, Paenibacillus larvae subsp. larvae and Paenibacillus larvae subsp. pulvifaciens, were reclassified as one species, Paenibacillus larvae (Genersch et al., 2006), although the subspecies are still referred to in the literature.
American foul brood is a serious disease of honey bees worldwide and causes considerable economic losses (Basualdo et al., 2008). It has caused a significant decrease in honey bee populations, beekeeping industries and agricultural production (Antúnez et al., 2010). Honey bees are important to the agricultural and horticultural sectors as pollinators, so any disease causing decline in bee populations will have a significant impact on their role in these industries. Once this disease becomes established in a region it is very difficult to eradicate (Matheson and Reid, 1992).
Host AnimalsTop of page
Hosts/Species AffectedTop of page
American foul brood of honeybees is a disease of the larval and pupal stages of honey bees, Apis mellifera and other Apis spp., and occurs in most countries where such bees are kept (OIE, 2013a).
Robber bees may enter a hive that has become weakened by American foul brood infection and take contaminated honey back to their hives, so assisting disease spread to other colonies and apiaries (Lindström et al., 2008).
DistributionTop of page
American foul brood has a worldwide distribution (D’Alessandro et al., 2007) and cases have been reported in almost all the beekeeping regions of the five continents (Antúnez et al., 2004). It appears to be uncommon or even absent in significant parts of sub-Saharan Africa (Fries and Raina, 2003), but has been reported from some countries there (Hansen et al., 2003).
Studies have shown geographical clustering of different genotypes; for example Peters et al. (2006) reported non-random distribution of five different genotypes in the district of Arnsberg, Germany.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.Last updated: 10 Jan 2020
DiagnosisTop of page
The most obvious clinical symptom of American foul brood is the creamy or dark brown, glue-like larval remains of infected larvae. This is not conclusive, and in addition, diseased cells can easily be overlooked during the early stages of infection (Graaf et al., 2006). At an intermediate stage of larval decay, the remains can be drawn out into a brown mucus-like thread 10-30 mm long; this is stated by FERA (2013) to be a reliable test for the presence of American foul brood.
Bzdil (2007) described a method for detecting spores of P. larvae in the debris and wax of honey bees using the homogenization agent Tween 80. Material suspected of containing spores is homogenized at 70±2 °C with distilled water and Tween 80. When compared to the method of dissolving wax samples in toluene or benzene and releasing them in a liquid medium, the Tween method was found to be more effective at detecting P. larvae spores.
However, although several sensitive and selective culture media are available for the isolation of this bacterium (Graaf et al., 2006) and clinical symptoms caused by this disease can be diagnosed using colony inspections, such as the method described by Bzdil (2007), Gillard et al. (2008) describe these as time-consuming.
Studies to investigate alternative methods of diagnosis concluded that analysis of honey samples and bees collected at the entrance of the hive are of limited value for diagnosis, because only 86 and 83%, respectively, of samples from colonies showing symptoms of infection were positive (Gillard et al., 2008). Gillard et al. (2008) recommended testing bee samples from the brood nest, edge frame or honey chamber for P. larvae spores.
Other studies have concentrated on decreasing diagnosis time by using real-time PCR diagnostics (e.g. Chagas et al., 2010; Martínez et al., 2010). Chagas et al. (2010) studied the detection of P. larvae using real-time PCR, with the aim of decreasing diagnosis time and ensuring that robustness was not lost, as with conventional PCR methods. They concluded that analysis by real-time PCR of the 16S rDNA gene of Paenibacillus represents an alternative, rapid diagnostic tool for the disease.
In addition to the development of PCR methods for identification and genotyping of P. larvae, other methods available for identification are biochemical profiling, bacteriophage sensitivity, immunological techniques and microscopy of suspect bacterial strains (Graaf et al., 2006).
OIE (2013a) provides an outline of the different diagnostic techniques.
Disease CourseTop of page
Goodwin et al. (1993) stated that there are three possible states of infection: contamination, where P. larvae is present in the hive, but causes no ill effects; subclinical infection, where it adversely affects at least the larvae, although no disease is apparent to observers; and clinical infection, where it adversely affect the larvae and visible signs of American foul brood are present.
Once a larva has become infected via contaminated food, the spores germinate in the larval gut and the vegetative bacteria move into the gut tissues where they multiply enormously in number. Infected larvae normally die after their cells are sealed, and millions of infective spores are formed in their remains. The dried remains of the larvae adhere to the cell walls and cannot easily be removed by bees, meaning that the comb remains contaminated (FERA, 2013).
EpidemiologyTop of page
P. larvae spores contaminate brood food. The spores are then ingested by larvae up to 3 days old and germinate in the gut of the larva. Spores do not germinate in larvae that are older than 3 days; larvae less than 24 hours old are the most susceptible to infection. The vegetative form of the bacterium develops and gains nourishment from the larva. Eventually the larva dies as a result of the growth of the bacteria and the vegetative form of the bacterium also dies, but before doing so it produces millions of spores. One hundred million spores may be contained in one dead larva (Pennsylvania Department of Agriculture, undated).
Adult bees spread American foul brood (AFB) throughout hives as they attempt to remove the dead larvae that contain spores, and thus contaminate brood food. The brood chamber fills with contaminated honey, because spores are contained in the nectar of contaminated cells. As the honey is moved up into the supers of the hive, the entire hive will be contaminated with spores (Pennsylvania Department of Agriculture, undated).
Robber bees prey on weakened hives and colonies are weakened by AFB infection. These bees may take contaminated honey back to their hives and so spread the disease to other colonies and apiaries. Beekeepers may also unwittingly spread the disease on equipment (Pennsylvania Department of Agriculture, undated). Recent studies have also shown that small hive beetles, Aethina tumida, are vectors of P. larvae (Schäfer et al., 2010).
The spores of P. larvae are very resistant to desiccation and can remain viable for more than 40 years in honey and on equipment. Beekeepers are therefore advised to avoid honey for feeding bees, if the source is unknown, and that used beekeeping equipment should be assumed to be contaminated unless known not to be (Pennsylvania Department of Agriculture, undated).
ImpactTop of page
American foul brood is a serious disease of honey bees worldwide and causes considerable economic losses (Basualdo et al., 2008). This disease has caused a significant decrease in honeybee populations, beekeeping industries and agricultural production (Antúnez et al., 2010). Honey bees are important to the agricultural and horticultural sectors as pollinators (the value of pollination is estimated to exceed the value of products from beehives many-fold -- Delaplane and Mayer, 2000), so any disease causing decline in bee populations will have a significant impact on their role in these industries.
The effect of American foul brood outbreaks on honeybee health will also have a significant impact on honey products and thus the livelihood of beekeepers.
Impact on habitats
A decline in bee numbers has been attributed to American foul brood, amongst other bee diseases. Bee decline will have a significantly negative affect on pollination within habitats that rely on these insects for development (Delaplane and Mayer, 2000).
Impact on biodiversity
A decline in native bees due to the spread of American foul brood will have a negative effect on bee biodiversity (Cuthbertson and Brown, 2009).
Disease TreatmentTop of page
Antibiotics are used to treat American foul brood (AFB) in a number of countries, but in the UK (at least) it is compulsory to destroy infected colonies – the use of antibiotics is prohibited on the grounds that they are ineffective and merely suppress signs of the disease without eradicating it (FERA, 2013).
The development of resistance to commonly used antibiotics such as oxytetracycline, and the presence of residues in honey, have triggered the need for alternative control agents.
Kloucek et al. (2008) have studied the antibacterial activity of the tree Paulownia tomentosa and tested 8 geranylflavanoids against P. larvae. They reported high antibacterial activity against the vegetative stages of P. larvae subsp. larvae strains.
Propolis is a derivative from plant resins collected by Apis mellifera and is antimicrobial. Several studies have investigated the use of propolis to treat hives infected with P. larvae (e.g. Bastos et al., 2008; Antúnez et al., 2008). Bastos et al. (2008) carried out tests in Brazil and Minnesota, USA, using propolis from various Brazilian states. Antúnez et al. (2008) evaluated the efficacy of a propolis ethanolic extract (PEE) against P. larvae, in vitro and in vivo, and as a therapeutic tool for the control of AFB. Toxicity against honeybees was also evaluated. They concluded that PEE appears to be a novel, natural and harmless alternative for the treatment of AFB-affected hives.
Following development of oxytetracycline-resistant P. larvae-strains, subsequent studies have looked at alternative antibiotics and essential oils (e.g. Elzen et al., 2002; Chirila et al., 2011; Maggi et al., 2011; Roussenova, 2011). Elzen et al. (2002) reported that tylosin, an antibiotic, is effective in controlling oxytetracycline-resistant P. larvae in honey bee colonies, with no effect on adult and larval bee mortality.
Later research by Chirila et al. (2011) found a mixed response to various antibiotics and essential oils against samples of P. larvae subsp. larvae from 4 counties in Transylvania, Romania. Bacterial isolates were sensitive to penicillin, erythromycin, oxytetracycline, lincomycin, and enrofloxacin. Thyme, pine and mint oil were most active against vegetative forms of P. larvae.
Evidence of inhibition of P. larvae by omega 3 polyunsaturated fatty acids has been documented (Rumanovská et al., 2011).
Preliminary studies have investigated the possibility of using ozone as a fumigant against honey bee diseases including AFB. Ozone is a powerful oxidant, capable of killing insects and microorganisms (as well as eliminating odours, taste and colour). Treatment with ozone served to sterilize P. larvae, but only when certain concentrations and exposure times were used in conjunction with temperatures of 50 C and ≥75% relative humidity (James, 2011). James (2011) concluded that further evaluation of ozone was required, tailored to acceptability and efficacy in the field.
Cherif et al. (2008) reported the discovery of entomocin 110, a bacteriocin from Bacillus thuringiensis subsp. entomocidus HD 110. It was found to be inhibitory against several Gram-positive bacteria, including P. larvae. Entomocin 110 is proteinaceous in nature, and with a bactericidal and bacteriolytic mode of action.
Bacteria antagonistic to P. larvae have been discovered in honeybees (Sabaté et al., 2009; Yoshiyama and Kimura, 2009) and honey samples (Alippi and Reynaldi, 2006; Sabaté et al., 2009). Both Gram-positive and Gram-negative bacteria were found in the digestive tract of Japanese honeybees, Apis cerana japonica, using histological and 16S rRNA gene sequence analyses (Yoshiyama and Kimura, 2009). Bacterial populations in the gut were found to be diverse and in vitro assays were used to determine inhibition of isolates against P. larvae. Out of 35 isolates tested, 7 showed potential as biocontrol agents against P. larvae, and most of these were Bacillus spp..
Bacillus subtilis was isolated from honeybee guts and honey samples, and shown to inhibit P. larvae. In particular, it was shown that surfactin inhibited P. larvae, which were immediately affected upon contact. It was concluded that apiculture may benefit from the co-productive activities of Bacillus strains in producing surfactin and a fungicide, to biologically control P. larvae (Sabaté et al., 2009).
There are other bacteria which are antagonistic to P. larvae: aerobic spore-forming Bacillus megaterium, Bacillus licheniformis and several isolates of Bacillus cereus (Alippi and Reynaldi, 2006).
Munawar et al. (2010) investigated the shook swarm method for control of AFB. This involved reducing spore numbers in the mouths of the bees by starving them and shifting them to new, clean hives with new foundation sheets. The results demonstrated that swarms decreased their spore load significantly.
Prevention and ControlTop of page
Beekeepers need to take care not to introduce the disease to their colonies, and to ensure that any new cases are recognised and promptly quarantined and dealt with before it can spread to other colonies. In the UK (at least), infected colonies must be destroyed by burning (FERA, 2013).
The OIE Terrestrial Animal Health Code (OIE, 2013b) regulates the movement of bees, equipment and bee products from countries or zones where the disease is or may be present -- adult bees must come from apiaries meeting certain conditions including an absence of local outbreaks, eggs, larvae and pupae must be inspected by a method in the OIE Terrestrial Manual (OIE, 2013a), equipment must be sterilised, and products must be sterilised or inspected.
In addition to the application of chemical control to the bees themselves, beekeepers can also safeguard against the spread of AFB, by disinfecting equipment, which can harbour infection and exacerbate the problem. Hives and appliances can be sterilised by scorching them with a blowlamp and clothing can be washed thoroughly in washing soda or hot soapy water (FERA, 2013). Studies showed that Huwa-san® TR 50 has sporocidal properties and can be used to disinfect metal, wood and wax combs (Gurgulova et al., 2007),
Bee hygienic behaviour refers to cell uncapping and the removal of diseased or parasitized larvae. Bee resistance to brood infectious diseases such as AFB can be increased by selecting for hygienic bees. Invernizzi and Rodríguez (2007) reported that colony hygienic behaviour increased from 77.7±20.9 to 98±1.7% after 6 generations, alongside a decrease in brood diseases from 50 to 0%. Less hygienic behaviour was observed in the diseased colonies than in the healthy ones.
Later, a study by Basualdo et al. (2008) aimed to determine the spread of AFB in a commercial apiary where queens had been selected for hygienic behaviour. Hives that were found to be positive for AFB were isolated from the rest of the apiary and the queens of the remaining hives were replaced with queens selected for hygienic behaviour. AFB prevalence was then monitored, visually and through spore isolation from honey and bee samples. It was concluded that sampling of the bees, compared to the honey, was a better option for early diagnosis of AFB as it was more sensitive. The researchers stated that the disease could be controlled sufficiently using bee sampling and hygienic bee lines.
(See also the ‘Disease Treatment’ section).
ReferencesTop of page
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OrganizationsTop of page
World: IBRA, International Bee Research Association, Unit 6, Centre Court, Main Avenue, Treforest, RCT, CF37 5YR, UK, www.ibra.org.uk
World: OIE (World Organisation for Animal Health), 12, rue de Prony, 75017 Paris, France, http://www.oie.int/
UK: British Beekeepers’ Association, National Beekeeping Centre, Stoneleigh Park, Stoneleigh, Warwickshire, CV8 2LG, UK, www.britishbeekeepers.com
ContributorsTop of page
23/03/2012: Original text by:
Dr Claire Beverley, CABI, Nosworthy Way, Wallingford, Oxfordshire, OX10 8DE, UK.
Distribution MapsTop of page
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