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European foul brood

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European foul brood

Summary

  • Last modified
  • 08 March 2019
  • Datasheet Type(s)
  • Animal Disease
  • Preferred Scientific Name
  • European foul brood
  • Overview
  • This datasheet is about European foul brood (EFB) disease of honey bees as defined by the World Organisation for Animal Health, or OIE (

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Identity

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Preferred Scientific Name

  • European foul brood

International Common Names

  • English: EFB; European foulbrood; European foulbrood disease; European foulbrood of honey bees; Infection of honey bees with Melissococcus plutonius

Overview

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This datasheet is about European foul brood (EFB) disease of honey bees as defined by the World Organisation for Animal Health, or OIE (OIE, 2013b), i.e. a disease of the larval and pupal stages of honey bees caused by the bacterium Melissococcus plutonius (formerly Melissococcus pluton or Streptococcus pluton). It is found on all continents where Apis mellifera is kept, and also affects A. cerana; it causes significant damage to the beekeeping industry, and is on the list of diseases notifiable to the OIE.

Hosts/Species Affected

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European foul brood is a disease of honey bees (genus Apis) (OIE, 2013b) and has been reported from colonies of Apis cerana (Ansary et al., 2001; Rana et al., 2004) as well as A. mellifera (FAO, 2006).

Wardell (1982) reported that bee midgut pH may be a factor affecting disease incidence. Studies carried out in Michigan, USA, to investigate the high incidence of EFB in colonies taken to pollinate Vaccinium corymbosum found that midgut pH rose to 6.0-6.5 in larvae fed on blueberry pollen. This is the optimum pH for development of Streptococcus pluton [M. plutonius]; control was effective using a soyabean supplement with an acidifying agent. It was also found that blueberry pollen contained 10 times as much manganese as non-blueberry pollen, and contents of other minerals were also higher, although it is not known whether this is linked to EFB.

Distribution

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European foul brood disease is distributed worldwide (Forsgren et al., 2013) on all continents where Apis mellifera is kept; it also affects A. cerana (FAO, 2006). The Distribution table contains records only for those countries where records are readily available, so it should not be taken as an exhaustive list of where the disease is present.

Distribution Table

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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.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

AfghanistanNo information availableOIE, 2009
ArmeniaDisease not reportedOIE, 2009
AzerbaijanDisease not reportedOIE, 2009
BahrainDisease never reportedOIE, 2009
BangladeshNo information availableOIE, 2009
BhutanDisease not reportedOIE, 2009
CambodiaNo information availableOIE, 2009
ChinaNo information availableOIE, 2009
-Hong KongNo information availableOIE, 2009
IndiaPresentSingh and Garg, 2000; OIE, 2009; Rana et al., 2012First recorded in 1989 in Himachal Pradesh
IndonesiaDisease not reportedOIE, 2009
IranRestricted distributionOIE, 2009
IraqDisease never reportedOIE, 2009
IsraelPresentOIE, 2009
JapanPresentOIE, 2009; Okumura et al., 2012
JordanNo information availableOIE, 2009
KazakhstanDisease not reportedOIE, 2009
Korea, Republic ofNo information availableOIE, 2009
KuwaitDisease not reportedOIE, 2009
KyrgyzstanDisease not reportedOIE, 2009
LaosNo information availableOIE, 2009
LebanonPresentOIE, 2009
MalaysiaRestricted distributionOIE, 2009
MongoliaNo information availableOIE, 2009
MyanmarNo information availableOIE, 2009
NepalNo information availableOIE, 2009
OmanNo information availableOIE, 2009
PakistanNo information availableOIE, 2009
PhilippinesNo information availableOIE, 2009
QatarNo information availableOIE, 2009
Saudi ArabiaNo information availableOIE, 2009
SingaporeDisease never reportedOIE, 2009
Sri LankaDisease never reportedOIE, 2009
SyriaNo information availableOIE, 2009
TajikistanDisease not reportedOIE, 2009
ThailandPresentNeramitmansook et al., 2003; OIE, 2009
TurkeyPresentOIE, 2009; Yalçinkaya and Keskin, 2010
United Arab EmiratesDisease not reportedOIE, 2009
VietnamNo information availableOIE, 2009
YemenNo information availableOIE, 2009

Africa

AlgeriaPresentOIE, 2009
AngolaNo information availableOIE, 2009
BeninNo information availableOIE, 2009
BotswanaDisease never reportedOIE, 2009
Burkina FasoNo information availableOIE, 2009
ChadNo information availableOIE, 2009
CongoNo information availableOIE, 2009
DjiboutiDisease not reportedOIE, 2009
EgyptNo information availableOIE, 2009
EritreaNo information availableOIE, 2009
EthiopiaNo information availableOIE, 2009
GabonNo information availableOIE, 2009
GambiaNo information availableOIE, 2009
GhanaNo information availableOIE, 2009
GuineaNo information availableOIE, 2009
Guinea-BissauNo information availableOIE, 2009
KenyaNo information availableOIE, 2009
LesothoDisease never reportedOIE, 2009
MadagascarDisease never reportedOIE, 2009
MalawiPresentMwale, 1992; OIE, 2009
MaliNo information availableOIE, 2009
MauritiusDisease never reportedOIE, 2009
MoroccoNo information availableOIE, 2009
MozambiqueNo information availableOIE, 2009
NamibiaNo information availableOIE, 2009
NigeriaNo information availableOIE, 2009
RwandaNo information availableOIE, 2009
SenegalNo information availableOIE, 2009
South AfricaDisease never reportedOIE, 2009
SudanDisease never reportedOIE, 2009
SwazilandNo information availableOIE, 2009
TanzaniaNo information availableOIE, 2009
TogoNo information availableOIE, 2009
TunisiaDisease not reportedOIE, 2009
UgandaNo information availableOIE, 2009
ZambiaNo information availableOIE, 2009
ZimbabweNo information availableOIE, 2009

North America

BermudaPresentSchotman, 1989
CanadaPresentOIE, 2009
GreenlandDisease never reportedOIE, 2009
MexicoDisease not reportedOIE, 2009
USAPresentWardell, 1982; OIE, 2009

Central America and Caribbean

BelizeDisease not reportedOIE, 2009
Costa RicaPresentOIE, 2009; Calderón and Sánchez, 2011
CubaPresentOIE, 2009
Dominican RepublicDisease not reportedOIE, 2009
El SalvadorPresentOIE, 2009
GuadeloupeNo information availableOIE, 2009
GuatemalaDisease not reportedOIE, 2009
HaitiNo information availableOIE, 2009
HondurasNo information availableOIE, 2009
JamaicaDisease not reportedOIE, 2009
MartiniqueNo information availableOIE, 2009
NicaraguaNo information availableOIE, 2009
PanamaNo information availableOIE, 2009

South America

ArgentinaPresentSchotman, 1989; OIE, 2009
BoliviaPresentSchotman, 1989; OIE, 2009
BrazilPresentBailey, 1984; Schotman, 1989; OIE, 2009
ChilePresentSchotman, 1989; OIE, 2009
ColombiaPresentSchotman, 1989; OIE, 2009
EcuadorDisease never reportedOIE, 2009
French GuianaDisease not reportedOIE, 2009
ParaguayPresentSchotman, 1989
PeruPresentSchotman, 1989; OIE, 2009
UruguayPresentOIE, 2009; Invernizzi et al., 2011
VenezuelaPresentSchotman, 1989; OIE, 2009

Europe

AlbaniaNo information availableOIE, 2009
AustriaDisease not reportedOIE, 2009
BelarusPresentAl'bert et al., 2002; OIE, 2009
BelgiumDisease not reportedOIE, 2009
BulgariaDisease not reportedOIE, 2009
CroatiaDisease not reportedOIE, 2009
CyprusDisease not reportedOIE, 2009
Czech RepublicDisease not reportedOIE, 2009
DenmarkDisease not reportedOIE, 2009
EstoniaDisease not reportedOIE, 2009
FinlandDisease not reportedOIE, 2009
FranceNo information availableOIE, 2009
GermanyDisease not reportedOIE, 2009
GreeceDisease not reportedOIE, 2009
HungaryRestricted distributionOIE, 2009
IcelandDisease never reportedOIE, 2009
IrelandDisease not reportedOIE, 2009
ItalyPresentGreatti, 2005; OIE, 2009
LatviaDisease not reportedOIE, 2009
LiechtensteinDisease not reportedOIE, 2009
LithuaniaDisease not reportedOIE, 2009
LuxembourgDisease not reportedOIE, 2009
MacedoniaAbsent, reported but not confirmedOIE, 2009
MaltaAbsent, reported but not confirmedOIE, 2009
MontenegroDisease never reportedOIE, 2009
NetherlandsDisease not reportedOIE, 2009
NorwayDisease not reportedOIE, 2009
PolandDisease not reportedOIE, 2009
PortugalDisease not reportedOIE, 2009
RomaniaDisease not reportedOIE, 2009
Russian FederationPresentOIE, 2009
SerbiaNo information availableOIE, 2009
SlovakiaDisease not reportedOIE, 2009
SloveniaDisease not reportedOIE, 2009
SpainPresentFlores et al., 2000; OIE, 2009
SwedenPresentOIE, 2009
SwitzerlandPresentOIE, 2009; Fried, 2012
UKPresentOIE, 2009; Budge et al., 2010
UkraineDisease not reportedOIE, 2009

Oceania

AustraliaPresentSchotman, 1989; Witte, 2003; OIE, 2009
French PolynesiaNo information availableOIE, 2009
New CaledoniaPresentOIE, 2009
New ZealandDisease never reportedOIE, 2009

Diagnosis

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It is unreliable to identify the presence of European foul brood (EFB) by signs of the disease in the field (OIE, 2013a). The most usual and obvious sign of EFB is larval death shortly before they are due to be sealed in their cells, but the cause of this can vary and is not necessarily EFB. Most infected colonies display few visible signs and in any case these often quickly subside before the end of the active season.

Diagnosis of EFB can be carried out by microscopy of suitable cultures, tube agglutination tests on the isolated bacterium, polymerase chain reaction (PCR) and hemi-nested PCR. Hemi-nested PCR can be used to analyse larvae, adults and honey bee products (Djordjevic et al., 1998; McKee et al., 2003; OIE, 2013a).

Diagnosis of the disease is well-documented by the OIE Terrestrial Manual (OIE, 2013a), which should be consulted for techniques in the areas of microscopy, immunological and culture methods, and PCR.

Disease Course

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As documented by the OIE (2013a), larvae that are infected, but not removed from the colony by nursery bees, become flaccid and light yellow, turning brown, and at the same time they decay into a semi-liquid mass. This then dries out, and forms a dark brown scale that is easily removed from the cells. Bee larvae usually die of this disease 1-2 days before being sealed in their cells, or occasionally shortly afterwards, but always before pupal development. However, Rana et al. (2004) found that Apis cerana larvae died at the prepupal-pupal stage.

Infected larvae die because they have been deprived of food by competition from the bacteria in their guts (FERA, 2013). A study by Kanbar et al. (2004) found that M. plutonius isolated from wounds of honey bee pupae caused by Varroa destructor produced a toxic compound, tyramine, and concluded that this was the causative agent of the observed toxic symptoms in bee larvae.

Epidemiology

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The OIE (2013a) states that European foul brood is most prevalent when colonies are growing quickly. Bee larvae usually die of this disease 1-2 days before being sealed in their cells, or occasionally shortly afterwards, but always before pupal development. However, Rana et al. (2004) reported a destructive foul brood disease in Himachal Pradesh, India, which attacked native bees, Apis cerana, in March 2002-November 2003 and resulted in death of the brood at the prepupal-pupal stage (like Thai sacbrood virus/American foul brood/ectoparasitic mite infestation rather than European foul brood), but nevertheless was shown on isolation of the causative organism to be M. plutonius infection. Conventional treatment with oxytetracycline failed to control the disease in A. cerana colonies and so this disease was tentatively designated as ‘Cerana’ European foul brood.

Nurse bees often detect sick larvae and remove them from the colony, but if the larvae go undetected, some may survive and develop through to adulthood. Defecation by these surviving larvae serves to propagate the bacteria because their faeces are infected (OIE, 2013a). Voiding of their gut contents at the time of pupation also contaminates the comb (FERA, 2013).

As documented by the OIE (2013a), larvae that are infected, but not removed from the colony by nursery bees, become flaccid and are light yellow, turning brown, and at the same time they decay into a semi-liquid mass. This then dries out, and forms a dark brown scale that is easily removed from the cells. If brood are severely affected, they may give off a very stale or sour odour, sometimes acidic. Contamination of the honeycombs enables the disease to persist from year to year (OIE, 2013a, b).

The disease can be spread by natural movement of bees, but the main cause of spread is the movement of bees and equipment by beekeepers (FERA, 2013).

Studies have implicated Varroa destructor as playing a role in European foul brood infection (Kanbar et al., 2004). Bacteria isolated from wounds of honey bee pupae caused by V. destructor were found to be M. plutonius. The bacteria were grown to produce a toxic compound, tyramine. The authors stated that this indicated that tyramine is the causative agent of the observed toxic symptoms in bee larvae.

Impact

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Economic Impact

Honey bees are important to agriculture and horticulture as pollinators, and European foul brood is a very serious and infectious disease (FERA, 2013). The value of pollination is estimated to exceed the value of products from beehives many-fold (Delaplane and Mayer, 2000). Any disease that causes a significant decrease in honeybee population will have an adverse effect on the beekeeping industry and agricultural production.

Social Impact

The effect of European foul brood outbreaks on honeybee health will also have a significant impact on honey products and thus the livelihood of beekeepers.

Environmental Impact

Impact on habitats

Bee decline will have a significantly negative affect on pollination in habitats that rely on these insects for development. The value of pollination is estimated to exceed the value of products from beehives many-fold (Delaplane and Mayer, 2000; Cuthbertson and Brown, 2006).

Impact on biodiversity

A decline in native bees, such as A. mellifera, due to the spread of European foul brood, will have a negative effect on bee biodiversity; Cuthbertson and Brown, 2009).

Disease Treatment

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In the UK at least, weak colonies infected with M. plutonius or those with a high proportion of diseased brood are usually destroyed, but lightly diseased colonies may in certain circumstances be treated with an antibiotic (FERA, 2013).

The use of antibiotics has been studied to control M. plutonius. Brazilian beekeepers were advised to use streptomycin in syrup after studies showed that while Streptococcus plutonius [M. plutonius] was resistant to terramycin, it was sensitive to streptomycin at concentrations over 50 μg/ml and to amplacylin at 2.5 μg/ml (Machado and Lemos, 1974).

In vitro tests using six antibiotics (ciprofloxacin, chlortetracycline, penicillin, oxytetracycline, cloxasillin [cloxacillin?] and tetracycline) against M. plutonius were carried out by Bahman and Rana (2003). They found that oxytetracycline was the most effective in inhibiting the growth of the bacterium. When this antibiotic was added to concentrated sugar syrup and used to treat a diseased colony, suppression of EFB was observed after the 8th day of treatment. The treatment continued to be effective 6 months later.

Unfortunately the use of tetracyclines to control foul brood can lead to traces of the antibiotic in honey. Bonta et al. (2007) determined a method for detecting residues in honey, using reversed-phase high performance liquid chromatography (HPLC) with UV detection.

Other in vitro tests have looked at plant products, namely Ecophil-P and Green TM, for use against the causative agents of brood diseases, including M. plutonius. Gurgulova et al. (2008) reported that Ecophil-P had adequately-expressed antibacterial and antifungal activity against the microorganisms tested. The minimum inhibitory concentration (MIC) of Green TM against M. plutonius, Paenibacillus larvae and P. alvei was comparatively low. The authors concluded with the recommendation that the investigated plant products were suitable for use in beekeeping.

M. plutonius was one of several bee disease and mycoses studied by Al’bert et al. (2002) in Belarus. They found that Bacillus cereus 494, B. subtilis 30043 and B. circulans showed the best probiotic properties.

Studies by Manning (2001) suggested that pollens with a high lipid concentration, dominated by linoleic, linolenic, myristic and dodecanoic acids, play a significant role in inhibiting growth of M. plutonius (amongst other spore-forming bacteria).

Wardell (1982) found that among larvae fed on blueberry pollen, which raises the pH in the midgut to the optimal level for development of M. plutonius, control was effective using a soyabean supplement with an acidifying agent, or terramycin extender patties, or both.

Recent research suggests that the ‘Shook Swarm’ method, in which the colony is transferred to entirely new uncontaminated combs in one operation, is very effective at combating EFB (FERA, 2013).

Integrated Pest Management using a variety of methods as appropriate is recommended by FERA (2013).

Prevention and Control

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It is important that beekeepers are vigilant and learn to recognise the signs of foul brood, and are careful not to risk introduction of the disease to their apiaries (Tomkies et al., 2009; FERA, 2013).

Spread between colonies can be restricted by quarantine systems and disinfection of equipment (FERA, 2013). Movement of bees and equipment from infected apiaries may be prohibited, for example in the UK (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 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.

Gamma radiation is used in the beekeeping industry to sterilize hive equipment contaminated with the causative agent of American foul brood, Paenibacillus larvae. Although studies have shown that gamma radiation significantly reduced numbers of M. plutonius (Hornitzy, 1986), Hornitzy (1994) reported that combs exposed to up to 8 kGy of gamma radiation still contained viable M. plutonius and the dose required for decontamination has not yet been determined. Irradiation and treatment with sodium hypochlorite solution are both recommended for sterilization of equipment by the OIE Terrestrial Animal Health Code (OIE, 2013b).

Integrated Pest Management using a variety of methods as appropriate is recommended by FERA (2013).

(See also the 'Disease Treatment' section).

References

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Al'bert RS, Birman BYa, Beznos TV, Lysak VV, Baeva IA, 2002. Investigations into probiotic preparations used in prevention of purulent diseases and mycoses in bees. Veterinarnaya Nauka - Proizvodstvu, No.36:219-226

Ansary AB, Hossain M, Bari MN, 2001. Analysis of honey and incidence of diseases, pests and predators in the colony of honeybee, Apis cerana (F.). Bangladesh Journal of Entomology, 11(1/2):21-30

Bahman S, Rana BS, 2003. Control of the European foul brood disease in Apis mellifera L. colonies with antibiotics. Pest Management and Economic Zoology, 11(1):31-36

Bailey L, 1984. A strain of Melissococcus pluton cultivable on chemically defined media. FEMS Microbiology Letters, 25:139-141

Bailey L, Collins MD, 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

Bailey L, Collins MD, 1982. Taxonomic studies on Streptococcus pluton. Journal of Applied Bacteriology, 53:209-213

Belloy L, Imdorf A, Fries I, Forsgren E, Berthoud H, Kuhn R, Charrière JD, 2007. Spatial distribution of Melissococcus plutonius in adult honey bees collected from apiaries and colonies with and without symptoms of European foulbrood. Apidologie, 38(2):136-140. http://www.edpsciences.org/journal/index.cfm?edpsname=apido

Bonta V, Marghitas LA, Dezmirean D, Moise A, Bobis O, Maghear O, 2007. Optimization of HPLC method for quantifying tetracycline residue in honey. Bulletin of University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca. Animal Science and Biotechnologies, 63/64:186-190. http://www.usamvcluj.ro

Budge GE, Barrett B, Jones B, Pietravalle S, Marris G, Chantawannakul P, Thwaites R, Hall J, Cuthbertson AGS, Brown MA, 2010. The occurrence of Melissococcus plutonius in healthy colonies of Apis mellifera and the efficacy of European foulbrood control measures. Journal of Invertebrate Pathology, 105(2):164-170. http://www.sciencedirect.com/science?_ob=ArticleURL&_udi=B6WJV-50BJNX2-1&_user=10&_coverDate=10%2F31%2F2010&_rdoc=9&_fmt=high&_orig=browse&_origin=browse&_zone=rslt_list_item&_srch=doc-info(%23toc%236888%232010%23998949997%232316759%23FLA%23display%23Volume)&_cdi=6888&_sort=d&_docanchor=&_ct=18&_acct=C000050221&_version=1&_urlVersion=0&_userid=10&md5=91d936109212dd95909050ba15c116c6&searchtype=a

Calderón RA, Sánchez LA, 2011. Diagnosis of bee diseases in Africanized honey bees in Costa Rica: prevalence and distribution from September to November 2007. (Diagnóstico de enfermedades en colmenas de abejas africanizadas en Costa Rica: prevalencia y distribución de Setiembre a Noviembre del 2007.) Agronomía Costarricense, 35(2):49-60. http://www.mag.go.cr/rev_agr/index.html

Cuthbertson AGS, Brown MA, 2006. Vital Pollinators: honey bees in apple orchards. The Biologist, 53:78-81

Cuthbertson AGS, Brown MA, 2009. Issues affecting British honey bee biodiversity and the need for conservation of this important ecological component. International Journal of Environmental Science and Technology, 6(4):695-699. http://www.ceers.org/ijest

Delaplane KS, Mayer DF, 2000. Crop pollination by bees. Wallingford, UK: CABI Publishing, xv + 344 pp. http://www.cabi.org/CABeBooks/default.aspx?site=107&page=45&LoadModule=PDFHier&BookID=26

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El-Naga AMA, 1987. Diagnosis of European foulbrood (EFB) in Saudi Arabia. Arab Gulf Journal of Scientific Research, B (Agricultural and Biological Sciences), 5(1):47-53

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Flores JM, Ruiz JA, Puerta F, Gutiérrez I, 2000. Important diseases of bee brood. (Principales enfermedades de la cría de las abejas.) Mundo Ganadero, 11(127):70-72, 74-75

Forsgren E, Budge GE, Charrière JD, Hornitzky MAZ, 2013. Standard methods for European foulbrood research. Journal of Apicultural Research, 52(1):52.1.12. http://www.ibra.org.uk/articles/The-COLOSS-BEEBOOK-European-foulbrood

Fried B, 2012. Sanitation of European Foul Brood in Werdenberg district, Switzerland: a field experiment. SAT, Schweizer Archiv für Tierheilkunde, 154(8):349-351. http://www.sat-zeitschrift.ch

Glinski Z, 1972. Properties and antigenic structure of Streptococcus pluton. I. Morphological and cultural characteristics. (Badania nad wlasciwosciami i budowa antygenowa Streptococcus pluton. I. Wlasciwosci morfologiczne i hodowlane.) Medycyna Weterynaryjna, 28(7):399-405

Greatti M, 2005. The principal pathologies of honey bee brood. (Le principali patologie della covata delle api.) Notiziario ERSA, 18(2):45-48

Gurgulova K, Zhelyazkova I, Malinova K, Takova S, 2008. Investigation of Ecophil-P and Green TM biological activity against the causative agents of infectious brood diseases. In: Sbornik dokladi ot nauchnata konferentsiya: Traditsii i s'vremenhost v'v veterinarnata meditsina. Sofia, Bulgaria: Lesotekhnicheski Universitet, 306-316

Hornitzky M, 1986. The use of gamma radiation in the control of honey bee infections. Australasian Beekeeper, 88(3):55-58

Hornitzky MAZ, 1994. Commercial use of gamma radiation in the beekeeping industry. Bee World, 75(3):135-142

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Kanbar G, Engels W, Nicholson GJ, Hertle R, Winkelmann G, 2004. Tyramine functions as a toxin in honey bee larvae during Varroa-transmitted infection by Melissococcus pluton. FEMS Microbiology Letters, 234(1):149-154

Kardakov VP, 1974. Morphological, cultural and biochemical properties of micro-organisms in collective and state-farm apiaries in Odessa province. Zaraznye i nezaraznye zabolevaniya sel'skokhozyaistvennykh zhivotnykh na yuge Ukrainy, editor I. A. Izmailov and 5 others. Odessa, Ukrainian SSR: Odesskii Sel'skokhozyaistvennyi Institut., 28-33

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Manning R, 2001. Fatty acids in pollen: a review of their importance for honey bees. Bee World, 82(2):60-75

McKee BA, Djordjevic SP, Goodman RD, Hornitzky MA, 2003. The detection of Melissococcus pluton in honey bees (Apis mellifera) and their products using a hemi-nested PCR. Apidologie, 34(1):19-27

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Neramitmansook W, Worarach A, Vongpakorn M, Tohmee N, 2003. Bacterial disease of honey bees in Thailand. Journal of the Thai Veterinary Medical Association, 54(3):9-17

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OIE (World Organisation for Animal Health), 2013. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. Paris, France: World Organisation for Animal Health. http://www.oie.int/en/international-standard-setting/terrestrial-manual/access-online/

OIE (World Organisation for Animal Health), 2013. Terrestrial Animal Health Code, edition 22. Paris, France: Office International des Epizooties. http://www.oie.int/international-standard-setting/terrestrial-code/access-online/

OIE, 2009. World Animal Health Information Database - Version: 1.4. World Animal Health Information Database. Paris, France: World Organisation for Animal Health. http://www.oie.int

Okumura K, Arai R, Okura M, Kirikae T, Takamatsu D, Osaki M, Miyoshi-Akiyama T, 2012. Complete genome sequence of Melissococcus plutonius DAT561, a strain that shows an unusual growth profile and is representative of an endemic cluster in Japan. Journal of Bacteriology, 194(11):3014. http://jb.asm.org/content/194/11/3014.full

Rana BS, Rana R, Gulshan Kumar, Sharma HK, Gupta JK, Kiran Dayal, 2004. 'Cerana' European foulbrood causing havoc to the native bee, Apis cerana F., in Himachal Pradesh. Pest Management and Economic Zoology, 12(1):109-111

Rana BS, Rao KM, Chakravarty SK, Sapna Katna, 2012. Characterization of Melissococcus plutonius causing European foulbrood disease in Apis cerana F. Journal of Apicultural Research, 51(4):306-311. http://www.ibra.org.uk

Schotman CYL, 1989. Plant pests of quarantine importance to the Caribbean. RLAC-PROVEG, No. 21:80 pp

Singh R, Garg R, 2000. Streptococcus pluton White on Apis mellifera Linnaeus in Paonta valley of Himachal Pradesh. Insect Environment, 6(2):64

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Trüper HG, Clari L de', 1998. Taxonomic note: erratum and correction of further specific epithets formed as substantives (nouns) 'in apposition'. International Journal of Systematic Bacteriology, 48:615

Wardell G, 1982. European foulbrood: association with Michigan blueberry pollination, and control. USA: Michigan State University, East Lansing, vii + 84 pp

Witte K de, 2003. European foul brood disease of honey bees. Agnote - Northern Territory of Australia, No.K14:3 pp

Yalçinkaya A, Keskin N, 2010. The investigation of honey bee diseases after colony losses in Hatay and Adana provinces of Turkey. Mellifera, 10(20):24-31. http://www.tkv-dft.org

Organizations

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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

Contributors

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23/03/2012: Original text by:

Dr Claire Beverley, CABI, Nosworthy Way, Wallingford, Oxfordshire, OX10 8DE, UK.

Distribution Maps

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