Scientific Opinion on the risk to plant health posed by Burkholderia caryophylli for the EU territory with the identification and evaluation of risk reduction options


Panel on Plant Health
EFSA Journal
EFSA Journal 2013; 11(1):3071 [91 pp.].
Panel members at the time of adoption
Richard Baker, Claude Bragard, Thierry Candresse, Gianni Gilioli, Jean-Claude Grégoire, Imre Holb, Michael John Jeger, Olia Evtimova Karadjova, Christer Magnusson, David Makowski, Charles Manceau, Maria Navajas, Trond Rafoss, Vittorio Rossi, Jan Schans, Gritta Schrader, Gregor Urek, Johan Coert van Lenteren, Irene Vloutoglou, Stephan Winter and Wopke van der Werf

The Panel wishes to thank the Working Group on Annex IIAII and in particular the members of the Bacteria Subgroup: Charles Manceau, David Makowski, Johannes van Doorn, Emilio Stefani, Ian K. Toth and Jean M. van der Wolf for the preparatory work on this scientific opinion and the hearing experts: EFSA staff: Gabor Hollo, Giuseppe Stancanelli and Olaf Mosbach-Schultz for the support provided to this scientific opinion.

Opinion of the Scientific Committee/Scientific Panel
On request from
European Commission
Question Number
31. Dezember 2012
23. Juli 2013
European Food Safety Authority (EFSA), Parma, Italy
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The EFSA Panel on Plant Health conducted a pest risk assessment for Burkholderia caryophylli for the EU territory under the scenario of current EU legislation and identified and evaluated risk reduction options. B. caryophylli is absent from the EU territory. The host range of B. caryophylli includes the genus Dianthus and three other incidental, minor, hosts (statice, lisianthus and gypsophila). Seven entry pathways were identified, with carnation cuttings and cut flowers being the most frequently traded. All pathways were considered unlikely as the pathogen is rarely associated with the pathways at origin mostly because of the high phytosanitary quality of the plant propagation material. The establishment is unlikely because outdoors the environmental conditions are not favourable to the pathogen and alternative hosts are not present, whereas in protected crops the cultural practices are very effective to keep the crop free from this bacterium. Only very short-distance spread within a crop is likely, and spread between different crops is unlikely. Risk reduction options addressing the sanitary status of the propagation material have the best effectiveness and feasibility. Effective control measures are based on healthy propagation materials (cuttings) and hygiene practices. With the existing certification scheme of carnation plant propagation material, the probability of spread through infected cuttings is largely reduced. The high effectiveness of current measures is ensured by the absence of B. caryophylli in the EU, as in recent decades no findings of B. caryophylli have been reported.B. caryophylli is reported to be present in some third countries in Asia, where it still causes high crop losses. If the current regulation were to be removed, major consequences or changes in the potential impact of B. caryophylli are expected if no voluntary certification scheme were applied, together with good sanitation standards, along the crop production chain.


Following a request from European Commission, the Panel on Plant Health was asked to deliver a scientific opinion on the pest risk of Pseudomonas (Burkholderia)caryophylli (renamed Burkholderia caryophylli in 1993 (Yabuuchi et al.,1993), for the EU territory, to identify risk management options and to evaluate their effectiveness in reducing the risk to plant health posed by the organism. In particular, the Panel was asked to provide an opinion on the effectiveness of the present EU requirements against this organism, which are laid down in Council Directive 2000/29/EC, in reducing the risk of introduction of this pest into, and its spread within, the EU territory.

The Panel conducted the risk assessment following the general principles of the “Guidance on a harmonized framework for pest risk assessment and the identification and evaluation of pest risk management options” (EFSA Panel on Plant Health (PLH), 2010) and of the “Guidance on evaluation of risk reduction options” (EFSA Panel on Plant Health (PLH), 2012). Given the fact that B. caryophylli (as well as all other harmful organisms listed in Annex II/A/II of Directive 2000/29/EC) has been regulated in the EU for many years, the Panel conducted the risk assessment considering the scenario of the current EU plant health legislation.

B. caryophylli is a single taxonomic species that can be adequately distinguished from other entities of the same genus. B. caryophylli could present a risk to the risk assessment area, as it is absent and has potential for establishment and causing consequences in the risk assessment area.

After consideration of the evidence, the Panel reached the following conclusions:

With regard to the assessment of the risk to plant health of B. caryophylli for the EU territory:

Under the scenario of the implementation of current phytosanitary measures, the conclusions of the pest risk assessment are as follows:


The likelihood of entry is assessed as very low to low because:

  • Owing to the strict sanitation procedures to be followed during production and certification of plants for planting (special requirements listed in Annex IV of Directive 2000/29/EC; EPPO, 2002), the probability for the pathogen being associated with the pathway at origin is very low and therefore entry into the risk assessment area with plant propagation material is very unlikely to unlikely.
  • Entry through the pathway of imported cut flowers and potted plants (Dianthus and other host plants) is unlikely, because these plants and plant parts are not used for propagation purposes but are produced almost exclusively for sale to the final consumers. In addition, it is unlikely that B. caryophylli would survive the waste management process owing to its biological characteristics.
  • Entry through the sphagnum peat pathway is also very unlikely, because there is no evidence in the literature that the bacteria associated with this matrix are truly phytopathogenic to carnation or other crops and there is no evidence of sphagnum peat import from areas where B. caryophylli is reported in this material.

There is, in general, low uncertainty on the assessment of the probability of entry. The only exception is in the case of the sphagnum peat pathway, for which the uncertainty is medium because of the lack of pathogenicity studies on B. caryophylli isolates from sphagnum peat, the lack of information on the import of this commodity from countries where this pathogen has been found in sphagnum and, in general, the lack of specific studies.


The likelihood of establishment is assessed as low because:

  • In open fields, the environmental conditions are not favourable to the pathogen and alternative hosts are, in general, not present.
  • In protected crops, although the environmental conditions are more favourable to the pathogen, current cultural practices and general control measures are very effective to keep the crop free from possible establishment of the bacterium.

Uncertainty on the probability of establishment is rated as medium to low. Information is still missing on the actual situation of carnation cultivation in Japan, the country where the disease appears to be an important threat to carnation production. Also, there is no information on pathogenicity to carnation or other host plants of strains from sphagnum peat bogs identified as B. caryophylli.


Despite the possibility of latent infection of plants and/or cuttings, which is the recognised key pathway for the spread of this disease, the likelihood of spread is assessed as very low because:

  • Natural dispersal in the soil is very limited, as the pathogen may spread in carnation crops for cut flower production only over very short distances, from plant to plant, as a result of handling plants or from water splashes.
  • There are no reports of outbreaks or spread of this disease in the EU in recent decades.
  • Certification schemes and sanitation procedures are in place in the EU during the production of propagation material.
  • Plant passporting for EU-produced material and surveys in EU production sites are effective phytosanitary measures.

Uncertainty on the probability of spread is at this moment rated as medium. The role of wild Dianthus spp. or other weeds present in the pest risk analysis (PRA) area as a reservoir for the pathogen has not been investigated. Information is missing on the causes of frequent disease outbreaks in Japanese carnation cultivation areas. No data are available in the literature on the role of insects as potential vectors of the pathogen. Also, it is not known whether and to what extent unauthorised propagation of carnation varieties outside the circuit of registered nurseries, and therefore outside the certification and plant passport schemes, occurs.

Endangered areas

Wherever there are areas suited for carnation production as a protected crop, those areas can be considered endangered. Areas with outdoors carnation crops are not considered at risk, although there are uncertainties owing to the lack of recent surveys and data from Japan, where B. caryophylli still seems to cause problems.


In the EU, no crop losses and no additional costs due to B. caryophylli have been reported in the last 25 years; therefore, the impact under current phytosanitary measures is considered as minimal.

In the absence of specific phytosanitary measures, the impact is expected to be minor to moderate. In the absence of any control measure (no certification, no sanitation and poor hygiene in production sites), the impact expected would be major.

There are no indications of environmental consequences associated with B. caryophylli within its current area of distribution. The control of B. caryophylli has minimal impact on the surrounding environment, biodiversity of other (host) plants or soil.

The uncertainty of the consequences is low, as historically no outbreaks of this bacterial disease have been reported in Europe since 1987.

With regard to the risk reduction options, the Panel evaluated the phytosanitary measures formulated in Council Directive 2000/29/EC and identified additional risk reduction options where relevant.

The risk reduction options identified as associating the best effectiveness and feasibility are those addressing the sanitary status of the propagation material.
The Panel considers that the current EU phytosanitary measures for B. caryophylli in carnation plants for planting (Directive 2000/29/EC, Annex IV A and Annex II, Part A, sections I and II) can be evaluated as having an overall high effectiveness. This analysis is supported by the fact that the disease has not been reported within carnation crops in the EU for several decades. However, the uncertainty is medium, as it is difficult to separate the effect of current quarantine regulations from the effects of the certification schemes and related hygiene and cropping practices.

Several weaknesses or loopholes in the current measures were identified during the present analysis. These concern the quality standards (mother plants tested only once in two years, entailing recontamination risks); the fact that it is not clear which kind of mother plants should be analysed, nor at which stage of production or to what extent; the methods used to implement the measures (e.g., the reliance on unreliable visual inspection to control imports); and the fact that non-carnation hosts of B. caryophylli are not addressed. However, since the occurrence of this disease has been rarely reported in these other crops, which are commonly propagated by seed, the Panel considers that the extension of current measures to statice, lisianthus and gypsophila would not result in a significant reduction of risk.

The implementation of several risk reduction options could be envisaged in order to make the current measures more effective by closing these loopholes. This would entail tightening the EU requirements by supplementing visual inspection with a measure of sampling and testing of mother plants and imported cuttings originating from third countries where the disease occurs. These measures would further improve the effectiveness of the current regulation. The high effectiveness of the current measures and the cultivation of carnation under protected cropping systems with high sanitation standards already limit (but do not exclude) the contamination risk from other carnation crops.

B. caryophylli is reported to be present in third countries in Asia, where it still causes high crop losses. If the current EU phytosanitary requirements were to be removed and not replaced by a voluntary certification including absence of B. caryophylli, a return to a high prevalence of B. caryophylli in carnation crops is expected, with ensuing detrimental effects, particularly if plant propagation material is imported from the areas of current distribution of B. caryophylli in Asia.

In contrast, no major consequences or changes in the potential impact of B. caryophylli would be expected if the current EU phytosanitary requirements were to be removed but a voluntary certification scheme including additional testing for B. caryophylli were to be used (EPPO, 2002, and 2006), together with the current strict hygiene practices, in propagation sites (Accati and Garibaldi, 1974; Fletcher, 1984). Uncertainties on this assessment are, however, medium, owing to the lack of information on the extent of application of certification schemes for carnation plant propagation material outside the EU.

Pseudomonas caryophylli, Burkholderia caryophylli, carnation, slow wilt, pest risk assessment, risk reduction, European Union
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