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Scientific Opinion on the risk to plant health posed by Chrysanthemum stunt viroid for the EU territory, with identification and evaluation of risk reduction options

EFSA Journal 2012;10(12):3027[87 pp.]. doi:10.2903/j.efsa.2012.3027
  EFSA Panel on Plant Health (PLH) Panel Members Richard Baker, Claude Bragard, Thierry Candresse, Gianni Gilioli, Jean-Claude GrĂ©goire, 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. Acknowledgment The Panel wishes to thank the members of the Working Group, Thierry Candresse, Francesco Di Serio and Adrian Fox, for the preparatory work on this scientific opinion and EFSA staff, Giuseppe Stancanelli and Gabor Hollo, for the support provided to this scientific opinion. Contact
Type: Opinion of the Scientific Committee/Scientific Panel On request from: European Commission Question number: EFSA-Q-2011-01190 Adopted: 22 November 2012 Published: 14 December 2012 Affiliation: European Food Safety Authority (EFSA), Parma, Italy

The Panel on Plant Health conducted a pest risk assessment for Chrysanthemum stunt viroid (CSVd) and identified and evaluated risk reduction options, particularly those listed in Council Directive 2000/29/EC. Three entry pathways were identified, with plants for planting being the most important and rated as moderately likely. CSVd is recorded in some EU Member States with a limited distribution and is regulated on chrysanthemum; host plants are widely cultivated in greenhouses and outdoors. Therefore, establishment is very likely. Short-distance spread within a crop is likely, whereas short-distance spread between different species is unlikely to moderately likely. For vegetatively propagated species, in the absence of an efficient certification system, long-distance spread is very likely and a major impact would be expected on chrysanthemum, with associated yield and quality losses. However, under the existing certification scheme for chrysanthemum plant propagation material, the probability of spread through infected cuttings is largely reduced and the direct consequences of viroid outbreaks are expected to be minor. Minimal impact is predicted for other ornamental hosts and a minor impact for solanaceous vegetable crops. The indirect effects of CSVd are considered to be limited, with the exception of eradication. Risk reduction options addressing the sanitary status of the propagation material are likely to be the most effective and feasible. These include the current EU measures, as well as a statutory certification system with associated statutory import requirements or, failing that, but potentially less effective, the use of voluntary industry standards. It is difficult to disentangle the benefits of the current legislation from those of the industry-developed chrysanthemum certification system. The high efficacy of current measures is supported by the absence or limited presence of CSVd in the EU and by the limited number of interceptions and findings. Possible improvements to current measures are described and uncertainties discussed.

© European Food Safety Authority,2012


Following a request from the European Commission the Panel on Plant Health was asked to deliver a scientific opinion on the pest risk of Chrysanthemum stunt viroid (CSVd) for the European Union (EU) territory, identifying risk management options and evaluating 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 measures 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 according to the general principles of the “Guidance on a harmonised framework for pest risk assessment and the identification and evaluation of pest risk management options” (EFSA Panel on Plant Health (PLH), 2010) and the guidance on evaluation of risk reduction options (EFSA Panel on Plant Health (PLH), 2012). Given the fact that CSVd (as well as all other harmful organisms listed in Annex II, Part A, Section II of Directive 2000/29/EC) is already locally present in the EU territory and 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.

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

With regard to the assessment of the risk to plant health of Chrysanthemum stunt viroid for the EU territory:

Three pathways have been identified for the potential entry of CSVd in the pest risk assessment area. The first one, which implicates vegetative propagation material (plants for planting), is identified as the most relevant. The botanical seeds pathway and that of plant products not intended for planting are considered to be of minor significance. For the botanical seeds pathway, this assessment is based on the negligible volume of chrysanthemum seed imported into the EU and on the absence of data on seed transmission and/or association with seeds of other susceptible species. In the case of plants not intended for planting it is based mainly on the unlikely probability of transfer of the pathogen to a host. In both pathways, a high degree of uncertainty applies to the assessment owing to the lack of precise information on some key points. In contrast, in the plants for planting pathway, pathogen transfer to a host is immediate, with no uncertainty, whereas survival during transport and survival of management procedures are both assessed as likely or very likely, with low uncertainty. For this pathway, the probability of association at origin is assessed as moderately likely with medium uncertainty. Overall, the probability of entry through the plants for planting pathway is rated as moderately likely, with medium uncertainty, mostly because of limited data on the association of CSVd with the pathway at origin.

CSVd has previously been recorded in 16 Member States (MSs), and is currently recorded in nine. In many cases, data on distribution and findings of affected plants are limited. In many MSs host plants are cultivated, and in southern MSs they are commonly grown in open conditions. The environment is generally conductive to viroid establishment, and cultural practices and control measures are unlikely to limit establishment in a major way. These factors combined result in an evaluation of the probability of establishment as very likely, with a low level of uncertainty.

Within a crop over a short distance, several mechanisms, including vegetative propagation, mechanical transmission, seed and pollen transmission and possibly insect-assisted transmission may contribute to the spread of CSVd. Although there are uncertainties as to whether all mechanisms apply to all CSVd–host combinations, at least several of these mechanisms are likely to be effective in any situation so that, overall, the probability of spread is evaluated as likely, with low uncertainty. Between different species over a short distance, the two mechanisms potentially involved in spread of CSVd are mechanical transmission and possibly insect transmission. An unlikely to moderately likely rating is proposed for the probability of spread, based on information available for other viroids, but this rating is associated with a high uncertainty level given the absence of any precise information in the case of CSVd.

Within the same species over long distances, spread can occur through vegetative propagation and seed transmission. By contrast, the contribution of mechanical transmission and of insect-assisted transmission to long-distance spread is expected to be low, even on a limited local scale. In the absence of an efficient plant material certification system the probability of spread over long distances is therefore evaluated as very likely for vegetatively propagated species, with a low rating for uncertainty. In the presence of the existing chrysanthemum certification programme and for non-vegetatively propagated species, long-distance spread is evaluated as unlikely to moderately likely, with a medium level of uncertainty.

As CSVd may cause both yield and quality losses in chrysanthemum, a major impact can be predicted for this crop in the absence of a widely used and efficient certification programme. In contrast, in the most developed ornamental industries, which adopt established certification schemes for plant propagation material and include CSVd among the pathogens to be routinely controlled, the risk of CSVd spread through contaminated cuttings is largely reduced and, accordingly, the direct consequences of the viroid outbreaks are expected to be minor, with a medium degree of uncertainty. Direct pest effects are expected to be different for the other potential host species, with a minimal impact predicted for alternative ornamental hosts and a minor impact predicted for solanaceous vegetable crops. This assessment is accompanied by a high degree of uncertainty owing to the limited available information. Indirect pest effects of CSVd are considered limited, with the possible exception of the eradication burden that can be incurred in cases of outbreaks or discovery of CSVd in chrysanthemum.

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

Similar to other pospiviroids (EFSA Panel on Plant Health (PLH), 2011), CSVd has several biological characteristics that strongly influence its epidemiology, its impact and the effectiveness of the risk reduction options that can be deployed to reduce the associated risks of introduction, spread and impact. The key biological properties identified in this respect are:

  • CSVd is a systemic pathogen and, as such, it is very efficiently transmitted by all vegetative multiplication techniques, which explains the importance of the plants for planting pathway.
  • Similar to other viruses and viroids, there is no effective curative treatment that can be applied to CSVd-infected plants in a production context, so it is best controlled through prophylaxis.
  • CSVd transmission mechanisms not associated with propagation material (i.e., mechanical transmission and insect-assisted transmission) are relatively inefficient over long distances, even on a limited local scale. CSVd, like other pospiviroids, is therefore not expected to give rise to large-scale epidemics but rather to localised outbreaks associated with contaminated planting material.

For these reasons, the risk reduction options identified as the most effective and feasible are those addressing the sanitary status of the propagation material. These include the current measures themselves (see below), as well as the implementation of a statutory certification system with associated statutory import requirements or, failing that, but potentially less effective, the use of voluntary industry standards.

It is difficult to disentangle the benefits of the current legislation from those of the industry-developed current certification system for chrysanthemum. The certification could indeed be perceived as the way developed by the industry to comply with the requirements imposed by the current legislation but could equally be perceived as resulting from efforts by the industry to improve the quality of the commercialised planting materials. Whatever the precise mix between these two rationales (and any other possible ones), the current measures can be evaluated as having a high efficiency overall. This analysis is supported by the fact that seven MSs described the status of CSVd as “no more present” or “absent, pest eradicated”, only four MSs reported CSVd as “present recently” in chrysanthemum, and there were a limited number of interception reports for CSVd.

Several weaknesses or loopholes have been identified in the current measures during the present analysis. These concern: the methods used to implement the measures (complete reliance on phytosanitary passports as unreliable visual inspection is generally used to control imports); the fact that non-chrysanthemum hosts of CSVd are not addressed; and the wording of Annex IV of the Council Directive 2000/29/EC and the quality standards it proposes (three generations allowed from tested plants, entailing recontamination risks). The implementation of several risk reduction options could be considered in order to make the current measures more efficient by closing these loopholes. This would entail making the standards more stringent by allowing fewer multiplication cycles from tested plants, supplementing visual inspection with a measure of sampling and testing of imported cuttings and addressing the other CSVd hosts. Although such measures would clearly further improve the effectiveness of the current measures, the improvement thus achieved is expected to be limited because of the high efficiency of the current measures combined with the industry-developed certification system and because of the limited importance of the non-chrysanthemum hosts.

Three parameters are important in the analysis of non-chrysanthemum hosts:

  1. With the possible exception of Argyranthemum, they develop asymptomatic CSVd infection and therefore are predicted to show minimal impact.
  2. Taken together they represent imports of less than 10 % of the imported chrysanthemum plants for planting.
  3. Even assuming that the relatively inefficient transmission mechanisms could allow occasional spillover of CSVd from these hosts to chrysanthemum or to susceptible solanaceous crops, this would not be expected to result in widespread epidemics but rather to limited localised outbreaks. In cases in which spillover to chrysanthemum propagation material occurred, which would have more important consequences, it should be controlled by the current certification system.

The overall conclusion, therefore, is that the non-chrysanthemum hosts are likely to have a minor influence on the CSVd situation at large, so that extending the current measures to cover these hosts would not be expected to result in a sizeable improvement in chrysanthemum health status (or in that of other potential hosts). This evaluation is, however, associated with high uncertainties due to the lack of specific data on the frequency and efficiency of interspecies transmission in CSVd.

If the current regulation were to be removed, no major consequences or changes in the potential impact of CSVd would be expected. This is largely owing to the important level of protection achieved by the chrysanthemum industry through the efficient and widely used chrysanthemum certification scheme, which is viewed by the Panel as reducing the risks of entry, spread and impact in a very significant fashion.

If, on the other hand, the current legislation were removed and the industry simultaneously ceased its voluntary certification activity or excluded CSVd from the list of organisms addressed, a deterioration in the current situation, with an increase in the prevalence of CSVd in chrysanthemum crops, would be expected, with ensuing detrimental effects.

In such a scenario, adopting in a coordinated fashion a range of risk reduction options with partial individual effectiveness on spread and impact could be envisaged (visual inspection and/or testing of plants in nurseries, exclusion conditions/separation of host plant cultivation, eradication of infected plants, hygiene best practice, ongoing surveillance, sanitation of production premises …) in order to reduce the spread and impact of CSVd outbreaks resulting from the use of contaminated planting material. Although providing some level of risk reduction, such a solution is, however, perceived by the Panel as being simultaneously less effective and more constraining either than the current measures or than the use of an efficiently enforced certification system.


Chrysanthemum, CSVd, Chrysanthemum stunt viroid, pest risk assessment, risk reduction, European Union