Datum 17 augustus 2009
Vrijwaringen ggo's
Geachte Voorzitter,
In het Algemeen Overleg biotechnologie van 18 juni jl. heb ik naar aanleiding van
een verzoek van het lid Waalkens toegezegd om de Kamer te informeren als er
sprake is van nieuwe vrijwaringsaanvragen in de komende 12 maanden. Ook alle
openbare informatie rond vrijwaringen wordt aan de Kamer aangeboden.
De EU-regelgeving voor markttoelating van ggo's geeft lidstaten de mogelijkheid
om het gebruik en/of de verkoop van in de Europese Unie (EU) toegelaten ggo's
tijdelijk op hun grondgebied te beperken of te verbieden. Deze mogelijkheid wordt
aangeduid met de term "vrijwaring". Lidstaten kunnen vrijwaringen instellen als
nieuwe gegevens die wijzen op gevaren voor mens, dier of milieu daartoe
aanleiding geven. Conform de Europese regelgeving dient vervolgens de Europese
Commissie (EC) te beoordelen of de genomen vrijwaringen gerechtvaardigd zijn.
De EC vraagt daarbij aan de Europese Voedselveiligheid Autoriteit (EFSA) om te
beoordelen of de nieuwe gegevens wijzen op nieuwe risico's.
Bij deze bied ik u drie wetenschappelijke opinies van de EFSA aan over
vrijwaringen die Oostenrijk heeft ingesteld om de in de EU toegelaten ggo-maďs
Mon863, de ggo-raapzaadvariëteiten GT73, MS8, RF3 en MS8xRF3 van het
Oostenrijks grondgebied te weren. De EFSA concludeert in de drie opinies dat
Oostenrijk geen nieuwe wetenschappelijke gegevens heeft aangeleverd die wijzen
op gevaren voor mens, dier of milieu.
De EC zal mede op basis van de EFSA-opinies beoordelen of de genoemde
Oostenrijkse vrijwaringen gerechtvaardigd zijn. Ik zal u dit oordeel van de
Commissie zenden, zodra het beschikbaar is.
DE MINISTER VAN LANDBOUW, NATUUR EN
VOEDSELKWALITEIT,
G. Verburg
The EFSA Journal (2009) 1151, 1-16
© European Food Safety Authority, 2009
SCIENTIFIC OPINION
Request from the European Commission related to the safeguard clause
invoked by Austria on oilseed rape GT73 according to Article 23 of
Directive 2001/18/EC1
Scientific Opinion of the Panel on Genetically Modified Organisms
(Question No EFSA-Q-2008-315)
Adopted on 15 June 2009
PANEL MEMBERS.
Hans Christer Andersson, Salvatore Arpaia, Detlef Bartsch, Josep Casacuberta, Howard
Davies, Patrick du Jardin, Lieve Herman, Niels Hendriksen, Sirpa Kärenlampi, Jozsef Kiss,
Gijs Kleter, Ilona Kryspin-Sørensen, Harry Kuiper, Ingolf Nes, Nickolas Panopoulos, Joe
Perry, Annette Pöting, Joachim Schiemann, Willem Seinen, Jeremy Sweet and Jean-Michel
Wal.
SUMMARY
On 27 July 2007, Austria invoked Article 23 of Directive 2001/18/EC (safeguard clause) to
provisionally prohibit the marketing of genetically modified oilseed rape GT73 on its
territory. Austria provided detailed reasons listed in supporting documents.
On 17 April 2008, the European Food Safety Authority (EFSA) has been requested by the
European Commission to provide a scientific opinion on the statement and documents
submitted by Austria in the context of a safeguard clause invoked under Article 23 of
Directive 2001/18/EC.
In light of the information package provided by Austria in support of its safeguard clause and,
having considered all relevant scientific publications, the Scientific Panel on Genetically
Modified Organisms (GMO Panel) of EFSA concludes that, in terms of risk to human and
animal health and the environment, no new scientific evidence was presented that would
invalidate the previous risk assessment of oilseed rape GT73. The EFSA GMO Panel also
concludes that no new scientific data or information was provided in support of adverse
effects of oilseed rape GT73 on the environment and on human and animal health in Austria.
1 For citation purposes: Scientific Opinion of the Panel on Genetically Modified Organisms on a request from the European
Commission related to the safeguard clause invoked by Austria on oilseed rape GT73 according to Article 23 of Directive
2001/18/EC. The EFSA Journal (2009) 1151, 1-16.
. (minority opinion) This opinion is not shared by 0 members of the Panel. / (conflict of interest) 0 members of the Panel did
not participate in (part of) the discussion on the subject referred to above because of possible conflicts of interest.
Safeguard clause invoked by Austria on oilseed rape GT73 according to Directive
2001/18/EC
The EFSA Journal (2009) 1151, 2-16
Therefore, no specific scientific evidence, in terms of risk to human and animal health and the
environment, were provided that would justify the invocation of a safeguard clause under
Article 23 of Directive 2001/18/EC.
Key words: GMOs, oilseed rape (Brassica napus), GT73, Austria, safeguard clause,
human and animal health, environment, Directive 2001/18/EC
Safeguard clause invoked by Austria on oilseed rape GT73 according to Directive
2001/18/EC
The EFSA Journal (2009) 1151, 3-16
TABLE OF CONTENTS
Panel Members ........................................................................................................................................ 1
Summary ................................................................................................................................................. 1
Table of Contents .................................................................................................................................... 3
Background ............................................................................................................................................. 4
Terms of reference as provided by the European Commission................................................................ 4
Acknowledgements ................................................................................................................................. 4
Assessment .............................................................................................................................................. 5
1. Introduction .................................................................................................................................... 5
2. Assessment of documents provided by Austria............................................................................... 5
2.1. Food and feed safety issues..................................................................................................... 6
2.1.1. Toxicological and allergenicity assessment........................................................................ 6
2.2. Environmental safety issues and post-market environmental monitoring .............................. 6
2.2.1. Environmental risk assessment........................................................................................... 6
2.2.2. Post-market environmental monitoring plan ...................................................................... 9
2.2.3. Conclusion......................................................................................................................... 9
Overall Conclusions and Recommendations............................................................................................ 9
Documentation provided to EFSA ......................................................................................................... 10
References ............................................................................................................................................. 10
Safeguard clause invoked by Austria on oilseed rape GT73 according to Directive
2001/18/EC
The EFSA Journal (2009) 1151, 4-16
BACKGROUND
On 27 July 2007, Austria notified to the European Commission a national safeguard clause on
genetically modified (GM) oilseed rape event GT73 under Article 23 of Directive
2001/18/EC. The notification was accompanied by the scientific document entitled "Scientific
arguments for an import ban of herbicide tolerant oilseed rape GT73 (notification
C/NL/98/11)".
On 17 April 2008, the European Food Safety Authority (EFSA) has received a request from
the European Commission to provide a scientific opinion from its Scientific Panel on
Genetically Modified Organisms (GMO Panel) on the statement and documents submitted by
Austria in the context of its invoked safeguard clause.
TERMS OF REFERENCE AS PROVIDED BY THE EUROPEAN COMMISSION
EFSA was requested, under Article 29(1) and in accordance with Article 22(5) of Regulation
(EC) No 178/2002, to provide a scientific opinion as to "whether, in accordance with
Article 23 of Directive 2001/18/EC, the statement and documents submitted by the Austrian
authorities comprise new or additional information affecting the environmental risk
assessment, such that detailed grounds exist to consider that the above authorised GMO, for
the uses laid down in the corresponding consent, constitute a risk to human health or the
environment".
ACKNOWLEDGEMENTS
The European Food Safety Authority wishes to thank the members of the Working Groups on
Molecular Characterisation, Food/Feed and Environment, as well as the following members
of its staff: Yann Devos and Sylvie Mestdagh for the preparation of this opinion.
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The EFSA Journal (2009) 1151, 5-16
ASSESSMENT
1. Introduction
Directive 2001/18/EC provides the possibility for Member States to invoke safeguards on
specific genetically modified organisms in the case where new or additional information,
made available since the date of the consent, would affect the risk assessment of an authorised
GMO. Provisions foreseen by Austria seek to provisionally prohibit the marketing of oilseed
rape GT73 for its intended uses on the Austrian territory.
The EFSA GMO Panel examined the set of supporting documents submitted by Austria. In
this respect, the EFSA GMO Panel assessed whether the submitted documents comprise new
scientific information that would change the outcome of previously performed risk
assessments, and if detailed grounds exist to consider that the authorised oilseed rape GT73,
for its intended uses, constitute a risk to human and animal health or the environment.
The EFSA GMO Panel looked for evidence for GMO-specific risks - including long-term
effects (e.g., BEETLE report, 2009) - taking into consideration the EFSA GMO Panel
guidance document for the risk assessment of GM plants and derived food and feed (EFSA,
2006a) as well as any related risk assessments carried out in the past. In addition, the EFSA
GMO Panel considered the relevance of raised concerns in light of the most recent scientific
data and relevant peer-reviewed publications.
2. Assessment of documents provided by Austria
A set of supporting documents, accompanying the mandate of the European Commission (see
Terms of Reference as provided by the European Commission), was forwarded to EFSA on
17 April 2008.
Austria provided the following set of documents in support of its safeguard clause:
- Austrian letter on new supplementary scientific evaluation (13 July 2007);
- Verbot des Inverkehrbringens von gentechnisch verändertem Raps aus der Ölrapslinie
GT73 in Ă–sterreich;
- Pascher, K., Narendja, F., Rau, D. (2006). Feral oilseed rape - Investigations on its
potential for hybridisation, Studie im Auftrag des Bundesministeriums fĂĽr Gesundheit
und Frauen, Forschungsberichte der Sektion IV, Band 3/2006;
- Scientific arguments for an import ban of herbicide tolerant oilseed rape GT73
(Notification C/NL/98/11).
Based on the supporting documents, several issues were identified and therefore considered
by the EFSA GMO Panel in the following two main areas: (1) the toxicological and
allergenicity risk assessment, and (2) the environmental risk assessment and post-market
environmental monitoring plan relating to the accidental spillage of oilseed rape GT73 seeds.
Issues related to the coexistence of oilseed rape cropping systems and the adventitious
presence of authorised GM material in non-GM products were not considered, as they fall
Safeguard clause invoked by Austria on oilseed rape GT73 according to Directive
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The EFSA Journal (2009) 1151, 6-16
outside the remit of the EFSA GMO Panel. In addition, the EFSA GMO Panel notes that it
only gives its opinion on the scientific quality of the post-market environmental monitoring
activities proposed by applicants, whilst the final endorsement thereof is done by risk
managers.
During its assessment, the EFSA GMO Panel identified issues raised by the Austrian
authorities that would require further clarifications. To present and clarify the provided set of
documents, an informal meeting between the Austrian delegation, several experts of the
EFSA GMO Panel and EFSA staff was held on 23 April 2009. A representative of the
European Commission attended the meeting as observer.
2.1. Food and feed safety issues
2.1.1. Toxicological and allergenicity assessment
The EFSA GMO Panel observes that the two publications related to toxicological and
allergenicity aspects of the risk assessment quoted by Austria (Spök et al., 2004, 2005) do not
provide new data specific on the safety of oilseed rape GT73: current approaches for
assessing toxicological and allergenicity risks of genetically modified organisms are
questioned in generic terms. The EFSA GMO Panel emphasises that the approach taken by
the Panel in order to assess the potential toxicological and/or allergenicity risks of GM plants
is in accordance with internationally developed guidelines (e.g., Codex Alimentarius, 2003).
With regard to toxicological assessment, Austria refers to various arguments provided by the
applicant in its technical report that have already been addressed in the previous EFSA GMO
Panel opinion on oilseed rape GT73 (EFSA, 2004). Because the compositional analysis of
oilseed rape GT73 gave no indications of any changes, no further in vitro or in vivo
toxicological testing was deemed necessary.
The general perspectives on the allergenicity assessment of GM food and feed to which
Austria refers are currently being considered by a dedicated working groof the EFSA
GMO Panel. The approach followed by the EFSA GMO Panel in its assessment of oilseed
rape GT73 and the transgenic proteins within the latter aligns with the 'weight of evidence'
approach described in the EFSA GMO Panel guidance document for risk assessment of GM
plants and derived food and feed products (EFSA, 2006a) and in the guidelines of Codex
Alimentarius (Codex Alimentarius, 2003), which have also been endorsed by Austria.
The EFSA GMO Panel concludes that the toxicological and allergenicity information
provided by Austria are not new and have already been considered in the respective opinions
of the EFSA GMO Panel.
2.2. Environmental safety issues and post-market environmental monitoring
2.2.1. Environmental risk assessment
In line with its previous scientific opinions on herbicide tolerant oilseed rape GT73 (EFSA,
2004), MS8xRF3 (EFSA, 2005) and T45 (EFSA, 2008), the EFSA GMO Panel confirms that
in regions where oilseed rape is grown and/or where oilseed rape seeds are imported and
transported, feral oilseed rape populations are likely to occur in non-natural disturbed
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The EFSA Journal (2009) 1151, 7-16
ecosystems (such as ports, processing facilities, margins of agricultural fields, roadside
verges, railway lines, and wastelands) (Bagavathiannen and Van Acker, 2008). It is wellknown
that human activity contributes to the dispersal of plants (Wichmann et al., 2009),
especially the transport of seeds by vehicles (Zwaenepoel et al., 2006; von der Lippe and
Kowarik, 2007a,b; Garnier et al., 2008).
In the scientific literature, the occurrence of feral oilseed rape populations has been reported
not only in Austria (Pascher et al., 2006), but also in Canada (Simard et al., 2002; Yoshimura
et al., 2006; Knispel et al., 2008), France (Pessel et al., 2001; Garnier et al., 2008; Pivard et
al., 2008a,b), Germany (Menzel, 2006; Reuter et al., 2008; Neuffer, 2009), Japan (Saji et al.,
2005; Aono et al., 2006; Kawata et al., 2008; Nishizawa et al., 2009) and the United Kingdom
(Crawley and Brown, 1995, 2004; Wilkinson et al., 1995; Charters et al., 1999; Norris and
Sweet, 2002). These populations can be large and show significant variation in size from one
year to the next (Crawley and Brown, 1995).
Due to its early germination potential and capacity to capture resources rapidly, oilseed rape
can take advantage of disturbed land (Blackshaw et al., 2003, 2004). However, successful
recruitment of oilseed rape from seed spillage from passing traffic mainly depends upon its
ability to compete for space with primary colonizers, particularly perennial grasses. In most
non-agricultural areas, oilseed rape lacks the ability to establish stable populations due to the
absence of competition-free gaps (Crawley et al., 1993; Warwick et al., 1999; Hails et al.,
2006). Once established, oilseed rape populations often become extinct after 2 to 4 years
(Crawley and Brown, 1995; Crawley et al., 2001; Norris and Sweet, 2002). If habitats are
disturbed on a regular basis (e.g., by mowing, herbicide application, soil disturbance) and
replenished with seed from seed spillage or recruitment from seeds produced by residents or
from seeds from the seedbank, then feral oilseed rape populations can persist for longer
periods (8-10 years) (Pessel et al., 2001; Pivard et al., 2008a,b). Using genetic analyses and
farmer surveys, Pessel et al. (2001) revealed that some members of feral oilseed rape
populations in road verges in France originated from varieties that had not been marketed for
at least 8 years.
Oilseed rape is generally regarded as an opportunistic species, and not as an environmentally
hazardous colonizing species (Warwick et al., 1999). Several field studies and model
predictions reported that the presence of herbicide tolerance in oilseed rape does not confer a
fitness advantage, unless the respective herbicide is applied (Crawley et al., 1993, 2001;
Fredshavn et al., 1995; Warwick et al., 1999, 2004; Norris and Sweet, 2002; Claessen et al.,
2005a,b; Simard et al., 2005; Garnier and Lecomte, 2006; Garnier et al., 2006). In the absence
of glyphosate-containing herbicide applications, oilseed rape GT73 is neither more likely to
survive, nor more invasive or persistent than its conventional counterpart. Moreover, there is
no evidence that tolerance to glyphosate enhances seed dormancy, and hence the persistence
of feral oilseed rape populations (Claessen et al., 2005a,b; Sweet et al., 2004; Lutman et al.,
2005, 2008; Messéan et al., 2007). Only where and when glyphosate-containing herbicides
are applied, is oilseed rape GT73 expected to have a fitness advantage. In this respect, the
scientific information provided in the Austrian safeguard clause notification does not give any
new information regarding increased likelihood of establishment or survival of feral oilseed
rape plants in case of accidental release into the environment of oilseed rape GT73 seeds
during transportation and processing.
The EFSA GMO Panel is aware that if feral oilseed rape plants derived from spilled seeds
remain uncontrolled and reproduce, they may survive, outcross and eventually disperse genes
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to cross-compatible plants such as Brassica rapa and Raphanus raphanistrum (Scheffler and
Dale, 1994; Eastham and Sweet, 2002; Chèvre et al., 2004; Warwick et al., 2003, 2004, 2008;
Claessen et al., 2005b; Jørgensen, 2007; BEETLE report, 2009: Devos et al., 2009; Jørgensen
et al., 2009). Scientific evidence suggests that feral oilseed rape populations may serve as a
reservoir that could hold and return (trans)genes to cultivated populations of oilseed rape in a
different place and time, and act as a genetic bridge delivering the (trans)genes to sympatric
cross-compatible plants (Saji et al., 2005; Aono et al., 2006; Pascher et al., 2006; Yoshimura
et al., 2006; Knispel et al., 2008; Nishizawa et al., 2009). In Canadian regions where GM
oilseed rape is frequently grown (e.g., Beckie et al., 2006), feral oilseed rape populations were
shown to actively outcross with cultivated populations of GM oilseed rape and to accumulate
transgenes (Knispel et al., 2008). However, compared to cultivated oilseed rape populations,
the contribution of feral oilseed rape plants in vertical gene flow is expected to be limited:
feral oilseed rape populations are small compared to cultivated populations and contribute
little to the pollen load in the environment (Colbach et al., 2001a,b, 2005; Devaux et al.,
2005, 2007, 2008; Gruber and Claupein, 2006; Knispel et al., 2008; Colbach, 2009). Recent
observations in Canada confirmed the persistence of a herbicide tolerance trait over a period
of 6 years into a population of B. rapa in the absence of herbicide selection pressure (with the
exception of possible exposure to the active substance glyphosate in 1 year) and in spite of
fitness costs associated with hybridisation (Warwick et al., 2008). However, so far, there are
no compelling data to suggest that the presence of an herbicide tolerance trait in a wild
relative changes the behaviour of the wild relative. In the absence of glyphosate-containing
herbicides, hybrids or wild relatives containing the herbicide tolerance trait do not show any
enhanced fitness and behave as conventional plants. Thus escaped plants and genes dispersed
to other cross-compatible plants would not create additional environmental impacts. If
needed, feral oilseed rape GT73 and hybridised/introgressed relatives can be managed by the
use of other herbicides and/or adequate mechanical practices (Beckie et al., 2004; Devos et
al., 2004; Warwick et al., 2004; Légère, 2005; Simard et al., 2005; Gruber et al., 2008;
Lutman et al., 2008).
The environmental exposure due to GM oilseed rape grain imports is anticipated to be low, as
the amounts of viable oilseed rape seeds imported in the EU are limited with most seeds being
imported by boat and crushed in or near the ports of entry. Some of the oilseed rape seeds
imported into the EU are likely to be transported inland to Austria by boat. Moreover, some
oilseed rape seeds entering Austria are transported by road or rail to processing plants. As
indicated above, survival and outcrossing from plants derived from seed spillage will be at
very low frequencies and have no hazardous environmental consequences compared to
current feral oilseed rape populations.
In conclusion, the EFSA GMO Panel confirms that feral oilseed rape plants are likely to occur
wherever oilseed rape is cultivated and/or transported and that transgenic oilseed rape is no
exception (e.g., Saji et al., 2005; Aono et al., 2006; Yoshimura et al., 2006; Bagavathiannen
and Van Acker, 2008; Kawata et al., 2008; Knispel et al., 2008; Nishizawa et al., 2009).
However, there is no evidence that the herbicide tolerance trait introduced by genetic
engineering results in increased invasiveness of oilseed rape GT73, except when glyphosatecontaining
herbicides are applied. As such, escaped plants and genes dispersed to other crosscompatible
plants would not create additional agronomic or environmental impacts. This -
together with the assessment that oilseed rape GT73 and hybridising relatives have no
enhanced fitness or invasiveness characteristics (except in the presence of glyphosatecontaining
herbicides) - confirms earlier conclusions of the EFSA GMO Panel.
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2.2.2. Post-market environmental monitoring plan
The EFSA GMO Panel maintains its position that the scope of the post-market environmental
monitoring plan provided by the applicant complies with (1) the intended uses of oilseed rape
GT73, which excludes cultivation, (2) the requirements of the EFSA GMO Panel guidance
document for the risk assessment of GM plants and derived food and feed products (EFSA,
2006a), and (3) the EFSA GMO Panel scientific opinion on post-market environmental
monitoring (EFSA, 2006b).
European operators importing, handling and processing viable oilseed rape commodities have
recently joined with the European Association of Bioindustries (EuropaBio) in developing
monitoring systems for GM oilseed rape imported through main points of entry and
processing facilities (Lecoq et al., 2007; Windels et al., 2008). These monitoring systems are
based on Hazard Analysis and Critical Control Points (HACCP) principles. Therefore, it is
anticipated that risk managers will opt for post-market environmental monitoring of imported
oilseed rape GT73 seeds in accordance with these arrangements.
2.2.3. Conclusion
The EFSA GMO Panel confirms its opinion that the likelihood of unintended environmental
effects as a consequence of spread of (trans)genes from oilseed rape GT73 will not differ
from that of conventional oilseed rape varieties in the context of its intended uses. The EFSA
GMO Panel agrees with the monitoring plan submitted by the applicant, especially now that
comprehensive arrangements have been made by applicants and operators for monitoring at
major points of import and processing in the EU. However, the EFSA GMO Panel continues
to recommend that appropriate management systems should be in place to minimise
accidental loss and spillage of transgenic oilseed rape seeds during transportation, storage and
handling in the environment, and processing into derived products. These conclusions are in
line with previous scientific opinions of the EFSA GMO Panel on the import and processing
of herbicide tolerant oilseed rape GT73 (EFSA, 2004), MS8xRF3 (EFSA, 2005) and T45
(EFSA, 2008).
OVERALL CONCLUSIONS AND RECOMMENDATIONS
The EFSA GMO Panel has investigated the claims and documents submitted in support of the
Austrian safeguard clause and presented at the informal meeting between the Austrian
delegation, several experts of the EFSA GMO Panel and EFSA staff on 23 April 2009. In
these documents, the EFSA GMO Panel did not identify any new data subject to scientific
scrutiny or scientific information that would change previous risk assessments conducted on
oilseed rape GT73 which currently has marketing consent in the EU. In addition, the Austrian
submission did not supply scientific evidence, that the environment or ecology of Austria was
different from other regions of the EU, sufficient to merit separate risk assessments from
those conducted for other regions in the EU.
Having considered the overall information package submitted by Austria as well as a broad
range of relevant scientific literature, the EFSA GMO Panel is of the opinion that there is no
specific scientific evidence, in terms of risk to human and animal health and the environment,
that would justify the invocation of a safeguard clause under Article 23 of Directive
2001/18/EC for the marketing of oilseed rape GT73 for its intended uses in Austria. In
conclusion, the EFSA GMO Panel finds that the scientific evidence currently available does
Safeguard clause invoked by Austria on oilseed rape GT73 according to Directive
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The EFSA Journal (2009) 1151, 10-16
not sustain the arguments provided by Austria, and therefore the EFSA GMO Panel reiterates
its previous scientific opinion on oilseed rape GT73.
DOCUMENTATION PROVIDED TO EFSA
1. Letter, dated 17 April 2008, with supporting documents from M.P. Carl, Director-General
Environment EC, to Catherine Geslain-Lanéelle, Executive Director EFSA (ref
ENV/B3/YK/gm D(2008) 518) requesting for a scientific opinion on the safeguard
notification submitted by Austria under Article 23 of Directive 2001/18/EC for oilseed
rape GT73 and comprising the following supporting documents:
- Austrian letter on new supplementary scientific evaluation (13 July 2007);
- Verbot des Inverkehrbringens von gentechnisch verändertem Raps aus der Ölrapslinie
GT73 in Ă–sterreich;
- Pascher, K., Narendja, F., Rau, D. (2006). Feral oilseed rape - Investigations on its
potential for hybridisation, Studie im Auftrag des Bundesministeriums fĂĽr Gesundheit
und Frauen, Forschungsberichte der Sektion IV, Band 3/2006;
- Scientific arguments for an import ban of herbicide tolerant oilseed rape GT73
(Notification C/NL/98/11).
2. Letter, dated 15 October 2008, from Catherine Geslain-Lanéelle, Executive Director
EFSA, to Jos Delbeke, Acting Director-General Environment EC (ref
CGL/RM/PB/SM/shv (2008) 3369831), acknowledging the receipt of the mandate
accompanied with the supporting documents.
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© European Food Safety Authority, 2009
SCIENTIFIC OPINION
Request from the European Commission related to the safeguard clause
invoked by Austria on maize lines MON863 according to Article 23 of
Directive 2001/18/EC1
Scientific Opinion of the Panel on Genetically Modified Organisms
(Question No EFSA-Q-2008-742)
Adopted on 15 June 2009
PANEL MEMBERS.
Hans Christer Andersson, Salvatore Arpaia, Detlef Bartsch, Josep Casacuberta, Howard
Davies, Patrick du Jardin, Lieve Herman, Niels Hendriksen, Sirpa Kärenlampi, Jozsef Kiss,
Gijs Kleter, Ilona Kryspin-Sørensen, Harry Kuiper, Ingolf Nes, Nickolas Panopoulos, Joe
Perry, Annette Pöting, Joachim Schiemann, Willem Seinen, Jeremy Sweet and Jean-Michel
Wal.
SUMMARY
On 16 July 2008, Austria invoked Article 23 of Directive 2001/18/EC (safeguard clause) to
provisionally prohibit the import of the MON863 maize lines on its territory. Austria provided
detailed reasons listed in supporting documents.
On 3 September 2008, the European Food Safety Authority (EFSA) has been requested by the
European Commission to provide a scientific opinion on the statement and documents
submitted by Austria in the context of the safeguard clause invoked under Article 23 of
Directive 2001/18/EC.
In the light of the information package provided by Austria in support of its safeguard clause
and, having considered all relevant scientific publications, the Scientific Panel on Genetically
Modified Organisms (GMO Panel) of EFSA concludes that, in terms of risk to human and
animal health and the environment, no new scientific evidence was presented that would
invalidate the previous risk assessment of maize MON863. The EFSA GMO Panel also
concludes that no new scientific data or information was provided in support of adverse
effects of maize MON863 on the environment and on human and animal health in Austria.
1 For citation purposes: Scientific Opinion of the Panel on Genetically Modified Organisms on a request from the European
Commission related to the safeguard clause invoked by Austria on maize lines MON863 according to Article 23 of
Directive 2001/18/EC. The EFSA Journal (2009) 1152, 1-18.
. (minority opinion) This opinion is not shared by x members of the Panel. / (conflict of interest) x members of the Panel did
not participate in (part of) the discussion on the subject referred to above because of possible conflicts of interest.
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Therefore, no specific scientific evidence, in terms of risk to human and animal health and the
environment, were provided that would justify the invocation of a safeguard clause under
Article 23 of Directive 2001/18/EC.
Key words: GMOs, maize (Zea mays L.), MON863, Austria, safeguard clause, human
health and animal health, environment, Directive 2001/18/EC
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TABLE OF CONTENTS
Panel Members........................................................................................................................... 1
Summary .................................................................................................................................... 1
Table of Contents ........................................................................................................................ 3
Background ................................................................................................................................ 4
Terms of reference as provided by the European Commission .................................................. 4
Acknowledgements ..................................................................................................................... 4
Assessment ................................................................................................................................. 5
1. Introduction ......................................................................................................................... 5
2. Assessment of documents provided by Austria .................................................................. 5
2.1. Food and feed safety issues................................................................................................. 6
2.1.1. Toxicological risk assessment........................................................................................ 6
2.1.2. Nutritional risk assessment
2.2. Molecular characterisation issues ............................................................................... 8
2.3. Environmental safety issues and post-market environmental monitoring8
2.3.1. Environmental risk assessment .................................................................................... 11
2.3.2. Post-market environmental monitoring plan.............................................................. 12
2.3.3. Conclusion ...................................................................................................................... 13
Overall Conclusions and Recommendations............................................................................. 13
Documentation provided to EFSA ............................................................................................ 14
References ................................................................................................................................ 14
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BACKGROUND
On 16 July 2008, Austria notified to the European Commission a national safeguard clause on
genetically modified (GM) maize MON863 under Article 23 of Directive 2001/18/EC. The
notification was accompanied by the scientific document entitled "Scientific arguments for an
import ban of genetically modified maize MON863 (Zea mays L., MON863) of Monsanto
notification C/DE/02/9".
On 3 September 2008, the European Food Safety Authority (EFSA) has received a request
from the European Commission to provide a scientific opinion from its Scientific Panel on
Genetically Modified Organisms (EFSA GMO Panel) on the statement and documents
submitted by Austria in the context of its invoked safeguard clause.
TERMS OF REFERENCE AS PROVIDED BY THE EUROPEAN COMMISSION
EFSA was requested, under Article 29(1) and in accordance with Articles 22(2) and 22(5)(c)
of Regulation (EC) No 178/2002, to provide a scientific opinion as to "whether, in
accordance with Article 23 of Directive 2001/18/EC, the statement and documents submitted
by the Austrian authorities comprise new information affecting the environmental risk
assessment, such that detailed grounds exist to consider that the above authorised GMO, for
the uses laid down in the corresponding consent, constitute a risk to human health, animal
health or the environment".
ACKNOWLEDGEMENTS
The European Food Safety Authority wishes to thank the members of the Working Groups on
Molecular Characterisation, Food/Feed and Environment, as well as the following members
of its staff: Jaime Aguilera, Yann Devos, Yi Liu and Sylvie Mestdagh for the preparation of
this opinion.
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ASSESSMENT
1. Introduction
Directive 2001/18/EC provides the possibility for Member States to invoke safeguards on
specific Genetically Modified Organisms (OGM) in the case where new or additional
information, made available since the date of the consent, would affect the risk assessment of
an authorised GMO. Provisions foreseen by Austria seek to provisionally prohibit the import
of maize lines MON863 into the Austrian territory.
The EFSA GMO Panel examined the set of supporting documents submitted by Austria. In
this respect, the EFSA GMO Panel assessed whether the submitted documents comprise new
scientific knowledge information that would change the outcome of previously performed risk
assessment, and if detailed grounds exist to consider that the authorised maize MON863, for
its intended uses, constitutes a risk to human and animal health or the environment.
The EFSA GMO Panel looked for evidence for GMO-specific risks - including long-term
effects (e.g., BEETLE report, 2009) - taking into consideration the EFSA GMO Panel
guidance for the risk assessment of genetically modified plants and derived food and feed
(EFSA, 2006a) as well as any related risk assessments carried out in the past. In addition, the
EFSA GMO Panel considered the relevance of raised concerns in the light of the most recent
scientific data and relevant peer-reviewed publications.
2. Assessment of documents provided by Austria
A set of supporting documents, accompanying the mandate of the European Commission (see
Terms of Reference as provided by the European Commission), was forwarded to EFSA on
3 September 2008.
Austria provided the following set of documents in support of its safeguard clause:
- Verbot des Inverkehrbringens von gentechnisch verändertem Mais der Linie
MON863;
- Scientific arguments for an import ban of maize MON863.
Based on the supporting documents, several issues were identified and therefore considered
by the EFSA GMO Panel in the following areas: (1) the toxicological and nutritional risk
assessment, (2) the safety assessment of the antibiotic resistance marker (ARM) gene nptII,
and (3) the environmental risk assessment and post-market environmental monitoring plan
related to the accidental spillage of maize MON863.
In addition, the EFSA GMO Panel notes that it only gives its opinion on the scientific quality
of the post-market environmental monitoring plan proposed by the applicant, whilst the final
endorsement thereof is done by risk managers.
During its assessment, the EFSA GMO Panel identified issues raised by Austria that would
require further clarifications. To present and clarify the provided set of documents, an
informal meeting between the Austrian delegation, several experts of the EFSA GMO Panel
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and EFSA staff was held on 23 April 2009. A representative of the European Commission
attended the meeting as observer.
2.1. Food and feed safety issues
The Austrian Competent Authority has provided EFSA with a document entitled "Scientific
Arguments for an Import Ban of Genetically Modified Maize MON 863 (Zea mays L., line
MON 863) of Monsanto (Notification C/DE/02/9)". This document focuses on a number of
details of toxicological and nutritional studies with maize MON863, which are cited by an
article by Hammond et al. (2006) describing the outcomes of the 90-day rat oral toxicity study
with maize MON863. The study by Hammond et al. (2006) refers to the same study for
which another technical report was previously provided to EFSA as part of the dossier that
was considered by the EFSA GMO Panel when formulating its opinion. In addition, various
other documents have been published by EFSA in response to issues previously raised on the
same 90-days study being part of the dossier (EFSA, 2004a; EFSA, 2004b; EFSA, 2007a;
EFSA, 2007b). None of the studies quoted by Austria provide new direct evidence of risks to
human and animal health associated with food and feed use of MON863, or its transgenic
components, which would have evolved after the publication of EFSA's opinion on maize
MON863 in 2004. In addition, the EFSA GMO Panel notes that 90-day study is not strictly
required in the internationally harmonized approach of comparative safety assessment of a
GMO versus its control. If the outcomes of the comparison of extensively analyzed
compositional and other parameters indicate equivalence of a GMO to conventional food and
feed, this would not trigger the performance of a 90-days study.
2.1.1. Toxicological risk assessment
The Austrian Competent Authority highlighted a number of details of the toxicological and
nutritional studies cited by Hammond et al. (2006) as what they consider as deficiencies in
experimental design and interpretation, which, as they assert, would impact on the
interpretability of the outcomes of these studies. With regard to toxicity, the Austrian
comments focus on the 90-days feeding study with diets containing kernels of MON863.
They highlight various perceived deficiencies in the original dossier report on the 90-days
study.
As the Austrian Competent Authority correctly notes, a report on the same 90-days oral rat
feeding study as described by Hammond et al. (2006) has been provided with the dossier on
MON863, albeit with more extensive coverage of experimental details.
With regard to the 90-days rat feeding study, the Austrian Competent Authority has made
detailed and extensive comments regarding the experimental design (no updated protocol,
inclusion of reference groups), diet formulation (Cry3Bb denaturation; contaminant analysis),
endpoints measured (not all organs/tissues checked for histopathology; various single
differences in performance and clinical chemistry). The same data of this study have already
been assessed in detail by the EFSA GMO Panel, including the various differences observed
(EFSA, 2004a; EFSA, 2004b; EFSA, 2007a; EFSA, 2007b)
Various general comments can be made, though, to the conclusions and assertions brought
forward in the Austrian document. The Austrian Competent Authority, for example, appears
to comment on the statistical analysis as performed by the applicant, including the asserted
disappearance of differences through an increase of the total number of animals used for the
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experiment, most of which comprise animals in reference groups fed diets containing
commercial maize. The EFSA GMO Panel, though, has considered the direct comparison
between the groups fed GM maize MON863 and the respective control groups. Any
difference thus identified can then be further compared with the background ranges provided
by the animals fed the reference diets. For example, the difference in reticulocytes that the
Austrian authorities point at, was also noted by the EFSA GMO Panel, as summarized in
section 4.2 of its opinion of 2004 (EFSA, 2004a). This approach of direct comparison of a
GMO with its appropriate comparator is in line with the internationally harmonized
comparative safety assessment principles for GM foods as laid down in Codex alimentarius
guidelines (to which the Austrian authorities have also subscribed) and further elaborated in
EFSA guidance document (EFSA, 2006a). Concerning the comment with regard to the
percentage (60-80%) of the reference groin overall sample size, it should be noted that it is
not the percentage of the reference groups within the sample size that is a problem in itself,
but the replication of the GM and comparator. If this replication is too small because of the
restrictions placed by having 60-80% reference varieties, then this could be a valid criticism.
However, if the replication is sufficient, then there is no reason why reference groups should
not contribute 60-80% of the sample size. In addition, the guidelines that were recently
drafted by the Commission and discussed with EU Member States' representatives at the
Standing Committee for the Food Chain and Animal Health recommend that compositional
field trials be done with at least 60% of the plots being allocated to commercial varieties
(reference groups).
Austria also refers to OECD guideline 408 (OECD, 1998) with regard to the number of doses
and other details, which would not have been strictly followed by the applicant. In the EFSA
GMO Panel's opinion, it has to be taken into account, though, that OECD guideline 408 has
been developed for the testing of pure chemicals and that adjustments may be required for the
testing of whole foods. This issue has also been extensively highlighted in the EFSA GMO
Panel's report on animal feeding trials (EFSA, 2008).
In addition, Austria notes that the Cry3Bb protein should have remained intact in the test diet
used in the 90-days rat feeding study, and therefore concludes that more details on the feed
manufacturing conditions and the presence and nature of the transgenic elements in the rat
diets should have been provided. Given the commonly low expression levels of transgenic
proteins in GM crops, the EFSA GMO Panel notes, though, that for testing the safety of
transgenic proteins, other models than whole-product feeding studies for testing purified
components would be recommendable, such as repeated-dose oral rodent studies with the
purified transgenic protein (see EFSA guidance document, EFSA, 2006a). Based on the data
provided in the dossier, Cry3Bb has been assessed by the EFSA GMO Panel for its safety.
The EFSA GMO Panel concludes that the data provided by the Austrian Competent Authority
do not indicate that there would be an additional need for further testing the safety of Cry3Bb.
The EFSA GMO Panel concurs with the Austrian notion that nutritional feeding studies in
food-producing animals cannot be considered toxicity studies. Again, the Austrian comments
pertain to conclusions made by other authors than the EFSA GMO Panel in its opinion on
MON863. The scientific opinions of the EFSA GMO Panel, including the one on MON863,
make a distinction between toxicity, allergenicity, nutrition, and other issues that may be of
relevance to food and feed safety.
In conclusion, no new data have been presented by the Austrian authorities that could be
considered evidence of potential toxic effects on maize MON863 and its transgenic
components on humans and animals. In the absence of such evidence, the EFSA GMO Panel
Safeguard clause invoked by Austria on maize MON863 according to Directive
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The EFSA Journal (2009) 1152, 8-18
cannot follow the Austrian recommendation for requiring additional toxicity tests for subchronic,
chronic, developmental, and reproductive toxicity of maize MON863.
2.1.2. Nutritional risk assessment
The Austrian Competent Authority refers to various nutritional studies that have appeared in
scientific journals, in which the performance of various food-producing animals fed
MON863, including poultry, beef and dairy cattle, and swine, have been measured. The
article on the poultry feeding study with MON863 (Taylor et al., 2003) is based on the same
feeding trial of which a report has been provided with the dossier assessed by EFSA. In
addition, the quoted article on the dairy cattle study (Grant et al., 2003) has also been
considered in the EFSA opinion. The other articles describing studies on beef cattle and swine
were published after the publication of the opinion.
The Austrian comments pertain to perceived shortcomings of the abovementioned nutritional
studies, such as to the composition of the diets (e.g., origin of the maize; certain
micronutrients not being measured; levels of transgenic components in final product),
experimental design (e.g., inclusion of reference groups; choice of animals; background
variability), and statistical analysis (e.g. limited information based on p-values alone). None
of these comments indicate that the new data cited by Austria demonstrate a potentially
relevant adverse effect of maize MON863 on animal nutrition.
The EFSA GMO Panel concurs with the Austrian general comment that the first comparison
to be made is between the GMO and its appropriate comparator, after which further
comparison with the background range of reference values may be made, if applicable. The
Austrian Competent Authority assert that whilst the transgenic identity of test materials has
been verified, the levels of transgenic proteins and DNA in the final feed product, rather than
in raw products, should be established. In the EFSA GMO Panel's opinion, these transgenic
components do not contribute to nutrition given their very low abundance.
Moreover, the Austrian comments and the cited studies do not provide evidence of potential
impacts of maize MON863 on nutrition that would lead the EFSA GMO Panel to deviate
from its previous opinion (EFSA, 2004a). It should be noted that this kind of studies is not
strictly required in the absence of indications of altered nutritional properties of a GMO based
on compositional analysis and other data (e.g. type of modification) according to EFSA
guidance. In the case of maize MON863, these data can therefore be regarded as
supplementary data.
2.2. Molecular characterisation issues
2.2.1. Safety assessment of the ARM gene aph(3')-IIa
Therapeutic relevance of kanamycin and neomycin in human and veterinary medicine
The aph(3')-IIa gene confers resistance to neomycin and kanamycin but not to other
aminoglycosides of clinical use. The aph(3')-IIa gene confers slightly reduced susceptibility
to amikacin for E. coli. However, amikacin is a poor substrate for the APH(3')-IIa enzyme
due to its hydroxyaminobutyryl side chain.
Antimicrobials are grouped into classes on the basis of chemical structure and mode of action.
Most antimicrobials used for the treatment of animals belong to classes that are also used in
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The EFSA Journal (2009) 1152, 9-18
human medicine. A list of antimicrobial classes was compiled by WHO in 2007 (the WHO
Expert Group on Critically Important Antimicrobials for Human Health) (WHO, 2007),
giving examples of substances used for the treatment of infections in humans. Antimicrobials
listed as 'Critically Important' in the WHO list are characterised as both: 1. 'sole therapy or
one of few alternatives to treat serious human disease', and 2. 'antimicrobials used to treat
diseases caused by organisms that may be transmitted via non-human sources or diseases
caused by organisms that may acquire resistance genes from non-human sources'. With
respect to this classification, kanamycin and neomycin were downscaled from "critically
important" to "highly important" compared to the WHO report of 2005 (WHO, 2005),
because they no longer were considered to comply with criterion 1. Antimicrobials classified
as 'Highly Important' meet either criterion 1 or criterion 2. The World Animal Health
Organisation (OIE) has similarly developed and adopted a list ranking the importance of
different antimicrobials for animal health (OIE, 2007). Aminoglycosides, as a group, is a class
of antibiotics critically important for veterinary medicine and animal production (OIE, 2007).
Kanamycin is rarely used systemically today due to its severe side effects although this
antibiotic remains a recognised second line choice in conditions of infections with multiple
drug resistant (MDR) Mycobacterium tuberculosis (MTB). Aminoglycoside resistance in M.
tuberculosis results from a mutation causing alterations in the antibiotic target molecule
within the mycobacterial cell; thus chromosomal resistance, and not the transfer of antibiotic
resistance genes , is the only identified mechanism resulting in resistance
to kanamycin (Goldstein et al., 2005 and references therein). Neomycin is poorly absorbed
from the gastrointestinal tract, and is nephrotoxic and ototoxic. The use of neomycin in
human medicine is limited to topical applications and gut irrigation/encephalopathy. By
killing bacteria in the intestinal tract, it keeps ammonia levels low and prevents hepatic
encephalopathy, especially prior to gastrointestinal surgery. In veterinary medicine
kanamycin and neomycin could be used for therapies of neonatal diarrhoea in piglets and
treatment of multi-resistant enteric gram-negative infections.
Transfer of ARM genes from GM plants to bacteria
Transfer of antibiotic resistance marker genes from GM plants to bacteria has not been
detected either under natural or laboratory conditions in the absence of pre-existing sequence
identity in the recipient organism. A number of studies have been published in which the
possible occurrence of bacterial transformants carrying GM plant-derived antibiotic resistance
marker genes in fields planted with GM plants were screened (Paget et al., 1998; Gebhard and
Smalla, 1999; Badosa et al., 2004; Demanèche et al., 2008, Kim et al., 2008). Nonetheless, in
none of these studies has transfer of antibiotic resistance marker genes from GM plant
material to bacteria been demonstrated. Nor could such transfer be detected from the existing
background.
In the cascade of events leading to clinical importance, the ARM genes present in GM plants
would need to be transferred to, stabilised and expressed in a bacterial cell. Absence of
sequence identity is known to be the major factor limiting the stable integration, by
homologous recombination, of DNA from a GM plant to a bacterial cell. Other factors
limiting the potential impact of the aph(3')-IIa marker gene used in maize MON863 include
the lack of stability of the plant DNA in different environments and the limited competence of
many bacterial cells.
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The EFSA Journal (2009) 1152, 10-18
ARM genes transfer from plants to bacteria has never been observed. There are limitations
related to sampling and detection methods, as well as challenges in estimating exposure levels
and in the inability to assign transferable resistance genes to a defined source.
Notwithstanding these uncertainties, and taking into account all the peer-reviewed data, the
probability of the transfer of antibiotic resistance genes from GM plants to bacteria must be
considered as zero or below the limit of detection. It has to be stressed that the dissemination
of antibiotic resistance genes between bacteria is not comparable with the potential transfer of
these genes from plants to bacteria. Transfer of ARM genes from plants to bacteria would
occur, if at all, with a very low frequency compared to that between bacteria.
Resistance in natural environments
Concerning the prevalence of the aph(3')-IIa gene and phenotypic kanamycin/neomycin
resistance, two basically different sets of data are available.
In different countries the resistance is monitored in indicator bacteria and pathogens. The
available data indicate that a pool of aph(3')-IIa-carrying bacteria occur in and outside
hospital-associated environments. There are environmental fluctuations in the prevalence of
the aph(3')-IIa gene and of the kanamycin/neomycin phenotypic resistance. During the
bilateral technical meeting between the GMO Panel and the Austrian delegation a mean
frequency of 0.74 % kanamycin resistant Salmonella has been reported in the Austrian
surveillance programme of human isolates from 1999-2008. A similar frequency has been
reported for neomycin resistant Campylobacter isolates from poultry from 2004-2007. This
should be considered as high frequency.
An additional and important source of information on the frequency and distribution of genes
conferring resistance to aminoglycoside antibiotics has been generated from metagenomic
analyses. These are based on the molecular detection of resistance determinants, and allow
the analysis of an extended bacterial population compared to conventional culturing methods.
The expanding metagenomic studies have revealed a high density of antibiotic resistance
genes in the environment (D'Costa et al., 2007). The resistance mechanisms identified include
inactivation of aminoglycoside antibiotics by phosphorylation and acetylation (Riesenfeld et
al., 2004). The results indicate that soil bacteria are a reservoir of antibiotic resistance genes
towards aminoglycosides with greater genetic diversity than previously accounted for. Even a
remote Alaskan soil, with no known exposure to antibiotics, harbours a great variety of
resistance determinants (Allen et al., 2009) and even before the clinical use of antibiotics,
antibiotic resistant bacteria were isolated (Wright, 2007). The ubiquitous distribution of the
wide variety of antibiotic resistance genes can be explained by the fact that many of these
genes are not just weapons against bacterial competitors but have other primary signalling
functions (e.g. detoxification of metabolic intermediates, virulence and signal trafficking)
(Martinez, 2008).
Selective antibiotic pressure in field environments
The EFSA GMO Panel agrees that selective antibiotic pressure can be present in several
environments. This selective pressure is the key factor in the selection of resistance from the
environmental reservoir and in the dissemination of antibiotic resistance between bacteria.
However, this does not increase the likelihood of transfer of ARM genes from GM plants to
bacteria. In the unlikely event that such a transfer to a bacterial cell occurs, it would not add
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The EFSA Journal (2009) 1152, 11-18
to the existing pool of naturally occurring resistance genotypes present in the microbial
resistome.
2.2.2. Conclusion
Kanamycin and neomycin are categorised by the WHO Expert Group on Critically Important
Antimicrobials for Human Health as 'Highly Important' antimicrobials. Kanamycin is used as
a second-line drug for the treatment of infections with multiple drug-resistant tuberculosis
(MTB). The increasing occurrence worldwide of "extensively drug-resistant" isolates of MTB
with resistance to second-line antibiotics such as kanamycin is a cause for global concern.
The aph(3')-IIa gene has not been implicated in such resistance.
The transfer of ARM genes from GM plants to bacteria has never been shown to occur under
laboratory or natural conditions in the absence of sequence identity. If transfer of ARM genes
from GM plants to bacteria occurs at all, its frequency is below the limit of detection. The
process is therefore considered unlikely to impact on the occurrence of antibiotic resistance in
humans, animals and the environment.
The genetic determinants conferring resistance to kanamycin and neomycin are detected in
the environmental resistome and in all environments analysed by metagenomic analyses.
They are also widespread among bacteria in different environments. Data provided from
Austria indicate the spread of this resistance in human food-borne pathogens at a frequency of
about 1%. Taking into account the theoretical transfer frequencies of ARM genes from GM
plants to bacteria, in the unlikely event of the transfer of the aph(3')-IIa gene from maize
MON863 to a bacterium, its contribution to the existing pool of kanamycin resistance in
bacteria would be negligible.
For further details concerning the safety assessment of the ARM gene aph(3')-IIa, the EFSA
GMO Panel refers to the EFSA statement (EFSA, 2009).
2.3. Environmental safety issues and post-market environmental monitoring
2.3.1. Environmental risk assessment
The intended uses of maize MON863 specifically exclude cultivation, so the environmental
exposure is mainly limited to exposure through manure and faeces from the gastrointestinal
tracts mainly of animals fed maize MON863, as well as to accidental release into the
environment of MON863 grains during transportation and processing and subsequently to
potential occurrence of sporadic feral plants.
Maize is highly domesticated and generally unable to survive in the environment without
cultivation. Maize plants are not winter hardy in most regions of Europe: they have lost their
ability to release seeds from the cob and do not occur outside cultivated land or disturbed
habitats in agricultural landscapes of Europe, despite cultivation for many years. In addition,
there are no cross-compatible wild relatives in Europe, and gene flow via pollen is largely
restricted to neighbouring maize crops.
Maize MON863 has been developed to provide protection against certain coleopteran pests
such as corn rootworms (Diabrotica spp.) by the introduction of a variant Bacillus
thuringiensis cry3Bb1 gene. The insect resistance trait can only be regarded as providing a
selective advantage for the GM maize in cultivation under corn rootworm infestation
Safeguard clause invoked by Austria on maize MON863 according to Directive
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The EFSA Journal (2009) 1152, 12-18
conditions. However, survival of maize outside of cultivation in Europe is mainly limited by a
combination of low competitiveness, absence of a dormancy phase, susceptibility to diseases
and to cold climate conditions. Since these general characteristics of maize MON863 are
unchanged, the inserted insect resistance trait is not likely to provide a selective advantage
outside of cultivation in Europe. Therefore, it is considered very unlikely that volunteers of
this GM maize, or its progeny, will differ from conventional maize varieties in their ability to
survive until subsequent seasons, or to establish feral populations under European
environmental conditions. Since studies in Europe and elsewhere with maize MON863 have
shown no altered survival, multiplication or dissemination characteristics except in the
presence of the specific target organisms, the EFSA GMO Panel is of the opinion that the
likelihood of unintended environmental effects as a consequence of spread of genes from this
maize due to accidental spillage will not differ from that of conventional maize varieties.
Considering the intended uses of maize MON863, the environmental risk assessment is
concerned with indirect exposure through manure and faeces from the gastrointestinal tracts
mainly of animals fed maize MON863. In its previous environmental risk assessment of
maize MON863 (EFSA, 2004a), the EFSA GMO Panel also considered the possibility that
gene products, particularly Cry proteins might enter the environment either from the intestinal
tracts of animals or through horizontal gene flow to bacteria. Data supplied by the applicant
and other data published in the scientific literature suggested that most proteins would be
degraded by enzymatic activity in the intestinal tract (Lutz et al., 2005; Wiedemann et al.,
2006), so that a small amount of Cry protein would remain intact to pass out in faeces.
Subsequently, there would be further degradation of proteins in the manure due to microbial
processes. Even though it has been observed that Cry proteins can bind to certain soil
particles (e.g., humic acids, clays) resulting in protection from degradation, a number of
studies revealed that there is no accumulation of Cry proteins from GM crops in soil (Herman
et al., 2001, 2002; Head et al., 2002; Baumgarte and Tebbe, 2005; Hopkins and Gregorich,
2005; Ahmad et al., 2005; Dubelman et al., 2005; Icoz and Stotzky, 2007; Krogh and
Griffiths, 2007; Lawhorn et al., 2009).
Having considered the different routes of exposure to the environment, the EFSA GMO Panel
reiterates its previous opinion that the likelihood of unintended environmental effects as a
consequence of spread of genes from this maize will not differ from that of conventional
maize varieties (EFSA, 2004a). The EFSA GMO Panel concludes that the Austrian
submission provided no new scientific data or information in support of an adverse effect of
maize MON863 on the environment and that would justify a national safeguard measure
concerning this product.
2.3.2. Post-market environmental monitoring plan
Austria questioned the adequacy, relevance and completeness of the post-market
environmental monitoring (PMEM) plan provided by the applicant for maize MON863. The
EFSA GMO Panel notes that it gives its opinion on the scientific quality of the PMEM plans
proposed by applicants. The definitive and final endorsement of post-market environmental
monitoring is done by risk managers. In this context, the EFSA GMO Panel refers to the
section 5.2 of its scientific opinion on post-market environmental monitoring of GM plants
(EFSA, 2006b) stating that 'Details of the specific plans and methods of monitoring in each
country should not be included in the original application. The GMO Panel advises that the
application should describe the general approaches and methods that the applicant would
apply in different commercialisation sites, including the type of dialogue that would be
Safeguard clause invoked by Austria on maize MON863 according to Directive
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The EFSA Journal (2009) 1152, 13-18
established with risk managers in each Member State. The implementation of general
surveillance data collection at a regional and national scale will be dependent on the local
circumstances prevailing at the time the consent is given. Thus detailed local arrangements
will be developed by the applicant after the application has been accepted and will depend on
where the crop will be grown, the scale of commercialisation, the nature of the cultivation
systems and a range of other factors. Applicants are encouraged to establish contacts with
national competent authorities at an early stage in the commercialisation planning.'
In its initial scientific opinion for the placing on the market of insect protected GM maize
MON863 and MON863xMON810 (EFSA, 2004a), the EFSA GMO Panel concluded that the
scope of the monitoring plan provided by the applicant was in line with the intended uses for
the GMO since the environmental risk assessment did not cover cultivation. In addition, the
EFSA GMO Panel advised that appropriate management systems should be in place to
prevent seeds of the GM maize entering cultivation, as the latter requires specific approval
under Directive 2001/18/EC.
The association of European traders, importing cereals, oilseeds and feedstuffs (Coceral) as
well as the association of European port silos (Unistock) have recently joined with the
European Association of Bioindustries (EuropaBio) in developing monitoring systems for
GM maize grains imported through the main ports of entry and processing facilities in Europe
(e.g., Spain, Portugal, Italy, the Netherlands). These monitoring systems are based on Hazard
Analysis and Critical Control Points (HACCP) principles. Therefore, it is anticipated that risk
managers will opt for post-market environmental monitoring of imported maize MON863 in
accordance with these arrangements.
Subject to post-market environmental monitoring activities under the coordinating system
established by EuropaBio, the EFSA GMO Panel maintains its opinion that the scope of the
post-market environmental monitoring plan provided by the applicant complies with (1) the
intended uses of maize MON863, which exclude cultivation, (2) the requirements of the
EFSA GMO Panel guidance on GM plants (EFSA, 2006a), and (3) the EFSA GMO Panel
scientific opinion on post-market environmental monitoring (EFSA, 2006a,b).
2.3.3. Conclusion
The EFSA GMO Panel confirms its opinion that the likelihood of unintended environmental
effects as a consequence of spread of (trans)genes from maize MON863 will not differ from
that of conventional maize varieties in the context of its intended uses. The EFSA GMO Panel
agrees with the monitoring plan submitted by the applicant, especially now that
comprehensive arrangements have been made by applicants and operators for monitoring at
major points of import and processing in European Union. However, the EFSA GMO Panel
continues to recommend that appropriate management systems should be in place to minimise
accidental loss and spillage of transgenic maize grains during transportation, storage and
handling in the environment, and processing into derived products.
OVERALL CONCLUSIONS AND RECOMMENDATIONS
The EFSA GMO Panel has investigated the claims and documents both submitted in support
of the Austrian safeguard clause and presented at the informal meeting between the Austrian
delegation, several experts of the EFSA GMO Panel and EFSA staff on 23 April 2009. In
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The EFSA Journal (2009) 1152, 14-18
these documents, the EFSA GMO Panel did not identify any new data subject to scientific
scrutiny or scientific information that would invalidate the previous risk assessment of maize
MON863. In addition, the Austrian submission did not supply scientific evidence, that the
environment or ecology of Austria was different from other regions of the EU, sufficient to
merit separate risk assessments from those conducted for other regions in the EU.
Having considered the overall information package submitted by Austria as well as relevant
scientific literature, the EFSA GMO Panel is of the opinion that there is no specific scientific
evidence, in terms of risk to human and animal health and the environment, that would justify
the invocation of a safeguard clause under Article 23 of Directive 2001/18/EC for the import
of maize MON863 for its intended uses in Austria. In conclusion, the EFSA GMO Panel finds
that the scientific evidence currently available does not sustain the arguments provided by
Austria, and therefore the EFSA GMO Panel reiterates its previous scientific opinions on
maize MON863.
DOCUMENTATION PROVIDED TO EFSA
1. Letter, dated 3 September 2008, with supporting documents from Jos Delbeke, Acting
Director-General Environment EC, to Catherine Geslain-Lanéelle, Executive Director
EFSA (ref ENV/B3/YK/lh ARES(2008) 24354) requesting for a scientific opinion on the
safeguard notification submitted by Austria under Article 23 of Directive 2001/18/EC for
maize lines MON863 and comprising the following supporting documents:
a. Verbot des Inverkehrbringens von gentechnisch verändertem Mais der Linie
MON863;
b. Scientific arguments for an import ban of maize MON863.
2. Letter, dated 15 October 2008, from Catherine Geslain-Lanéelle, Executive Director
EFSA, to Jos Delbeke, Acting Director-General Environment EC, acknowledging the
receipt of the mandate accompanied with the supporting documents.
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© European Food Safety Authority, 2009
SCIENTIFIC OPINION
Request from the European Commission related to the safeguard clause
invoked by Austria on oilseed rape MS8, RF3 and MS8xRF3 according to
Article 23 of Directive 2001/18/EC1
Scientific Opinion of the Panel on Genetically Modified Organisms
(Question No EFSA-Q-2008-743)
Adopted on 15 June 2009
PANEL MEMBERS.
Hans Christer Andersson, Salvatore Arpaia, Detlef Bartsch, Josep Casacuberta, Howard
Davies, Patrick du Jardin, Lieve Herman, Niels Hendriksen, Sirpa Kärenlampi, Jozsef Kiss,
Gijs Kleter, Ilona Kryspin-Sørensen, Harry Kuiper, Ingolf Nes, Nickolas Panopoulos, Joe
Perry, Annette Pöting, Joachim Schiemann, Willem Seinen, Jeremy Sweet and Jean-Michel
Wal.
SUMMARY
On 15 July 2008, Austria invoked Article 23 of Directive 2001/18/EC (safeguard clause) to
provisionally prohibit the marketing of genetically modified oilseed rape MS8, RF3 and
MS8xRF3 on its territory. Austria provided detailed reasons listed in supporting documents.
On 31 July 2008, the European Food Safety Authority (EFSA) has been requested by the
European Commission to provide a scientific opinion on the statement and documents
submitted by Austria in the context of a safeguard clause invoked under Article 23 of
Directive 2001/18/EC.
In light of the information package provided by Austria in support of its safeguard clause and,
having considered all relevant scientific publications, the Scientific Panel on Genetically
Modified Organisms (GMO Panel) of EFSA concludes that, in terms of risk to human and
animal health and the environment, no new scientific evidence was presented that would
invalidate the previous risk assessment of oilseed rape MS8, RF3 and MS8xRF3. The EFSA
GMO Panel also concludes that no new scientific data or information was provided in support
of adverse effects of oilseed rape MS8, RF3 and MS8xRF3 on the environment and on human
1 For citation purposes: Scientific Opinion of the Panel on Genetically Modified Organisms on a request from the European
Commission related to the safeguard clause invoked by Austria on oilseed rape MS8, RF3 and MS8xRF3 according to
Article 23 of Directive 2001/18/EC. The EFSA Journal (2009) 1153, 1-16.
. (minority opinion) This opinion is not shared by 0 members of the Panel. / (conflict of interest) 0 members of the Panel did
not participate in (part of) the discussion on the subject referred to above because of possible conflicts of interest.
Safeguard clause invoked by Austria on oilseed rape MS8, RF3 and MS8xRF3
according to Directive 2001/18/EC
The EFSA Journal (2009) 1153, 2-16
and animal health in Austria. Therefore, no specific scientific evidence, in terms of risk to
human and animal health and the environment, were provided that would justify the
invocation of a safeguard clause under Article 23 of Directive 2001/18/EC.
Key words: GMOs, oilseed rape (Brassica napus), MS8, RF3, MS8xRF3, Austria,
safeguard clause, human and animal health, environment, Directive
2001/18/EC
Safeguard clause invoked by Austria on oilseed rape MS8, RF3 and MS8xRF3
according to Directive 2001/18/EC
The EFSA Journal (2009) 1153, 3-16
TABLE OF CONTENTS
Panel Members ........................................................................................................................................ 1
Summary ................................................................................................................................................. 1
Table of Contents .................................................................................................................................... 3
Background ............................................................................................................................................. 4
Terms of reference as provided by the European Commission................................................................ 4
Acknowledgements ................................................................................................................................. 4
Assessment .............................................................................................................................................. 5
1. Introduction .................................................................................................................................... 5
2. Assessment of documents provided by Austria............................................................................... 5
2.1. Food and feed safety issues..................................................................................................... 6
2.1.1. Toxicological and allergenicity assessment........................................................................ 6
2.2. Environmental safety issues and post-market environmental monitoring .............................. 6
2.2.1. Environmental risk assessment........................................................................................... 6
2.2.2. Post-market environmental monitoring plan ...................................................................... 9
2.2.3. Conclusion......................................................................................................................... 9
Overall Conclusions and Recommendations............................................................................................ 9
Documentation provided to EFSA ......................................................................................................... 10
References ............................................................................................................................................. 10
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The EFSA Journal (2009) 1153, 4-16
BACKGROUND
On 15 July 2008, Austria notified to the European Commission a national safeguard clause on
genetically modified (GM) oilseed rape events MS8, RF3 and MS8xRF3 under Article 23 of
Directive 2001/18/EC. The notification was accompanied by the scientific document entitled
"Scientific arguments for an import ban of herbicide tolerant oilseed rape Ms8, Rf3 and
Ms8xRf3 (notification C/BE/96/01) in Austria".
On 31 July 2008, the European Food Safety Authority (EFSA) has received a request from
the European Commission to provide a scientific opinion from its Scientific Panel on
Genetically Modified Organisms (GMO Panel) on the statement and documents submitted by
Austria in the context of its invoked safeguard clause.
TERMS OF REFERENCE AS PROVIDED BY THE EUROPEAN COMMISSION
EFSA was requested, under Article 29(1) and in accordance with Article 22(5) of Regulation
(EC) No 178/2002, to provide a scientific opinion as to "whether, in accordance with
Article 23 of Directive 2001/18/EC, the statement and documents submitted by the Austrian
authorities comprise new or additional information affecting the environmental risk
assessment, such that detailed grounds exist to consider that the above authorised GMO, for
the uses laid down in the corresponding consent, constitute a risk to human health or the
environment".
ACKNOWLEDGEMENTS
The European Food Safety Authority wishes to thank the members of the Working Groups on
Molecular Characterisation, Food/Feed and Environment, as well as the following members
of its staff: Yann Devos, Yi Liu and Sylvie Mestdagh for the preparation of this opinion.
Safeguard clause invoked by Austria on oilseed rape MS8, RF3 and MS8xRF3
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The EFSA Journal (2009) 1153, 5-16
ASSESSMENT
1. Introduction
Directive 2001/18/EC provides the possibility for Member States to invoke safeguards on
specific genetically modified organisms in the case where new or additional information,
made available since the date of the consent, would affect the risk assessment of an authorised
GMO. Provisions foreseen by Austria seek to provisionally prohibit the marketing of oilseed
rape MS8, RF3 and MS8xRF3 for its intended uses on the Austrian territory.
The EFSA GMO Panel examined the set of supporting documents submitted by Austria. In
this respect, the EFSA GMO Panel assessed whether the submitted documents comprise new
scientific information that would change the outcome of previously performed risk
assessments, and if detailed grounds exist to consider that the authorised oilseed rape MS8,
RF3 and MS8xRF3, for its intended uses, constitute a risk to human and animal health or the
environment.
The EFSA GMO Panel looked for evidence for GMO-specific risks - including long-term
effects (e.g., BEETLE report, 2009) - taking into consideration the EFSA GMO Panel
guidance document for the risk assessment of GM plants and derived food and feed (EFSA,
2006a) as well as any related risk assessments carried out in the past. In addition, the EFSA
GMO Panel considered the relevance of raised concerns in light of the most recent scientific
data and relevant peer-reviewed publications.
2. Assessment of documents provided by Austria
A set of supporting documents, accompanying the mandate of the European Commission (see
Terms of Reference as provided by the European Commission), was forwarded to EFSA on
31 July 2008.
Austria provided the following set of documents in support of its safeguard clause:
- Austrian letter on new supplementary scientific evaluation (10 July 2008);
- Verbot des Inverkehrbringens von gentechnisch verändertem Raps aus den
Ă–lrapslinien MS8, RF3 and MS8xRF3 in Ă–sterreich;
- Scientific arguments for an import ban of herbicide tolerant oilseed rape MS8, RF3
and MS8xRF3 (Notification C/BE/96/01) in Austria.
Based on the supporting documents, several issues were identified and therefore considered
by the EFSA GMO Panel in the following two main areas: (1) the toxicological and
allergenicity risk assessment, and (2) the environmental risk assessment and post-market
environmental monitoring plan relating to the accidental spillage of oilseed rape MS8, RF3
and MS8xRF3 seeds.
Issues related to the coexistence of oilseed rape cropping systems and the adventitious
presence of authorised GM material in non-GM products were not considered, as they fall
outside the remit of the EFSA GMO Panel. In addition, the EFSA GMO Panel notes that it
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The EFSA Journal (2009) 1153, 6-16
only gives its opinion on the scientific quality of the post-market environmental monitoring
activities proposed by applicants, whilst the final endorsement thereof is done by risk
managers.
During its assessment, the EFSA GMO Panel identified issues raised by the Austrian
authorities that would require further clarifications. To present and clarify the provided set of
documents, an informal meeting between the Austrian delegation, several experts of the
EFSA GMO Panel and EFSA staff was held on 23 April 2009. A representative of the
European Commission attended the meeting as observer.
2.1. Food and feed safety issues
2.1.1. Toxicological and allergenicity assessment
The EFSA GMO Panel observes that these two publications related to toxicological and
allergenicity aspects of the risk assessment quoted by Austria (Spök et al., 2004, 2005) do not
provide new data specific on the safety of oilseed rape MS8, RF3 and MS8xRF3: current
approaches for assessing toxicological and allergenicity risks of genetically modified
organisms are questioned in generic terms. The EFSA GMO Panel emphasises that the
approach taken by the Panel in order to assess the potential toxicological and/or allergenicity
risks of GM plants is in accordance with internationally developed guidelines (e.g., Codex
Alimentarius, 2003).
Specific issues raised by Austria pertain to what they perceive as insufficient, inappropriate,
or lacking data in the dossier. Moreover, Austria points to the observed differences in
glucosinolate levels. The EFSA GMO Panel notes, however, that it has already taken the
issues raised by Austria into account in its opinion on MS8xRF3, including the acute toxicity
of phosphinothricin acetyltransferase (PAT), the safety of PAT if it would sustain food /feed
processing, and variability in glucosinolate levels. The rabbit and chicken studies mentioned
and considered inappropriate by Austria have not been included into the safety assessment of
MS8xRF3 as summarized in the EFSA GMO Panel's opinion. Again, no new data indicating
potential adverse effects of MS8xRF3 have thus been provided by Austria, whilst the data
provided do not lead the EFSA GMO Panel to diverge from its previous opinion on the
potential toxicity and allergenicity of MS8xRF3 (EFSA, 2005).
2.2. Environmental safety issues and post-market environmental monitoring
2.2.1. Environmental risk assessment
In line with its previous scientific opinions on herbicide tolerant oilseed rape GT73 (EFSA,
2004), MS8xRF3 (EFSA, 2005) and T45 (EFSA, 2008), the EFSA GMO Panel confirms that
in regions where oilseed rape is grown and/or where oilseed rape seeds are imported and
transported, feral oilseed rape populations are likely to occur in non-natural disturbed
ecosystems (such as ports, processing facilities, margins of agricultural fields, roadside
verges, railway lines, and wastelands) (Bagavathiannen and Van Acker, 2008). It is wellknown
that human activity contributes to the dispersal of plants (Wichmann et al., 2009),
especially the transport of seeds by vehicles (Zwaenepoel et al., 2006; von der Lippe and
Kowarik, 2007a,b; Garnier et al., 2008).
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In the scientific literature, the occurrence of feral oilseed rape populations has been reported
not only in Austria (Pascher et al., 2006), but also in Canada (Simard et al., 2002; Yoshimura
et al., 2006; Knispel et al., 2008), France (Pessel et al., 2001; Garnier et al., 2008; Pivard et
al., 2008a,b), Germany (Menzel, 2006; Reuter et al., 2008; Neuffer, 2009), Japan (Saji et al.,
2005; Aono et al., 2006; Kawata et al., 2008; Nishizawa et al., 2009) and the United Kingdom
(Crawley and Brown, 1995, 2004; Wilkinson et al., 1995; Charters et al., 1999; Norris and
Sweet, 2002). These populations can be large and show significant variation in size from one
year to the next (Crawley and Brown, 1995).
Due to its early germination potential and capacity to capture resources rapidly, oilseed rape
can take advantage of disturbed land (Blackshaw et al., 2003, 2004). However, successful
recruitment of oilseed rape from seed spillage from passing traffic mainly depends upon its
ability to compete for space with primary colonizers, particularly perennial grasses. In most
non-agricultural areas, oilseed rape lacks the ability to establish stable populations due to the
absence of competition-free gaps (Crawley et al., 1993; Warwick et al., 1999; Hails et al.,
2006). Once established, oilseed rape populations often become extinct after 2 to 4 years
(Crawley and Brown, 1995; Crawley et al., 2001; Norris and Sweet, 2002). If habitats are
disturbed on a regular basis (e.g., by mowing, herbicide application, soil disturbance) and
replenished with seed from seed spillage or recruitment from seeds produced by residents or
from seeds from the seedbank, then feral oilseed rape populations can persist for longer
periods (8-10 years) (Pessel et al., 2001; Pivard et al., 2008a,b). Using genetic analyses and
farmer surveys, Pessel et al. (2001) revealed that some members of feral oilseed rape
populations in road verges in France originated from varieties that had not been marketed for
at least 8 years.
Oilseed rape is generally regarded as an opportunistic species, and not as an environmentally
hazardous colonizing species (Warwick et al., 1999). Several field studies and model
predictions reported that the presence of herbicide tolerance in oilseed rape does not confer a
fitness advantage, unless the respective herbicide is applied (Crawley et al., 1993, 2001;
Fredshavn et al., 1995; Warwick et al., 1999, 2004; Norris and Sweet, 2002; Claessen et al.,
2005a,b; Simard et al., 2005; Garnier and Lecomte, 2006; Garnier et al., 2006). In the absence
of glufosinate-ammonium-containing herbicide applications, oilseed rape MS8, RF3 and
MS8xRF3 is neither more likely to survive, nor more invasive or persistent than its
conventional counterpart. Moreover, there is no evidence that tolerance to glufosinateammonium
enhances seed dormancy, and hence the persistence of feral oilseed rape
populations (Crawley et al., 1993, 2001; Claessen et al., 2005a,b; Sweet et al., 2004; Lutman
et al., 2005; Messéan et al., 2007). Because glufosinate-ammonium-containing herbicides are
not widely used in ruderal ecosystems in the European Union (EU), feral oilseed rape plants
ensuing from spilled seeds of oilseed rape MS8, RF3 and MS8xRF3 would not show any
enhanced fitness and would thus behave as conventional plants. Only where and when
glufosinate-ammonium-containing herbicides are applied, is oilseed rape MS8, RF3 and
MS8xRF3 expected to have a fitness advantage. Likewise, there are no indications that the
barstar/barnase gene complex would alter seed survival characteristics and confer a selective
advantage (Fredshavn et al., 1995; Sweet et al., 2004; Lutman et al., 2008). The scientific
information provided in the Austrian safeguard clause notification does not give any new
information regarding increased likelihood of establishment or survival of feral oilseed rape
plants in case of accidental release into the environment of oilseed rape MS8, RF3 and
MS8xRF3 seeds during transportation and processing.
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The EFSA Journal (2009) 1153, 8-16
The EFSA GMO Panel is aware that if feral oilseed rape plants derived from spilled seeds
remain uncontrolled and reproduce, they may survive, outcross and eventually disperse genes
to cross-compatible plants such as Brassica rapa and Raphanus raphanistrum (Scheffler and
Dale, 1994; Eastham and Sweet, 2002; Chèvre et al., 2004; Warwick et al., 2003, 2004, 2008;
Claessen et al., 2005b; Jørgensen, 2007; BEETLE report, 2009; Devos et al., 2009; Jørgensen
et al., 2009). Scientific evidence suggests that feral oilseed rape populations may serve as a
reservoir that could hold and return (trans)genes to cultivated populations of oilseed rape in a
different place and time, and act as a genetic bridge delivering the (trans)genes to sympatric
cross-compatible plants (Saji et al., 2005; Aono et al., 2006; Pascher et al., 2006; Yoshimura
et al., 2006; Knispel et al., 2008; Nishizawa et al., 2009). In Canadian regions where GM
oilseed rape is frequently grown (e.g., Beckie et al., 2006), feral oilseed rape populations were
shown to actively outcross with cultivated populations of GM oilseed rape and to accumulate
transgenes (Knispel et al., 2008). However, compared to cultivated oilseed rape populations,
the contribution of feral oilseed rape plants in vertical gene flow is expected to be limited:
feral oilseed rape populations are small compared to cultivated populations and contribute
little to the pollen load in the environment (Colbach et al., 2001a,b, 2005; Devaux et al.,
2005, 2007, 2008; Gruber and Claupein, 2006; Knispel et al., 2008; Colbach, 2009).
Moreover, there are no compelling data to suggest that the presence of an herbicide tolerance
trait in a wild relative changes the behaviour of the wild relative so far (e.g., Warwick et al.,
2008). In the absence of glufosinate-ammonium-containing herbicides, hybrids or wild
relatives containing the herbicide tolerance trait do not show any enhanced fitness and behave
as conventional plants. Thus escaped plants and genes dispersed to other cross-compatible
plants would not create additional environmental impacts. If needed, feral oilseed rape
MS8xRF3 and hybridised/introgressed relatives can be managed by the use of other
herbicides and/or adequate mechanical practices (Beckie et al., 2004; Devos et al., 2004;
Warwick et al., 2004; Légère, 2005; Simard et al., 2005; Gruber et al., 2008; Lutman et al.,
2008).
The environmental exposure due to GM oilseed rape grain imports is anticipated to be low, as
the amounts of viable oilseed rape seeds imported in the EU are limited with most seeds being
imported by boat and crushed in or near the ports of entry. Some of the oilseed rape seeds
imported into the EU are likely to be transported inland to Austria by boat. Moreover, some
oilseed rape seeds entering Austria are transported by road or rail to processing plants in
Austria. As indicated above, survival and outcrossing from plants derived from seed spillage
will be at very low frequencies and have no hazardous environmental consequences compared
to current feral oilseed rape populations.
In conclusion, the EFSA GMO Panel confirms that feral oilseed rape plants are likely to occur
wherever oilseed rape is cultivated and/or transported and that transgenic oilseed rape is no
exception (e.g., Saji et al., 2005; Aono et al., 2006; Yoshimura et al., 2006; Bagavathiannen
and Van Acker, 2008; Kawata et al., 2008; Knispel et al., 2008; Nishizawa et al., 2009).
However, there is no evidence that the herbicide tolerance trait introduced by genetic
engineering results in increased invasiveness of oilseed rape MS8, RF3 and MS8xRF3, except
when glufosinate-ammonium-containing herbicides are applied. As such, escaped plants and
genes dispersed to other cross-compatible plants would not create additional agronomic or
environmental impacts. This - together with the assessment that oilseed rape MS8, RF3 and
MS8xRF3 and hybridising relatives have no enhanced fitness or invasiveness characteristics
(except in the presence of glufosinate-ammonium-containing herbicides) - confirms earlier
conclusions of the EFSA GMO Panel.
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The EFSA Journal (2009) 1153, 9-16
2.2.2. Post-market environmental monitoring plan
The EFSA GMO Panel maintains its position that the scope of the post-market environmental
monitoring plan provided by the applicant complies with (1) the intended uses of oilseed rape
MS8, RF3 and MS8xRF3, which excludes cultivation, (2) the requirements of the EFSA
GMO Panel guidance document for the risk assessment of GM plants and food and feed
products (EFSA, 2006a), and (3) the EFSA GMO Panel scientific opinion on post-market
environmental monitoring (EFSA, 2006b).
European operators importing, handling and processing viable oilseed rape commodities have
recently joined with the European Association of Bioindustries (EuropaBio) in developing
monitoring systems for GM oilseed rape imported through main points of entry and
processing facilities (Lecoq et al., 2007; Windels et al., 2008). These monitoring systems are
based on Hazard Analysis and Critical Control Points (HACCP) principles. Therefore, it is
anticipated that risk managers will opt for post-market environmental monitoring of imported
oilseed rape MS8, RF3 and MS8xRF3 seeds in accordance with these arrangements.
2.2.3. Conclusion
The EFSA GMO Panel confirms its opinion that the likelihood of unintended environmental
effects as a consequence of spread of (trans)genes from oilseed rape MS8, RF3 and MS8xRF3
will not differ from that of conventional oilseed rape varieties in the context of its intended
uses. The EFSA GMO Panel agrees with the monitoring plan submitted by the applicant,
especially now that comprehensive arrangements have been made by applicants and operators
for monitoring at major points of import and processing in the EU. However, the EFSA GMO
Panel continues to recommend that appropriate management systems should be in place to
minimise accidental loss and spillage of transgenic oilseed rape seeds during transportation,
storage and handling in the environment, and processing into derived products. These
conclusions are in line with previous scientific opinions of the EFSA GMO Panel on the
import and processing of herbicide-tolerant oilseed rape GT73 (EFSA, 2004), MS8xRF3
(EFSA, 2005) and T45 (EFSA, 2008).
OVERALL CONCLUSIONS AND RECOMMENDATIONS
The EFSA GMO Panel has investigated the claims and documents submitted in support of the
Austrian safeguard clause and presented at the informal meeting between the Austrian
delegation, several experts of the EFSA GMO Panel and EFSA staff on 23 April 2009. In
these documents, the EFSA GMO Panel did not identify any new data subject to scientific
scrutiny or scientific information that would change previous risk assessments conducted on
oilseed rape MS8, RF3 and MS8xRF3 which currently has marketing consent in the EU.
Furthermore, the Austrian submission did not supply scientific evidence, that the environment
or ecology of Austria was different from other regions of the EU, sufficient to merit separate
risk assessments from those conducted for other regions in the EU.
Having considered the overall information package submitted by Austria as well as a broad
range of relevant scientific literature, the EFSA GMO Panel is of the opinion that there is no
specific scientific evidence, in terms of risk to human and animal health and the environment,
that would justify the invocation of a safeguard clause under Article 23 of Directive
2001/18/EC for the marketing of oilseed rape MS8, RF3 and MS8xRF3 for its intended uses
in Austria. In conclusion, the EFSA GMO Panel finds that the scientific evidence currently
Safeguard clause invoked by Austria on oilseed rape MS8, RF3 and MS8xRF3
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The EFSA Journal (2009) 1153, 10-16
available does not sustain the arguments provided by Austria, and therefore the EFSA GMO
Panel reiterates its previous scientific opinion on oilseed rape MS8, RF3 and MS8xRF3.
DOCUMENTATION PROVIDED TO EFSA
1. Letter, dated 31 July 2008, with supporting documents from Jos Delbeke, Acting
Director-General Environment EC, to Catherine Geslain-Lanéelle, Executive Director
EFSA (ref ENV/B3/AA/lh ARES(2008) 18278), requesting for a scientific opinion on the
safeguard notification submitted by Austria under Article 23 of Directive 2001/18/EC for
oilseed rape MS8, RF3 and MS8xRF3 and comprising the following supporting
documents:
- Scientific arguments for an import ban of herbicide tolerant oilseed rape MS8, RF3
and MS8xRF3 (notification C/BE/96/01) in Austria.
2. Letter, dated 15 October 2008, from Catherine Geslain-Lanéelle, Executive Director
EFSA to Jos Delbeke, Director-General Environment EC (ref CGL/RM/PB/SM/shv
(2008) 3369831), acknowledging the receipt of the mandate accompanied with the
supporting documents.
REFERENCES
Aono, M., Wakiyama, S., Nagatsu, M., Nakajima, N., Tamaoki, M., Kubo, A., Saji, H., 2006.
Detection of feral transgenic oilseed rape with multiple-herbicide resistance in Japan.
Environmental Biosafety Research, 5: 77-87.
Bagavathiannen, M.V., Van Acker, R.C., 2008. Crop ferality: implications for novel trait
confinement. Agriculture, Ecosystems and Environment, 127: 1-6.
Beckie, H.J., SĂ©guin-Swartz, G., Nair, H., Warwick, S.I., Johnson, E., 2004. Multiple
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