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The GM Contamination Register: a review of recorded contamination incidents associated with genetically modified organisms (GMOs), 1997–2013

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Since large-scale commercial planting of genetically modified (GM) crops began in 1996, a concern has been that non-GM crops may become contaminated by GM crops and that wild or weedy relatives of GM crops growing outside of cultivated areas could become contaminated. The GM Contamination Register contains records of GM contamination incidents since 1997 and forms a unique database. By the end of 2013, 396 incidents across 63 countries had been recorded. Analysis of the Register database reveals rice has the highest number of GM contamination incidents of all crops (accounting for a third of incidents), despite there being no commercial growing of GM rice anywhere in the world. The majority of these incidents derive from two distinct cases of contamination of unauthorised GM rice lines, LLRICE from the USA and BT63 rice from China. Maize accounts for 25% of GM contamination incidents, whilst soya and oilseed rape account for approximately 10% of incidents. Although factors such as acreage grown, plant biology, designation as a food or non food crop and degree of international trading can potentially affect the frequency and extent of contamination, it is not possible to determine which are dominant. The Register records a total of nine cases of contamination from unauthorised GM lines, i.e. those at the research and development stage with no authorisation for commercial cultivation anywhere in the world. An important conclusion of this work is that GM contamination can occur independently of commercialisation. Some of these cases, notably papaya in Thailand, maize in Mexico and grass in USA have continued over a number of years and are ongoing, whilst other contamination cases such as Bt10 maize and pharmaceutical-producing GM crops occur only with a single year. The route(s) of contamination are often unclear. The detection of GMO contamination is dependent on both routine and targeted monitoring regimes, which appears to be inconsistent from country to country, even within the EU. The lack of an analytical methodology for the detection of GM crops at the field trial stage (i.e. pre-commercialisation) can hamper efforts to detect any contamination arising from such GM lines.
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D A T A A R T I C L E Open Access
The GM Contamination Register: a review of
recorded contamination incidents associated
with genetically modified organisms (GMOs),
19972013
Becky Price
1
and Janet Cotter
2*
Abstract
Background: Since large-scale commercial planting of genetically modified (GM) crops began in 1996, a concern
has been that non-GM crops may become contaminated by GM crops and that wild or weedy relatives of GM crops
growing outside of cultivated areas could become contaminated. The GM Contamination Register contains records
of GM contamination incidents since 1997 and forms a unique database. By the end of 2013, 396 incidents across
63 countries had been recorded.
Results: Analysis of the Register database reveals rice has the highest number of GM contamination incidents of all
crops (accounting for a third of incidents), despite there being no commercial growing of GM rice anywhere in the
world. The majority of these incidents derive from two distinct cases of contamination of unauthorised GM rice
lines, LLRICE from the USA and BT63 rice from China. Maize accounts for 25% of GM contamination incidents, whilst
soya and oilseed rape account for approximately 10% of incidents. Although factors such as acreage grown, plant
biology, designation as a food or non food crop and degree of international trading can potentially affect the
frequency and extent of contamination, it is not possible to determine which are dominant.
The Register records a total of nine cases of contamination from unauthorised GM lines, i.e. those at the research
and development stage with no authorisation for commercial cultivation anywhere in the world. An important
conclusion of this work is that GM contamination can occur independently of commercialisation. Some of these
cases, notably papaya in Thailand, maize in Mexico and grass in USA have continued over a number of years and
are ongoing, whilst other contamination cases such as Bt10 maize and pharmaceutical-producing GM crops occur
only with a single year. The route(s) of contamination are often unclear.
Conclusions: The detection of GMO contamination is dependent on both routine and targeted monitoring
regimes, which appears to be inconsistent from country to country, even within the EU. The lack of an analytical
methodology for the detection of GM crops at the field trial stage (i.e. pre-commercialisation) can hamper efforts to
detect any contamination arising from such GM lines.
Keywords: Genetically modified; Contamination; Gene flow; Crops; Food; Feed; Field trial
* Correspondence: janet.cotter@greenpeace.org
2
Greenpeace Resaerch Laboratories, Innovation Centre Phase 2, University of
Exeter, Exeter EX4 4RN, UK
Full list of author information is available at the end of the article
© 2014 Price and Cotter; licensee Springer. This is an Open Access article distributed under the terms of the Creative Commons
Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction
in any medium, provided the original work is properly credited.
Price and Cotter International Journal of Food Contamination 2014, 1:5
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Background
Large scale commercial planting of genetically modified
(GM) crops began in 1996. Alongside concerns regard-
ing the long term health, environmental and socio-
economic impacts of these crops, a specific concern has
been that of contamination of non-GM crops by GM
crops and also of relatives established outside planted
areas. Concerns regarding GM contamination of non-
GM crops include loss of markets, particularly those re-
quiring GM-freeproducts; future supply of non-GM
seed (especially for seed saved from open pollinated
crops) and possible introgression (spreading) of the GM
trait into both wild and feral populations of crop rela-
tives (Marvier and van Acker 2005; Mellon and Rissler
2004; Bauer-Panskus et al. 2013).
Contamination of non-GM crops by GM crops has oc-
curred, and there are several well-documented cases, e.g.
Starlink corn (Fox 2001), Liberty Link rice (LLRICE; US
Food and Drug Administration 2006). Reviews of GM
contamination by Marvier and van Acker (2005) and
Bauer-Panskus et al. (2013) considered that there are
many factors contributing to the likelihood of GM con-
tamination, and that containment of any contamination
can be problematic, even unlikely. For example, Marvier
and van Acker (2005) considered of the movement of
transgenes a virtual certainty via routes such as gene flow
during cultivation, reintroduction of transgenes from
volunteer and feral crop populations, seed transport
(including between continents) and human error such as
co-mingling of seed. Bauer-Panskus et al. (2013) consid-
ered that domestication and ease of hybridization with
wild or weedy relatives important factors. Possible envir-
onmental consequences of introgression of transgenes into
wild or feral population include increased invasiveness as
a result of a fitness enhancing trait such as insect resist-
ance (Snow et al. 2003; Samuels 2013), reduced capacity
for co-existence of GM and non-GM crops (Marvier and
van Acker 2005) and hampering future breeding efforts
(Bauer-Panskus et al. 2013). However, Ellstrand (2012)
found that transgene escape to wild varieties was rare, but
that transgenes tended rather to move into other varieties
of the same species.
The United Nations (UN) Cartagena Protocol on Bio-
safety to the Convention on Biological Diversity partly
addresses the control of living genetically modified or-
ganisms (GMOs) (termed living modified organisms
within the convention), covering seeds (UN Cartagena
Protocol on Biosafety 2014). In 2002, this established an
advance informed agreement procedure meaning that
only those living GMOs (primarily seeds) with formal
approval from the receiving countrys national body can
be imported. In addition to the UN Cartagena Protocol,
many governments around the world, including the
European Union (EU), have established national regulatory
regimes that issue formal authorisation (or, in the USA,
deregulation) for any deliberate release of GMOs into the
environment (i.e. outside of laboratory containment) and
marketing as seed, human food and animal feed products.
Specific GMOS may be authorised either as experimental
field trials (e.g. for testing of agronomic traits), for com-
mercial cultivation and for marketing as human food and/
or animal feed. Authorisations can be granted for a GMO
to be marketed without cultivation, e.g. if the GMO is to
be imported into a country, but not grown. Databases of
authorisations for the cultivation and marketing of GMOs
are available both globally (Center for Environmental Risk
Assessment 2014) and also for certain regions such as the
EU (EC 2014a). In contrast, databases for experimental
field trials of GMOs are held by national or regional
authorities, e.g. for the USA (Information Systems for
Biotechnology 2014), Australia (Office of the Gene
Technology Regulator 2014), the European Union
(EC 2014b). In many countries, such databases do not
exist, or are not publically available.
The presence of globally unauthorised GMOs (i.e.
those without any authorisation for cultivation or mar-
keting anywhere in the world) and unapproved GMO
crops (i.e. those without authorisation for cultivation
and/or marketing in that country or region) in food/feed
or seed can be grounds for either product recalls or re-
jection of imports at national borders. Where labelling
of GMO ingredients is mandatory (e.g. the EU for food/
feed), the presence of GMO ingredients in unlabelled
foodstuffs above a prescribed threshold (0.9% for the EU,
EC 2003) is also grounds for either rejection of imports
or product withdrawal. Labelling is not required for GM
non food products (e.g. biofuels or materials such as cot-
ton) in the EU (EC 2003). Global organic farming stan-
dards require that both seed and food are free from
GMOs (International Foundation for Organic Agricul-
ture Movements 2002) and many national organic farm-
ing bodies have defined thresholds of the maximum
permitted adventitious GMO content (usually between
0.1% and 0.9%). The presence of GMOs above permitted
thresholds can result in loss of organic certification.
Methodologies for the detection of GMOs fall into
two broad categories: protein-based methods which tar-
get the novel protein(s) produced by the GMO and de-
oxyribonucleic acid (DNA)-based methods which target
the inserted genetic construct(s). Protein-based methods
typically employ an enzyme-linked immunosorbent assay
(ELISA). Commercially-available ELISA kits comprise ei-
ther qualitative immunochromotographic (lateral flow)
strips, which can be used both in the field and labora-
tory, or well plates enabling quantitative analysis. In con-
trast, DNA-based methods utilise polymerase chain
reaction (PCR) and require a specialised laboratory set
up. The EC Joint Research Centre (JRC) has developed
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and validated methods for the detection and quantifica-
tion of individual GMO events (EC JRC 2010, 2014a)
and run international collaborative programmes, pre-
dominantly with governmental laboratories, to increase
harmonisation and standardisation of methodologies for
analysing GMOs (EC JRC 2014b). In practice, protein-
based methods (especially qualitative assays) tend to be
used to screen for the presence of GMOs (Ermolli et al.
2006), whilst DNA-based methods offer more robust
analysis (Miraglia et al. 2004).
Despite the concerns regarding GM contamination,
there is no systematic global monitoring or recording of
GM contamination incidents. In the EU region, however,
recording of GM contamination incidents in food/feed
products is afforded by the European Commission (EC)
Rapid Alert System on Food and Feed (RASFF) (EC
RASFF 2014). RASFF members consist of the European
Union countries together with Iceland, Liechtenstein,
Norway and Switzerland. To date, the RASFF provides
the most comprehensive data set of GM contamination
in food/feed provided by a national or regional regula-
tory body. Along with other food contaminants, the
RASFF records positive results on its website (EC
RASFF 2014) for unapproved GM ingredients in food/
feed products both from within the EU region and im-
ports into the EU region. Outwith the RASFF, individual
incidents of GM contamination are generally reported
via national governments, non governmental organisa-
tions (NGOs) and/or the media.
In the absence of global systematic monitoring of GM
contamination incidents, GeneWatch UK and Greenpeace
International established the GM Contamination Register
(hereafter termed The Register) to record these inci-
dents. The website (GM Contamination Register 2014) is
a searchable database used by individuals, public interest
groups and governments. It is recognised by the UN Bio-
safety Clearing-House, an information exchange facility
for the Cartagena Protocol. The Register now holds a
database of recorded incidents of GM contamination over
17 years, from 1997 to the present time. This paper pre-
sents an analysis of the recorded incidents from 1997 to
the end of 2013. We investigate the frequency of GM con-
tamination incidents over this period, the principal crops
and countries associated with these incidents and focus on
contamination arising from unauthorised GM crops. Fi-
nally, we investigate the contribution of the contribution
of analytical methodologies and monitoring regimes to the
detection of GM contamination incidents.
Methodology
The GM Contamination Register is based on individual in-
cidents reported by governmental and inter-governmental
authorities, non governmental organisations (NGO)s and/
or the media. Monitoring English speaking media, science
journals and internet-based news groups provides alerts to
these incidents. Organisations testing for the presence of
GMOs (such as NGOs) are invited to send their results to
the Register. Coverage is global, and GM animals and
plants are included. GM microbes are not excluded, al-
though there have been no recorded incidences of con-
tamination by these organisms to date. The Register
commenced in 2005, was backdated to 1997. The Register
is still active although only those incidents recorded to the
end of 2013 are included here.
Each report of a contamination incident is evaluated for
its dependability. The Register includes only incidents
where the contamination can be verified to a reasonable
degree of certainty. That is, either an announcement by a
producer of a GM crop, a governmental body or from
an NGO based on the identification of the GM crop
resulting from PCR analysis. The PCR methodologies
need to be accredited to the International Organization
for Standardization (ISO), i.e. ISO standard 17025
(ISO 2005) and this usually entails contracting analysis
to a commercial or governmental laboratory. GM con-
tamination incidents based on protein testing are ex-
cluded from the Register. Incidents reported via the
RASFF are regarded as verified as they originate from
government bodies. Similarly, those published in peer
reviewed journals are also regarded as verified. Where
the incident is announced by an NGO, copies of PCR
results are requested as verification.
Where an incident cannot be verified from original or
governmental sources, it is accepted for the Register if the
reportage is via a reputable newspaper or news agency,
preferably an international agency such as Reuters or
Agence France-Presse. Such cases are reviewed after one
year and internet searches are made for further evidence.
In cases where the contamination findings are refuted or
reasonable doubt cast on them, the incident is removed
from the Register until any new evidence emerges.
For inclusion in the GM Contamination Register, inci-
dents must meet at least one of the following criteria:
a breach of national or international law; sale of
food/feed derived from GMOs that does not comply
with regional or national labelling regulations,
presence of unauthorised or unapproved GMO
traits in crops and/or seed batches or, for approved
GMO traits, presence above applicable thresholds,
illegal plantings of GMOs or unauthorised releases
to the environment or food/feed chain.
establishment of feral population(s) of a GM crop or
presence of the genetic insert within wild or feral
populations, including wild or weedy relatives.
If a GM incident has been verified and fulfils one of
the criteria, brief details of the contamination incident
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(generally what, where, when and, if known, the source
and route of contamination) are entered into the data-
base. Only incidents that have been publicly documented
are recorded on the Register. The Register does not, and
cannot, record incidents that remain undetected. There-
fore, those reported here represent the minimum num-
ber of GM contamination incidents.
The nature of GM contamination is such that once a
single contamination incident has been identified, test-
ing and monitoring can quickly result in the identifica-
tion of several more contamination incidents involving
the same GM line, often within the same month or year.
In addition, international trading of agricultural com-
modities can result in repeated findings of contamin-
ation by the same GM line in many countries within the
same year. These are termed repeated contamination
incidents and could skew the Register towards particu-
lar GM lines that are frequently tested for, or countries
that conduct more thorough monitoring. To avoid this,
the Register only records a new incident each time a
GM line is found to be present within a country in a
particular year. If the same GM line repeatedly contami-
nates within the same country and in the same year, no
new incident is recorded and details are added to the
existing incident instead. This enables the Register to
indicate the extent of spread, both geographically and
over time, of any given contamination episode whilst
minimising any skew towards repeated contamination
incidents.
Results and Discussion
As of 31 December 2013, the Register had recorded 396
incidents since 1997 (i.e. over a period of 17 years) and
across 63 different countries (Additional file 1). Since 2000,
there have been more than 10 incidents per year and, since
2005, more than 20 incidents per year (Figure 1). For 2006,
there is a sharp spike in the number of incidents to nearly
60. This spike primarily relates to the discovery and spread
of GM rice from the USA, which accounted for 28 inci-
dents that year.
GM contamination incidents by country
The distribution of the total number of GM contamin-
ation incidents over the 17 year period by country dis-
plays an exponential decay type of pattern with a sharp
initial decrease from the highest number of incidents
per country and a long tail of countries with a much
lower number of incidents (Figure 2). 50% of the total
number of incidents are accounted for by 11 countries,
each with more than 12 incidents. This group is domi-
nated by RASFF countries, together with North America
and Australia. In contrast, 28 countries (just under half
the total number of countries) with 3 or less reported in-
cidents account for just under 10% (9.1%). The remain-
der of the RASFF countries, several Asian countries,
South Korea, China and Mexico recorded between 3 and
12 incidents per country.
The 4 countries reporting the highest number of inci-
dents were Germany, USA, France and United Kingdom,
three of which contribute to the RASFF. Together, these
countries make up 27% of the total number contamination
incidents. This does not correspond to the countries with
the highest acreage of GM crops, which are USA, Brazil,
Argentina and Canada (International Service for the Ac-
quisition of Agri-biotech Applications 2013).
The RASFF database accounts for a significant number
of incidents in the Register, approximately 60% (244 out
of 396) (Figure 3). The importance of recording repeated
contamination events associated with the same GM line,
within the same year and same country as one incident
is illustrated by RASFF. If each notification for RASFF
were included on the Register, they would account for
nearly 80% of the total number of incidents (585 out of
736), dominating the Register and producing a skew
Figure 1 Total number of incidents recorded on the GM Contamination Register for all countries per year, 19972013.
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towards these repeated contamination events. The promin-
ence of GM contamination incidents recorded for the EU
via RASFF does not necessarily reflect a higher degree of
GM contamination. It is more likely that there is routine
monitoring and a mechanism for reporting such incidents.
GM contamination by crop
Rice is associated with the highest number of GM con-
tamination incidents of all crops (Table 1), accounting
for about a third of the total number of incidents. This
is despite a global absence of any commercial cultivation
of GM rice. There is a sharp peak in the number of inci-
dents of GM rice contamination for 2006/7 (Figure 4).
The majority of these incidents derive from two distinct
cases of contamination from unauthorised GMOs, one
in the USA (LLRICE) and one in China (Bt63) and are
further discussed in the section on globally unauthorised
GM crops below. GM maize gives rise to the second
most number of contamination incidents, accounting
for a quarter of incidents (Table 1) with consistent con-
tamination of between 5 and 10 incidents per year since
1999 (Figure 4). Soya and oilseed rape (canola) are the
next most frequently associated with GM contami-
nation, each accounting for approximately 10% of inci-
dents (Table 1) with between 0 and 10 incidents per
year (Figure 4).
Figure 2 Total number of incidents recorded on the GM Contamination Register per country, for all years 19972013.
Figure 3 Comparison of GM Contamination Register with the EC RASFF database by country, for all years 19972013. EC RASFF
database records notifications for each incident, including those relating to a single GM line in the same country and year. In the GM
Contamination Register, these are recorded as a single incident, resulting is a lower total no. of incidents for each RASFF country. This prevents a
skew of the data towards RASFF countries and the reportage of repeated incidents.
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The acreage of a GM crop has potential to influence
the number of contamination incidents because it could
increase the opportunities for cross-pollination and co-
mingling with non-GM seed/grain. International trading
of a crop could also affect the number of incidents as
many reported GM contamination incidents originate
from national border checks. Maize, soya and oilseed
rape are all major commodity crops and also the princi-
pal GM feed/food crops that are commercially grown.
GM varieties are widely grown in many countries where
they are authorised for cultivation. For example, in the
USA, where GM crops were first cultivated, GM crop
acreage accounted for 93% of all soya and 90% of corn
in 2013 (USDA Economic Research Service 2014). A
pilot study in the US found that DNA derived from GM
crops was found in 50% of non-GM varieties of corn
and soy, and 83% of non-GM oilseed rape (Mellon and
Rissler 2004). Although these findings are not regarded
as contamination because no regulations have been in-
fringed, it demonstrates that GMO traits are widespread
in the USA. These GMO traits can enter into non-GM
crops destined for export to countries/regions where
they may not be approved or require labelling (e.g. the
EU).GMcottonwasalsowidelygrownintheUSAin
2013, accounting for 90% of the crop acreage but only
accounting for < 4% of contamination incidents. This
may be because it is a non food crop, and therefore not
subject to labelling in the EU or inclusion in the RASFF.
In contrast, the acreage of GM rice grown is extremely
small, amounting only to field trials. However, rice is a
highly traded commodity crop, with approximately 1.2
million tonnes imported into the EU during 2012/3
(EC 2013). In addition, there has been specific monitor-
ing for unauthorised GM varieties in many countries
post 2006, when the unauthorised cases of contamin-
ation were discovered. These two factors could have
contributed to the high number of contamination inci-
dents associated with GM rice, despite the global ab-
sence of commercial growing.
Plant biology, and specifically the tendency to out-
cross, is a factor that could affect the number of GM
contamination incidents. GM maize is reported as
medium to highrisk and oilseed rape as highrisk for
pollen mediated gene flow (Eastham and Sweet 2002)
and this may also contribute to the high number of
Table 1 Total number of incidents recorded on the GM
Contamination Register for each crop for all countries
and all years, 19972013
Crop No. of incidents % Total no. of incidents
Rice 134 34
Maize 98 25
Oilseed rape/canola 40 10
Soybean 37 9
Flax 26 6.5
Papaya 18 4.5
Cotton 14 3.5
Fish 5 1.3
Grass 4 1
Pigs 4 1
Sugar beet 4 1
Arabidopsis thaliana 3 0.75
Potato 2 0.5
Alfalfa 1 0.25
Plum 1 0.25
Tomato 1 0.25
Wheat 1 0.25
Zucchini 1 0.25
Pollen in honey* 1 0.25
Cherry, kiwi & olive trees** 1 0.25
Total 396
*Pollen from GM corn, oil seed rape & soya was found in honey imported into
Switzerland (Greenpeace 2009).
**Experimental field trials of these GM trees exceeded the length of permit in
Italy and are recorded together as one incident (Genetic Rights
Foundation 2012).
Figure 4 Incidents of GM contamination for rice, maize, oilseed rape (canola) and soya for all countries per year, 19972013.
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incidents reported for these two crops, but wouldntbe
a strong factor for cotton and soya. Gene flow from GM
rice, despite being regarded as a largely self pollinating
crop, has been recorded, albeit at low levels and over
short distances (Rong et al. 2007). Although factors
such as acreage grown, plant biology, designation as a
food or non food crop and degree of international trad-
ing can affect the number of contamination incidents
recorded, it is not possible to determine from these data
which are dominant. Indeed, for rice, the specific moni-
toring for unauthorised varieties of GM rice may to be
an additional factor.
For maize and canola, there has been much international
interest in specific cases of GM contamination, notably
those associated with Starlink maize, maize in Mexico and
establishment of feral GM oilseed rape populations. GM
Starlink maize was only authorised for use in animal feed in
1998 (Bucchini and Goldman 2002, US Environmental
Protection Agency 2008) but was found in USA food
products intended for human consumption in 2000 by a
coalition of non governmental groups (Fox 2001). The
contamination persisted in the US at least until 2003,
despite efforts to recover Starlink seed (Marvier and
van Acker 2005). Starlink maize was the first contami-
nation case with international ramifications. Contami-
nation incidents were reported in 6 further countries
(Bolivia, Canada, Egypt, Guatemala, Japan and South
Korea) during both 2000 and 2001. Starlink was also re-
ported in food aid to Bolivia in 2004 (Meridian Institute
2002) and present in foods in Saudi Arabia in 2009 and
2010 (Elsanhoty et al. 2013).
In Mexico, GM contamination of open-pollinated trad-
itional varieties or landraces of maize was initially reported
in a highly controversial publication in 2001 (Quist and
Chapela 2001). The contamination was thought to origi-
nate from imports of GM maize from North America.
The GM contamination was not detected in a 2003/4
study (Ortiz-Garcia et al. 2005) but later studies (Piñeyro-
Nelson et al. 2009; Dyer et al. 2009) did find GM contam-
ination of landraces. It is now generally accepted that GM
transgenes are present in at least some maize landraces in
Mexico (Dalton 2008, Snow 2009).
The establishment of feral populations of GM oilseed
rape in both Canada and Japan has recently been reviewed
in-depth by Bauer-Panskus et al. (2013). They describe
that, in Canada, two types of feral GM oilseed rape popu-
lations conferring tolerance to two different herbicides,
glufosinate ammonium (trade name: Liberty or Basta) and
glyphosate (trade name: Roundup) occur in provinces
where they are widely grown, or through which the grain
is transported. In places, these have hybridized to be toler-
ant to both herbicides. In Japan, cultivation of GM oilseed
rape is minor, but much oilseed rape is imported from
Canada. Feral populations of GM oilseed rape tolerant to
glufosinate, glyphosate or both have been reported in and
around Japanese ports.
Globally Unauthorised GMOs
Several of the GM contamination incidents recorded on
the Register are associated with unauthorisedGM
lines. That is, lines that were not authorised for com-
mercial cultivation or marketing anywhere in the world
at the time of the contamination incident but were ex-
perimental, or in development. Thus, risk assessments
for food/feed and environmental safety have generally
not been performed. Contamination incidents involving
unauthorised GM lines tend to have a higher media pro-
file than incidents originating from approved GM lines
because of their disruptive effects on trade, as well as in-
creased food and environment safety concerns (Holst-
Jensen 2008) because of the lack of risk assessment.
Hence, these incidents are further described.
GM Rice
Two unauthorised GM contamination cases account for
128 of the 133 rice incidents on the Register. These are
LLRICEfrom the United States and Bt63 ricefrom
China.
In April 2005, Greenpeace announced that they had
evidence of illegal sales and cultivation of unauthorised
GM rice in the Hubei province of China (Greenpeace
2005; Zi 2005). Field trials of insect resistant GM rice
Bt63 had been carried out in this province for a number
of years (Tu et al. 2000, Huang et al. 2005). In 2006, GM
rice continued to contaminate food products in China,
including baby foods produced by Heinz (Greenpeace
2006a). Bt63 also started to be detected in Europe, with
Greenpeace, Friends of the Earth and European govern-
ments announcing it had been identified in imported
products in Austria, France, UK and Germany. This led
to 5 recorded incidents on the Register for 2006
(Figure 5). In 2007, the contamination was also identi-
fied in products imported into further countries with re-
ports coming from Japan, Cyprus, Germany, Greece,
Italy, Sweden and the UK.
In 2008, the EU Commission announced emergency con-
trols on all rice products from China to prevent imports
of unauthorised GM rice (EC 2008, Huggett 2008) with
further measures imposed 3 years later (EC 2011). These
restrictions require consignments to be certified as not
containing GM rice and imports to be subjected to
sampling and document checks at the EU port of entry.
Although Figure 5 does not show any reduction in GM
contamination incidents as a result of these EU mea-
sures, it is possible that this is an artefact of increased
monitoring, which could have resulted in a greater
detection of GM contamination.
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In the USA, two varieties of glufosinate-tolerant GM
rice, LLRICE62 and LLRICE06, were authorised for cul-
tivation and marketing (i.e. afforded deregulated status)
in 2000 (Center for Environmental Risk Assessment
2014). These GM varieties have never been grown com-
mercially. A separate glufosinate-tolerant line of GM
rice, LL601, was under development by Bayer Crop
Science until development (and field trials) ceased in
2001. In August 2006, the 2005 crop of (non-GM) rice
in the USA was contaminated with LLRICE601 (US
Food and Drug Administration 2006). Following the an-
nouncement, LLRICE601 was given deregulated status in
the US (Center for Environmental Risk Assessment 2014).
However, at the time of contamination it was unautho-
rised for cultivation and marketing anywhere the in the
world. Further, in March 2007, the United States Depart-
ment of Agriculture (USDA) confirmed that rice line had
become contaminated with yet another unauthorised GM
rice line LLRICE604, also developed by Bayer Crop Sci-
ence (USDA 2007). However, LL604 does not appear to
have caused as widespread contamination as LL601.
The Register data show how, following the initial an-
nouncement in the USA, LLRICE (predominantly LL601)
was discovered in 28 countries around the world including
EU member states, Sierra Leone, Ghana, Philippines,
Kuwait, Mexico and United Arab Emirates, all during
2006. The following 3 years show a rapid fall off rate
(Figure 5) but despite this, 6 years elapsed from discovery
of the contamination to the last recorded case in 2011.
The two cases of GM rice contamination both caused
disruption to international trade but have different his-
tories of contamination rates (Figure 5). Chinese Bt63
continues to be detected in EU imports from its initial
discovery in 2005 through to 2013. US LLRICE, how-
ever, saw a rapid decline in incidents from 20062009
with few cases after this date. This may possibly repre-
sent an ease of halting the GM contamination and/or
differing monitoring regimes, although these data do not
allow further speculation.
There are 5 incidents of GM contamination of rice
other than LLRICE and Bt63 (Figure 5). Of these, 4 inci-
dents relate to GM contaminated basmati rice either in,
or imported from, India and Pakistan and 1 relates to
GM contaminated animal feed imported from the USA.
GM grass
Between 1999 and 2005, Scotts company conducted field
trials of GM creeping bentgrass (Agrostis stolonifera),
tolerant to the herbicide glyphosate in the USA. How-
ever, the USA Animal and Plant Health Inspection Ser-
vice (APHIS) found that the company failed to prevent
escape of the GM grass during 2003 (US APHIS 2004)
and had failed to remove immature seed heads in 2005
(US APHIS 2007a). Gene flow from GM bentgrass can
occur over large distances and has been detected over
21 km from source (Watrud et al. 2004). The GM bent-
grass was found to have established in non agronomic
habitats up to 3.8 km away from an Oregon field test
site (Reichman et al. 2006). GM bentgrass remains
present in uncultivated habitats in Oregon (Charles
2011) and has hybridised with a naturalised grass species
(Zapiola and Mallory-Smith 2012). This is an ongoing
case of GM contamination and, because of the nature of
grass pollen and seeds, it may prove difficult to contain
and eradicate (Reichman et al. 2006, Charles 2011).
Pharmaceutical-producing GM crops
In 2001, ProdiGene conducted field trials in Iowa, USA
of GM maize producing a vaccine against a pig disease.
In September 2002, government inspectors discovered
Figure 5 Frequency of GM contamination of rice 20052013. Number of incidents recorded on the GM Contamination Register for all
countries per year for three unauthorised GM rice cases: US LLRICE; Chinese Bt63 and other, comprising principally GM contaminated basmati
rice either in, or imported from, India and Pakistan.
Price and Cotter International Journal of Food Contamination 2014, 1:5 Page 8 of 13
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volunteer maize plants growing in a soybean field that
was used as a test site for the experimental GM maize in
2001 (US APHIS 2002). Additionally, because the GM
maize volunteers may have pollinated neighbouring
commercial maize fields, all maize seed and plant mate-
rial within 1,320 ft (400 m) of the previous years test
plot was destroyed (US APHIS 2002). At a second site in
the same year, APHIS destroyed 500,000 bushels (esti-
mated value US$2.7 million) after soya from a field con-
taining volunteer GM maize was harvested and mixed
with other soya (US APHIS 2002).
In 2004, volunteer GM pharmaceutical corn was again
found growing and flowering within the fallow zone sur-
rounding a field trial site and in a nearby sorghum field.
The company destroyed all maize volunteers within the
1 mile (1,610 m) isolation zone, and to plough under the
sorghum field (US APHIS 2007b).
A further incident of contamination involving
pharmaceutical-producing GM crops occurred in
March 2008. The Belgium competent authorities noti-
fied the EC RASFF that traces of a protein derived from
unauthorised GM Arabidopsis thaliana in a food sup-
plement. The transgenic protein was intended to be
used in the measurement of vitamin B12 in laboratory
medicine (Bor et al. 2003), and not intended as a food
supplement. The product had been imported into Belgium
from Denmark.
GM Papaya
Several different lines of GM papaya resistant to papaya
ringspot virus (PRSV) have been under development
in tropical regions. However, only two have been
authorised for commercial growing, both in the USA
(Center for Environmental Risk Assessment 2014). A total
of 18 cases of GM contamination have, however, been
recorded on the Register. These relate to contamination
arising from the development of GM papaya resistant to
PRSV in Taiwan and Thailand. Papaya is a widely grown
in these two countries, both domestically and for export.
Neither country has ever authorised GM papaya for
cultivation.
In 2003, GM papaya resistant to PRSV was discovered
growing on Taiwanese farms and for sale in local market
places (Yu-Tzu 2003). Japan halted Taiwanese papaya
imports and the Taiwanese government imposed a ban
on GM papaya. The government warned that anyone
found growing or selling such fruits could face a fine,
and reiterated this warning in 2006 (Taiwan News 2006).
The origin of the experimental GM papaya is thought to
be government agricultural laboratories developing GM
papaya resistant to PRSV.
A similar case of GM papaya contamination arose in
Thailand. GM papaya has not been authorised for culti-
vation in Thailand. In 2004, however, Thai government
officials confirmed a Greenpeace finding of the presence
of GM papaya in famersfields (Davidson 2008). A
government research station had been developing GM
papaya resistant to PRSV, including conducting field tri-
als, but was also selling (non-GM) seed to farmers. Gov-
ernment testing found a sample of sold seed which
contained GM papaya. This selling of GM contaminated
seed is thought to be the source of the contamination
(Davidson 2008). 85 north-eastern farmers were found to
have inadvertently grown GM papaya in 2004 (Greenpeace
2006b) when the government ordered the destruction of
all GM papaya plants, including the field trial. In 2005,
GM papaya was found in more regions of Thailand
(Greenpeace 2006b).
GM papaya was also detected in Thai exports of pa-
paya. The Register records 11 RASFF alerts for GM pa-
paya entering the EU since 2007, with 4 incidents
recorded in 2012, and 12 in 2013. GM contamination in
Thai papaya appears to be either ongoing. With the ex-
ception of Japan, no countries outwith RASFF have re-
ported GM contamination from Thai papaya imports
but it is not clear what, if any, inspection regimes exist.
GM Maize Bt10
The first case of an unauthorised GM line contaminating
international food supplies was recorded in 2005. Syn-
genta had produced two types GM maize lines, Bt10 and
Bt11 with two traits, insect-resistance and herbicide tol-
erance. Only one Bt11 maize was eventually com-
mercialised. However, Syngentas quality control systems
had apparently failed to detect Bt10 seeds had been con-
taminating commercial stocks of Bt11 for 4 years prior
to the discovery (Macilwain 2005). Despite this, the case
gave rise to only 4 incidents on the Register, primarily
because the EU commission made a report on behalf of
the whole of the EU. No incidents are recorded for Bt10
contamination beyond 2005.
GM Linseed (Flax)
GM linseed (or flax) line FP967, named Triffid,was
developed by a public research institution in Canada. It
was authorised for commercial use in both Canada and
the United States in the late 1990s. However, Triffid GM
seed was never sold for commercial production and, in
2001, Triffid was de-registered and it was believed that
all known stocks had been identified and destroyed
(Canadian Grain Commission 2010, Ellstrand 2012).
In September 2009, Germany found unauthorised
genetic material in linseed imported from Canada (EC
RASFF 2009), which was subsequently confirmed as
Triffid. This led to further testing for GM contamin-
ation of linseed and in 2009 the Register recorded a
total of 16 incidents in Canada and 15 in the RASFF
countries. In 2010, there were 8 incidents recorded on
Price and Cotter International Journal of Food Contamination 2014, 1:5 Page 9 of 13
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the RASFF and a further one recorded in 2011. Positive
test results were found in Canada 20092011. The
levels of GM contamination were reported as falling
during these years (Franz-Warkentin 2011) and ongoing
efforts include encouraging producers to grow only li-
cenced flax varieties that are free of GM contamination
(Flax Council of Canada 2014).
GM wheat
One case of GM wheat contamination has been reported
(Table 1). In 2013, an Oregon farmer noticed that some
volunteer wheat did not die-back as expected when
sprayed with glyphosate. Analysis by Oregon State Univer-
sity and the USDA determined these volunteers to be a
glyphosate tolerant GM wheat line, MON71800 (USDA
2013). Although MON71800 was passed for food and feed
consumption in the USA in 2004 (Center for Environmen-
tal Risk Assessment 2014), it is included here as the deve-
lopment of the GM wheat line was discontinued in 2004
(Monsanto 2004) and the application for commerciali-
sation (deregulation) was withdrawn. Exports of wheat
from the USA where disrupted whilst testing took place
(USDA 2013), but no detection of GM wheat has been re-
ported by importer countries. To date, the route of this
contamination is unknown but it appears to be an isolated
incident.
GM animals
The Register records 4 incidents (one per year 2001
2005) where experimental GM pigs have entered into
the food or feed supply unauthorised. These are either
accidentally comingled with non-GM livestock at the abat-
toir, sometimes due to mislabelling or, in one case, deliber-
ately stolen (Westphal 2001). Rather than an environmental
release, these are an unauthorised entry of a GMO into
food or feed. No incidents of contamination of GM fish or
insects have been recorded on the Register to date. On the
whole, terrestrial GM livestock are considered less prone to
escape and establishment of feral populations than GM fish
or insects (National Research Council 2004). Especially,
experimental GM livestock tend to be kept in animal
houses, rarely allowed into an open environment and each
individual is tagged and monitored. However, these cases
suggest that these too can cause GM contamination.
Detection and monitoring of GM contamination
The Register records only reported and/or verified inci-
dents of GM contamination. As such, the Register does
not represent all contamination incidents that have
taken place globally. There are undoubtedly other GM
contamination incidents that remain undetected or un-
reported. This could be because it is not possible to de-
tect the GMO, that monitoring for GM contamination
either does not take place or is insufficient to detect all
or many GM contamination incidents and/or that GM
contamination is not reported.
The RASFF is the only database which systematically
records GM contamination events but is only for the EU
region. The high number of incidents documented on
the Register from RASFF (approximately 60% of the
total) demonstrates its effectiveness. Nevertheless, the
RASFF database is the product of national monitoring,
and dependent on the effectiveness of national monitor-
ing regimes for monitoring GM contamination. The high
number of events recorded by the RASFF countries of
Germany, France and United Kingdom may reflect more
efficient monitoring programmes, rather than a high
number of products or imports containing unapproved
GMOs.
GMO detection relies on the establishment of an ana-
lytical methodology specific to that GMO, e.g. the PCR
methodologies collated by the EC JRC (EC JRC 2010,
2014a). Any contamination by unauthorised GMOs,
such as those in experimental field trials, may not be
readily detectable, as most (if not all) national regulatory
authorities do not require companies to submit an ana-
lytical methodology for detection of the test GM crop
when seeking approval for field trials. The lack of an
analytical methodology can make detection of GM con-
tamination extremely difficult, if not impossible. PCR
screening for elements that are common to many GM
crops (e.g. the cauliflower mosaic virus promoter, CaMV
35S) can indicate of whether GM material is present.
However, it does not allow identification of the gene that
confers the trait, which is necessary to identify the spe-
cific GM line. For example, whilst detection methodolo-
gies are now available for both LLRICE and Chinese
Bt63 (EC JRC 2014a), these were not available until after
the GM contamination had been reported. For the cases
of pharmaceutical-producing GM crops, no detection
methodology is available. Thus, it would not be possible
for any third party to monitor for the presence/absence
of these GM crops in subsequent crop harvests, if con-
tamination was suspected.
The Register reports cases of contamination from un-
authorised GM crops. These cases include LLRICE, Bt63
rice, grass, pharmaceutical maize, papaya, and Bt10
maize all of which were at the research or development
stage, and Triffid linseed and wheat which had under-
gone some safety assessment, but were not authorised
for cultivation. These nine cases clearly show that GM
contamination can occur independently of commercial-
isation, e.g. escapes from field trials or illegal plantings.
Once a GM contamination incident has been detected,
this often leads to monitoring specifically for the associated
GM line and can result in a high number of incidents im-
mediately after the initial discovery (e.g. LLRICE). This can
lead to a sharp increase in the number of contamination
Price and Cotter International Journal of Food Contamination 2014, 1:5 Page 10 of 13
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incidents per year for that crop, e.g. as seen for rice in
2006/7. The pattern of GM contamination incidents
varies a great deal between cases. For example, the cases
of Bt10 and all pharmaceutical GM crops cases only ex-
tend over a year. Starlink, LLRICE and FP967 flax show
a sharp decrease after 2/3 years but with ongoing iso-
lated incidents of GM contamination. It is not clear why
some cases of contamination fall rapidly and others not
so rapidly. Governments and trading bodies wish reduce
any economic impact from GM contamination as soon
as possible. In some cases at least, this has evidently
spurred governments and companies to make efforts
to eliminate contamination, such as the destruction of
GM papaya in Thailand, or licensing GM-free flax va-
rieties. Internationally-traded commodity crops, there-
fore, are likely to receive the most efforts to reduce
GM contamination.
The seed supply system is a factor in determining the
persistence of GM contamination. GM contamination of
maize landraces in Mexico may be difficult to eradicate
because these varieties are dominantly open-pollinated,
where seed is saved from harvest for next years planting.
The GM traits could even introgress through these pop-
ulations (Dyer et al. 2009). In contrast, hybrid seed sys-
tems are more centrally controlled. Hybrid seed is
purchased each year and hybrid seeds are produced via
crossing of specified varieties. This allows the testing of
the parental varieties for the absence GM material prior
to breeding, each year if necessary.
GM grass in the western USA could represent the first
case where a GM crop has entered into wild or natural-
ized populations, and it remains to be seen whether it
will introgress through those populations.
Routes of GM contamination
Many cases of GM contamination are not investigated,
but those from unauthorised events have been investi-
gated the most. Cross pollination is not the sole route of
GM contamination. A number of routes have been iden-
tified including escape of seeds (grass), illegal plantings
(Bt63 rice), incorrect labelling (pigs) and volunteers from
previous years crops have all been identified as the
cause of GM contamination. Its also possible that a GM
contamination case arises from two or more routes.
Often, the route of GM contamination is not clear. For
example, Bayer was unable to identify the route of con-
tamination responsible for the LLRICE case, calling it
an act of God(Weiss 2006).
Finally, it is beyond the scope of the Register or this
paper to speculate about health or environmental implica-
tions from these specific contamination cases. However, if
GMOs that have not undergone any food/feed or environ-
mental risk assessments enter the food/feed chain or en-
vironment, this gives regulators cause for concern.
Conclusions
Nearly 400 incidents of GM contamination have been
recorded on the Register since 1997. There does not ap-
pear to be an overall pattern relating to any one particu-
lar factor. Instead, factors could include, but may not be
limited to global acreage, international trade, plant biol-
ogy and monitoring frequency. Experimental GM live-
stock have, on occasion, entered either human food or
animal feed.
All three principal, commercially grown GM food and
feed crops (oilseed rape, soya and maize) have been as-
sociated with GM contamination incidents over the past
17 years. There have also been nine cases of contamin-
ation associated with GM lines with no authorisation for
cultivation anywhere in the world, mostly at the research
and development stage. An important conclusion of this
work is that GM contamination can occur independently
of commercialisation. Indeed, GM lines of rice, the crop
associated with the highest number of incidents, has
never been grown commercially. The detection of GMO
contamination is dependent on both routine and
targeted monitoring regimes, which appears to be in-
consistent from country to country, even within the
EU. The lack of an analytical methodology for the de-
tection of GM crops at the field trial stage (i.e. pre-
commercialisation) can hamper efforts to detect any
contamination arising from such GM lines.
Additional file
Additional file 1: GM contamination database - analysis.xlsb.
Abbreviations
APHIS: Animal and Plant Health Inspection Service; DNA: Deoxyribonucleic
acid; EC: European commission; ELISA: Enzyme-Linked Immunosorbent Assay;
EU: European Union; EPA: Environmental Protection Agency; GM: Genetically
modified; GMO: Genetically modified organism; ISO: International
organisation for standardization; JRC: Joint research centre; LL: Liberty link;
NGO: Non-governmental organisation; PRSV: Papaya ringspot virus;
PCR: Polymerase chain reaction; RASFF: Rapid alert system for food and feed;
UN: United Nations; USA: United States of America; USDA: United States
Department of Agriculture.
Competing interests
Neither author has competing financial interests although both authors are
employed by NGOs which oppose the environmental release of GM crops.
Authorscontributions
The GM Contamination Register is maintained by B.Price and part funded by
Greenpeace. Both authors contributed equally to the preparation of this
manuscript. Both authors read and approved the final manuscript.
Author details
1
Consultant for GeneWatch UK, 60 Lightwood Road, Buxton SK17 7BB, UK.
2
Greenpeace Resaerch Laboratories, Innovation Centre Phase 2, University of
Exeter, Exeter EX4 4RN, UK.
Received: 22 May 2014 Accepted: 26 September 2014
Price and Cotter International Journal of Food Contamination 2014, 1:5 Page 11 of 13
http://www.foodcontaminationjournal.com/content/1/1/5
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Cite this article as: Price and Cotter: The GM Contamination Register: a
review of recorded contamination incidents associated with
genetically modified organisms (GMOs), 19972013. International
Journal of Food Contamination 2014 1:5.
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... This device was implemented to satisfy the precautionary principle introduced by the community 'White Paper' of 2001 (Aerni, 2019). The complete integration of the general procedures for traceability and alerts in the EU has enabled the development of a reliable traceability system for GMOs, included in the RASFF 12 alert system, without additional cost (Demortain, 2011;Parisi et al., 2016;Price and Cotter, 2014). However, despite these regulatory controls, fraud, adulteration and accidental contamination, whether or not due to human error, are still possible, although control systems such as the blockchain, may reduce the products' falsifiability (Demestichas et al., 2020). ...
... The history of GMOs is indeed a long process of unexpected contamination of seeds and food chains, due to human errors in particular, for example, by unauthorised products such as StarLink® (intended for the industry) or Prodigene (intended for pig vaccination) corn varieties (Ellstrand, 2003;Price and Cotter, 2014). This inability to trace GMOs in some areas of the world was exacerbated after September 2001 when the US authorities' concern increased about their failure to protect themselves from malicious GMOs, especially if they were possible weapons of bioterrorism/biowarfare. ...
... Nevertheless, the immunological tests have proven their usefulness for operators, particularly in some particular cases such as Cry9C, the only reported case of a protein specific to a transformation event. Indeed, immunological tests were used to remove StarLink®, a GM corn approved for industrial use and animal feed, from the food market, which would have cost nearly US$1 billion 17 (Bratspies, 2003;Diaz et al., 2002;Price and Cotter, 2014;Schmitz et al., 2005). StarLink® was the first example of a long and controversial series of contaminations due to insufficient supply chain segregation. ...
... Only GM traits approved by the regulatory bodies of both exporting and importing countries can enter the destination market (Price & Cotter, 2014). Suppose Argentina shipped soybean to China in a bulk container. ...
... In short, contamination can and does happen. The GM Contamination Register records 396 incidents across 63 countries over just seventeen years (from 1997 through the end of 2013), and this despite the absence of global systematic monitoring of GM contamination incidents-there are surely more (Price & Cotter, 2014). The consequences of a contamination case are likely to be more harmful for countries in the global South than for more diversified and/or less export-dependent countries (Nicita & Rollo, 2015). ...
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Debates about the benefits and risks of genetically modified (GM) crops need to acknowledge two realities: (1) the movement of transgenes beyond their intended destinations is a virtual certainty; and (2) it is unlikely that transgenes can be retracted once they have escaped. Transgenes escape via the movement of pollen and seeds, and this movement is facilitated by the growing number of incidents involving human error. Re-examination of our risk management policies and our assumptions about containment is essential as genes coding for pharmaceutical and industrial proteins are being inserted into the second generation of GM food crops. Even the best designed risk management can be foiled by human error, a reality that is underestimated by most GM crop-risk analyses. Thus, our evaluation of risk should assume that whatever transgene is being examined has a good chance of escaping.
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An indefinite moratorium on the commercial release of Bt brinjal in India was incurred in 2010, but there is much pressure from proponents of GM technology to review this. The Ministry of Agriculture of the Government of India has been reviewing ERA information for Bt brinjal, since August 2012 (http://164.100.47.134/Isscommittee/Agriculture/GM_Report.pdf). A dearth of experimental data often hampers the evaluation of potential risks associated with the introduction of transgenic crops into centres of diversity [12xIntroduction of transgenic crops in centers of origin and domestication. Gepts, P. : 119–134See all References[12], and the case of Bt brinjal is no exception. The urgent need for a more detailed understanding of the floristics, systematics, and interfertility relationships of brinjal and its wild, weedy, and cultivated relatives should be pinpointed by the Ministry of Agriculture review. Such crucial information should be generated by thorough, in-depth studies, in order to provide data that are extensive, interpretable, and unambiguous. The implications for plant diversity of the commercial cultivation of genetically engineered Bt brinjal cannot be fully assessed in their absence. Furthermore, the risk assessment of pollen-mediated transgene flow from Bt brinjal, if cultivated in Bangladesh or the Philippines, should not rely on the inadequate, previously undertaken ERA tests.