The precautionary principle: Making managerial decisions on GMOs is difficult

Abstract

The precautionary approach of the Cartagena Protocol on Biosafety, if incorporated into legislation of countries as a precautionary principle (PP), could cause great difficulty in decision-making on genetically modified organisms. No consensus seems to be possible on the interpretation of the PP, as responsibility often is passed on to political decision-making and, eventually, to court rulings. A case study on the assessment of possible unintended effects of endogenous allergens illustrates the complexity decision-makers may experience. We review the descriptions of the PP and the debate on the interpretation and conclusions that a number of authors have come to, as a step closer to a solution in decision-making. South Africa may have to consider the PP in the broader context of its food security needs, which would require improved communication as an additional step in the process of risk analysis.

Full text

1Volume 111 | Number 3/4
March/April 2015
South African Journal of Science
http://www.sajs.co.za
Review Article Analysis of the precautionary principle: GMOs
Page 1 of 9
AUTHORS:
Fredrika W. Jansen van Rijssen1
Jacobus N. Eloff1
E. Jane Morris2
AFFILIATIONS:
1Paraclinical Sciences, University
of Pretoria, Pretoria, South Africa
2School of Biology, University of
Leeds, Leeds, United Kingdom
CORRESPONDENCE TO:
Fredrika Jansen van Rijssen
EMAIL:
wilnajvr@telkomsa.net
POSTAL ADDRESS:
Paraclinical Sciences, University
of Pretoria, Private Bag X04,
Onderstepoort 0110, South Africa
DATES:
Received: 15 Aug. 2013
Revised: 07 Mar. 2014
Accepted: 08 July 2014
KEYWORDS:
genetically modified organisms;
South Africa; risk assessment;
endogenous allergens
HOW TO CITE:
Jansen van Rijssen FW, Morris
EJ, Eloff JN. The precautionary
principle: Making managerial
decisions on GMOs is difficult.
S Afr J Sci. 2015;111(3/4),
Art. #2013‑0255, 9 pages.
http://dx.doi.org/10.17159/
sajs.2015/20130255
© 2015. The Author(s).
Published under a Creative
Commons Attribution Licence.
The precautionary principle: Making managerial
decisions on GMOs is difficult
The precautionary approach of the Car tagena Protocol on Biosafety, if incorporated into legislation of countries
as a precautionary principle (PP), could cause great difficulty in decision‑making on genetically modified
organisms. No consensus seems to be possible on the interpretation of the PP, as responsibility often is
passed on to political decision‑making and, eventually, to court rulings. A case study on the assessment
of possible unintended effects of endogenous allergens illustrates the complexity decision‑makers may
experience. We review the descriptions of the PP and the debate on the interpretation and conclusions that
a number of authors have come to, as a step closer to a solution in decision‑making. South Africa may
have to consider the PP in the broader context of its food security needs, which would require improved
communication as an additional step in the process of risk analysis.
Introduction
A lack of coherence is observed in decisions made by governments for control of genetically modified (GM) crops.
Examples include rejection by some African countries of donor GM maize; increased regulatory requirements;
indecisiveness regarding new applications for permits with many delays and negative consequences to producers
and consumers; and creation of negative perceptions towards genetically modified organisms (GMOs). There
are many reasons for this situation, one of which is the variable application of precaution in decision‑making,
in particular different interpretations of the precautionary principle (PP). The control of GMOs by legislation and
international interventions in this respect jointly speak of a cautious approach to risks from new technologies.
However, genetic modification is no longer a new technology. Although international agreement exists on the
general approach to risk and safety assessment of food from genetic modification, and many countries follow the
international guidelines, debates on matters such as possible unintended effects from this technology are currently
prominent. The difficulty that decision‑makers often experience is illustrated by issues of possible unintended
effects of the genetic modification on endogenous allergens. An understanding of the PP could give perspective to
the burning issues, such as food security, with which decision‑makers are confronted.
Description of terms and concepts
Risk, risk assessment, uncertainty
Risk analysis describes a dynamic iterative process composed of risk assessment, risk management and risk
communication.1 The term ‘risk’ describes the probability of an adverse (health, environmental) effect (leading
to harm or undesired consequence) and the severity of that effect, consequential to a hazard(s) or threat(s).1,2 In
scientific terms, zero risk is non‑existent.3 Some uncertainty is always present4 and forms an inherent and integral
element of scientific analysis and risk assessment5‑7.
Evolution of crop plants
Plant breeding
The assessment of the safety of food from GM crops should be placed in the context of the evolution of crop
plants which started thousands of years ago when plants were first domesticated. A recent example is the Chinese
gooseberry, which is not edible, but with breeding has become palatable, and is now called kiwi fruit. Today
every crop plant that is grown is related to a wild species that occurred naturally in its centre of origin. Dramatic
phenotypic changes occurred through new mutations and natural hybridisation that farmers selected for and then
maintained as landraces. Scientific developments in agriculture, such as knowledge of genetics, contribute to
improved plant‑breeding practices. An array of scientific tools is now used to increase existing genetic variation,
for example: hybrid embryo rescue; application of colchicine, a chemical employed to induce polyploidy; ionising
irradiation; mutagenic chemicals and somaclonal variation (cell culture). Gene transfer techniques to develop GM
crops are considered a logical extension of the continuum in the scientific development to improve plant breeding.8
Interesting new developments
Recent molecular techniques have shown that the techniques used in traditional (non‑transgenic) plant breeding
are associated with genetic changes such as mutations, deletions, insertions and rearrangements.9 These changes
occur in addition to the movement of mobile genetic elements such as transposons (jumping genes) that are
responsible for most genome plasticity.9 Many of these genetic alterations occur in nature.10 Plant breeders
traditionally eliminate observed off‑types during the evaluation process. Despite the dynamic nature of the
genomes, and the effect of traditional breeding on the genome, only a few safety concerns from traditional plant
breeding have been recorded over years. Several recent articles have shown that traditional breeding causes more
inherent variability than GM.11,12
Arguments for less stringent requirements or exemption from regulation are heard frequently.13,14 There may also be
a need for policy reform to take into account the new developments.15

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Food safety assessment of GM crops
The Codex Alimentarius Commission, a body under the joint auspices
of the Food and Agriculture Organization and the World Health
Organization, played a prominent role in the development of guidelines
for the risk and safety assessment of food products from GMOs.16
These guidelines outline the safety and risk assessment of food from
GMOs in a precautionary way by proposing the steps to be taken in the
assessment. Substantial equivalence, a concept mentioned in the Codex
guidelines, was previously mistaken as the endpoint of the assessment.
The concept has been replaced by an improved description of the
approach for safety and risk assessment, which involves a comparative
analysis of the composition and of the phenotype.17,18 This approach is
preferred as animal toxicity studies would be difficult because of the
complex nature of food compared with chemical molecules such as
pesticides. Molecular characterisation is included in this starting point of
the assessment to identify hazards. The composition of the edible parts
of the genetically modified crop is compared with those of its near‑isoline
with a history of safe use. A broad range of parameters (macro‑ and
micronutrients, antinutrients, toxicants and secondary compounds) is
considered in the comparative analysis. Safety assessments of intended
changes and of unintended significant differences are the next step in
the safety assessment. Differences need not necessarily be unintended
effects of genetic modification, but can be caused by slightly different
genetic backgrounds or environmental effects. Compositional safety
is considered in the context of the normal composition of the crop
by including a number of commercial non‑GM crops in the trials that
are conducted across several environments. Safety is informed by
considering the normal array of compound levels present in crops
that have a history of safe consumption19 including the antinutrients,
toxicants and endogenous allergens of the crop. The nutritional value of
the crops is an important consideration in the assessment. Endogenous
allergens had not received serious attention from regulatory authorities
until recently.20
South African precautionary approach to GMOs
The establishment in South Africa of SAGENE (South African Committee
for Genetic Experimentation)21 in 1978 is evidence of the environmental
and human health concerns of scientists when progressing with a
new technology such as genetic engineering (also known as genetic
modification or modern biotechnology). The need for a precautionary
approach to possible environmental threats and concern for human health
is illustrated by several South African laws. A precautionary approach
in managing risks is included, for example, in the two South African
environmental management Acts,22,23 which provide for ‘a cautious
approach which takes into account the limits of current knowledge about
the consequences of decisions and actions’. The Genetically Modified
Organisms Act of 1997, as amended, incorporates the requirements of
the Cartagena Protocol on Biosafety (CPB), and, in the regulations to the
Act, requirements are described for the protection of human health and
the environment against possible risk from GMOs.24 No mention is made
of cost/benefit or risk/benefit, or proportionality of risk in applying the
P P, 24(p.3) although the GMO Act does refer to ‘socio‑economic impact’,
with the implication that an impact could be positive or negative.
South Africa has published a number of guiding documents. However,
different South African government departments represented on the
GMO Council apparently hold different positions. The absence of specific
policies is obvious in the recent mandatory GMO labelling requirements
in which regulations were promulgated by the Department of Trade and
Industry25 without consideration of existing GMO labelling regulations of
the Department of Health. The Depar tment of Environmental Affairs, in its
‘framework’26, refers to ‘null risk’, ‘avoid’ and ‘prevent’, which describe
precaution at its extreme, whereas other government departments do
not seem to have any specific interpretation of the GMO Act in terms of
their mandate.
There seems to be a need for policy and guidance on matters such as
the PP, new breeding technologies and dealing with possible unintended
effects from endogenous allergens. The new strategy on bio‑economy is
a step in the right direction to address national policies.27
The precautionary principle
Cartagena Protocol on Biosafety
Against the background to risk assessment and the decisions with
which regulatory authorities are confronted when dealing with genetic
modification of crops, an understanding of the PP is important.
A precautionary approach was originally developed to provide risk
managers with a tool for making decisions on environmental threats
from processes or substances that had not undergone safety evaluation
or regulatory approval.28 Cooney29 has summarised the history of the
development that resulted in a number of international agreements.
The CPB30 is one of a number of important agreements among nations to
consider possible harm to the environment and human health. It requires
countries to introduce measures to safely manage transboundary
movement of living modified organisms. Countries that became
signatories to the CPB were expected to incorporate the CPB into
legislation and to adhere to the requirements for environmental safety
and human health. A precautionary approach in consideration of risks,
articulated in the CPB as well as in other international agreements and
environmental law, is the cause of ongoing debates on the interpretation
and implementation of precaution.29
The PP was first incorporated into the World Trade Organization’s (WTO)
Agreement on Sanitary and Phytosanitary Measures (SPS Agreement)
in 1994.31 Article 5.7 makes it possible to obtain additional information
within ‘a reasonable period of time’31(p.72) when existing information is
inadequate, whereas Article 3.3 allows for more stringent protection than
relevant international standards, if there is ‘scientific justification’31(p.70).
The Codex standards are accepted by WTO as references.
Many debates seem to have ignored the fact that the point of departure
in assessing biosafety of living modified organisms is determined
in Article 4 of the CPB. The focus of the Protocol is on LMOs [living
modified organisms] that may have adverse effects on biodiversity as
well as risks to human health (Article 1)30(p.3) and ‘risk assessments shall
be carried out in a scientifically sound manner’ (Annex III, para 3)30(p.28).
Furthermore, the directive for application of a precautionary approach
has been set in Principle 15 of the Rio Declaration,32 namely, ‘Where
there are threats of serious or irreversible damage, lack of full scientific
certainty shall not be used as a reason for postponing cost‑effective
measures to prevent environmental degradation’32(p.2). Neither of these
approaches demands that all applications of biotechnology or of genetic
modification must undergo extensive assessments to comply with the
precautionary approach and neither implies that biotechnologies are
inherently unsafe. The interpretation of the requirements of the CPB in
many aspects has been debated for a number of years. Some of the
implementation procedures seem not to be in proportion to the risk or a
cost/benefit analysis; for example, the need for milling GMO commodities
such as maize in the Southern Africa Development Community.
A principle or an approach?
Legislating GMOs by pre‑market regulatory requirements for risk
assessment and by managing risks at the different steps of the
development and production of GM crops are precautionary measures.
On the other hand, the ‘precautionary approach’ as applied according to
the CPB, intends to address uncertainties that occur in risk assessment.
‘Precaution’ is generally recognised – not as a hypothesis, theory or
methodological rule – but as a normative principle for making practical
decisions under conditions of scientific uncertainty.33 A normative
principle implies obligations to ‘anticipate harm and moral obligations
in judging the adequacy of available knowledge’34(p.263). ‘Normative’ is
defined in the Collins English Dictionary as (1) Implying, creating, or
prescribing a norm or standard, as in language: normative grammar;
(2) Expressing value judgements or prescriptions as contrasted with
stating facts.35 In teaching of religion, distinction is very broadly made
between the ‘regulative principle’ of worship meaning binding in exact
accordance to the Holy Scripture, whereas ‘normative principle’ of
worship in general means nonbinding.36

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The implementation of the PP ‘requires different normative commitments
and choices’37(p.2). Ahteensuu describes the PP as a principle of ‘practical
decision‑making which may be justified on the basis of ethical and
socio‑political grounds and/or as a form of rational action’37(p.2). The
obligatory nature of this normative principle has resulted in more than
policy design criteria, but becomes a ‘regulatory philosophy’38(p.23) when
included in legislation, which, in turn, has to be interpreted by regulators.
Von Schomberg39 explains the normative challenges for application and
implementation of the PP. The scope of PP deliberations stretches across
broad political debate, policy level (political and societal), science–policy
interface and risk management.
Authors such as Recuerda40(p.5) analysed the legal interpretations of the
US versus the European system. The conclusion was that ‘principle’
had the connotation of legal language, of law, a ‘principle of law’, which
is the status of the PP in Europe, whereas the USA considers it an
approach with no legal connotation. The English language version of
the CPB30 uses the word ‘approach’, French ‘l’approche de précaution’,
German ‘Vorsichtprinzip’ and Spanish ‘principio’. It seems that the
words ‘approach’ and ‘principle’ are used without clear distinction in
different languages.
The precautionary approach is recognised as a precautionary principle
when included in legislation with obligations, as explained by authors
such as Levidow et al.34 and Löfstedt38. Cooney29 reasoned that the PP
would not determine a specific outcome or decision, unless a specific
formulation required it. Therefore, the terms ‘precautionary approach’
and ‘precautionary principle’ were used interchangeably. The PP
nomenclature is followed in this paper.
Definitions
A normative principle may be interpreted in various ways. This
multi‑interpretation is illustrated by about 19 definitions of the PP
(Table 1). Central to the PP is the obligation of action to reduce harm to
the environment and human health, and the moral obligation that action
be taken even if scientific evidence is inconclusive. These obligations
are formulated in different ways – strong ‘obligatory’ versions and weak
‘optional’ versions (Table 2). The strong form of the PP, for example
the Wingspread Statement (1998), is advocated by Greenpeace41 and
UNESCO‑COMEST42, while an example of a weak form is included in the
Rio Declaration. The difference between weak and strong precaution lies
mainly in the greater emphasis on risk avoidance, provision of safety
and the obligation to take safety measures. Variations in the scope of
‘precaution’ from narrow to broader accounts are reflected in (1) prior
risk assessment, (2) what triggers the use of the PP and (3) the scope
of action.7,34,43
Core of the debate on the precautionary principle
As threats to health and the environment become more complex,
uncertain and global in nature, the PP is increasingly being debated.45
Cognisance has to be taken of the debate. At the core of the debate on
the PP is the degree of scientific uncertainty in risk assessment and what
decisions should be made by managers in the face of uncertainty, when
to apply precaution, and what precautionary measures should be taken
to achieve certain levels of protection.46
Klinke and Renn47 identified five major noteworthy themes in this debate.
These themes can be grouped into two very closely related issues: how
risks are perceived by different people and how regulatory authorities
deal with these risks.
Perception of risks and evaluation of uncertainties
There are two camps on the perception and evaluation of risks. One
claims that risks are mental constructs that originate in human minds
and are only real within a specific group of people. The opposing camp
argues that technical estimates of risks are true representations of
observable hazards and that the effect is predictable, regardless of the
analyst’s beliefs. In between these two viewpoints are those who believe
that a combination of the two is more realistic.48
Table 1: Definitions and description of the precautionary principle
Codex Alimentarius Commission16:
Precaution is an inherent element of risk analysis. Many sources of uncertainty
exist in the process of risk assessment and risk management in food related
hazards to human health. The degree of uncertainty and variability in the available
scientific information should be explicitly considered in the risk analysis. Where
there is sufficient scientific evidence to allow Codex to proceed to elaborate a
standard or related text, the assumption used for the risk assessment and the
risk management options selected should reflect the degree of uncertainty and
the characteristics of the hazard.
Rio Declaration, Principle 1532 and the Cartagena Protocol on Biosafety to
the Convention on Biological Diversity30:
In order to protect the environment, the precautionary approach shall be widely
applied by States according to their capabilities. Where there are threats of serious
or irreversible damage, lack of full scientific certainty shall not be used as reason
for postponing cost-effective measures to prevent environmental degradation.
The precautionary principle, South Africa’s position44:
Proportional to risk, non-discriminatory, consistent, based on cost-effect
assessment, subject to review, capable of assigning responsibility for producing
scientific evidence.
UNESCO-COMEST42(p.14):
When human activities may lead to morally unacceptable harm that is
scientifically plausible but uncertain, actions shall be taken to avoid or diminish
harm ... Morally unacceptable harm is ... (1) threatening to human life or
health, (2) serious and effectively irreversible, (3) inequitable to present or
future generations, (4) imposed without ... consideration of ... human rights
... The judgment of plausibility should be grounded in scientific analysis ...
Uncertainty may apply to, but need not be limited to, causality or the bounds of
the possible harm. Actions are interventions that are undertaken before harm
occurs that seek to avoid or diminish the harm. Actions should be chosen that
are proportional to the seriousness of the potential harm, with consideration
of their positive and negative consequences and with an assessment of their
moral implications of both action and inaction. The choice of action should be
the result of a participatory process.
Wingspread Statement on the Precautionary Principle41:
Where an activity raises threats of harm to human health or the environment
precautionary measure should be taken even if some cause and effect
relationships are not fully established scientifically. In this context the proponent
of the activity, rather than the public, should bear the burden of proof.
The concept of ‘sound science’ that is included in international
agreement s and guidelines16,30,49 is being challenged. It is questioned7,34,43,50
whether scientists can conduct objective analyses of risks because
they interpret information according to their scientific knowledge and
values. Anti‑commercial sentiment is also often observed in literature
on the PP, by remarks on the integrity and independence of scientists,
the regulators’ public accountability and those with ‘financial stake in
scientific development’51(p.376).
Charnley52, former president of the Society for Risk Analysis, has it
that risk analysis is ‘threatened by a serious, growing, anti‑risk analysis
sentiment that is challenging the legitimacy of science in general, and risk
analysis in particular’52(p.3). Scientists and managers receive blame for
many ‘risky’ incidents, although there is perhaps an implication here that
the PP replaces risk assessment. Berry53(p.7) responded to the accusations:
Evaluation of data obtained from scientic
investigations is not easy and the process often
seems counter‑intuitive to the uninformed. Some
hold the conviction that ideological motives colour
all deliberations – this makes it easy to suggest that
in any scientic debate an opponent’s reason for
holding a particular viewpoint or belief depends
on his or her motives rather than their knowledge
base. This position may be useful in providing the

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scientists are poor communicators,59 resulting in a gap in knowledge
transfer to the public at large, while some sensational media contributions
have led to misguided public perceptions. The debate also focuses on the
legitimate role of public deliberations in risk analysis and management.
The International Risk Governance Council’s position on values is that all
dimensions of risk, both the factual and the socio‑cultural60(p.12), need to
be considered.
The ‘contextual variables of risk’ as they affect perceptions of consumers
are important.47(p.1077) One of the many issues is trust in regulatory
agencies and risk handling, often described as credibility.38
The debate in perspective
Risk is a societal construct as well as a physical reality.49 Results from the
continued debate are observed in changes in the process of risk analysis,
the critical assessment of approaches to risk assessment and proposals
for improved structured communication.61 Some valid arguments have
been raised. Inclusion of public concern/social criteria needs further
research. The inclusion of sociological issues in decision‑making is
anything but simple. There are many aspects – such as cultural differences,
country needs, human nature, philosophies, religions and political issues
– to take into account.
Analysis of the precautionary principle and its application
Critique of the precautionary principle
Vlek58 groups the multiple criticisms of the PP into ten objections. Some
of the objections are that: the PP is vague and broadly ambitious62;
serious or irreversible harm is ill defined62,63; it is dependent on
plausibility reasoning64; it is a policy of risk avoidance65; it is too absolute
and obligatory, thereby blocking or slowing down technology innovation
and progress66; it demands ‘impossible’ proof of safety; identifying the
nature and likelihood of possible serious harm may yield high costs of
safety tests and long delays in relevant policy decisions67; and it can be
misused by powerful interest groups51.
Vlek’s58(p.533) conclusion was that the PP has ‘an unusually protective
inclination towards foregoing an activity or imposing strict(er) safety
measures upon it, both of which are induced by large uncertainty about
possible disastrous consequences’.
Peterson63 rejected the use of the PP as a basis for decision‑making,
citing examples of decisions on conducting clinical trials, mobile phones
and GM‑derived foods. He said, ‘the precautionary principle therefore
replaces the balancing of risks and benefits with what might best be
described as pure pessimism’ 63(p.306). He argued:
We need a principle that tells what to do and what
not to do for each possible input of qualitative
information...no generally accepted formulation will
ever emerge as the PP is not a single well dened
idea...it makes more sense to describe it as a cluster
of vague related intentions about risk aversion,
burden of proof, irreversible damage and normative
obligations [and] any reasonable formulation of the
PP will imply a value judgment that no rational
decision maker would be prepared to accept.63(p.306,307)
With respect to the burden of proof, Petersen claimed, ‘It rests with
anyone who makes a claim, regardless of what is being claimed’ and
concluded, ‘There is nothing wrong with the precautionary principle – as
long as it is not used for decision‑making’63(p.308).
Berry53(p.7) commented that ‘convictions with ideological motives colour
all deliberations’. He mentioned the PP as a good example of only
considering results that fit a preconceived viewpoint. He asserted:
But it should be made clear when political or
socio‑economic judgments are being made and
the pretence that they are scientic judgment,
should be eschewed. It is comforting to pretend
Table 2: Accounts of the precautionary principle7,34
Narrow accounts Broad accounts
Prior risk assessment
The burden of evidence is inherently
shifted from demonstrating risk to
demonstrating safety
The burden of evidence depends
on the questions asked: asking the
right questions needs stakeholder
involvement
Trigger for precautionary principle
The precautionary principle can
be triggered only by an objective
scientific evaluation, indicating
reasonable grounds to expect
potentially dangerous effects (or
established scientific uncertainty)
The precautionary principle can be
triggered also by initial suspicions
about risk. The precautionary
principle can justify measures to
control undesirable effects (including
potentially dangerous ones)
Scope of action
Analyse policy: regulatory action
versus inaction e.g. through a cost–
benefit analysis
Provide the means to demonstrate that
alternative solutions are less harmful.
Establish a dialogue on social issues,
e.g. what options are desirable and
feasible?
grounds on which to mount a polemic against
any perceived threat (drugs in modern medicine,
pesticides in intensive agriculture or genetically
modied organisms). The conviction that opinions
cannot be based on independent thought, has
led to a disregard of professionalism and the
development of the view that who pays you
determines your opinion – not your science.
The debate also includes evaluation of uncertainty in risk assessment,
the validity of animal models54, variability in data19 and lack of sufficient
knowledge47. Approaches to assessment of GMOs, for example the
substantial equivalence, and concepts of familiarity and ‘history of
safe use’ have been criticised as pseudoscience.55 As an alternative, a
‘holistic’ approach is advocated by some.55‑57
Instead of gaining more knowledge about uncertainties, alternative
management strategies could be proposed – for example, human
interventions that are manageable.47 Additional and more stringent
control to the point of embargos or refusal to avoid any risk as a
precautionary measure might be detrimental to progress. Steering
direction is difficult in these situations without clear policies at every
level of decision‑making.
There is no well‑established classification of uncertainty in risk
assessment.47 Renn and Klinke48 have described six groups of risks
named from Greek mythology. They grouped GMO technology with
disintegrating polar ice sheets because of uncertainty in both probability
of occurrence and extent of damage.48 Vlek58 grouped GMOs with risks
such as the AIDS epidemic as a ‘diffuse source’ with the potential risk
of long‑term and extensive effects. Risks associated with conventional
agricultural plant breeding are not mentioned; neither are far less precise
techniques such as induced‑mutation breeding in which plants or seeds
are exposed to ionising radiation for which regulatory control does not
exist or is more lenient than that for GMOs.
Public interest
Public perception on how uncertainty in risk assessment is handled is a
valid issue to some47 and engagement of interested and affected parties
in appraisal is also a matter of scientific rigour7. In a survey on people’s
opinions on some scientific issues in the UK, some responded that most

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stringent management were added.72 In the case of an appeal by
Biowatch against the decision to grant general release of Bt11 maize, the
appeal board ruled against the appellant.73 Valuable lessons were learned
from this case, one of which was that demands for additional data, as a
matter of ‘nice to know’, illustrating the interpretation of ‘precaution’ by
some groups in the society could result in costly delays to the applicant,
as well as the complainant and government.
Acceptable solutions in the precautionary principle debate?
Key issues in the precautionary principle
Having summarised the issues in the debate, the reality is that clear
guidance is needed to facilitate regulatory decisions based on an
even‑handed approach to precaution. In order to come to acceptable
solutions, the key issues at this stage are:
• Key inherent problems with the application of the PP and the
corresponding precautionary approach were identified by Vlek58; for
example, (1) substantive issues such as determining the plausibility,
nature and seriousness of possible harm or damage and (2)
procedural issues, for instance optional versus obligatory precaution,
and the need for further research and policy development. These
problems are also described as factors triggering recourse, which
is the decision to act or not to act, and the measures on how to act.
• The PP applies to serious uncertain risks or threats; it is inclined
to be unusually protective or even preventative; the proponent has
a large burden of demonstrating the likelihood of safety; and there
is the tendency to delay risk‑taking until sufficient new information
becomes available.58,74
• A number of authors have described models for decision‑making
based on assessment of risks in general.58,74,75 These risks rest
upon axioms and assumptions that are not always valid in practice,
such as perceptions of cultural differences.
In trying to find a way forward, the following comments on the application
of the PP by Feintuck51 are noteworthy: ‘The PP is currently applied as
a procedural rather than a substantive device’ and ‘substantive content
and value‑orientation’ are necessary. Feintuck51 contended that if the ‘PP
is devoid of intrinsic values, these may simply be filled by the values of
dominant groups’. His conclusion, after studying the development and
implementation of the PP, was that it is a ‘complex picture of interaction
between science, economics, public policy and law’51(p.377,392).
Risk governance of GMOs
The European Commission46 places the burden of determining an
acceptable level of risk for society as a judgement of an eminently political
responsibility: ‘Decision‑makers faced with an unacceptable risk, scientific
uncertainty and public concer ns have a duty to find answers’46(p4). Guidance
from the European Commission perspective is followed by, for example,
the South African regulatory authorities for GMO governance (Table 1).44
The International Risk Governance Council – a private, independent,
not‑for‑profit foundation – was established in 2003 to support governments,
industries, non‑governmental organisations and other organisations to
deal with major and global risks and to foster public confidence in risk
governance. Debates within the PP protagonist circles focus on the
relative importance of substance versus procedure. At the very least, it
is important to be in agreement on the impor tance of procedural steps
in instances of great uncertainty about the available evidence, possible
consequences, feasible options, long‑term effects and minority views.
The International Risk Governance Council has developed a framework to
assist governments in decision‑making on all kinds of risks.60
The designers of the International Risk Governance Council’s framework60
emphasise the importance of stakeholder par ticipation. This is also
elaborated on by a number of proponents of the PP.37,43,76 One can
conclude that interaction at different levels is required, but it would have
specific challenges.
that we know more than we think, but damaging
to pretend too much.53(p.7)
In summary, Vlek58 said that the PP is mostly derogated for its general
inclination and motivation, its dependence on plausibility reasoning, its
lack of comparative risk evaluation, its lack of explicit decision‑making
considerations, its openness with regard to legal obligations, and its
implied shift of the burden of proof of safety.
Decisions from arbitration
Proof of the difficulty in interpretation of the meaning of the PP concept
lies in the opinions of jurists who are grappling with it because of its
‘philosophical characteristic, inherent uncertainty, and ambiguous and
arbitrary nature’66{p10). The PP is open ended and undefined, which ‘gives
regulators almost unlimited discretion to impose restrictions’66(p.32).
Ultimately, the courts will have to flesh out the principle.51,66,68,69 The reality
is that prevailing social and political values influence to some degree the
trend in case law. In legal formulation, UNESCO‑COMEST42(p.22) advises:
‘first, the recognition of a value by a society is worthy of protection, and,
second, the provision of a legislative tool [is] in order to protect this new
recognised value’.
A WTO31 ruling on GMOs illustrates the application of the PP in inter national
trade. A long‑standing dispute existed between the USA and Europe over
the European Commission and several European member states’ de facto
moratorium on approval of GMOs. The moratorium lasted from 1998 to
2004. In 2003, the USA, Canada and Argentina sought legal recourse
at the WTO under WTO SPS (Sanitary and Phytosanitary) law based on
unjustified and illegal denial of access to European markets (EC Biotech
Products case) that resulted in financial losses to US farmers. The WTO
based its final decision in 2006 on failure of the defendant to conduct
‘adequate’ risk assessments (SPS Article 5.1 and Annex A (4)) by not
taking into account risk assessment techniques (protocols) of relevant
international organisations. Although their scientists’ conclusions were
based on scientific methods, the WTO panel found that legislators
often based decisions on ‘unverifiable facts and public fears’70(p.2). The
European Commission’s arguments apparently rested on concerns by
regulators on ‘scientific uncertainty’, thereby ignoring their own risk
assessments. The WTO panel rejected the defendant’s arguments
(Articles 5.1 and 2.2). The argument that there was ‘insufficient scientific
evidence’ (Article 5.7) was also rejected as the European Commissions’
scientific committees indeed reviewed the relevant information and did
not question their previous conclusions. Therefore, additional information
in this case was not an issue. ‘Scientific uncertainty’ and ‘insufficient
scientific evidence’ are not the same (SPS Article 5.7). The WTO also
concluded that the European Commission had acted inconsistently with
its obligation under Annex C (1) (a) and Article 8 because of the undue
delay. The European Commission accepted the ruling.
Europe introduced legislation to improve the framework for assessing the
application of GM plants and introduced strict labelling and traceability
requirements for GMOs in 2003 to accommodate public perception
and address fears. An assessment of the WTO panel’s decision is not
pursued further in this study.
The interpretation of uncertainty, and perhaps consumer perceptions,
is further illustrated by the November 2011 ruling of the two highest
courts in the European Union – the European Cour t of Justice and
the Conseild’Etat of France – against the French ban on planting of
GM Bacillus thuringiensis maize (Bt maize). The ban was based on a
European Union ‘safeguard clause’ and legal provision for ‘emergency
measures’ in case of evidence of serious hazards to human health and
the environment. The courts ruled that France did not present any such
new evidence to substantiate their ban on Bt maize. France responded by
stating that it will reinstate the ban.71
In South Africa, appeals72 against several decisions made by the GMO
Executive Council on the general release of Bt11 maize, the use of
biofortified sorghum for greenhouse studies and planting of cassava
field trials, resulted in the Appeal Board ruling in favour of the applicants,
although in the latter two cases certain conditions which require more

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Vlek58 suggested that the parties involved might do well to attend carefully
to the kind of participants, structure, content and process making up
the relevant assessment and management strategy. Vlek58 also warned
against ‘individual judgements and social decision‑making, for
example allowing room for prior beliefs and biases, selective information
processing, authoritative dominance and groupthink at the cost of minority
views’58(p.535). In participative, multi‑stakeholder situations, these could
lead to disputable judgements, decisions and actions.51
In a democratic political situation, and to improve credibility of risk
governance, improved interaction with stakeholders (for example the
public, scientists and the owners of the technology) has to be considered.
Much more thought will have to go into defining the nature and substance
of such interactions. Participation has to be correctly defined, as
accountability remains with the regulatory authority. Codex1 describes
an interphase for determination of ‘risk assessment policy’ as a specific
component of risk management interaction among risk managers,
risk assessors and stakeholders that governments could consider to
improve communication.
Case study: Assessment of endogenous allergens
This case study illustrates some of the complexities with which
decision‑makers could be confronted in the governance of risks.
Codex’s guidance for risk assessment, as a precautionary approach,
describes the case‑by‑case process to be followed in the safety/risk
assessment of GMO products (see section on safety assessment
of GM crops). Keeping in mind the conclusions from the molecular
characterisation, phenotypic and agronomic comparative studies as
well as comparative analyses of the nutrients, toxicants and antinutrients
would follow. Codex16 considers that endogenous allergens should be
included in the compositional comparative safety assessment. The
safety/risk assessments of possible unintended effects of endogenous
allergens pose problems, as described in the sections following.
Step: Risk assessment framing
Policy development
A precautionary/risk assessment debate regarding inclusion of
endogenous allergens in the safety and risk assessment may proceed
as follows.
GM‑derived foods are assessed according to regulatory requirements
and, if approved for human consumption, different laws of a country
may have additional requirements (e.g. labelling of food). Labelling in
many countries includes information on the eight food allergens (Box 1).
A possible question is: Would it be necessary to include endogenous
allergens in the compositional analysis of those eight foods when
derived from GMOs when allergenicity labelling is a standard required?
Another question could be: What about possible unintended increased
levels of the endogenous allergen in these eight allergenic foods? It
is difficult to determine the prevalence of allergenicity, as consumers
tend to avoid foods to which they are allergic. Although allergenicity to
some foods, such as peanuts and tree nuts, could affect up to 1% of the
population, none of these foods has been withdrawn from the market.
However, some countries do require analysis of these allergenic foods.20
Another question could be: What about possible unintended increased
levels of endogenous allergens in GM‑derived food in addition to the
eight allergenic foods? This question provokes a number of issues;
hypothetically, it is possible for someone to be allergic to any food,
processed or raw. A question on concentration levels would be: What
level would trigger a tolerance level that could serve as a point for
decision‑making by regulators? Information that could stimulate more
questions is given in Box 1.
Box 1: Endogenous food allergen information
The prevalence of food allergenicity is unknown, but it is estimated that over
90% of reported food allergies are those to the eight most common allergens –
peanuts, soybean, tree nuts, wheat, cow’s milk, eggs, fish and crustaceans77,78
– which affect up to 3% of adults and up to 6% of infants in the population.79,80
Each of the allergenic foods contains multiple allergens. It is not possible to predict
who will become allergic and to which foods and which proteins in foods.81 There
are stable and abundant proteins that do not cause allergy as well as moderately
abundant proteins that do cause allergy.82 Sensitivity reactions to the same
concentration of allergen vary between mild rashes to anaphylactic shock.83
There is a wide variation in IgE binding to different varieties of the same species
of non‑GM crops.84
Natural variability in plant components is a result of genetics, environmental
factors and post‑harvest conditions, but the variation in expression of levels
of various allergenic proteins has not been documented. Food processing and
interactions with the food matrix also affect the allergic potential.20
Specific serum screening to confirm allergenicity may not be possible for many
food allergens because of difficulties in the identification of a sufficient number
of donors, cross‑reactivity and other problems.20,82 The number of sera samples
needed is dependent on the required degree of protection to the population.
Animal models are in general considered not validated and inconclusive for
assessment.20,85 Sufficient sensitivity and specificity to guarantee absence
of false negative and false positive results are not yet possible. Analytical
and profiling techniques or in‑vitro protein analysis and proteomics methods
need to be assessed for accuracy, sensitivity, specificity and feasibility before
being routinely used for allergenicity assessment.20
Uncertainty in answering these questions because of a lack of sufficient
scientific information is illustrated in the following discussion in the case
of maize.
Maize – a staple food for many people – is a crop that has been genetically
modified to introduce a number of new traits. To better understand the
complexity encountered in decision‑making, a hypothetical case is made
for endogenous allergens of maize. Known allergen information is given
in Box 2. A general conclusion from this information is that there are
a number of issues that would make it difficult to make a decision of
absolute safety unless more information is generated. The shortage of
serum donors would be critical in most cases.
Box 2: Consideration of endogenous allergens in maize
The main allergen in maize, Zea m 14, is a lipid transfer protein – a true pan‑
allergen86,87 that maintains its structure after cooking at high temperatures.88
Cross‑sensitivity with other fruits and vegetables occurs.86 Prevalence is unknown.
Incidences of allergenicity have been reported from regions in Italy86 and
Mexico.89 Serum tests would be very difficult to conduct because of the scarcity
of allergic consumers.82
The population in general, has been exposed for many years to fluctuating
concentrations because of environmental effects and hybrid variability. Normal
variation of lipid transfer protein in maize could be up to 15‑fold across genetic
and environmental differences.90
There are more questions and issues. It would only be possible to
consider the tolerance levels once the range of endogenous allergen
levels has been determined for each crop plant. How sensitive are the
tests and what serum sample size is required? What percentage (or
concentration) increase above the range of natural biological variation
is acceptable? What percentage of the population should be protected?
What levels would cause reactions in patients, from mild to severe?
What percentage of severe reactions such as anaphylactic shocks has
been documented for the population?
There is also a question on the labelling regime for those GM‑derived
foods which are not one of the mentioned eight allergenic foods. And
should elevated levels of the endogenous allergens be detected, could
it be shown that they were explicitly caused by the genetic modification

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and not by normal variability? Would an Identification Preservation
System be feasible, practical and affordable?
More recently, the results from information accumulated over more than
20 years, as described in this paper, showed no significant differences in
the composition of tested components (excluding endogenous allergens)
between GM crops and the near‑isolines. Furthermore, consumers have
been exposed to GM‑derived foods through a number of different crop
species and traits – all assessed case‑by‑case – with no adverse effects
recorded. These are important observations that regulators should take
into consideration.
The final question that a managerial team could ask might be: Does the
case under consideration qualify as a situation of serious uncertainty
and an irreversible risk? This question may not be easy to answer.
Regulating the assessment of endogenous allergens of GMOs?
Decision‑makers are confronted with a number of challenges. A study
of the literature on natural allergens and GM crop plant endogenous
allergens shows that many questions remain unanswered. It seems that
some regulatory authorities are overreacting by asking for more and
more information to confirm possible unintended differences between
the endogenous allergens of the GMO and its non‑GMO near‑isoline.
Adequacy of the assessment of allergenicity is debated. A school of
allergen specialists81 commenting on the validation of the tests, and
particularly availability of serum for testing, contended that the ‘extreme
precautionary position is not scientifically defensible’81. They opined that
‘we need to know more about endogenous allergen levels and natural
variation and have not seen data that demonstrate an enhanced risk to
the consumer, based on the observed variation’. Upregulation of allergen
levels is contested by Herman and Ladics91. There is no evidence tabled
on consumers showing adverse reactions owing to allergens from
eating approved GMO products. Therefore, the postulated risk remains
a hypothetical one.
Regulatory authorities have to make decisions, while scientists continue
to debate at technical level. Before requesting additional studies, policies
on risk to consumers should be placed in the broader context of the
country’s needs. The example shows the need for proactively considering
the approach to be followed. These should be included in a risk
assessment policy interface that does not exist in many risk governance
situations. Consequences for additional precautionary requirements that
are not well thought through are far reaching. Knowledge gathered over
many years and now assessed, brings new perspectives on the effect
of different plant‑breeding practices, including genetic modification.
The need for assessment of endogenous allergens is under debate.
The case study with endogenous allergens illustrates the difficulty
decision‑makers may experience in implementing Codex guidelines.
These guidelines are not compulsory regulatory instruments, but are
significant in international trade. New knowledge of the genome and
the place of genetic modification compared to traditional plant‑breeding
technologies, with respect to unintended effects, could influence the
outcome of potential international trade disputes.
Conclusions and recommendations
The debate on the PP illustrates the diverse opinions on safety
requirements for GM crop plants. Some consider GM crops irreversibly
harmful, while others view them as representing only a continuum of
existing knowledge and agricultural practices. The key problem with
the PP is that it is a normative principle – ill‑defined and vague. The
rational way forward seems to be that a number of experts, including
stakeholders, should be included in a structured way to contribute to
policy development and to frame the risk assessment.
Recommendations for South Africa
• A new dispensation in South African risk governance of GMOs
should be considered that requires benefits of modern biotechnology
(including genetic modification) to be given adequate consideration
and applied to the advantage of the population.
• The new Bio‑Economy Strategy for South Africa27, published in
2013, addresses, inter alia, food security and economic growth as
some of the key imperatives. The strategy specifically mentions:
identifying ‘areas of public policy that can remove barriers’ and
‘improve cooperation between stakeholders’27(p.7). These matters
should be investigated with a view to establishing an interface
between risk management (decision‑making) by the GMO council
member departments, the scientific GMO advisory committee and
stakeholders. Stakeholders should include the relevant scientific
communities, such as specialist agricultural scientists, as the
most trusted parties for credibility of information. Socio‑economic
matters should be proactively considered during this phase of the
iterative interactions of risk analysis.
• Development of policy and guidelines on issues of risk
assessment is a matter of importance. These include, inter alia,
the principle of precaution; consideration of dealing with possible
unintended effects from genetic modification; and a policy on new
plant‑breeding techniques.
Relevance to other countries
A number of countries are in the process of finding a way forward in
terms of the regulation of GM crops, and, in so doing, are determining
their own approaches to decision‑making and the application of the PP.
The issues raised in this paper may be useful in their deliberations on
the way forward.
Acknowledgements
The study was made possible by a grant from the National Research
Fund. We thank the anonymous reviewers for their comments on the
manuscript. The article was submitted in revised form as a chapter in
the PhD thesis of F.W.J.v.R.
Authors’ contributions
F.W.J.v.R authored the manuscript; E.J.M. and J.N.E co‑supervised
the study.
References
1. Codex Alimentarius Commission (CAC). Procedural manual. 23rd ed. Rome:
FAO/WHO Food Standards Programme; 2015. Available from: ftp://ftp.fao.
org/codex/Publications/ProcManuals/Manual_23e.pdf
2. United States Environmental Protection Agency (US–EPA). Risk assessment
[document on the Internet]. No date [cited 2015 Feb 20]. Available from:
http://www.epa.gov/risk_assessment/basicinformation.htm
3. Querci M, Kleter G, Malingreau JP, Broll H, Van den Eede G. Scientific and
technical contribution to the development of an overall health strategy in the
area of GMOs. JRC–IHCP Reference Reports. EUR 23542. Luxembourg:
European Committee; 2008.
4. De Bruijn J, Ten Heuvelhof E. Scientific expertise in complex decision‑making
processes. Sci Public Policy. 1999;26(3):179–184. http://dx.doi.
org/10.3152/147154399781782428
5. Renn O. Risk governance: Coping with uncertainty in a complex world.
London: Earthscan; 2008.
6. Wolt JD. Understanding risk and safety assessment for genetically modified
plants [document on the Internet]. c2008 [cited 2015 Feb 19]. Available from:
http://agribiotecj.info/details/wolt‑riskassessmentoweb02.pdf.
7. Stirling A. On ‘precautionary’ and ‘science‑based’ approaches to risk
assessment and environmental appraisal. In: Stirling A, editor. On science
and precaution in the management of technological risk. JRC‑IPTS Technical
Report. EUR19056/EN/2.2001 [document on the Internet]. c2001 [cited
2015 Feb 20]. Available from: http://ftp.jrc.es/EURdoc/eur19056llen.pdf.
8. Prakash CS. The genetically modified crop debate in the context of agricultural
evolution. Plant Physiol. 2001;126:8–15. http://dx.doi.org/10.1104/
pp.126.1.8
9. Weber N, Halpin C, Hannah LC, Jez JM, Kough J, Parrot W. Crop genome
plasticity and its relevance to food and feed safety of genetically engineered
breeding stacks. Plant Physiol. 2012;160:1842–1853. http://dx.doi.
org/10.1104/pp.112.204271

8Volume 111 | Number 3/4
March/April 2015
South African Journal of Science
http://www.sajs.co.za
Review Article Analysis of the precautionary principle: GMOs
Page 8 of 9
10. Lusser M, Parisi C, Plan D, Rodríguez‑Cerezo E. New plant breeding
techniques: State‑of‑the‑art and prospects for commercial development.
JRC‑IHCP Scientific and Technical Repor ts. EUR 24760 EN. Luxembourg:
European Committee; 2011.
11. Batista R, Saibi N, Lourenco T, Oliveira MM .Microarray analyses reveal that
plant mutagenesis may induce more transcriptomic changes than transgene
insertion. Proc Natl Acad Sci USA. 2008;105(9):3640–3645. http://dx.doi.
org/10.1073/pnas.0707881105
12. Kogel KH, Voll LM, Schäfer P, Jansen C, Wu Y, Langen G, et al. Transcriptome
and metabolome profiling of field‑grown transgenic barley lack induced
differences but show cultivar‑specific variance. Proc Natl Acad Sci USA.
2010;107:6198–6203. http://dx.doi.org/10.1073/pnas.1001945107
13. Herman RA, Chassy BM, Parrott W. Compositional assessment of
transgenic crops: An idea whose time has passed. Trends Biotechnol.
2009;27(10):555–557. http://dx.doi.org/10.1016/j.tibtech.2009.07.003
14. Parrott W, Chassy B, Ligon J, Meyer L, Petrick J, Zhou J, et al. Application of
food and feed safety assessment principles to evaluate transgenic approaches
to gene modulation in crops. Food Chem Toxicol. 2010;48:1773–1790. http://
dx.doi.org/10.1016/j.fct.2010.04.017
15. Durham T, Doucet J, Snyder LU. Risk of regulation or regulation of risk?
A de minimus framework for genetically modified crops. Agbioforum.
2011;14(2):61–70.
16. Codex Alimentarius Commission (CAC). Food derived from modern
biotechnology. 2nd ed. Rome: FAO/WHO Food Standards Programme
[document on the Internet]. c2009 [2015 Feb 20]. Available from: ftp://ftp.
fao.org/docrep/fao/011/a1554e/a1554e00.pdf.
17. Kuiper HA, Kleter GA, Notebor n HPJM, Kok EJ. Assessment of the food safety
issues related to genetically modified foods. Plant J. 2001;27(6):503–528.
http://dx.doi.org/10.1046/j.1365‑313X.2001.01119.x
18. Kok EJ, Kuiper HA. Comparative safety assessment for biotech crops.
Trends Biotechnol. 2003;21(10):439–444. http://dx.doi.org/10.1016/j.
tibtech.2003.08.003
19. Herman RA, Price WD. Unintended compositional changes in genetically
modified (GM) crops: 20 Years of research. Agric Food Chem.
2013;61:11695–11701. http://dx.doi.org/10.1021/jf400135r
20. European Food Safety Authority (EFSA). Scientific opinion on the assessment
of allergenicity of GM plants and micro‑organisms and derived food and feed.
EFSA Journal. 2010;8(7):1700–1868.
21. South African Committee on Genetic Experimentation (SAGENE). Government
Gazette 15420. 1994;48:17–18.
22. South Africa. National Environmental Management Act (Act No. 107 of 1998).
Government Gazette 19519. 1998;401, Article 4(a)(vii) [online]. c1998 [cited
2015 Feb 20]. Available from: http://www.gov.za/sites/www.gov.za/files/
a107‑98.pdf
23. South Africa. National Environmental Management: Biodiversity Act (Act No.
10 of 2004). Government Gazette 26436/467. 2004; Chapter 5 Part 3 Section
78:62–64 [online]. c2004 [cited 2015 Feb 20]. Available from: https://www.
environment.gov.za/sites/default/files/gazetted_notices/nemba_gypaetus_
barbatus.pdf
24. South Africa. Genetically Modified Organisms (Act No. 15 of 1997). Government
Gazette 18029, 1997;323; as amended (Act No. 23 of 2007), Government
Gazette 29803, 2007;502; Regulations: Government Gazette 32966,
2010;120 [online] c2010 [cited 2015 Feb 16]. Available from: http://www.
daff.gov.za/daffweb3/Branches/Agricultural‑Production‑Health‑Food‑Safety/
Genetic‑Resources/Biosafety/Legislation/
25. South Africa. Consumer Protection Act (Act No. 68 of 2008). Government
Gazette 32186. 2009;526; Regulations (R293, 1 April 2011), Government
Gazette 34180. 2011;550 [online]. c2011 [cited 2015 Feb 20]. Available from:
http://www.thedti.gov.za/business_regulation/acts/consumer_protection.PDF
26. Department of Environmental Affairs (DEA). Environmental risk assessment
framework for genetically modified organisms: A guidance document.
Pretoria: DEA; n.d.
27. Department of Science and Technology (DST). The Bio‑economy
strategy. Pretoria: DST; 2013. Available from: http://www.pub.ac.za/files/
Bioeconomy%20Strategy.pdf
28. Hathcock JN. The precautionary principle – An impossible burden of proof for
new product. Agbioforum. 2001;3(4):255–258.
29. Cooney R. The precautionary principle in biodiversity conser vation and natural
resource management: An issues paper for policy‑makers, researchers
and practitioners. IUCN Policy and Global Change Series Issue 2. Gland:
World Conservation Union; 2004. Available from: http://www.sehn.org/pdf/
PrecautionaryPrincipleissuespaper.pdf
30. Cartagena Protocol on Biosafety to the Convention on Biological Diversity
(CPB): Text and Annexes. Montreal, Canada: Secretariat of the Convention
on Biological Diversity; 2000. Available from: http://www.cbd.int/doc/legal/
cartagena‑protocol‑en.pdf
31. World Trade Organization (WTO). Uruguay Round Agreement: Agreement on
the application of sanitary and phytosanitary measures. [document on the
Internet]. c1995 [cited 2015 Feb 15]. Available from: http://www.wto.org/
english/docs_e/legal_e)15sps_01_e.htm
32. United Nations Environmental Programme (UNEP). Rio Declaration on
Environment and Development [document on the Internet]. c1992 [cited
2015 Feb 14]. Available from: http://www.unep.org/Documents.Multilingual/
Default.asp?documentid=78&articleid=1163
33. Cranor CF. Learning from the law to address uncer tainty in the precautionary
principle. Sci Eng Ethics. 2001;7:313–326. http://dx.doi.org/10.1007/s11948‑
001‑0056‑0
34. Levidow L, Carr S, Wield D. European Union regulation of agri‑biotechnology:
Precautionary links between science, expertise and policy. Sci Public Policy.
2005;32(4):261–276. http://dx.doi.org/10.3152/147154305781779452
35. Collins English Dictionary [online]. 10th ed. London: HarperCollins Publishers.
Normative. [cited 2015 Feb 20]. Available from: http://www.collinsdictionary.
com/dictionary/english/normative?showCookiePolicy=true
36. Masters P. Is the Bible always binding for today? [document on the Internet].
c1995 [cited 2015 Feb 20]. Available from: http://www.reformedbaptist.
co.uk/Normative.htm
37. Ahteensuu M. Rationale for taking precautions: Normative choices and
commitments in the implementation of the precautionary principle. In: Risk
& RationalitiesConference Proceedings; 2007 March 29–31; Cambridge, UK
[online]. c2007 [cited 2015 Feb 20]. Available from: http://www.kent.ac.uk/
scarr/events/ahteensuu.pdf
38. Löfstedt R. The swing of the pendulum in Europe: From precautionary principle
to (Regulatory) impact assessment. J Risk Uncertain. 2004;28(3):237–260.
http://dx.doi.org/10.1023/B:RISK.0000026097.72268.8d
39. Von Schomberg R. The precautionary principle and its normative challenges.
In: Fisher E, Jones J, Von Schomberg R, editors. Implementing the
precautionary principle; perspectives and prospects. Cheltenham, UK: Edwin
Elgar; 2006. p. 19–42 Available from: http://www.oecd.org/agriculture/
agricultural‑policies/43891297.pdf
40. Recuerda MA. Dangerous interpretations of the precautionary principle and
the foundational values of European Union food law: Risk versus risk. J Food
Law Policy. 2008;4(1):1–44.
41. Wingspread. Wingspread consensus statement on the precautionary principle
[homepage on the Internet]. c1998 [cited 2015 Feb 16]. Available from:
http://sehn.org/wingspread‑conference‑on‑the‑precautionary‑principle/
42. United Nations Educational Scientific and Cultural Organization (UNESCO)
and World Commission on the Ethics of Scientific Knowledge and Technology
(COMEST). The precautionary principle. Paris: UNESCO; 2005. Available
from: http://unesdoc.unesco.org/images/0013/001395/139578e.pdf
43. Stirling A. Risk at a turning point? J Risk Res. 1998; 1(2):97–109.
44. South Africa Parliamentary Hearing on the GMO Amendment Bill; 2004
January 17–19. Response from the Department of Agriculture [unpublished].
45. Martuzzi M, Tickner JA, editors. The precautionary principle: Protecting
public health, the environment and the future of our children. Copenhagen:
WHO Regional Office for Europe; 2004. Available from: http://www.euro.who.
int/__data/assets/pdf_file/0003/91173/E83079.pdf.
46. Commission of the European Communities. Communication from the
Commission on the precautionary principle. Brussels: Office for Official
Publications of the European Communities; 2000. Available from: http://
ec.europa.eu/dgs/health_consumer/library/pub/pub07_en.pdf
47. Klinke A, Renn O. A new approach to risk evaluation and management:
Risk‑based, precaution‑based, and discourse‑based strategies. Risk Anal.
2002;22(6):1071–1094.

9Volume 111 | Number 3/4
March/April 2015
South African Journal of Science
http://www.sajs.co.za
Review Article Analysis of the precautionary principle: GMOs
Page 9 of 9
48. Renn O, Klinke A. Risk evaluation and risk management for institutional and
regulatory policy. In: Stirling A, editor. On science and precaution in the
management of technological risk. JRC‑IPTS Technical Repor t. EUR19056/
EN/2.2001 [document on the Internet]. c2001 [cited 2015 Feb 20]. Available
from: http://ftp.jrc.es/EURdoc/eur19056llen.pdf.
49. Organization for Economic Cooperation and Development (OECD). Emerging
systemic risks in the 21st century: An agenda for action [document on
the Internet]. c2003 [cited 2015 Feb 15]. Available from: www.oecd.org/
dataoecd/20/23/37944611.pdf
50. Wynne B. Creating public alienation: Expert cultures of risk and ethics on
GMOs. Sci Cult (Lond). 2001;10(4):445–481.
51. Feintuck M. Precautionary maybe, but what’s the principle? The
precautionary principle, the regulation of risk, and the public domain. J Law
Soc. 2005;32(3):371–398.
52. Charnley G. Annual meeting. Past president’s message: Risk analysis under
fire. Risk Newsletter. 2000;20(3):3.
53. Berry CL. Relativism, regulation and the dangers of indifferent science: The
Sir Roy Cameron Lecture of the Royal College of Pathologists. Toxicology.
2010;267(1):7–13.
54. Bartolomeus A, Parrott W, Bondy G, Walker K. The use of whole food animal
studies in the safety assessment of genetically modified crops: Limitations
and recommendations. Crit Rev Toxicol. 2013;43(S2):1–24.
55. Millstone E, Brunner E, Mayer S. Beyond substantial equivalence. Nature.
1999;401(6753):525–526.
56. Traavik T, Ching LL. Biosafety first: Holistic approaches to risk and uncer tainty
in genetic engineering and genetically modified organisms. Trondheim: Tapir
Academic Press; 2007.
57. Hilbeck A, Meier M, Römbke J, Jänsch S, Teichmann H, Tappeser B.
Environmental risk assessment of genetically modified plants – Concepts and
controversies. Environmental Sciences Europe. 2011;23(1):1–13. Available
from: http://www.enveurope.com/content/23/1/13
58. Vlek C. Judicious management of uncertain risks I: Developments and criticisms
of risk analysis and precautionary reasoning. J Risk Res. 2010;13(4):517–543.
59. Castell S, Charlton A, Clemence M, Pettigrew N, Pope S, Quigley A, et al.
Public attitudes to science [document on the Internet]. c2014 [cited 2015
Feb 14]. Available from: http://www.ipsos‑mori.com/Assets/Docs/Polls/
pas‑2014‑main‑report.pdf
60. International Risk Governance Council (IRGC). White paper: Risk governance
towards an integrated approach [homepage on the Internet]. c2005 [cited
2015 Feb 14]. Available from: http://irgc.org/wp‑content/uploads/2012/04/
IRGC_WP_No_1_Risk_Governance__reprinted_version_3.pdf
61. Dreyer M, Renn O. Food safety governance: Integrating science, precaution
and public involvement. Berlin: Springer‑Verlag; 2009.
62. Majone G. What price safety? The precautionary principle and its policy
implications. J Common Mark Stud. 2002;40(1):89–109.
63. Peterson M. The precautionary principle should not be taken as a basis for
decision‑making: Talking point on the precautionary principle. EMBO Rep.
2007;8(4):305–308.
64. Gray J. Statistics and the precautionary principle. Mar Pollut Bull.
1990;21(4):174–176.
65. Baker T. Liability and insurance after September 11: Embracing risks
meets the precautionary principle. Geneva Papers on Risk and Insurance.
2002;27(3):349–357.
66. Marchant GE, Mossman KL. Arbitrary and capricious: The precautionary
principle in the European Union courts. Washington DC: American Enterprise
Institute; 2005.
67. Hanekamp J, Bast A. Food supplements and European regulation within a
precautionary context: A critique and implications for nutritional, toxicological
and regulatory consistency. Crit Rev Food Sci Nutr. 2007;47(3):267–285.
68. De Sadeleer N. The precautionary principle as a device for greater
environmental protection: Lessons from EC courts. Rev Eur Comm Int Environ
Law. 2009;18(1):3–10.
69. Peel J. Interpretation and application of the precautionary principle: Australia’s
contribution. Rev Eur Comm Int Environ Law. 2009;18(1):11–25.
70. Kogan LA. WTO r uling on biotech foods addresses ‘precautionary principle’.
Legal Backgrounder. 2006;21(38):1–4.
71. EuropaBio. Highest courts in France and EU confirm Frances ban on biotech
crops is illegal [homepage on the Internet]. c2011 [cited 2015 Feb 14].
Available from: www.europabio/agricultural/press
72. South African Department of Agriculture, Forestry and Fisheries (DAFF).
Minutes of the GMO Executive Council [document on the Internet]. c2006–
2015 [cited 2015 Feb 20]. Available from: http://www.daff.gov.za/daffweb3/
Branches/Agricultural‑Production‑Health‑Food‑Safety/Genetic‑Resources/
Biosafety/Information
73. Morris EJ, Van Rensburg JBJ, Hoffmann JH, Lazarus P. Good agricultural
practices for developing countries – Lessons learned in South Africa from
an appeal under the GMO Act. In: Ninth ICABR International Conference on
Agricultural Biotechnology: Ten Years Later; 2005 Jul 6–10; Ravello, Italy.
Available from: http://www.economia.uniroma2.it/conferenze/icabr2005/
papers/Morris_Jane_paper.pdf
74. Resnik DB. Is the precautionary principle unscientific? Studies in history and
philosophy of science. Part C: Stud Hist Phil Biol Biomed Sci. 2003;34:329–344.
75. Salo A. On the role of decision analytic modelling. In: Stirling A, editor. On
science and precaution in the management of technological risk. JRC‑IPTS
Technical Repor t EUR19056/EN/2.2001 [document on the Internet]. c2001
[cited 2015 Feb 20]. Available from: http://ftp.jrc.es/EURdoc/eur19056llen.pdf.
76. De Marchi B. Public participation and risk governance. Sci Public Policy.
2003;30(3):171–176.
77. Bush RK, Hefle SL. Food allergens. Crit Rev Food Sci Nutr. 1996;36(S1):119–163.
78. Hefle SL, Nordlee JA, Taylor SL. Allergenic foods. Crit Rev Food Sci Nutr.
1996;36(S1):69–89.
79. Sampson H. Food allergy – Accurately identifying clinical reactivity. Allergy.
2005;60(suppl. 79):19–24.
80. Zuberbier T, Edenhar ter G, Worm M, Ehlers I, Reimann S, Hantke T, et al.
Prevalence of adverse reactions to food in Germany – A population study.
Allergy. 2004;59(3):338–345.
81. Goodman RE, Vieths S, Sampson HA, Hill D, Ebisawa M, Taylor SL, et al.
Allergenicity assessment of genetically modified crops: What makes sense?
Nat Biotechnol. 2008;26(1):73–81.
82. Goodman RE, Tetteh AO. Suggested improvements for the allergenicity
assessment of genetically modified plants used in foods. Curr Allergy Asthma
Rep. 2011;11(4):317–324.
83. Anderson JA. Allergic reactions to foods. Crit Rev Food Sci Nutr.
1996;36(S1):19–38.
84. Sten E, Skov PS, Andersen SB, Torp A, Olesen A, Bindslev‑Jensen U, et al. A
comparative study of the allergenic potency of wild‑type and glyphosate‑tolerant
gene‑modified soybean cultivars. APMIS. 2004;112(1):21–28.
85. Ladics GS, Knippels LM, Penninks AH, Bannon GA, Goodman RE,
Herouet‑Guicheney C. Review of animal models designed to predict the
potential allergenicity of novel proteins in genetically modified crops. Regul
Toxicol Pharmacol. 2010;56(2):212–224.
86. Pastorello EA, Farioli L, Pravettoni V, Ispano M, Scibola E, Trambaioli C, et
al. The maize major allergen, which is responsible for food‑induced allergic
reactions, is a lipid transfer protein. J Allergy Clin Immunol. 2000;106
(4):744–751.
87. Asero R, Mistrello G, Roncarolo D, De Vries SC, Gautier MF, Ciurana CLF, et
al. Lipid transfer protein: A pan‑allergen in plant‑derived foods that is highly
resistant to pepsin digestion. Int Arch Allergy Immunol. 2001;124(1–3):67–69.
88. Pastorello EA, Pompei C, Pravettoni V, Farioli L, Calamari AM, Scibilia J, et
al. Lipid‑transfer protein is the major maize allergen maintaining IgE‑binding
activity after cooking at 100 degrees C, as demonstrated in anaphylactic
patients and patients with positive double‑blind, placebo‑controlled food
challenge results. J Allergy Clin Immunol. 2003;112(4):775–783.
89. Zavala MPV, Robledo GBV, Olivas MAS, Diaz RJD, Oviedo C. Maize (Zea
mays): Allergen or toleragen? Participation of the cereal in allergic disease and
positivity incidence in cutaneous tests. Rev Alerg Méx. 2006;53(6):207–211.
90. Goodman RE, Panda R, Ariyarathna H. Evaluation of endogenous allergens
for the safety evaluation of genetically engineered food crops: Review of
potential risks, test methods, examples and relevance. J Agric Food Chem.
2013;61:8317–8332.
91. Herman RA, Ladics GS. Endogenous allergen upregulation: Transgenic vs.
traditionally bred crops. Food Chem Toxicol. 2011;49:2667–2669.