Harmful Algae 40 (2014) 63–74

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Harmful Algae
journal homepage: www.elsevier.com/locate/hal

Current approaches to cyanotoxin risk assessment and risk

management around the globe
Bas W. Ibelings a,*, Lorraine C. Backer b, W. Edwin A. Kardinaal c, Ingrid Chorus d
a
Institute F.-A. Forel and Institute of Environmental Sciences University of Geneva, 10 Route de Suisse, 1290 Versoix, Switzerland
b
National Center for Environmental Health, 4770 Buford Highway NE, MS F-57, Chamblee, GA 30341, USA
c
KWR, Watercycle Research Institute, Groningenhaven 7, 3433 PE Nieuwegein, The Netherlands
d
German Federal Environment Agency, Corrensplatz 1, 14195 Berlin, Germany

A R T I C L E I N F O A B S T R A C T

Article history: Toxic cyanobacteria became more widely recognized as a potential health hazard in the 1990s, and in
Received 2 April 2014 1998 the World Health Organization (WHO) first published a provisional Guideline Value of 1 mg L1 for
Received in revised form 3 October 2014 microcystin-LR in drinking-water. In this publication we compare risk assessment and risk management
Accepted 3 October 2014
of toxic cyanobacteria in 17 countries across all five continents. We focus on the three main (oral)
Available online 5 November 2014
exposure vehicles to cyanotoxins: drinking-water, water related recreational and freshwater seafood.
Most countries have implemented the provisional WHO Guideline Value, some as legally binding
Keywords:
standard, to ensure the distribution of safe drinking-water with respect to microcystins. Regulation,
Algal blooms
Drinking-water
however, also needs to address the possible presence of a wide range of other cyanotoxins and bioactive
Eutrophication compounds, for which no guideline values can be derived due to insufficient toxicological data. The
Guideline-values presence of microcystins (commonly expressed as microcystin-LR equivalents) may be used as proxy for
Microcystins overall guidance on risk management, but this simplification may miss certain risks, for instance from
Recreation dissolved fractions of cylindrospermopsin and cyanobacterial neurotoxins. An alternative approach,
often taken for risk assessment and management in recreational waters, is to regulate cyanobacterial
presence – as cell numbers or biomass – rather than individual toxins. Here, many countries have
implemented a two or three tier alert level system with incremental severity. These systems define the
levels where responses are switched from Surveillance to Alert and finally to Action Mode and they
specify the short-term actions that follow. Surface bloom formation is commonly judged to be a
significant risk because of the elevated concentration of microcystins in a scum. Countries have based
their derivations of legally binding standards, guideline values, maximally allowed concentrations (or
limits named otherwise) on very similar scientific methodology, but underlying assumptions such as
bloom duration, average body size and the amount of water consumed while swimming vary according
to local circumstances. Furthermore, for toxins with incomplete toxicological data elements of expert
judgment become more relevant and this also leads to a larger degree of variation between countries’
thresholds triggering certain actions. Cyanobacterial blooms and their cyanotoxin content are a highly
variable phenomenon, largely depending on local conditions, and likely concentrations can be assessed
and managed best if the specific conditions of the locality are known and their impact on bloom
occurrence are understood. Risk Management Frameworks, such as for example the Water Safety Plan
concept of the WHO and the ‘bathing water profile’ of the European Union are suggested to be effective
approaches for preventing human exposure by managing toxic cyanobacteria from catchment to
consumer for drinking water and at recreational sites.
ß 2014 Elsevier B.V. All rights reserved.

* Corresponding author. Tel.: +41 223790313.

E-mail address: bastiaan.ibelings@unige.ch (B.W. Ibelings).

http://dx.doi.org/10.1016/j.hal.2014.10.002
1568-9883/ß 2014 Elsevier B.V. All rights reserved.
64 B.W. Ibelings et al. / Harmful Algae 40 (2014) 63–74

1. Introduction Box 1. Abbreviations

Cyanobacteria cause problems worldwide, and the major cause ATX Anatoxin(s)-a/a(s)
for the global occurrence of nuisance blooms is eutrophication of BMAA Beta-N-methylamino-L-alanine
surface water, in particular through excessive use of fertilizer and Chl-a Chlorophyll-a
CYN Cylindrospermopsin
manure in agriculture as well as through sewage discharges.
ELISA Enzyme linked immunosorbent assay
Climate warming also seems to play a role (Paerl and Huisman, EU BWD European Union Bathing Water Directive
2009), whether through direct effects of warming or earlier, EU DWD European Union Drinking Water Directive
prolonged or higher water column stability (Carey et al., 2012). EU WFD European Union Water Framework Directive
Eutrophication and climate may act together in supporting GDWQ WHO Guideline Values for Drinking Water
GV Guideline value
cyanobacterial blooms (Brookes and Carey, 2011; Carey et al.,
HACCP Hazard analysis and critical control points
2012), although the evidence for synergistic interactions seems (H)AL (Health) Alert level
strongly dependent on trophic state and the cyanobacterial taxa i.p. Intraperitonial (injection in body cavity)
involved (Rigosi et al., 2014). Blooms have been reduced IARC International agency for research on cancer
successfully in a large number of lake restoration programs, which MCYST Microcystin(s)
N(L)OAEL No (lowest) observed adverse effect level
almost invariably include abatement of nutrient loading in the NOD Nodularin
catchment (Schindler, 2006; Schindler et al., 2008), sometimes in OATP Organic anion transporting polypetides
combination with additional measures like biomanipulation to PHRMP Public Health Risk Management Plans
interrupt the hysteresis of the turbid stable state (Jeppesen et al., (P)MAC (Provisional) Maximum concentration
(P)MAV (Provisional) Maximum value
2007). In some cases internal measures like artificial mixing of
PST Paralytic shellfish toxins
lakes have been successful in removing nuisance blooms even in RMF Risk management framework
the absence of nutrient reduction (Visser et al., 1996). S Standard value
Toxic cyanobacteria started to be more widely recognized as a STX Saxitoxin(s)
potential health hazard in the 1980s, a number of case studies were TDI Tolerable daily intake
TWQR Target water quality range
published attributing illness to cyanobacterial toxins (see Kuiper- UF Uncertainty factors
Goodman et al., 1999; Chorus et al., 2000), and numerous cases of US EPA USA Environmental Protection Agency
animal deaths along water courses afflicted with cyanobacterial WHO World Health Organization
blooms were calling public attention to the issue. Progress in the WSP Water Safety Plan
elucidation of the chemical structures of a number of cyanotoxins
and in the availability of chemical detection methods suitable for
routine analyses picked up speed in the mid 1980s, and by the late Maximal cyanotoxin concentrations in a given waterbody,
1990s a wider understanding of both their modes of action and however, largely depend on the concentrations of cyanobacterial
their occurrence was available (Chorus and Bartram, 1999). The biomass – modified by the ratio of toxic to non-toxic strains,
accumulating data suggested that, among the chemicals found in currently or previously present. In particular, concentration via
water or used for drinking or recreation, cyanotoxins may well be scum formation (i.e. the accumulation of floating cyanobacteria at
among the substances occurring most frequently at potentially the lake surface during periods of calm weather) may increase
harmful concentrations. In 1998 the World Health Organization toxin levels by orders of magnitude Therefore the amount of
(WHO; see Box 1 for all abbreviations) first published a provisional cyanobacteria observed can serve as a basis for alert level
drinking-water Guideline Value of 1 mg L1 for one very common frameworks and risk assessment well before, or even without
cyanotoxin, microcystin-LR (MCYST-LR), in its Addendum to Volume toxin analysis. Accordingly, some countries are implementing alert
2 of the Guidelines for Drinking-water Quality (see Chorus and level frameworks and risk-based approaches on basis of cyano-
Bartram, 1999). Since then, the number of countries which have bacterial cell numbers or biovolume in their national guidance or
addressed the cyanotoxin hazard has increased and further countries regulations, sometimes complementary to regulating maximum
are currently discussing the most appropriate regulatory approach cyanotoxin concentrations.
for their respective conditions. The primarily hepatotoxic micro- In principle, regulatory approaches differ for the main three
cystins – a family of more than 80 different congeners, commonly exposure routes to cyanotoxins, i.e. oral, pulmonary and dermal.
measured and expressed as total MCYST-LR equivalents – are Dermal symptoms caused by freshwater cyanobacteria are
probably the most widespread and best studied group of cyanotoxins typically mild and self-limiting, thus requiring some public
(Dittmann et al., 2013; Ferrao-Filho and Kozlowsky-Suzuki, 2011; education and guidance, but not necessarily regulation. Concern
Ibelings and Havens, 2008; Kozlowsky-Suzuki et al., 2012). Data on regarding pulmonary exposure to date is based on two early
the occurrence of other cyanotoxins are increasingly becoming studies, i.e. one exposing guinea pigs experimentally (Falconer and
available, particularly for cylindrospermopsin (CYN), neurotoxins like Humpage, 2005) and one evaluating atypical pneumonia of army
saxitoxin (STX) or anatoxins (ATX) (Metcalf et al., 2008; Seifert et al., cadets submersed during their training (Lawton and Codd, 1991).
2007; van Apeldoorn et al., 2007; van der Merwe et al., 2012) and However, more recent studies confirming this exposure route to be
information on new classes arising (e.g. jamaicamides, Neilan et al., relevant are lacking, and uptake through aspiration usually also
2013). Regulations and guidelines, however, have been struggling involves swallowing, thus at least partially occurring via the oral
with the multitude of cyanobacterial toxins that might occur, be it pathway. Accordingly, regulations and guidelines to date focus on
other microcystins or different classes of toxins, particularly as for the main vehicles of oral exposure, i.e. ingestion of toxins via
most of them, toxicological data are insufficient for the derivation of drinking-water, recreation or consumption of fish, molluscs and
concentration limits. crayfish from freshwater bodies, which we term ‘freshwater
To some extent toxin levels respond to environmental seafood’. The literature on exposure through drinking-water (e.g.
conditions so that the toxin content per cell may vary several Falconer and Humpage, 2005; Hitzfeld et al., 2000; Zamyadi et al.,
fold (Neilan et al., 2013; van der Merwe et al., 2012; Wiedner et al., 2012) is more extensive than that for other possible exposure
2003); also the proportion of different MCYST congeners may vehicles, notably recreational exposure (Backer et al., 2010; Chorus
change with changes in the environment (Tonk et al., 2005). et al., 2000) and uptake via food (Ibelings and Chorus, 2007). The
 B.W. Ibelings et al. / Harmful Algae 40 (2014) 63–74 65

focus on drinking-water may be attributed to its exceptional role 2. Methods

as basis for life, with daily consumption in the range of liters and
little means for individuals to avoid exposure when it is During the VI and the VIII International Conference on Toxic
contaminated. On the other hand in countries where drinking Cyanobacteria, held in Norway (2004) and Turkey (2010),
water is usually well treated while eutrophication is still scientists and regulators reported on regulations aimed at
widespread and blooms are common, recreation may be the controlling the risks of exposure to toxic cyanobacteria in their
major exposure vehicle (Codd, pers. comm.). respective countries, and all conference participants were invited
The 1998 WHO provisional Guideline Value (GV) of 1 mg L1 for to submit a summary of regulations in their country for a report
the concentration of MCYST-LR in drinking-water was based upon entitled ‘‘Current approaches to cyanotoxin risk assessment, risk
laboratory studies with mice which resulted in a No Observed management and regulations in different countries’’, compiled and
Adverse Effect Level (NOAEL) of 40 mg kg1 bodyweight d1; the edited by Chorus (2005, 2012). A wide variety of contributions was
GV was derived using the following equation: submitted from countries in Africa, Australasia, Europe and the
Americas, although neither compilation attempted to be compre-
hensive or globally balanced. From both reports we have amassed
1 1 1 data to summarize current regulations for drinking-water (Sup-
GV ¼ 40 mg kg bw d  60 kg  0:8=2 L d  1000
plementary materials Table S1), recreational waterbody use
where 60 kg is the average bodyweight of an adult, 0.8 the (Table S2) and freshwater food (Table S3). A priori it appears
proportion of daily intake of MCYST attributed to drinking-water, valuable to compare regulatory approaches taken in various
2 L the average consumption per day, and the factor of 1000 to countries who greatly differ in lake types (e.g. depth or trophic
account for intra- and interspecies variation (a factor of 10 each) state), regional climate, lake use (drinking-water production,
and for uncertainties in the data, i.e. lack of data on lifetime recreational intensity, etc.), public awareness of the issue, legal
exposure and carcinogenicity of MCYST-LR (a further factor of 10). status of the guidelines and regulations, governance structure
The Tolerable Daily Intake (TDI) is calculated from the NOAEL (federal vs. de-centralized) and presence or absence of overarch-
divided by the factor of 1000, i.e. 0.04 mg kg1 bw d1. This TDI ing, even international frameworks like the BWD in European
was also used as one basis for WHO Guidelines for safe recreational countries.
exposure (Chorus et al., 2000). We emphasize that none of the contributions to Chorus (2005,
In addition to their production of toxins, cyanobacteria owe 2012) which are used as a basis for this manuscript represent
their reputation as the ‘scourge of water management’ (Visser formal government contributions, rather these are inputs from
et al., 2005) to a further specific trait, the production of scientists or managers working in their respective countries.
intracellular gas-vacuoles (Kinsman et al., 1991; Walsby et al., Nevertheless for ease of understanding we will refer to countries
1991). These gas-vacuoles provide cyanobacteria with buoyancy, by their names in Sections 3 and 4.
so that in the absence of water-body mixing cyanobacterial cells
and colonies suspended in the water may float to the lake surface 3. Results
and accumulate in dense surface scums. Since microcystins are
predominately intracellular, when biomass accumulates micro- Most countries that regulate cyanotoxins define limits for
cystin concentrations increase manifold and risk assessment needs concentrations in finished drinking-water and, albeit less widely,
to take this into account. Scums often drift toward the shore, where in water used for recreational purposes. Such limits are defined for
the risk of human or animal contact with such high concentrations MCYST in general or specifically for MCYST-LR, while other
of cyanobacteria and the toxins they contain or release when cells cyanotoxins are rarely explicitly regulated. The status of limits
lyse is considerably higher (Ibelings et al., 2003). While this applies varies between countries, as is reflected in terminology such as
to cyanotoxins which are pre-dominantly intracellular, in particu- guideline value, standard maximum acceptable value, maximum
lar to microcystins, this accumulation mechanism may be less acceptable concentration or health alert level, some of which are
pronounced for other cyanotoxins, such as saxitoxins or cylin- explicitly labeled ‘provisional’ (see Box 1 for abbreviations). In
drospermopsin, of which a larger fraction often occurs extracellu- some countries regulations or guidance for toxin concentrations in
larly – more than 50% or even almost all of the toxin (Saker and water are supplemented and supported by the implementation of
Griffiths, 2000). alert level frameworks to indicate the risk of cyanotoxin
Countries have implemented cyanotoxin guidelines or stan- occurrence. For drinking-water this is the case in e.g. Australia,
dards and procedures to assess and manage the risk of cyanotoxins. France, Finland, New Zealand, and Singapore. For recreational
These standardized guidelines and regulations address the waterbody use, most guidance or regulations are based on some
concentrations of cyanobacteria or their toxins that should not measure of cyanobacterial bloom intensity, using parameters such
be exceeded. Usually together with immediate, short-term actions as cell number, biovolume or pigment concentration (Chl-a or –
to take if these concentrations are exceeded in order to prevent or more specifically for cyanobacteria–phycocyanin/phycoerythrin,
minimize exposure to harmful cyanobacteria and their toxins. both detectable in situ by fluorometry probes) to reflect the
Herein we report these national guidelines, distinguishing concentration of cyanobacterial biomass. Such alert level frame-
regulations for the major oral exposure vehicles, i.e. drinking- works typically define 2 or 3 levels of cyanobacterial biomass to
water and recreation, and including those for food from those few guide responses (e.g. intensified monitoring) or interventions (e.g.
countries which have implemented regulations. We assess the upgrading treatment or temporarily banning site use).
progress in regulatory approaches toward cyanotoxins and discuss The full results of the international survey are presented in
why countries choose to implement different guidelines and Supplementary Material Tables S1 (drinking-water), S2 (recrea-
regulations, based upon the same scientific underpinnings. We tion) and S3 (food), with summary data and typical examples from
further show how this progress has moved from a focus on some countries presented in graphs and discussed in the text.
monitoring based on guideline values to more comprehensive
approaches of risk assessment and risk management, in particular 3.1. Drinking-water
with reference to the WHO Water Safety Plan concept (see Ibelings
& Chorus, 2007) and the Bathing Water Directive (BWD) of the Most countries with regulations or guidance on cyanotoxin in
European Union. drinking-water base their limit for the concentration in finished
66 B.W. Ibelings et al. / Harmful Algae 40 (2014) 63–74

drinking-water on the provisional WHO Guideline Value for toxins). PMAVs are informed by current scientific understanding,
MCYST-LR of 1 mg L1 or they use the underlying TDI of 0.04 mg per even if incomplete. Cyanobacteria and cyanotoxins do not fall in
kg body-weight with some minor national adaptations (for the highest priority class (which contains infectious microorgan-
amount of water consumed and/or average body-weight). In isms), but are listed as Priority Class 2 determinants, together with
consequence, variations between the limits thus derived by chemical pollutants. Of interest is the remark that unlike other
different countries are minor, i.e. limits range from 1.0 to Class 2 contaminants cyanotoxins can increase rapidly, as the
1.5 mg L1 (Fig. 1). A number of countries define a legally binding source in cyanobacterial blooms and scums fluctuates with
standard value (S) of 1 mg L1 MCYST-LR in the final product (tap environmental conditions. New Zealand, like Australia has a Risk
water) e.g. Brazil, Uruguay, The Czech Republic, France and Spain Management Framework (see Section 4) in place, and the authors
(Azevedo, Vidal and Britos, Marsalek et al., Griscya, Quesada et al., report this as having been effective in preventing concentrations
in Chorus, 2005, 2012). Some countries like Canada, the Czech exceeding the PMAVs in drinking-water reservoirs from having
republic or Singapore (Giddings et al., Marsalek et al., Wong et al., reached consumers (Wood and Williamson in Chorus, 2012).
in Chorus, 2012) explicitly refer only to MCYST-LR, more often In the European Union, national drinking-water legislation is
microcystins are expressed as MCYST-LR equivalents (sum of all required to be based on the Drinking Water Directive. This
variants), e.g. in Australia, France or Finland (Mulvenna and Orr, stipulates an overall objective ‘‘to protect human health from the
Griscya, Rapala et al., in Chorus, 2012). Other toxins for which some adverse effects of any contamination of water intended for human
countries give guidance (but not legally binding standards) include consumption by ensuring that it is wholesome and clean’’ and that
CYN (1 mg L1 in Australia and New Zealand or 15 mg L1 in Brazil), it is ‘‘free from any micro-organisms and parasites and from any
STX (3 mg L1 in Australia, New Zealand and Brazil) or ATX-a substances which, in numbers or concentrations, constitute a
(3.7 mg L1 in Canada, 6 mg L1 in New Zealand) (Burch and potential danger to human health’’. However, it does not explicitly
Humpage, Wood and Williamson, in Chorus, 2005, 2012). address cyanobacterial toxins. For Poland, Mankiewicz-Boczek
Health Canada assessed MCYST-LR as potentially carcinogenic, et al. (in Chorus, 2012) explain that while a GV of 1 mg L1 for
based upon limited evidence in experimental animals; Canada has MCYST-LR had been included in Polish legislation in 2002, this was
implemented a provisional Maximum Acceptable Concentration repealed in 2012 since the DWD does not specify MCYST. Also
(PMAC) for MCYST-LR of 1.5 mg L1 in treated drinking-water, Denmark, Germany, Greece, Hungary and the Netherlands
aimed to protect against the sum of all MCYST (Giddings et al., in (Christoffersen and Warming, Chorus, Kagalou et al., Törökne,
Chorus, 2012). The value is slightly higher than the provisional Ibelings et al., in Chorus, 2005, 2012) have no specific regulations
WHO GV because Health Canada assumes a somewhat greater for cyanobacteria and their toxins in drinking-water. For Denmark,
bodyweight and smaller intake of drinking-water (as the bloom Germany and Hungary the authors explain that one reason why
season lasting only 3–4 months). The US federal government has this is not considered necessary is that direct use of surface water
not established regulations or guidelines to define acceptable contributes only a minor percentage of the drinking-water
levels of cyanotoxins in drinking-water (or recreational water), (Christoffersen and Warming 2012 in Chorus, 2005; Törökné
although cyanobacteria and their toxins are on the Drinking-Water 2005, in Chorus, 2005, 2012). The German Drinking Water
Contaminant Candidate List and assessments on whether or not to Ordinance, however, explicitly requires that no substances may
regulate them are ongoing; however, three of the fifty states of the occur in hazardous concentrations, and this means that if MCYST is
USA have regulations or health advisory levels for them in found, operators or health authorities would turn to the
drinking-water (Hudnell et al. in Chorus, 2012). provisional WHO GV to assess whether the concentration found
New Zealand has regulations for the largest range of toxins in would qualify as ‘‘hazardous’’.
drinking-water: MCYST-LR eq., STX-eq., ATX (a + a(s)), NOD, and
Homoanatoxin-a. Cyanotoxins are regulated through Provisional 3.2. Recreation
Maximum Acceptable Values (PMAVs), since there are no WHO
guidelines for most of them – other than the provisional WHO Many countries apply a two or three tier alert level framework
guideline for MCYST-LR (see Table S2 for PMAVs for the respective with incremental severity, based upon the immediate, short term
assessment of cyanobacterial cell numbers or biovolume at a
recreational site. The lowest level ‘Surveillance Mode’ typically
2.0
does not result in any public action, it merely leads authorities to
continue or intensify their monitoring efforts. The next level ‘Alert
Mode’ is a consequence of an indicator like microcystin (Fig. 2, top
1.5 panel) or cyanobacterial cell counts/biovolume (Fig. 2 middle and
lower panel) exceeding a threshold value. At Alert Mode, typically
Microcystins (μg / L)

the public is warned via on site signs, information via the Internet,
telephone hotlines, etc. Warning signs may inform the public about
1.0 the increased risks for skin irritation and gastro-intestinal illness.
The highest level ‘Action Mode’ is based upon one of several
conditions: (i) the presence of persistent cyanobacterial blooms or
surface scums, (ii) surpassing the next level threshold in
0.5
cyanobacterial biomass (as pigment concentration, cell counts
or biovolume), or (iii) any report of toxic effects attributed to
cyanobacteria. In this mode the public is typically advised to
0.0
refrain from recreation involving water contact (particularly with
the risk of oral uptake), and authorities may actually temporarily
Turkey
Canada

New Zealand

Australia

Brazil

France
Czech Republic

Singapore

Spain

South Africa

Ohio

Oregon
Argentina

Florida

close waterbodies for primary contact recreation like swimming.

Australia (Burch, 2008, Mulvenna and Orr in Chorus, 2012)
distinguishes two further levels of ‘Action Mode’: level one is
based upon adverse health effects from ingestion of known toxins,
Fig. 1. Guideline values for microcystin in drinking-water compared internationally. based upon toxicity data for MCYST-LR; level two is based on the
 B.W. Ibelings et al. / Harmful Algae 40 (2014) 63–74 67

likelihood of adverse health effects resulting from exposure to high

cell densities, irrespective of the presence of known toxins.
The three tier based cyanobacterial protocol for use in
recreational waters shown in Fig. 3, as used in the Netherlands
(Ibelings et al., in Chorus, 2012) is a typical example of an alert
levels framework for recreational water-body use: bathing sites in
this country are monitored on at least a fortnightly basis.
Professionals take samples at representative locations for subse-
quent analysis of cyanobacterial biomass using a microscope or
DNA analysis (qPCR). They are also equipped with pictures of
surface scums of increasing intensity as well as with a FluoroProbe
(BBE Moldaenke GmbH) that measures cyanobacterial pigment
(phycocyanin) concentration to assist their immediate on-site
assessment. Scums of categories I and II lead to up-scaling from
Surveillance to Alert Mode, and so does cyano-chlorophyll-
a > 12.5 mg L1 or cyano-biovolume > 2.5 mm3 L1. At this alert
level, where health risks are deemed limited, the monitoring
frequency increases from fortnightly to weekly, and a warming is
posted: ‘‘Warning toxic blue-green algae, risk of skin irritation or
intestinal problems’’. The warning may be evaluated on a daily
basis if on-site inspection is available. In case of scums of the
highest category III or cyano-chlorophyll-a > 75 mg L1 or cyano-
biovolume > 15 mm3 L1 the alert level is raised to Action Mode,
and bathing is dissuaded by the following warning: ‘‘Warning toxic
blue-green algae. You are advised not to bathe in this water’’. Local
authorities have the right to close the site for recreation.
Canada (Giddings et al., in Chorus, 2012) applies only a single
level as guideline value for recreation, a GV of 20 mg L1 MCYST-
LR-eq., based upon the NOAEL of 40 mg kg 1 bodyweight (Fawell
et al., 1999) and an uncertainty factor of 100. In this case no
additional uncertainty factor for life time exposure is taken into
account, given that recreation is short lived and episodic. Moreover
the GV was developed with children in mind as through their lower
bodyweight and behavior they are more at risk than adults
(assumption of a 13 kg child ingesting 0.25 L of lake water).
Singapore (Wong et al., in Chorus, 2012) also uses a single Chl-a
based Alert/Action level of >50 mg L1: over a 3 year period water
quality must comply with this standard during 95% of the time. If
not, freshwater systems can be judged to be unsuitable for
swimming, and the public would be notified of this. In the US,
there are no federal guidelines, water quality criteria, or
regulations concerning the management of harmful algal blooms,
either in drinking water or recreational waters. However, 21 of
the fifty states have implemented some form of guidance on
cyanobacterial or cyanotoxin occurrence in recreational waters
(Hudnell et al. in Chorus, 2012). For example, Ohio has a
regulatory limit of 1 mg L1 of microcystin in drinking water. In
addition, a health advisory or ‘‘no contact’’ advisory is posted
when recreational water concentrations of microcystin are
6 mg L1 or 20 mg L1, respectively.
New Zealand (Wood and Williamson, in Chorus, 2012) is one of
only two countries where benthic mats of cyanobacteria are also
part of the classification (see Table S2). Similar to planktonic
cyanobacteria three alert levels – corresponding to Surveillance,
Alert and Action Mode –are distinguished. Photographs to assist in
sampling and risk assessment are provided. Surveillance Mode is
Fig. 2. Alert levels for toxic cyanobacteria in recreational waters compared based upon up to 20% coverage of the sediment with potentially
internationally on basis of microcystins (top panel), cell numbers (middle panel) toxigenic benthic cyanobacteria and results in fortnightly surveys
and biovolume of cyanobacteria (lower panel). White means Surveillance mode,
black Alert mode and hatched Action mode. See text for details. The upper end of the
at representative locations in the water body. In Alert Mode (20–
scale is ‘‘open’’, meaning that for instance any level of microcystin exceeding the 50% coverage) the sampling frequency and intensity is increased,
upper boundary of Alert mode automatically falls into Action mode, but the public health unit is informed and toxicity testing is
concentrations (in particular in scums) clearly can be higher than the maximum recommended. When coverage of benthic, potentially toxigenic
value of 150 mg L1 on the y-axis of the top panel a (analogous for middle and lower
cyanobacteria exceeds 50% (or when up to 50% coverage, but
panels).
benthic cyanobacteria are visibly detaching from their substrate)
the alert level is raised to Action Mode, amongst others resulting in
notification of the general public.
68 B.W. Ibelings et al. / Harmful Algae 40 (2014) 63–74

Fig. 3. Example of a cyanobacterial protocol used for uniform risk assessment and management of recreational waters in the Netherlands.

In Finland (Rapala et al., 2012 in Chorus, 2012) cyanobacteria and take action to improve water quality and protect human
are monitored weekly on 300 predetermined sites. Four levels of health. In line with EU Bathing Water Directive (BWD) it does not
algal (including cyanobacteria) abundance are based upon visual specify the actions to be taken but rather their required outcome.
inspection by environmental or public health professionals or For member states of the European Union (EU) the BWD
trained volunteers. The observations are ranked in four classes, and provides the basis for regulating recreational water use. Its revision
levels increase from no algae visible (Level 0) to greenish flakes or in 2006 first introduced a risk-based framework for freshwater and
narrow stripes (Level 1), to strong coloration or small surface coastal recreational sites – the ‘‘bathing water profiles’’. These
scums (Level 2) and widespread and dense surface scums or require the responsible authorities to assess potentially contami-
aggregates of floating cyanobacteria at the lake shore (Level 3). nating conditions influencing the site to enable timely identifica-
Although the system is based upon visual inspection, microscopic tion of health risks, and amongst others this includes describing
analysis of cyanobacteria or analysis of toxin concentrations is the potential risk of cyanobacterial proliferation for individual
advised. Regional authorities make the information available via bathing waters (see Table S2). While the BWD describes risk
LakeWiki. A weekly report summarizing the information for assessment and regulations in general terms, most EU member
Finland as a whole is created and published, including a color states specify this through more specific regulations, in many cases
coded map and a cyanobacterial ‘‘abundance barometer’’. The based upon quantitative analysis of cyanobacterial density or
LakeWiki database in addition contains basic information of all biomass. Interestingly, while the two- or three-tiered alert level
55 821 lakes larger than 1 ha in Finland. Citizens are invited to frameworks used by many countries show similarities, the
update information, amongst others with pictures of cyanobacter- thresholds they use to increase alerts from one level to the next
ial blooms. are much more variable than the guideline values or standards for
The German system is also based upon visual assessment of drinking-water. For moving the alert level from basic (Monitoring/
sites, combined with assessment of cyanobacterial occurrence; Surveillance Mode) to the next level (Alert Mode), thresholds span
MCYST analyses are included as optional element intended to two orders of magnitude: in terms of cells mL1 from 500 in New
avoid unnecessary restrictions on recreation. Secchi disk readings Zealand, over 5000 in Australia and 20 000 in the Czech Republic,
of less than 1 m and Chl-a exceeding 40 mg L1 with a dominance France and Turkey 20 000–50 000 cells mL1 in Hungary. Likewise
of cyanobacteria result in bathing being discouraged, while whereas many countries change to the highest alert level, Action
presence of scums and MCYST above 100 mg L1 result in the Mode, at 100 000 cells mL1, Australia applies a cut-off at ca. half
recommendation that bathing sites are temporarily closed. this cell density and certain US states (e.g. Texas, Maryland) at yet
The proposed procedure for risk assessment in Polish bathing much lower levels.
waters (Mankiewicz-Boczek et al., in Chorus, 2012) is specific in Alert levels defined on basis of biovolume show similar
that it is the only protocol at present to include molecular variation between countries. In New Zealand for example
detection of toxigenic cyanobacterial strains (PCR amplification of Monitoring Mode is below 0.5 mm3 L–1, Alert Mode between
mcy genes). When positive, the detection of strains capable of 0.5 and <1.8 mm3 L1 and Action Mode is implemented when
producing MCYST is followed by actual screening of MCYST cyanobacterial biovolume is 1.8 mm3 L1 (if potentially toxic
concentration in the surface water. When concentrations mea- cyanobacteria dominate or 10 mm3 L1 for all cyanobacteria). In
sured with ELISA exceed 2.5 mg L1 a more quantitative and Australia these values are >0.04 to <0.4 mm3 L1 for Surveillance
qualitative analysis using HPLC follows. The Polish Water-law of Mode, respectively 0.4 to <4 mm3 L1 for Alert Mode and
2010 states that when bathing water does not meet the required 4 mm3 L1 (when known toxin producers are present) for Action
standards, authorities must determine the cause of the pollution Mode. In the Netherlands >2.5 and >15 mm3 L1 are used for
 B.W. Ibelings et al. / Harmful Algae 40 (2014) 63–74 69

raising the alert levels from Monitoring to Alert and Action Mode As pointed out by WHO, (WHO, 2009), ‘‘the GDWQ provide the
respectively (in the Netherlands dominant cyanobacteria almost scientific point of departure for standard setting and Regulation‘‘; they
invariably belong to toxin producing genera, so that values for are ‘‘based upon the best available evidence and scientific consensus’’
biovolume in the Netherlands can be compared to the more strict . . . and ‘‘are derived so as to take account of the needs of an individual
values for Australia and New Zealand). Germany recommends through a normal lifetime, including changes in sensitivity that may
temporary closure of waterbodies when blooms are conspicuous occur between life stages’’; in particular they ‘‘are the collective
and particularly if MCYST levels exceed 100 mg L1, Italy prohibits product of many experts and of extensive recovered experience‘‘.
bathing at 25 mg L1, while at this level Turkey discourages However, WHO also emphasizes that it is up to national
recreation. In the US California applies a low MCYST based alert governments to decide for which chemicals to set legally binding
level of 0.8 mg L1 for Action Mode, Oklahoma in comparison uses national standards and whether or not to set these at the level
20 mg L1. suggested by the WHO GDWQ. Countries have indeed taken into
account their respective conditions and circumstances, some with
3.3. Food setting somewhat higher values, some with including all micro-
cystins, and some with giving values also for further cyanotoxins,
There are far fewer regulations for exposure via food as though not as legally binding standard, but rather in advisory
compared to exposure via drinking-water. The reason for this fashion, i.e. as guideline values, provisional maximum values or
difference is unclear. It may be unintentional, or it may be that concentrations, or health alert levels.
jurisdictions are prioritizing the drinking-water pathway (see Where guideline values (GV) or preliminary maximum con-
however Ibelings and Chorus, 2007 who demonstrate that in some centrations (PMAC) are given for CYN or neurotoxins, they vary
cases intake through food may exceed that through drinking- more than the relatively fixed GV for MCYST-LR, due to incomplete
water). Of the US states only California provides guidelines and toxicological data and in consequence a need to fill gaps with
regulations on cyanotoxins in fish (Hudnell et al. in Chorus, 2012). assumptions – and assumptions are more variable. Regardless of
California limits cyanotoxins in fish for human consumption as how many cyanotoxins are regulated (New Zealand lists a total of
follows: for MCYST (LA, LR, RR, YR) up to 10 ng g1 wet weight seven different toxins) it is clear that some risk of exposure
(ww), for CYN 66 ng g1, and for ATX 1100 ng g1 ww (Table S3). through drinking-water may remain regarding further unknown
With the exception of STX for marine shellfish Australia (Mulvenna and possibly harmful metabolites produced by cyanobacteria.
and Orr, in Chorus, 2012) does not provide GV on safe levels of
cyanotoxins in freshwater seafood on a national level; Victoria, 4.2. Microcystin as guidance or lead toxin in drinking water
however, does provide Health Alert Levels (HAL; see Table S3 in
Supplementary material): for CYN and deoxy-CYN the HAL is 18– A number of countries implicitly use the toxicological assess-
39 mg kg1 ww of whole organism while for MCYST-LR or ment of MCYST-LR to define maximum accepted concentrations
equivalent hepatotoxins it is 24–51 mg kg1 ww and for STX for all microcystins, based on the assumption that as no other
(800 mg kg1) of whole organism. variant is known to have a higher acute i.p. toxicity this approach is
Denmark (Christoffersen and Warming 2012, in Chorus, 2012) likely to be conservative, i.e. reflecting a worst-case scenario. There
has no specific regulations for cyanotoxins, but harvesting and are indications that this may not be the case. Results of a study by
distribution of mussels is only allowed if no algal toxins – of all Fischer et al. (2010) on the activity of specific organic anion
known types – are detected in water and animals and standards for transporting polypeptides (OATPs) indicate enhanced cellular
food hygiene regulations are met. A new order has been put in uptake of the more hydrophobic MCYST-LW and -LF, which could
place in 2011 – implementation of EU Regulations on food hygiene result in higher toxicity of these congeners, however results
and control of products from animal origin – targeted specifically obtained with cellular assays cannot be quantitatively extrapolat-
at monitoring algae and their toxins for sites where breeding and ed to whole organisms. Microcystins are often measured as the
harvesting of mussels takes place, hence aimed at marine sum of all variants and then expressed as MCYST-LR equivalents.
environment (Mytilus edulis and marine toxins). At present this Furthermore, where cyanobacterial numbers or biomass are used,
specific EU regulation does not appear to be used for protection their tolerable levels are set on the basis of ratios of microcystins to
against cyanotoxins in freshwater seafood. France also recognizes biomass or chlorophyll-a, or on the basis of content per cell. This
the primary focus on marine seafood but does acknowledge that adds a further assumption, i.e. that ratios or cellular content will be
based on a chronic TDI of 0.04 mg kg1 bw d1 a daily consumption in the same range for other cyanotoxins. The question thus is: how
of fish of 86 g and an intake of 2 L drinking-water per day (at justified is the use of a value for MCYST-LR as general ‘indicator’ of
1 mg L1), the limit for adults consuming freshwater species would cyanotoxin risk?
be 5.6 mg MCYST per kg fish (for edible parts of fish). For children A justification implicitly or explicitly encountered is the
with a lower bodyweight and lower consumption, the limit value frequency of MCYST occurrence, which particularly at high
would be 1.4 mg kg1 of fish. Similarly, Greece acknowledges that a concentrations in scums or high density of dispersed filamentous
300 g serving of carp would exceed the TDI for lifelong consump- cyanobacteria in hypertrophic lakes carries potential sub-acute
tion 14-fold. Also consumption of Astacus astacus and Rana and even acute health risks (see Ibelings and Chorus, 2007).
epirotica would exceed the TDI approximately six-fold. Moreover, indeed the maximum reported ratios of toxins to
cyanobacterial biomass so far published do not tend to be higher
4. Discussion for any of the other known cyanotoxins. Thus, an alert level based
on a maximum ratio of MCYST-LR to biomass is likely to provide a
4.1. Guideline values similar level of protection if the toxin is not MCYST-LR but e.g. CYN
or ATX. The more critical issue may be that the underlying
A conspicuous outcome of the comparison of regulatory assumption of oral toxicity being in a similar range as that of
approaches is the homogeneity of the values used for microcystins MCYST-LR is not well understood. For microcystin-congeners other
in drinking-water: 11 countries use the provisional WHO than MCYST-LR, the above mentioned recent findings by Fischer
Guideline value for Microcystin-LR of 1 mg L1 in their national et al. (2010) on toxicokinetics of MCYST-LW and MCYST-LF have
approaches to cyanotoxins. This reflects a high level of acceptance led to a call for a MCYST congener specific approach in risk
of the WHO Guidelines for Drinking-water Quality (WHO GDWQ). assessment (Faassen and Lurling, 2013).
70 B.W. Ibelings et al. / Harmful Algae 40 (2014) 63–74

A relevant – though implicit – justification for orienting 4.4. Cyanobacterial biomass in recreational waters
cyanotoxin guidance along MCYST-LR is that measures taken to
mitigate exposure against MCYST-LR or microcystins will also be As discussed in Section 4.2, the toxicity of Microcystin-LR is
effective against other cyanotoxins. In drinking-water treatment widely used as rough orientation for defining action levels to
this applies to the removal of cell-bound cyanotoxins, but it is protect bathers (Backer et al., 2010; Chorus et al., 2000; Falconer
important to keep in mind that this does not work for cyanotoxins and Humpage, 2005; Fromme et al., 2000; Pilotto et al., 1997), but
dissolved in water – while microcystins are largely cell-bound, this these levels are then defined in terms of cyanobacterial biomass,
is not the case for most other cyanotoxins. Measures taken in the cell numbers or both. These are preferred over cyanotoxins in order
catchment or the water-body address the proliferation of to facilitate monitoring and immediate interventions in response
cyanobacterial cells rather than specific toxins. In consequence, to the results and to account for the potential presence of further
if they are successful against microcystin-producing cyanobac- cyanobacterial metabolites causing for instance the irritating and
teria, they are likely to mitigate the biomass of further inflammatory symptoms reported. A few countries (e.g. Germany,
cyanobacterial taxa that produce other cyanotoxins. This assump- Italy) include the option of a direct measurement of MCYST
tion holds in many cases. Chorus and Niesel (2011) show a very concentration to assess the risk due to toxic cyanobacteria in their
clear dependency of cyanobacterial dominance on the concentra- recreational waters. Others like the Netherlands have abandoned
tions of total phosphorus from a statistical analysis of data from such an approach (cf. contributions Ibelings et al. to Chorus, 2005,
3000 samples collected from 210 waterbodies throughout Europe: 2012) because of the potential relevance of toxins or irritants other
cyanobacterial biovolumes above 0.1 mm3 L1 proved highly than MCYST. Indeed many other metabolites have been identified
unlikely at total phosphorus concentrations below 25 mg L1. as products produced by cyanobacteria (Sivonen et al., 2010;
Welker et al., 2012), but there are very few data on their toxicity. It
4.3. The role of national and local experience in setting guideline is well known, however, that crude extracts of cyanobacterial
values or standards blooms are more toxic than the purified toxins extracted from
them (Ibelings and Havens, 2008), which may be due to
A further factor influencing national approaches to setting unidentified toxic substances or due to synergistic effects between
guideline values or standards is experience. Brownson et al. (2009) known toxins (Pires et al., 2011). As indicator of biomass,
explain that evidence based public healthcare relies upon cyanobacterial cell densities have been commonly used, but
quantitative (e.g. epidemiological, laboratory animal or ecological biovolume or cyano-Chl-a are increasingly preferred (see Table S2)
experiments) as well as qualitative (e.g. narrative accounts) because they are better indicators for potential toxin levels, as
information. Narrative and anecdotal information, however, varies these relate more directly to biomass than to cell numbers (as cell
between countries on basis of national experience with for size differs widely between species). Box 2 gives an overview of the
instance severity of eutrophication and possible calamities with advantages and disadvantages of different assessment methods
harmful cyanobacteria like the Palm Island, Australia or Caruaru, used by various countries for quantification of cyanobacterial
Brazil incidents (Carmichael et al., 2001) which caused the biomass.
hospitalization or death, respectively, of dozens of people (see Although alert levels in Netherlands are distinctively higher
Chorus et al., 2000). In contrast, in many regions of northern than in most other countries the application of these alert levels in
Germany with eutrophication and blooms having been widely risk management still results in warnings or even closure of
prevalent for several decades without human illness having waterbodies on a fairly extensive scale by the responsible
become conspicuous, in spite of intensive recreational water- authorities. This is a country known for the highly eutrophic state
body use, the first discussions in the early 1990s of the need to of its lakes (despite some successful restoration efforts, Gulati and
address cyanobacterial toxins faced considerable skepticism, and it Van Donk, 2002), where stricter alert levels might result in
was dog deaths in the media that convinced the public in the extended closure of many lakes. In the two densely populated
regions where they occurred that actions were required. In western provinces (North- and South-Holland) warnings were
contrast, regulators were soon convinced by the strong weight issued 34 and 90 times, respectively in summer of 2010, whilst
of the scientific evidence in relation to the criteria well accepted for bathing was dissuaded in 9 and 15 cases. A bathing prohibition was
other toxins; moreover, once convinced of the necessity to address given 2 and 7 times. The alert levels in the Netherlands were
the issue, the majority in the commission drafting Germany’s first developed as the outcome of intensive discussions between
advisory for recreational use in 1992 voted in favor of more strict scientists, lake managers and policy makers. The chief objective
measures than mere information and warning, i.e. including of a process of cyanobacterial risk assessment and management, as
closure of bathing sites during blooms. The argument at the time formalized in the protocols, is the prevention of the public from
was that in the German regulatory culture a strong signal like lake being exposed to harmful concentrations of cyanobacterial toxins,
closure is important for such to be taken seriously unless more while at the same time avoiding unnecessary costs and carbon
drastic measures like temporary closure are a real option. In footprints (e.g. in production of drinking water), restrictions on
addition the role played by individual scientists, managers and recreational activities and consumption of freshwater seafood (in
policy makers in countries, as well as their personal view on particular where this may be an important source of nutrition – see
cyanobacterial risks have an effect on which guidelines and Ibelings and Chorus, 2007). The protocol used in the Netherlands –
regulations are implemented. in addition to health risks – takes into account the promotion of
Thus although procedures for risk assessment in different outdoor activities, feasibility, complexity and costs of monitoring
countries are likely to share common scientific elements, the or risk control of cyanobacteria, as well as the ease of
assumptions being made will vary according to political, social and communication to the public. Likewise, the approach in Germany
economic context (Chorus and Bartram, 1999), and this is fully in suggests MCYST measurements in order to avoid undue restric-
line with the aims of the WHO Guidelines for Drinking-water tions on recreational use of waters where blooms occur, but their
Quality, which emphasize that ‘‘The judgment of safety – or what is a toxin content is low.
tolerable risk in particular circumstances – is a matter in which society This quite wide variability in approaches to toxic cyanobac-
as a whole has a role to play. The final judgment as to whether the teria in water-bodies used for recreation reflects not only the
benefit resulting from the adoption of any of the guidelines given in the differences between the realities of settings, but also implicit
GDWQ justifies the cost is for each country to decide’’ (WHO, 2009). differences in the acceptance of risk. The recently risk-based
 B.W. Ibelings et al. / Harmful Algae 40 (2014) 63–74 71

approaches to regulation have adopted the view that it is

Box 2. Abundance and biomass of cyanobacteria
important to make differences in the acceptance of risk explicit
and transparent.
Cyanobacterial protocols for recreational waters, like the example from the
Netherlands shown in Fig. 3, commonly focus on cyanobacterial abundance 4.5. Risk-based approaches
and biomass rather than on microcystin concentrations. This avoids a focus
on a single toxin. The disadvantage of this approach is that no clear relation
A broader concept of risk assessment (widely used in many
between a biomass signal and toxin concentrations exists because all
cyanobacteria as well as planktonic algae contribute biomass or contain sectors besides public health, e.g. also in the insurance business),
pigments, while not all cyanobacteria produce toxins. Thus, measures of while making use of the available information on the generic
cyanobacterial abundance or biomass provide only an indication of the properties of the hazard, sets the focus on the setting or situation,
upper limit of cyanotoxin concentrations to be expected. Nonetheless this i.e. it calls for estimating how large the risk caused by a certain
information is useful for risk assessment and management if either a worst-
case assumption for toxins per biomass is used or if this relationship can be
hazard is likely to be in that specific case (within this concept the
gleaned from experience within the given water-body. Different methods to generic toxicity assessment discussed above would be ‘‘hazard
estimate the abundance or biomass can be applied: characterization’’ rather than risk assessment). This concept
Chlorophyll-a estimates the likelihood of the hazard to occur in relation to the
Method based on spectrophotometric analysis after extraction of the
severity of its impact – e.g. on human health. This is particularly
pigments with e.g. ethanol. Advantage of this method is the ease of use. The
parameter can be routinely measured and is therefore relatively fast and useful for prioritizing hazards and – in consequence – measures to
cheap. Disadvantage is that the method is not specific for cyanobacteria; all abate them. Risk-based approaches focus on understanding the
phytoplankton contains chlorophyll a. Extraction and analysis of specific potentially occurring hazards in specific, individual supply
cyanobacterial pigments like phycocyanin is less straightforward. However, systems or recreational settings, the system’s efficacy in control-
the analysis of chlorophyll-a can be supplemented by qualitative
microscopy, i.e. estimating (without cell counting, usually within 10 min or
ling them, the development of management plans to ensure
less) whether the phytoplankton largely consists of cyanobacteria or not. controls are working, emergency and contingency strategies, clear
Fluorescence lines of communication, and on documentation of the risk
Part of the light which is used for photosynthesis by phytoplankton cells may assessments as well as records of system performance. In such a
be re-emitted as fluorescence and this can be used as an indicator of biomass.
comprehensive management system guideline values and standards
Modern sensors measure not only chlorophyll-a fluorescence, but also
cyanobacteria specific pigments which differ in their absorption maximum, take on an additional role: they still serve as measure for overall
i.e. phycocyanin or phycoerythrin, and thus allow the distinction of verification that the system is working, i.e. the water to which people
cyanobacteria from other phytoplankton. Advantage of the method is the may be exposed should not contain concentrations exceeding these
instantaneous results of the measurements, which can even be obtained in values. However, in the context of risk-based approaches guideline
situ. The parameter can be routinely measured and is therefore relatively fast
and cheap. The fluorescence signal, however, is not always straight forward
values or standards are also important for defining targets for the
to interpret since quenching of fluorescence depends on environmental system’s performance in managing the risks. For cyanotoxins, a
conditions and the physiological state of the cells. target for MCYST-LR or MCYST-LR equivalents translates to targets
Microscopic counts/estimates for cyanobacterial biomass. The target for cyanobacterial biomass in
Method based on the analysis of concentrated cells, preferably in a
turn translates to a concentration of total phosphorus which, if met,
sedimentation chamber and counted under an inverted microscope
(Uthermohl method). Advantage of this method is the direct insight into the renders higher biomass levels quite unlikely. Last but not least, the
composition of the phytoplankton population in general and the possible target concentration for total phosphorus determines the target for
abundance of potential toxin producing genera/species of cyanobacteria. phosphorus loading to the water-body (see Fig. 4). If these targets
Disadvantage is that the method is time consuming (and therefore relatively cannot be met and this results in a risk of cyanotoxin occurrence in
expensive) and a specialist job. The quantification is complicated by growth
forms of cyanobacteria, i.e. colonies or filaments, the latter sometimes coiled
raw water used for drinking-water abstraction, barriers need to be in
or twisted. Cell counts compared between laboratories may show a high place for off-take schemes and treatment methods that mitigate cell
level of variation. A further disadvantage is the variation in cell size: some and toxin concentrations. Risk-based approaches include an
picoplanktonic cyanobacteria are extremely small, and this may result in assessment of how effectively the whole set of measures and
very high cell counts even if the water appears clear.
barriers control cyanobacterial occurrence and/or remove and
Biovolume
Like above (microscopic counts), but in addition the cell numbers are reduce cyanotoxin concentrations.
multiplied by the mean cell volume of each genus/species (either obtained
from measuring key geometric dimensions of 10–20 cells per sample, or 4.6. Water Safety Plans
from literature) to provide an estimate of biomass. Advantage of using this
method is that the relative biomass of cyanobacteria in relation to other
A truly risk-based regulatory approach to cyanotoxins requires
phytoplankton genera can be estimated, and toxin concentrations relate to
biomass much more tightly than to cell numbers. Cell sizes are incorporated such a comprehensive system assessment and management concept
in the measurements, dominance of phytoplankton genera and species can for the individual water use system. It can use an audit as tool to
be more reliably evaluated. Disadvantage of the method is equal to that of demonstrate compliance in the sense of an independent assessment
the microscopic counts. Furthermore, this method introduces an additional
of the quality of the risk assessment and management system
parameter, the mean cell volume of each taxon, with a certain distribution
and variation and hence additional scope for uncertainty. designed for the specific water supply or recreational site. Risk
DNA-copy detection assessment and management is being increasingly widely used. The
Method based on the extraction of DNA and the multiplication of certain Public Health Risk Management Plans in New Zealand are one
gene targets. Targets are either on the phycocyanin genes or on the genes example. For drinking-water the WHO Guidelines for Drinking-
encoding for the toxin production. Advantage of the method is the objective
water Quality (http://www.who.int/water_sanitation_health/dwq/
quantification and that the targets are genus specific. The method is
relatively fast (result within hours) and sensitive, so that low concentrations guidelines/en/) have introduced the concept of developing situation-
of cells can be detected. Disadvantage is the need for a well-equipped specific Water Safety Plans (http://www.who.int/water_sanita-
laboratory and pcr-expertise. Besides, the relation between cell numbers and tion_health/publication_9789241562638/en/) related to the Codex
DNA copies can be a source of variation. Overestimation of the cell densities
Alimentarius Arius HACCP concept. This Hazard Assessment and
may occur. Detection of toxic genes may not relate to actual toxin production
and concentrations.
Critical Control Points concept emphasizes that monitoring the end
product only (e.g. tap water) will not guarantee safety. A
comprehensive risk assessment of the whole chain involved in
production of drinking-water or food should identify the critical
control points or measures to be implemented and closely
72 B.W. Ibelings et al. / Harmful Algae 40 (2014) 63–74

that if a bathing water profile for an individual site indicates the

potential for cyanobacterial proliferation, appropriate monitoring
shall be carried out to enable timely identification of health risks. If
proliferation does occur and risks have been identified adequate
measures shall be taken immediately to prevent exposure,
including information to the public. The DWD provides a general
degree of protection, without mentioning cyanobacteria specifi-
cally: it is intended to protect human health by ensuring that
drinking-water does not contain microorganisms, parasites or
substances in concentrations which constitute a potential health
risk. Member states shall take any action which is required to
guarantee and purity of water intended for human consumption.
On a similar note the Clean Water Act in the USA(http://
www2.epa.gov/laws-regulations/summary-clean-water-act) aims
at restoration and maintenance of the chemical, physical and
biological integrity of the Nation‘s waters. The US EPA designated
Fig. 4. Schematic representation of risk management of toxic cyanobacteria, numerical criteria for phosphorous and nitrogen as a priority for
conforming to the Water Safety Plan concept of the WHO (protection from controlling freshwater eutrophication, which has rapidly increased
catchment to consumer). over the past few decades (EPA, National Lake Assessment; http://
water.epa.gov/type/lakes/lakessurvey_index.cfm). To reduce harmful
algal blooms a policy of watershed management is the basis, in
monitored to ensure that they are working at all times. For WSP this some cases effectively supplemented by manipulations within
means risk assessment and control from ‘‘catchment to consumer’’. water-bodies.
Control of eutrophication, the most sustainable way to tackle the
problem of harmful algal blooms, usually requires management 4.8. Remaining challenges
measures at the catchment scale.
The key advantage of the WHO Water Safety Plan concept for Regardless as to whether regulatory approaches chiefly call for
regulating the occurrence of toxic cyanobacteria is that it compliance to standards or for a risk assessment and management
encourages and facilitates tackling the problem at its source. As system, it is difficult to set targets or define tolerable levels without
preliminary step to develop a Water Safety Plan, the concept calls an understanding of the toxicity of cyanobacterial compounds. For
for the formation of a team of stakeholders well familiar with the this purpose, gaps in data on chronic oral toxicity are a substantial
local circumstances, including those in the catchment, possibly issue for assessing the risks from exposure to most cyanotoxins.
including external expertise. This provides an excellent platform While the potential carcinogenicity of microcystin or nodularin has
for cyanobacterial management, which can rarely be achieved been categorized by the International Agency for Research on
solely by the water supplier, the public health authority or the Cancer (IARC, 2010), quantitative data are lacking for re-assessing
authority responsible for water-body management. The Water whether taking carcinogenicity into account would change the
Safety Plan team can bring together the expertise and local system provisional WHO Guideline value for MCYST-LR. Using epidemio-
understanding to assess the given system, i.e. the factors causing logical data for setting guidelines or standards is notoriously
eutrophication, to plan measures to control the conditions leading difficult due to the many confounders, and where they are used,
to cyanobacterial blooms – and/or to implement barriers against this is often from workplace exposure where cause-effect relation-
human exposure if blooms cannot be prevented. ships become clearer – an approach which is scarcely viable for
cyanotoxins. New toxicological studies providing data for the
4.7. Overarching legislation with implications for cyanotoxins derivation of guidelines or standards have scarcely been
published in recent years, as producing such data still requires
For member states of the European Union, three European animal experiments which, however, are expensive and increas-
Directives are relevant for the hazards due to cyanobacterial ingly unpopular. Alternative concepts based on sets of sub-
blooms: The aim of the Water Framework Directive (http:// organismic assays testing a range of endpoints and toxic
ec.europa.eu/environment/water/water-framework/index_- mechanisms are currently being developed, but are not yet at
en.html) is that all European waters meet criteria for good the point of providing data on the basis of a widely harmonized
ecological status by 2015. Criteria are of hydromorphological, concept that would be accepted by regulators as a basis for
physical, chemical and biological nature (e.g. Allan et al., 2006), and defining tolerable concentrations.
this is to be achieved by management plans for the specific River A challenge scarcely addressed to date is that of benthic
Basin Districts, i.e. natural geographical and hydrological units. cyanobacteria, which are increasingly linked to animal deaths,
Eutrophication control in these River Basin Districts is a necessary caused by neurotoxins in benthic cyanobacterial (Phormidium)
means to achieve the goals of the WFD, to which all EU member mats that become detached and float to the surface. While these
states are committed. A good ecological status of waterbodies are difficult to quantify, New Zealand has taken the pragmatic
should greatly benefit the aims of EU Bathing Water Directive approach of using percentage coverage of the stream bottom
(http://ec.europa.eu/environment/water/water-bathing/) and the together with river flow as an indicator of this risk.
EU Drinking Water Directive (http://ec.europa.eu/environment/ Representative sampling of cyanobacteria is widely perceived
water/water-drink/index_en.html). The BWD lays down provi- as a challenge when monitoring compliance with standards or
sions for developing a bathing water profile. This calls for assessing guideline values, as their distribution can be highly patchy with
potential sources of contamination of the bathing site, i.e. assessing strong temporal variation. However, this situation is not necessar-
risks, and it defines the classification of bathing water quality, its ily different for other hazards. Many contaminants typically occur
management and the provision of information to the public. By sporadically rather than on a regular basis, i.e. due to storm water
2015 all bathing waters are required have an acceptable minimum inflows, prolonged dry periods or to activities in the catchment
water quality. With respect to cyanobacteria the BWD stipulates taking place at irregular intervals. A basic principle for developing a
 B.W. Ibelings et al. / Harmful Algae 40 (2014) 63–74 73

Water Safety Plan therefore is to consider not only the hazard and numbers or biomass, rather than toxin concentrations, and alert
its human health impact, but particularly the hazardous events level frameworks are a widespread approach. In stark contrast to
that cause it to occur in a water course. This approach moves the the uniformity of standards or guideline values for drinking water,
regulatory focus away from endpoint monitoring toward under- different countries apply very different values as thresholds in
standing the respective system and casting this understanding into their alert level systems, with for example California scaling up to
a management plan. Action level at less than 1% of the MCYST concentration used in
At the technological or methodological level these are scarcely Germany, or New Zealand scaling up to the highest intervention
conceptual challenges, as approaches to preventing and reducing level at only 7% of the cyanobacterial biovolume used in the
nutrient loading to water courses are well understood, as are Netherlands. We do not feel that it is up to the authors of this
methods for managing water-bodies to create conditions less publication to judge which country has the more evidence-based
favorable for cyanobacteria and techniques to remove cells and approach, since local conditions and experiences play an important
toxins in drinking-water treatment. The primary challenge here role in such decisions. In each country there are knowledgeable
would be to choose the best technological approach and methods, scientists and managers to develop the concept that works best for
taking duration of toxin occurrence, costs and carbon footprints of their local or national situation.
removal through treatment into account and balancing this against A key conclusion from this overview of different countries’
the – usually longer-term – success chances and costs for measures approaches and the uncertainties involved might be that it is
in the catchment that would effectively control eutrophication and difficult to employ regulatory approaches for cyanotoxin concen-
thus mitigate blooms. trations that focus on compliance. A possible way forward would
In many regions of the world, in spite of all we know about be the implementation of a comprehensive framework for risk
eutrophication and how to control it, the perhaps biggest challenge assessment and management. The concept outlined by the WHO of
of all is to preserve water resources of high quality, in face of developing a Water Safety Plan for the specific drinking-water
increasing pressures from changes in land-use, climate change and supply system offers a suitable approach for implementing such a
a still expanding human population. framework. For recreational water-body use, the concept of
developing bathing water profiles, as required by the EU Bathing
4.9. Impact of cyanotoxin regulations Water Directive, follows a similar line of thinking. Both partially
evade the issue of toxicological uncertainties by focusing on
The regulatory approaches in place have been developed to be developing management plans that control cyanobacterial prolif-
precautionary, i.e. to safely prevent illness or even death, as is eration and/or remove toxins, thus directing regulatory attention
standard for regulating concentrations of chemicals in drinking- to mitigating the problem at its source. Nonetheless, toxicological
water. The primary outcome of public health concern associated assessments can still serve two important roles; setting health-
with exposure to cyanotoxins is liver cancer (from exposure to based targets to guide such management plans and to provide a
microcystins and possibly cylindrospermopsin). However, even for measure to verify that the water is safe to use for drinking or
those toxins, causal relationships are difficult to glean from recreation. The lacking chronic toxicity data therefore appear to be
epidemiologic studies because there are many other possible the most important knowledge gap to close in order to improve the
causative factors. Individual responses are not measured or basis for cyanotoxin regulations.
estimated and other biological or chemical contaminants in
surface waters typically have not been ruled out (USEPA, 2006).
For example, in the studies specifically designed to assess the Author declaration
association between microcystin exposure and subsequent liver
cancer in China (IARC, 2010) the study population was also B.W. Ibelings wrote substantial parts of the manuscript.
exposed to aflatoxin and hepatitis, other potential causes of liver L. Backer provided substantial contributions to compilation of
cancer. For cyanotoxins, as well as for many of the other chemicals the international data set on which the manuscript is based and
found in drinking water, the effects from reducing exposure provided substantial input to the text. E. Kardinaal provided
through regulations specifying maximum allowable concentra- substantial contributions to the structure and content of the
tions cannot easily be measured in terms of disease prevention. manuscript through many rounds of revision, authored Box 2 and
prepared the graphs. I. Chrous edited 2 international reports
4.10. Summary and conclusions published by the German Environment Agency and which
provided the input for the current manuscript. She also wrote
Given that eutrophication is still a growing problem in many substantial parts of the manuscript.
countries, possibly acerbated by climate warming, cyanobacterial
blooms are here to stay for quite a while yet. It is widely accepted Acknowledgement
that cyanobacterial blooms pose a threat to the safe production of
drinking water, the consumption of freshwater seafood and BWI is grateful for numerous discussions on cyanobacteria and
recreational activities, and an increasing number of countries how to monitor or model them in the EU COST Actions CyanoCOST
worldwide are responding to this threat with regulations or and NETLAKE[SS].
guidance for drinking water and recreation, and occasionally for
food. Almost invariably countries base their guidance on the WHO
Appendix A. Supplementary data
provisional Guideline Value for drinking-water of 1 mg L1 MCYST-
LR. While authorities struggle to regulate toxins other than MCYST-
Supplementary data associated with this article can be found, in
LR, given the paucity of toxicological data, we argue that MCYST-LR
the online version, at doi:10.1016/j.hal.2014.10.002.
can serve as orientation or ‘guidance toxin’ for risks from other
microcystins and even other classes of toxins, provided the
limitations of this approach are kept in mind, particularly with References
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