Download Potential risks posed by macroalgae for application as feed and food

Report
2016
Potential risks posed by macroalgae for
application as feed and food
- a Norwegian perspective
17. June 2016
Arne Duinker, Irja Sunde Roiha, Heidi
Amlund, Lisbeth Dahl, Erik-Jan Lock,
Tanja Kögel, Amund Måge and Bjørn
Tore Lunestad
Nationalinstitutt
Institute
of Nutrition
Nasjonalt
for ernæringsog and
Seafood
Research
(NIFES)
sjømatforskning (NIFES)
TABLE OF CONTENTS
1.
Summary .............................................................................................................................. 2
2.
Sammendrag ........................................................................................................................ 3
3.
Introduction.......................................................................................................................... 5
4.
Contaminants and biohazards: Content and implications in food and feed ............................. 6
Heavy metals and other elements ...................................................................................................... 6
1.
Occurrence data ...................................................................................................................... 6
2.
Comments to the occurrence data.......................................................................................... 9
3.
Implications for food safety .................................................................................................. 11
4.
Implications for feed safety ................................................................................................... 12
Iodine ................................................................................................................................................. 12
Persistent organic pollutants (POPs) ................................................................................................. 14
Toxins and anti-nutrients .................................................................................................................. 14
Radioactivity ...................................................................................................................................... 15
Micro-organisms................................................................................................................................ 15
Microplastics ..................................................................................................................................... 18
Digestibility of seaweed carbohydrates. ........................................................................................... 18
5.
Conclusions......................................................................................................................... 19
6.
Literature list ...................................................................................................................... 20
1
1. SUMMARY
Macroalgae comprise a large and diverse group of organisms living predominantly in salt and brackish
waters. Based on the colour of the dominating pigments of the macroalgae, they can coarsely be
divided into brown algae (Phaeophyceae) comprising the perennials and kelps, green algae
(Chlorophyceae) and red algae (Rhodophyceae).
The consumption of macroalgae is not recorded in dietary surveys and it is therefore difficult to
estimate the intake of the different nutrients and non-nutrients in the population from macroalgae.
So far, the amount of utilised macroalgae for direct consumption in Norway has been limited, but lately
an increased interest in both the cultivation and harvest from wild stocks is seen.
The available occurrence data indicate that Norwegian macroalgae may contain elevated levels of
inorganic arsenic, total arsenic and cadmium, while the levels of mercury and lead are low. High levels
of inorganic arsenic and cadmium are particularly found in brown algae and may limit their use as food
and feed ingredients. There are currently no regulations for macroalgae used as food. More occurrence
data are needed to describe the seasonal variation of especially inorganic and total arsenic and
cadmium in macroalgae from Norwegian waters.
The level of iodine in macroalgae is in general relatively high and brown algae seems to have the
highest levels. Only a small intake of dried brown algae will contribute with an excessive iodine intake,
however, the frequency of intake will be crucial in the evaluation of how this may affect the thyroid
function. It is also important to assess the bioavailability of iodine and the loss of iodine during food
processing (e.g. boiling). More knowledge about these factors are of importance when estimating the
iodine intake and its effect on the thyroid function.
The levels of persistent organic pollutants in macroalgae are low compared to other foods, as expected
due to low levels of fats. Data are however scarce.
Certain algae produce neurotoxins as secondary metabolites. There are no recorded poisoning related
to macroalgae reported in Europe so far. Only a few studies describe toxins in European waters, and
the levels reported are low and of no concern for human health. Poisoning have been reported,
however, in Asia caused by blue-green algal epiphytes on macroalgae.
Macroalgae do accumulate radionuclides, but few studies focus on food safety and no levels of concern
for food safety were found.
The surface of macroalgae form favourable habitats for microbes, where the load and diversity differ
between the various algal species and may differ from the surrounding water communities, indicating
algae-microbe interactions. Such interactions seem to be important for host health and infection
defence. Most studies concerning microbial communities associated with macroalgae have an ecologic
focus, describing the numbers, diversity and role of bacteria on the surfaces of the algae. Based on the
studied literature, the question regarding possible enhanced survival of faecal bacteria and potential
human pathogens associated to macroalgae remain largely unresolved. Some of the bacteria found on
macroalgae have a potential as human pathogens, or could give challenges during processing and
storage, but the importance of algae in feed or food borne disease cannot be expected to be higher
than for other non-filtering marine organisms used for such purposes, including fish.
Microplastics, defined as plastic particles smaller than five millimeters, are now common at all levels
of the marine environment. Such particles are prone to accumulation of organic contaminants, which
again can adsorb onto macroalgae, potentially introducing the particles and their associated
contaminants into animals feeding on them, including humans. The possible implications of this are
however not known.
2
Macroalgae contain different polysaccharides compared to terrestrial plant. The energy content for
human and animal nutrition seems to be low, but is not very well documented. This might be positive
in the perspective of too high energy density in some human diets. However in a perspective of feed
the lack of energy availability from polysaccharides might be a problem.
2. SAMMENDRAG
Makroalger utgjør en sammensatt gruppe organismer som i hovedsak er å finne i sjø eller brakkvann.
På bakgrunn av de mest dominerende pigmentene, deles makroalger grovt inn i brunalger
(Phaeophyceae) som inkluderer tang og tare, grønnalger (Chlorophyceae) og rødalger
(Rhodophyceae).
Data for inntak av makroalger er ikke inkludert i kostholdsstudier, og det er derfor vanskelig å estimere
mengden næringsstoffer og andre stoffer enn næringsstoffer makroalgene står for i kostholdet. Så
langt har det bare blitt benytte mindre mengder makroalger til direkte humant konsum, men i det siste
har en sett økt interesse for dyrkning og høsting fra ville populasjoner.
Tilgjengelig informasjon om metaller i norske makroalger indiker at en kan finne forhøyede
konsentrasjoner av uorganisk arsen og kadmium, særlig hos brunalger. Konsentrasjonene av kvikksølv
og bly er lave i makroalger. De høye konsentrasjonene av arsen og kadmium kan sette begrensinger
for bruk av makroalger til mat og som fôringrediens. Det mangler fremdeles undersøkelser for å
karakterisere forekomst av arsen og andre tungmetaller i norske makroalger på en tilfredsstillende
måte.
Konsentrasjon av jod i makroalger er forholdsvis høy og brunalger synes å ha de høyeste nivåene. Selv
et lavt inntak av tørkede brune alger vil gi et jodbidrag over anbefalt dagsdose. Hvor ofte det inntas
makroalger er imidlertid avgjørende for hvordan dette kan påvirke skjoldbruskkjertelens funksjon. Det
er også viktig å vurdere biotilgjengeligheten til jod og tapet av jod under prosessering av mat (f.eks.
koking). Det er behov for mer kunnskap om disse faktorene og hvordan dette påvirker både jodinntaket
og skjoldbruskkjertelens funksjon.
Makroalger er svært lite fettrike. Som forventet er konsentrasjoner av persistente organiske miljøgifter
i makroalger lavere enn det en finner hos andre organismer som kan brukes til mat og fôr.
Noen alger produserer nervegifter som sekundære nedbrytningsprodukter. Det er så langt ikke
rapportert om forgiftninger fra slike giftstoffer i Europa. Et fåtall studier beskriver toksiner i europeiske
farvann, men nivåene som er rapportert er lave. Forgiftninger forårsaket av blågrønnalger som vokser
som epifytter på makroalger er rapportert fra Asia.
Ved gjennomgang av litteraturen, er det ikke funnet informasjon om at makroalger kan representere
en utfordring med tanke på radioaktivitet.
Makroalger er et yndet habitat for mikroorganismer og store mengder bakterier lever på overflaten av
algene. Mengden og sammensetningen varierer mellom de ulike algeartene og kan være forskjellig fra
vannet de lever i, noe som indikerer spesifikke alge-bakterie interaksjoner. Denne vertsspesifikke
diversiteten ser ut til å være viktig for algens helse og infeksjonsforsvar. De fleste studier tar for seg
3
mikrobielle samfunn assosiert med makroalger i et økologiske perspektiv. Der er svært få publikasjoner
knyttet til humanpatogene bakterier fra makroalger fra nordlige farvann, eller som tar for seg
problemstillingen knyttet til alger og bakterier fra fekal forurensning. Literturstudien viser at spørsmål
knyttet til overlevelse av tarmbakterier og human patogener assosierte med makroalger stort sett er
ubesvarte. Det kan konkluderes med at det på overflaten av makroalger finnes store mengder
bakterier og at noen av disse potensielt kan skape problem ved prosessering eller ikke-optimal lagring.
Betydning av disse kan ikke ses på som større enn for andre ikke-filtrerende organismer som fisk.
Mikroplast defineres som partikler mindre enn 5 mm. Slike partikler er nå vanlige i det marine miljøet.
Mikroplast vil lett knytte organiske forurensningsstoffer til seg, og kan siden bli oppkonsentrert på
overflaten av makroalger som så kan bringe stoffene over i mat eller fôr. Når dyr som strandsnegl
beiter på overflaten av makroalger, vil mikroplast og organiske forurensningsstoff kunne komme inn i
næringskjeden. Hvilken risiko dette kan medføre er ukjent.
Makroalger inneholder uvanlige polysakkarider sammenlignet med det er finner i terrestrisk planter,
og næringsverdien av disse karbohydratene er til dels lav eller lite kjent. Fra et folkehelseperspektiv
kan dette være fordelaktig da det kan gi redusert energitetthet. Fra at dyrefôrperspektiv kan dette
representere et problem.
4
3. INTRODUCTION
The Norwegian Food Safety Authority (NFSA) have asked NIFES for an assessment on potential negative
effects on the health of humans and animals posed by the consumption of macroalgae harvested from
Norwegian waters. This report summaries the current available knowledge on organic and inorganic
contaminants, naturally found toxins and anti-nutrients in certain macroalgae, micro-organisms of
health concern and the effects of microplastics in the environment, as well as aspects of digestibility
of algal carbohydrates.
Macroalgae comprise a large and diverse group of plants living predominantly in salt and brackish
waters. The macroalgae are, in contrast to most land-living plants, not differentiated into root, steam
and leaf. Based on the colour of the dominating photosynthetic pigments, these algae can coarsely be
divided into the brown algae (Phaeophyceae) comprising the perennials and kelps, green algae
(Chlorophyceae) and red algae (Rhodophyceae). Although we use the term plants here for simplicity,
it should be noted that only the green algae are classified together with land plants in the phylum
Plantae, whereas the red and brown algae are not (La Barre, Potin et al. 2010). Depending on different
regional human or agricultural habits, these algae have traditionally been used for food, as feed or soil
fertilizers. In addition, several industrially produced compounds, as alginate and carrageen, are utilized
as thickeners, gelling agents, stabilizers and emulsifying agents in a variety of food and feed. The
refined products from algae are however not evaluated or discussed in this report. The most relevant
species for farming, commercial or public harvest are listed in Table 1.
Red algae
Green algae
Kelp
Brown
annuals
Brown
perennials
Table 1. List of relevant species of macroalgae for direct consumption in Norway.
Norwegian
Grisetang
Blæretang
Sauetang
English
Rockweed, egg wrack
Bladderwrack
Channeled wrack
Latin
Ascophyllum nodosum
Fucus vesiculosus
Pelvetia canaliculata
Martaum, åletang
Sea lace
Chorda filum
Remtang
Sea spaghetti
Himanthalia elongata
Sukkertare
Fingertare
Butare
Stortare
Havsalat
Sugar kelp
Oarweed
Alaria, winged kelp
Tangle
Sea lettuce
Tarmgrønske
Gut weed, mermaids hair
Pollpryd
Søl
Fjærehinne
Sponge seaweed
Dulse, dillisc
Laver
Grisetangdokke
Wrack siphon weed
Krusflik
Irish moss
Saccharina latissima
Laminaria digitata
Alaria esculenta
Laminaria hyperborea
Ulva lactuca
Enteromorpha
intestinalis
Codium fragile
Palmaria palmata
Porphyra purpurea
Polysiphonia
(Vertebrata) lanosa
Chondrus crispus
5
Several aspects of the macroalgae biology may influence the levels of contaminants. The chemical
composition of macroalgae differs from other types of seafood in the high content of specific
polysaccharides in the structural components of the algae. The types of polysaccharides differ between
brown, red and green algae, with alginate in brown algae as the most utilised one. The polysaccharides
have metal-binding characteristics that may affect both the levels of metals and the availability of these
metals through the digestion processes. The algae have generally low levels of lipids, and thus low
levels of organic, lipid-soluble contaminants is expected. The shape of the fronds on the other hand,
with a large surface area in contact with the water, will facilitate uptake of such contaminants.
So far, the amount of macroalgae utilised for direct human consumption in Norway has been limited,
but lately an increased interest in the cultivation and harvest from wild stocks is seen. An overview of
the most relevant macroalgae in Norway are given in Table 1. The increased interest for algal cuisine
is also relatively new in the rest of Europe, and so far, no regulations with maximal levels for
contaminants exists for seaweed as food in Norway or the EU. Further, there is increasing interest on
marine algae in animal feed, especially since the Norwegian demands for ingredients for fish feed is
growing. The safety of these new food and feed materials is however not elucidated and this is subject
for discussions in the EU committees, in particular regarding arsenic, cadmium and iodine.
4. CONTAMINANTS AND BIOHAZARDS: CONTENT AND
IMPLICATIONS IN FOOD AND FEED
Heavy metals and other elements
1. Occurrence data
Some recent studies on elements in macroalgae harvested in Norway have been performed and
some are ongoing, and the data are compiled in Tables 2 to 7. The data includes published
information (Duinker 2014), as well as unpublished data from an ongoing research project (AquaFly,
NIFES ).
The level of copper, iodine, selenium and zinc in macroalgae collected in Norway are summarized in
Tables 2 and 3. These elements are important nutrients but can be toxic at elevated levels. As can be
seen, the levels of copper and selenium are low, ranging from 1.6 to 17 mg/kg dry weight (d.w.) and
from 0.02 to 0.53 mg/kg d.w., respectively. The levels of zinc are generally also low, but rather high in
some species (Table 2). High levels of zinc were found in the red algae Vertebrata lanosa (81 mg/kg
d.w.), the green algae Ulva lactuca (176 mg/kg d.w.) and the brown algae Laminaria digitata (70
mg/kg d.w.) and Saccharina latissima (138 mg/kg d.w.) (Table 2). Data collected in an ongoing
research project supports these findings, as higher levels of zinc were found in red and brown algae
(Table 3). Based on the data collected so far, copper, selenium and zinc levels in macroalgae do not
pose a risk when applied as food and feed.
Table 2. Analysed concentrations of copper, iodine, selenium and zinc in selected macroalgae
harvested in Norway. All concentrations are given in mg/kg dry weight (d.w.).
Species
Copper
Iodine
6
Selenium
Zinc
Reference
Red algae Palmaria
palmata
Green
algae
Brown
algae
Polysiphonia
lanosa
Cladophora
rupestris
Enteromorpha
intestinalis
Ulva lactuca
Alaria
esculenta
Laminaria
digitata
Laminaria
hyperborea
Fucus
vesiculosus
Pelvetia
canaliculata
Saccharina
latissima
4.9
260
0.14
29
-
57-414
0.06-0.15
24-40
8
1300
0.53
81
17
63
0.066
30
4.9
130
0.028
25
6
21
0.049
8
-
60-288
0.04-0.12
10-176
2.4
220
0.041
49
1.6
3100
0.021
24
-
2136-4375
0.02-0.04
34-70
1.7
3500
0.033
22
1.8
130
0.03
26
2.6
210
0.035
31
-
2103-3378
0.04-0.06
24-138
1655
Mæhre et al.
2014
Duinker
2014
Mæhre et al.
2014
Mæhre et al.
2014
Mæhre et al.
2014
Mæhre et al.
2014
Duinker
2014
Mæhre et al.
2014
Mæhre et al.
2014
Duinker
2014
Mæhre et al.
2014
Mæhre et al.
2014
Mæhre et al.
2014
Duinker
2014
Lunig
and
Mortensen
2015
Table 3. Concentrations of copper, iodine, selenium and zinc in selected macroalgae harvested in
Norway as a part of the ongoing AquaFly project at NIFES. Mean concentrations are given in mg/kg
d.w. ± SD, with min-max values in parenthesis.
Copper
Iodine
Selenium
Zinc
n
Red algae*
7.0 ± 2.2
134 ± 111
0.13 ± 0.08
43 ± 20
8
(3.7-10)
(14-340)
(0.05-0.29)
(23-72)
Green algae**
7.5 ± 1.8
190 ± 196
0.43 ± 0.34
16 ± 4.4
4
(5.7-10)
(43-480)
(0.14-0.76)
(12-21)
Brown algae***
2.2 ± 1.0
1438 ± 2624
0.10 ± 0.11
43 ± 30
15
(0.77-3.9)
(59-10000)
(0.02-0.49)
(16-120)
*Chondrus crispus, Furcellaria lumbricalis, Mastocarpus stellatus, Palmaria palmata, Porphyra dioica,
Porphyra purpurea, and Porphyra umbilicalis
**Cladophora rupestris, Ulva intestinalis and Ulva lactuca
***Alaria esculenta, Ascophyllum nodosum, Chordaria flagelliformis, Fucus serratus, Fucus spiralis,
Fucus vesiculosus, Halidrys siliquosa, Himanthalia elongata, Laminaria digitata, Pelvetia canaliculata,
and Saccharina latissima
7
The levels of cadmium, mercury, lead and arsenic in macroalgae collected in Norway are summarized
in Tables 4 and 5. The levels of mercury and lead are low in all analysed species. The level of cadmium
is low (0.08 – 0.22 mg/kg d.w.) in green algae, while for red and brown algae the content of cadmium
varies from 0.1 to 3.8 mg/kg d.w. (Table 4). The highest concentrations were found in the red algae
Vertebrata lanosa and the brown algae Alaria esculenta, Laminaria digitata and Laminaria hyperborea.
Data collected in an ongoing research project supports these findings, as low levels of cadmium were
found in green algae and higher levels were found in red and green algae (Table 5). The levels measured
were comparable for all three datasets. The levels of arsenic were high, ranging from 4.9 to 107 mg/kg
d.w. in all samples (Table 4). Higher levels of arsenic were found in brown algae, where the
concentration ranged from 28 to 107 mg/kg d.w., with highest levels found in L. digitata (Table 4). The
concentration of inorganic arsenic were determined in a few samples; the level of inorganic arsenic
seems to be low, but one samples of the brown algae L. digitata contained as high as 7.7 mg/kg d.w.
(Table 4), whereas other species were below 0.12 mg/kg d.w. (Duinker 2014). These observations are
supported by data collected in an ongoing research project. Brown algae contained higher levels of
total arsenic than red and green algae (Table 5). However, the level of inorganic arsenic (0.05 – 2.4
mg/kg d.w.) was low compared to total arsenic (Table 5). The levels measured were comparable for all
three datasets.
Table 4. The levels of cadmium, mercury, lead and arsenic in selected macroalgae collected in
Norway. Concentrations are given in mg/kg d.w.
Red
algae
Green
algae
Brown
algae
Species
Cadmium
Mercury
Lead
Arsenic
Palmaria
palmata
0.48
0.005
-
10
Inorganic
arsenic
-
0.12-0.26
<0.005-0.01
0.09-1.12
9-12
0.05
3.8
0.01
-
9.3
-
0.091
0.006
-
9.4
-
0.12
0.014
-
4.9
-
0.092
0.005
-
7.9
-
0.08-0.22
0.00-0.01
0.18-0.23
6-13
0.12
3.4
<0.005
-
48
-
0.1
0.006
-
64
-
0.33-1.94
0.01-0.02
0.08-0.22
73-107
0.1-7.7
0.48
0.007
-
55
-
1.2
0.011
-
41
-
Polysiphonia
lanosa
Cladophora
rupestris
Enteromorpha
intestinalis
Ulva lactuca
Alaria
esculenta
Laminaria
digitata
Laminaria
hyperborea
Fucus
vesiculosus
8
Reference
Mæhre et
al. 2014
Duinker
2014
Mæhre et
al. 2014
Mæhre et
al. 2014
Mæhre et
al. 2014
Mæhre et
al. 2014
Duinker
2014
Mæhre et
al. 2014
Mæhre et
al. 2014
Duinker
2014
Mæhre et
al. 2014
Mæhre et
al. 2014
Pelvetia
0.48
0.047
canaliculata
Saccharina
0.28-0.46 0.01-0.02
0.19-0.72
latissima
Maximum level
Feed
0.5 (1*)
0.1 (0.2*)
5
Feed material
1
0.1
10
* Fish feed, ** Commision directive 2002/32/EC and amendments
28
-
61-66
0.03-0.07
2 (10*)
40
-
Mæhre et
al. 2014
Duinker
2014
**
**
Table 5. The levels of cadmium, mercury, lead and arsenic in selected macroalgae collected in Norway
as a part of the AquaFly project. Concentrations are given in mg/kg d.w., mean ± SD (min-max) Mean
concentrations are given in mg/kg dry weight (d.w.) ± SD, with min-max values in parenthesis.
Species
Cadmium
Mercury
Lead
Arsenic
Inorganic
n
arsenic
Red algae*
0.73 ± 0.00
0.01 ± 0.00
0.26 ± 0.18
15 ± 6.8
0.09 ± 0.09
(0.07-3.1)
(<0.005-0.01)
(0.05-0.58)
(6.4-24)
(0.01-0.24)
8
Green algae**
0.18 ± 0.06
1.5 ± 1.1
8.6 ± 2.2 0.28 ± 0.17
0.01 ± 0.00
(0.12-0.27)
(0.36-3.0)
(6.4-11)
(0.05-0.44)
4
Brown algae***
1.1 ± 1.5
0.01 ± 0.01
0.26 ± 0.26
41 ± 26
0.33 ± 0.64
(0.03-5.9)
(<0.005-0.04)
(0.05-1.1)
(19-120) (0.02-2.4)
15
*Chondrus crispus, Furcellaria lumbricalis, Mastocarpus stellatus, Palmaria palmata, Porphyra dioica,
Porphyra purpurea, and Porphyra umbilicalis
**Cladophora rupestris, Ulva intestinalis, and Ulva lactuca
***Alaria esculenta, Ascophyllum nodosum, Chordaria flagelliformis, Fucus serratus, Fucus spiralis,
Fucus vesiculosus, Halidrys siliquosa, Himanthalia elongata, Laminaria digitata, Pelvetia canaliculata,
and Saccharina latissima
2. Comments to the occurrence data
There are few analytical data on metals in macroalgae from Norwegian waters thus far, and there is
particularly need for more data on the commercial species as Laminaria hyperborea from wild
harvest, as well as farmed Saccharina latissima and Alaria esculenta. More data are also warranted
on geographical and seasonal variations.
Metal concentrations in macroalgae varies between species. However, within a species variations in
metal concentrations appear to be site-specific, related to seaweed growth rates and differs between
different parts of the seaweed. These growth rates are affected by ambient environmental conditions,
as well as factors enhancing or reducing accumulation, such as temperature, light, nutrients and
salinity (Morrison, Baumann et al. 2008), and causes a seasonal variation of metal concentrations in
macroalgae.
9
Location
Myklestad et al. (1978) described the effect of water zinc and copper concentrations at two locations,
Hardangerfjord and Trondheimsfjord, on accumulation in Ascophyllum nodosum. Ascophyllum is
perennial and it appears that metal concentrations increase with increasing age of the algae (Table 6).
At that time, inner Hardangerfjorden, was highly contaminated by several heavy metals (Julshamn et
al., 2001) It is assumed that the fast growth of the younger parts dilute the metal concentrations.
Table 6. Metal concentrations in A. nodosum from Hardangerfjord as a function of age. The higher
the internode number the older the part of the algae. All concentrations are given in mg/kg d.w.
Tips
Internode 1
Internode 2
Internode 3
Internode 4
Internode >4
Zn
1000
1710
2206
2708
2973
3597
Cu
20
24
58
59
56
82
Pb
11
13
18
24
33
54
Cd
3.5
6.3
6.3
7.3
7.7
7.3
Hg
0.33
0.50
0.87
1.16
1.43
4.48
In the same study, A. nodosum was transfered from Hardangerfjord to Trondheimfjord. Metal
concentration, exemplified with zinc, in inner Hardangerfjord was at the time between six and 50 times
higher compared to Trondheimsfjord, and subsequent metal concentrations in A. nodosum was 10
times higher in Hardangerfjord compared to Trondheimsfjord. After the transfer from Hardangerfjord
to Trondheimsfjord, the metal concentrations in A. nodosum decreased. The younger the internode
the more pronounced the decrease was. A similar pattern was seen for mercury and in a lesser extent
for lead (Table 7). A similar observation has been made for Saccharina latissima sampled at Lindesnes
were lower levels of cadmium were found in the tip than at the stem (Duinker 2014). In the case for
the annual kelp species, however, the tip represents the older part and the growth zone near the stem
the younger parts, as opposed to what is seen in the perennial A. nodosum.
Table 7. Zinc content in different age groups of A. nodosum as a function of growth locality. All
concentrations are given in mg/kg d.w.
Age groups
Tips
New vesicle
Internode 1
Internode 2
Internode 3
Locality
Hardanger
July
Oct
900
1100
1130
1430
2050
1650
2660
2090
3390
2640
Trondheim
July
Oct
70
90
120
130
180
155
230
230
240
265
10
Trondheim (transplant from Hardanger)
May
July
Sept
Oct
130
140
100
840
320
295
240
1710
840
560
515
2380
1750
1210
1050
2710
1950
2060
1430
Seasonal variability - environmental factors
The uptake and availability of metals in the water are related to factors like salinity (Struck, Pelzer et
al. 1997), pH (Gutknecht 1963), temperature (Munda 1979) and irradiance (Gutknecht 1963) creating
a diurnal as well as a seasonal pattern (Stengel, Macken et al. 2004).
Seasonal changes in levels of different metals followed a seasonal pattern in Ulva sp., with lowest
metal concentrations found in summer plants and maximum values in autumn/winter plants. This is
most likely caused by a dilution effect due to growth during favourable periods and in winter to a large
decrease in metabolic rates (Villares, Puente et al. 2002).
In A. nodosum concentrations of both Cu and Fe in apical tissue of A. nodosum exhibited more than
two-fold changes between October and February, but there were contrasting trends for the two
metals, as Cu concentrations decreased and Fe concentrations increased (Stengel, McGrath et al.
2005). A reduction in the concentration of cadmium from early to late spring was seen in macroalgae
(Laminaria digitata, Palmaria palmata and Ulva lactuca) growing at Lindesnes (Duinker 2014).
Seasonal fluctuations in metal concentration of marine algae are mainly considered a result of seasonal
growth patterns. However, contrasting data have been published on the relationship between
different tissue concentrations of different metals and growth rate. Accumulation of essential
elements (e.g. Cu, Fe, Mn) increased during periods of fast growth, but less accumulation occurred
during slow growth of Ulva fasciata (Rice and Lapointe 1981). Uptake of metals, such as Cd and Cu,
during kelp culture decreased as growth increased (Markham, Kremer et al. 1980), (Stengel, McGrath
et al. 2005).
Some of the variations in metal concentrations between different plants may be caused by epiphytes
rather the macroalgae themselves. Moreover, different parts of the plants can have different
concentrations of heavy metals, e.g. differences between stems and tips of various brown seaweed
species (Stengel and Dring 2000; Stengel, McGrath et al. 2005).
Specific compounds in seaweed that bind metals
Presence of components of alginic acid (Vreeland 1972) and metal-cheating polyphenols, have been
shown to determine binding affinities to metals in macroalgae. In red algae, variations in metal
accumulation can be due to antagonistic effects of different polyvalent cations binding to sulphydryl
groups of carageenan and sulphated galactans of agar (Paskinshurlburt, Tanaka et al. 1976). Also, Zn
uptake by L. digitata in the laboratory was reduced in the presence of Cd or Cu. Differences in alginic
acid compositions may alter the metal binding properties of brown algae.
3. Implications for food safety
The European food legislation aims to protect the consumer and sets maximum permitted levels for a
range of contaminants in foodstuffs (Commission Regulation (EC) 1881/2006 and amendments). Below
is a summary of current maximum levels (wet weight) for foodstuffs. For cadmium and lead, there are
maximum levels for vegetables, but seaweed are excluded from these maximum levels. For cadmium,
lead and mercury there are maximum levels for food supplements that also apply for macroalgae. They
are 3.0, 3.0 and 0.1 mg/kg wet weight, respectively. For cadmium it is specified that the maximum level
applies to “Food supplements consisting exclusively or mainly of dried seaweed, products derived from
seaweed, or of dried bivalve molluscs”. There are currently no maximum levels for arsenic in
vegetables or food supplements.
The levels of cadmium, mercury and lead in algae collected in Norway are low (Tables 4 and 5), and
below the current maximum levels for these elements in food supplements.
There are currently no maximum level of arsenic in vegetables or food supplements. However, the
elevated levels of inorganic arsenic in some species of seaweed may be of concern. In 2015, the
Superior Health Council of Belgium conducted a risk assessment of the exposure to inorganic arsenic
11
though the consumption of edible algae, i.e. macroalgae. They recommend that the consumption of
Hijiki (a non-European species known to contain high levels of inorganic arsenic) should be avoided,
and that the consumption of other algae should be limited to 7 g dried material per day (the Superior
Health Council of Belgium, 2015). The dietary exposure to inorganic arsenic in the general European
population is high (EFSA 2009, 2014), and consumption of algae with a high level of inorganic arsenic
will lead to an additional exposure. Seaweed contains inorganic arsenic and organic forms of arsenic,
mainly arsenosugars. Little is known of the toxicity of arsenosugars.
4. Implications for feed safety
The European feed legislation aims to protect animals, the consumer and the environment, and sets
maximum permitted levels for a range of undesirables substances in feed ingredients and complete
feedingstuffs (Commission Directive 2002/32/EC and amendments). Below is a summary of current
maximum levels (12% moisture content) for feed materials and feed. The maximum arsenic level in
feed materials from seaweed and products thereof is 40 mg/kg. The maximum arsenic level in feed is
2 mg/kg, and 10 mg/kg for fish feed. The Directive recognises that inorganic arsenic is the most toxic
arsenic form and that marine feed ingredients mainly contain organic arsenic compounds. The
maximum levels are set for the level of total arsenic, not inorganic arsenic. In addition, authorities can
request documentation showing that the level of inorganic arsenic in macroalgae and products
thereof, and in marine feed ingredients are below 2 mg/kg. For cadmium and lead, the current
maximum permitted level in fish feed is 1 and 5 mg/kg, respectively, while for feed ingredients it is 1
(feed materials of vegetable origin) and 10 mg/kg, respectively. The current maximum level of mercury
in fish feed and marine feed ingredients are 0.1 and 0.2 mg/kg, respectively.
Algae collected in Norway contains levels of mercury and lead that are below the current maximum
levels. The levels of cadmium in some of the analysed algae exceeds the current maximum level of 1
mg Cd/kg feed (12% moisture content), and this limits the use of some macroalgae as a feed ingredient.
Red and green algae contain levels of arsenic that are below the current maximum level of 40 mg As/kg
feed (12% moisture content) (Tables 4 and 5). Most of the analysed samples of brown algae contained
levels of arsenic exceeding the current maximum limit, and this limits their use as a feed ingredient.
There is limited data on the occurrence of inorganic As in Norwegian seaweed (Tables 4 and 5).
Available data suggest that the levels of inorganic arsenic are low, but may be elevated in the brown
algae Laminaria digitata. Levels of inorganic arsenic exceeding 2 mg/kg (12% moisture content) limits
the use of macroalgae as a feed ingredient.
Based on the data collected so far, copper, selenium and zinc levels in macroalgae do not pose a risk
for the use of macroalgae as feed or feed ingredient.
Iodine
Iodine is an essential micronutrient required for the synthesis of the thyroid hormones
triiodothyronine (T3) and thyroxine (T4). As iodine intake is important for the activity of the normal
thyroid gland, the iodine intake of a population should be brought to the level at which iodine
deficiency disorders are avoided (Laurberg, Nøhr et al. 2000).
Iodine is a non-metallic element and elemental iodine can exist in oxidation stages ranging from -1 to
+7, but the main oxidation state is -1 as iodide.
The healthy human adult body contain approximately 15-20 mg iodine, of which 70-80% is present in
the thyroid gland. Ingested inorganic iodine and iodate are reduced to iodine and almost completely
absorbed from all levels of the gastrointestinal tract. Most of the iodine is transported to the thyroid
12
gland and transforms through a series of metabolic steps into T3 and T4. Iodine also exist in the thyroid
gland as inorganic iodine, monoiodotyrosin (MIT), diiodtoyrosin (DIT), polypeptides containing
thyroxine and thyroglobulin.
The main source of iodine in humans is food, but the iodine concentration of different foodstuffs varies
considerably. ). Determination of the iodine content in Norwegian foods shows that seafood, milk and
dairy products, as well as eggs have the highest iodine concentration (Dahl, Johansson et al. 2004).The
highest iodine content is found in foods of marine origin. Iodine in fish is reported in the range of 30
to 3500 µg/kg wet weight. Macroalgae are particularly high in iodine and concentrations are 100 to
1000 times higher than found for fish (NNR 2014, Mæhre et al. 2014). Our own data shown in tables 2
and 3 confirm this and values as high as with up to 5 000 mg/kg dry weight, and even 10 000 have been
found in L. digitata (Lock unpublished data). These values poses challenges that must be further
adressed.
The intake of iodine from macroalgae is difficult to estimate since such data are not collected in dietary
surveys. However, if a small amount of seaweed such as dried brown algae is consumed, the risk of
having an excess iodine intake is substantial. In the study by Mæhre et al. (2014) and in the report from
Duinker (2014), iodine in samples of different common macroalgae species in Norway were
determined (Table 2). According to these analyses, the levels of iodine are highest in brown algae, but
it should be noted that the variation within the same species is large and the levels between different
groups of algae (brown, green and red) varies considerably. According to the literature, season, salinity
of the water, depth, water temperature, which part of the seaweed used, age of the seaweed and
post-harvest storage conditions are all factors that affect the iodine content (Teas, Pino et al. 2004). In
addition, food preparation and cooking methods will also be factors in determining the final iodine
content (Teas, Pino et al. 2004).. Results from a study showed that the level of iodine was reduced by
70% after five minutes of boiling in water (Lüning and Mortensen 2015). The bioavailability of iodine
is also of interest. In a cross over study from UK the bioavailability and impact of 2 week daily seaweed
supplementation (potassium iodide and seaweed; 712 µg iodine/day) among non-pregnant women
(n=22) were tested (Combet, Ma et al. 2014). They reported increased 24h iodine excretion, however,
the increase differed between the iodine sufficient and the iodine insufficient groups of women;
meaning that the women with the lowest iodine level increased mostly. The level of serum thyroid
stimulating hormone (TSH) also increased in the groups with the exception of two women having
concentrations exceeding the normal range. One important and interesting finding was the lower
excretion of iodine per hour after seaweed intake and lower maximum peak compared to the salt. This
indicate that the bioavailability of iodine from seaweed was lower compared to the iodine intake from
potassium iodide (Combet, Ma et al. 2014). The Norwegian Nutrition Council has recently launched a
report about the iodine situation in Norway and recommends that the use of dried seaweed products
should be used with caution when the iodine level is unknown or if the level is very high as the daily
iodine intake should not exceed 600 μg/day.
The recommended daily intake of iodine varies depending on age of the subject. Recommended intake
is 150 µg/day for adults and children of 10 years or older according to Norwegian, Nordic and WHOs
recommendations (NNR 2014). Recommended daily iodine intake levels are set at 90 µg for children
of 2 to 5 years, and 120 µg for children of 6 to 9 years. For pregnant women the recommendation is
175 µg/day and for lactating women 200 µg/day. The lowest recommended daily intake of iodine for
adults is 70 µg/day. The safe upper level for adults is proposed to be 600 µg/day for adults according
to the Nordic nutrition recommendations (NNR 2014) and the Scientific Committee on Food (SCF
2002). Proposed upper level of iodine intake for children 1-3 years, 4-6 years, 7-10 years, 11-14 years
and 15-17 years is 200, 250, 300, 450, 500 µg/day, respectively (SCF 2002).
Excess iodine is known to affect thyroid function, and in predisposed individuals, even a moderately
increased iodine intake may cause hypothyreosis or hyperthyreosis (Jørgensen and Svindland 1991).
An iodine intake in excess of 2 mg/day can cause sensitivity reactions such as rhinitis, nasal congestion,
13
swollen salivary glands, headache, and acne like skin changes (NNR 2014). A high intake of iodine from
e.g. drugs, certain types of algae or supplements in amounts corresponding to 1 mg up to 10 mg
iodine/day has resulted in increased incidence of iodine goitre, in certain cases with hyperthyroidism
or myxoedema (NNR 2014). Persons with a normal thyroid function can in general tolerate prolonged
consumption of iodine up to 1 mg/day, but even a moderately increased iodine intake of up to 300
µg/day may cause hypothyreosis or hyperthyreosis. The thyroid is also shown to return to normal
function within two-three months after cessation of the intake of seaweed or iodine supplement
(Jørgensen and Svindland 1991). Chronic intake of moderate or large doses of iodine decrease the
serum level of thyroid hormones and increases TSH levels (SCF 2002).
Persistent organic pollutants (POPs)
The POPs are organic, lipid soluble pollutants including dioxins and PCBs. Macroalgae contain very little
fats and it is therefore rather unlikely that the fat soluble pollutants (POPs) should accumulate to high
levels. On a global basis, there are few data on dioxins and PCBs in seaweed. Macroalgae have in
general lower concentrations of PCBs than other foods (Moon, Lee et al. 2005) and dioxin
concentrations in Porphyra yessoensis and Eisenia bicyclis were 50 times lower than phytoplankton
dominated by diatoms (which was higher than zooplankton) (Okumura, Yamashita et al. 2004). Few
data are available with concentration of identified congeners of dioxins and PCBs. Okumura et al.
(2004) found low levels of sum TEQWHO1998 dioxins and dioxin-like PCBs in Porphyra yessoensis and
Eisenia bicyclis with 0.00027 and 0.0013 pg/g ww, respectively. Hashimoto and Morita (1995) found
higher values with sum TEQWHO1998 dioxins and dioxin-like PCBs of 0.015-0.14 pg/g ww in Eisenia bicyclis
and 0.33-0.79 in Undaria pinnatifida. However, all these concentrations are well below the regulatory
limit for fish and other seafood animals.
Toxins and anti-nutrients
Some macroalgae may produce or be a carrier of toxins of relevance for food and feed safety and in
some instances also interesting for therapeutic value.
The presence of pinnatoxin in Norwegian S. latissima were most likely due to the presence of epiphytic
benthic dinoflagellates attached to the kelp. The concentrations were low, however, making a
poisoning unlikely, and 10-100 fold higher concentrations were found in shellfish (Iglesia, del Río et al.
2014).
Among the rare poisonings that have been described after intake of macroalgae, are intoxication from
aplysiatoxin and debromoaplysiatoxin most probably derived from epiphytic blue-green algae on
Gracilaria from Hawaii (Nagai, Yasumoto et al. 1996) .
Three different classes of compounds have been identified in poisonings with species in the genus
Gracilaria. They are prostaglandin E-2 from G. verrucosa in Japan, aplysiatoxins and related compounds
from G. coronopifolia in Hawaii, and polycavernosides from G. tsudai in Guam (Higa and Kuniyoshi
2000).
Sato et al. (1996) and references therein described Kainic acid and domoic acid in japan, found in red
and green algae, but not brown algae. No toxic levels or intoxications were reported, and probably
none of these species are found in Europe.
Seaweeds contain antinutrients as protective substances against grazing. Several publications describe
effects of these substances as for instance polyphenols, on fish (Van Alstyne and Paul 1990). However,
when searching for negative effects of polyphenols on humans, the literature is dominated on medical
14
uses and their anti-oxidant or anti-cancer (Brown et al 2014). We have not been able to find
publications documenting negative effects of antinutrients from seaweeds.
Certain species of macroalgae have been used in medicine due to their content of neurotoxins, as for
example the red alga Digenea simplex which has been used for the treatment of roundworm disease
for centuries, due to the content of kainic acid (KA) (Higa and Kuniyoshi 2000). Kainic acid is the only
toxin reported as produced by macroalgae found in Europe. Mouritsen (2013) reviewed the content
of kainic acid in dulce, excluding the markedly higher levels reported by Ramsey (1994), indicating that
this work had methodological problems or epiphytes as source of Kainic acid. Algae containing both
domoic acid and kainic acid have been used for medical purposes including treatment of roundworms
(Holdt and Kraan 2011). High doses of kainic acid can cause neurotoxic effects, but such high doses are
unlikely to be obtained from consumption of dulce (Mouritsen, Dawczynski et al. 2013).
Radioactivity
There are few publications that describe food safety aspects of radionuclides in macroalgae.
However, Fucus spp. are known to have a high uptake of the radionuclide Technetium-99 (Sjotun,
Heldal et al. 2011), with increasing concentrations from young to older growth segments (Heldal and
Sjotun 2010). Tuo et al (2016) found no higher levels of different radionuclides in different seaweed
species compared to other seafood, vegetables or meat products. Similarly, Moreda-Piñeiro et al.
(2011) concluded that radiation levels in typical Japanese and Korean foodstuff, which include
seaweed, are safe and at the same level as other countries. In general, no levels of concern with
respect to food safety has been found in seafood (pers. comm. J. Klungsøyr, Institute of Marine
Research, Bergen, Norway).
Micro-organisms
The surface of macroalgae represents important habitats for micro-organisms (Bolinches, Lemos et al.
1988; Jensen, Kauffman et al. 1996; Friedrich 2012) and like all eukaryotes, they harbour microbes in
high numbers and of a rich diversity (Lachnit, Blumel et al. 2009; Lachnit, Meske et al. 2011; Bengtsson,
Sjotun et al. 2012; Lachnit, Fischer et al. 2013; Hendriksen and S. 2014; Marzinelli, Campbell et al.
2015). In particular, the bacterial microbiota is ample. Bacterial numbers from 101 to 108/cm2 are
reported, and the numbers seem to increase with higher water temperatures. The bacterial cell
densities in the biofilms of healthy individuals varies between the different macroalgae species
(Bengtsson, Sjotun et al. 2010; Wahl, Shahnaz et al. 2010). Furthermore, epiphytic communities on
macroalgae may be similar in their composition, however could be different form the surrounding
water communities (Bolinches, Lemos et al. 1988) indicating algae-microbe interactions.
Even though the nature of interactions between macroalgae and bacteria is very complex and poorly
understood, these micro-organisms seem to play a role in the host health and infection defence
(Matsuo, Imagawa et al. 2005; Fernandes, Case et al. 2011; Campbell, Verges et al. 2014). However,
some bacteria may also be pathogenic to the algae itself.
The diversity of bacteria on the surface of macroalgae is dependent on a variety of biotic and abiotic
factors, such as the algal species and physical characteristics, habitat and the bacterial load of the
surrounding waters (Egan, Thomas et al. 2008; Egan, Harder et al. 2013). The microbiota occupying the
surface of macroalgae may be indigenous to the marine or brackish water, or originate from terrestrial
areas. Bacteria associated with macroalgae in unpolluted areas originate from the microbiota of the
surrounding waters, and they grow and form biofilms on the surface of the algae. In waters with
anthropogenic influence, including livestock associated activity, intestinal bacteria found in sewage or
run of from land, may add to the macroalgae microbiota.
15
Bacteria associated with macroalgae may be beneficial to the algae (Wahl 2008; Goecke, Labes et al.
2010), and thus live in a symbiotic relations (Egan, Harder et al. 2013), or are related to disease in and
decomposition of dead algae (Largo, Fukami et al. 1995; Largo, Fukami et al. 1997; Largo, Fukami et al.
1999; Vairappan, Suzuki et al. 2001; Wang, Shuai et al. 2008). The algal bacterial pathogens associated
with macroalgae are predominantly non-pathogenic to humans. Bacteria associated with macroalgae
may produce toxins, signalling compounds, and secondary metabolites, however rather than posing a
threat to human health, these may act as an interesting reservoir for novel bioactive compounds (Egan,
Thomas et al. 2008).
Most studies concerning microbial communities associated with macroalgae have an ecologic focus,
describing the numbers, diversity and role of bacteria on the surfaces of the algae (Bolinches, Lemos
et al. 1988; Jensen, Kauffman et al. 1996; Egan, Thomas et al. 2008; Lachnit, Blumel et al. 2009;
Bengtsson, Sjotun et al. 2010; Goecke, Labes et al. 2010; Olson and Kellogg 2010; Bengtsson, Sjotun et
al. 2012; Friedrich 2012; Egan, Harder et al. 2013; Lachnit, Fischer et al. 2013; Martin, Barbeyron et al.
2015). There are however, considerably fewer publications dealing with human pathogenic bacteria
associated with macroalgae, compared to those dealing with antagonistic activities of algae-derived
substances against human bacterial pathogens. When combining the name of algae and pathogen in a
literature search, exemplified by Laminaria digitata + «human pathogen», would give a reference
related to antimicrobial activity against Mycobacterium tuberculosis (McDowell, Amsler et al. 2014).
Searching for all the relevant macroalgae species + “Bacillus cereus”, all references found dealt with
antibacterial activity against this pathogen.
A key issue is if macroalgae may act as reservoirs for faecal bacteria, including potential human
pathogens, and if so do the microbe-algae association enhance the survival time of such bacteria in
the marine environment. Faecal bacteria are commonly detected in near shore marine waters (Boehm
2007) and in organisms performing water filtration, such as bivalves (Lunestad, Frantzen et al. 2016).
Human pathogenic bacteria not originating from the sea may, occasionally be found on macroalgae.
Theoretically, any pathogen derived from man or animal may find its way to the sea and contaminate
the surface of any marine animal or plant, including algae. Several studies describe this phenomenon,
but the risk associated with algae cannot be expected to be higher than what is found for other nonfiltering organism. Moore et al. (2002) examined the surface microbiota of dried dulce (Palmaria
palmata) collected from the coast of Northern Ireland, and detected no intestinal pathogens using
conventional microbiological techniques. The authors included analysis for toxigenic E. coli, bacteria in
the genii Campylobacter and Salmonella, as well as Staphylococcus aureus, Listeria monocytogenes
and fungi.
Whitman et al. (2003) investigated the occurrences of E. coli and enterococci of Cladophora from Lake
Michigan and abundant occurrences were found (up to 97 %), with mean log densities of 5.3 ± 4.8 and
4.8 ± 4.5 per gram dry weight. Both E. coli and enterococci survived for more than six months in sundried Cladophora mats stored at 4°C, and the remaining bacteria in the dried alga readily grew upon
rehydration. As a follow-up, in experiments by Byappanahalli et al. (2003) it was shown that indicator
bacteria like E. coli and enterococci can persist for extended periods and are even able to grow on the
surface of Cladophora sp., particularly during warm summer months. These findings are from fresh
water, however, and Cladophora is probably not used for food purposes.
The indigenous microbiota of brackish and marine water are, predominantly not considered to have a
direct pathogenic potential in humans, with one important exception; some of the bacteria in the
genus Vibrio. In contrast to most other bacteria of importance for seafood safety, members of this
group have the marine and estuarine environment as the main natural habitat (Baumann, Furniss et
al. 1984; West 1989; Sakata 1990). There is no documented correlation between the occurrence of
vibrio and indicator bacteria of faecal origin, thus commonly applied indicator organisms as coliforms
do not give information on presence of potentially pathogenic vibrio.
16
The incidence and density of human pathogenic vibrio in the environment, and consequently in
seafood products including macroalgae, are highly dependent on the ambient water temperatures. It
is well documented that these bacteria are occurring in considerably higher numbers at increased
water temperatures (West 1989; O'Neil, Jones et al. 1992; Høi, Larsen et al. 1998; Baffone, Pianetti et
al. 2000; Oliver and Kaper 2001; Dalsgaard 2002; Adams and Moss 2008).
Bacteria in the genus Vibrio may be detected in seawater, bivalve mussels and marine sediments in
Norway during the summer months (Gjerde and Bøe 1981; Ellingsen 2008). However, the isolates are
neither of the pandemic types (O1, O139), nor carrying pathogenicity genes (tdh, trh). Typical summer
maximum seawater temperatures in Norway may wary from approximately 10C in northern parts to
25C in southern parts.
Several of the human pathogenic vibrios are described associated with macroalgae. From Japanese
waters V. parahaemolyticus have been isolated from Ulva sp., Fucus sp., Laminaria sp., and
Porphyra sp. (Mahmud, Neogi et al. 2007) and V. vulnificus were found on Porphyra sp., Undaria sp.,
Laminaria sp., and Fucus sp. (Mahmud, Neogi et al. 2008). In a study by Chan and McManus (1969),
vibrios were found to be the predominant bacteria growing on Ascophyllum nodosum.
Even though domestically acquired food borne infections with vibrios have been observed sporadically
in Norway, the registered numbers are very limited and no cases have been shown connected to
consumption of macroalgae. Furthermore, bacteria in this genus are not considered robust, are
relatively sensitive to heating, drying, and several other preservation techniques, as well as the low pH
in the stomach of humans. Thus, it is not likely that vibrios will survive the production processes
relevant for macroalgae for food and feed with the exception of algae used directly or after freezing.
Some environmental bacteria not having the aquatic habitat as its niche, may also pose a challenge for
food safety without giving a direct risk of infection. Of highest importance are the spore formers
Bacillus sp. and Clostridium sp., originating from soil by run of from land. As in other food and feed,
members of these geni may produce toxins of health concern, if products are stored under improper
time and temperature conditions. The risk for these agents for products from macroalgae are however
largely unknown, and more work should be done to unravel the possible challenges posed by spore
formers.
Many macro-algae are rich in bioactive compounds, which have antioxidant properties, and also have
antimicrobial activities against food pathogenic microorganisms. Dussault et al. (2016) showed that
macroalgal extract had antibacterial activity against Listeria monocytogenes, Bacillus cereus and
Staphylococcus aureus. Meillisia et al. (2013) found that extracts of Saccharina (Laminaria) japonica
showed antibacterial activity against Salmonella Typhimurium, Staphylococcus aureus and Bacillus
cereus. Amiguet el al. (2011) found that glycolipid-rich extracts of Fucus evanescens in culture have
antibacterial activity against Haemophilus influenzae, Legionella pneumophila, Propionibacterium
acnes, Streptococcus pyogenes, Clostridium difficile and methicillin-resistant Staphylococcus aureus.
In an ongoing study, macroalgae harvested from Norwegian waters have been analysed for the
presence of Listeria monocytogenes, pathogenic vibrios, enterococci, coliforms and thermotolerant
coliforms, and none of these were detected in any of the samples (NIFES unpublished results).
Based on the studied literature, the question regarding the possible enhanced survival faecal bacteria
and potential human pathogens associated to macroalgae remain largely unresolved.
Viruses rank among the most important infective agents causing food- and waterborne gastrointestinal
disease worldwide (Cook and Richards 2013). In particular, norovirus cause large outbreaks in all age
groups. For seafood organisms, the filter feeders are particularly prone to virus accumulation. As nonfilter feeders, the macroalgae are not considered risk organisms for food or feed borne viral
17
transmission. So far only a very limited number of outbreaks have been linked to macroalgae (Park,
Jeong et al. 2015).
In conclusion, macroalgae are densely populated by bacteria on their surfaces. Some of these bacteria
have a potential as human pathogens or could make challenges during processing and improper
storage, but the importance of algae in feed or food borne disease cannot be expected higher than for
other non-filtering marine organisms used for such purposes, including fish. Furthermore, the
macroalgae are not considered risk organisms for food or feed borne viral transmission.
Microplastics
Recently, interaction of microplastics with macroalgae have been addressed for the first time. In
laboratory experiments, the seaweed Fucus vesiculosus retained suspended microplastics on its
surface (Gutow, Eckerlebe et al. 2016). Any organism feeding on such algae might consume the plastic
particles as well. This hypothesis was corroborated by studying the periwinkle Littorina littorea, which
readily consumed such algae without preference for uncontaminated ones (Gutow, Eckerlebe et al.
2016). The potential entrance pathway for microplastics and associated contaminants from
macroalgae to humans should be investigated. The possibility of bioaccumulation would be one aspect
of such investigation. Retention levels of the plastic on the algae only reflected the concentration of
the surrounding waters, but suspended particles do accumulate in macrophyte habitats (Gutow,
Eckerlebe et al. 2016). Therefore, bioaccumulation might not occur within in the plant, but through
the macroscopic properties of the habitat. Concerning the consequences for the macroalgae
themselves, it can be speculated that, at high concentrations of microplastics pollution, their
photosynthesis might be hampered, as it was shown for microalgae (Bhattacharya, Lin et al. 2010),
with increasing effects at decreasing particle size (Sjollema, Redondo-Hasselerharm et al. 2016). This
might affect the growth efficiency of the algae.
Digestibility of seaweed carbohydrates.
While most land plants store carbohydrate as starch with high energy value, the marine algae is known
to possess several other polysaccharides with lesser energy value when applied in food or feed.
In brown algae, including kelp of the Laminaria family, alginates are predominant. Alginates are
polysaccharides consisting of long chains of mannuronic and guluronic acids. These are in literature
mainly regarded as fibre with little or no energy content.
The most important red algae used for consumption in Norway is dulce (Palmaria palmata). Red alga
polysaccharides mainly consist of carrageenans and agar. Data on nutrient content of dried Nori
(macroalgae used in Japanese style dishes) varies considerably. In the Norwegian food composition
table (www.matvaretabellen.no) it is stated to have 12% water and to contain 55 % carbohydrate in
the form of starch, and no fibre. This data seems to need updating. The given protein content in the
Norwegian vs. the Canadian food table is also very different, but here methodology might be an
important issue.
Also Sea lettuce (Ulva lactuca), the only major green algae used for human consumption, is known for
special content of its polysaccharides. This includes high level of the unusual sugar rhamnose, also
found in pectin.
It is important to adjust the impression that the carbohydrates in marine algae gives energy in line with
vegetables from terrestrial environments. On the other hand, from a human health point of view, an
increased consumption of indigestible components as well as reduced energy intake might be
18
favourable. For macroalgae, this is particularly relevant as they may contain other essential
compounds such as trace elements.
Frequent eating of seaweed alters gut microflora (Hehemann, Correc et al. 2010), and further studies
on the possible effects on altered digestibility have to be conducted.
5. CONCLUSIONS
The present evaluation is based on the scarce data available. The occurrence data indicate that
Norwegian algae may contain elevated levels of arsenic and cadmium, particularly in brown algae. The
levels of arsenic and cadmium may limit the use of some macroalgae as feed and food ingredients.
More occurrence data are needed to fully describe the occurrence of arsenic and the heavy metals in
algae from Norwegian waters. New data sets should cover seasonal variation and different locations
along the coastline.
The lipid content of macroalgae is low and the levels of persistent organic pollutants is in accordance
with this also low and lower than comparable food items. There are, however, very few published data
available in the field.
Levels of iodine in different types of macroalgae is high and only a small intake of dried macroalgae
may exceed the recommendation of iodine intake. At the same time, more knowledge of the
bioavailability needs to be considered as it is of importance that the iodine status is brought to the
level that the population is euthyroid.
Some species of macroalgae produce toxins and other toxins are produced by epiphytes attached to
the algae. No poisonings have been reported in Europe, and for the toxins that have been reported
from a few European studies, the levels have been low and without any concern for human health.
Some incidents of poisoning have been reported from Asia where epiphytic blue-green algae are the
most probable source. Anti-nutrients such as polyphenols are present in macroalgae, giving negative
effects on grazing snails and fish. However, no documentation of negative effects from algal
consumption in humans could be found, while use of such substances in medicine is well described.
Macroalgae do accumulate radionuclides, but few studies focus on food safety and no levels of concern
for food safety have been found.
Macroalgae are densely populated by bacteria on their surfaces. Some of these bacteria have a
potential a human pathogens, or could make challenges during processing if improperly stored.
However, the importance of algae in feed or food borne disease, including viral contagious agents,
cannot be expected to be higher than for other non-filtering marine organisms used for such purposes,
including fish.
Microplastics, defined as plastic particles smaller than five millimetres, are now common at all levels
of the marine environment. Such particles are prone to accumulation of organic contaminants, and
may subsequently adsorb onto macroalgae, potentially introducing the particles and their associated
contaminants to animals and humans by food and feed.
Macroalgae contain polysaccharides that are rather different form land living food and feed plants,
where starch is the major polysaccharide. The knowledge of the available energy content of these are
low but in many cases they are more fibre than energy giving compounds. From a human health point
of view, an increased consumption of indigestible components as well as reduced energy intake could
be favourable. In feed perspective this could be a problem.
19
The available information on the amount of macroalgae or products from macroalgae used in feed and
as food in Europe, including Norway is sparse. As possible health impact on animals and humans is
connected to exposure, more information on human consumption and feed applications are
considered necessary.
The possible effect of processing on the bioavailability of components in macroalgae is largely
unknown. However, for iodine food preparation and cooking methods will influence the final iodine
content in the product, with an observed reduction of up to 70% after five minutes of boiling in water.
One should keep in mind that the boiling water may be consumed by inclusion in e.g. soups, and the
iodine lost from the macroalgae during boiling may be reintroduced.
After reviewing the literature on possible risks associated with macroalgae as food and feed, it became
obvious that there is a substantial lack of data on most factors of relevance. More work to examine
the prevalence and importance of chemical and biological risk factors should be considered. For further
risk evaluation of food safety associated with macroalgal consumption, information on bio availability
will be necessary. The structural polysaccharides of macroalgae have low digestibility and may bind
certain heavy metals. More absorption studies including iodine, cadmium and inorganic arsenic from
macroalgal matrices should be performed in order to provide such information. To challenge the
assumption that there is a low risk of finding pathogenic bacteria on macroalgae, microbial studies of
macroalgae compared with molluscs from contaminated waters should be performed.
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