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Evaluation of the Hazard of Microcystis Blooms for Human Health through Fish Consumption
Collaborators
Juli Dyble, GLERL
Duane Gossiaux, GLERL
Steve Pothoven, GLERL
Alan Wilson, CILER
Erin Sedgman, Western Michigan University (WMU web site)
Robert Hecky, University of Waterloo (UW web site)
Stephanie Guildford, University of Waterloo
This research is funded by the NOAA Center of Excellence for Great Lakes and Human Health
Executive Summary
The initial investigation of the role of fish consumption on human health hazard was begun in FY 05 and continued through FY 06. Last year a method was established and fish concentrations were measured for fish of opportunity collected from Lake Erie by the Ohio Department of Natural Resources (ODNR web site) through the summer. The concentrations in fish (walleye and yellow perch), were low (0.03 0.45 ng g -1) wet muscle tissue. These concentrations would have led to exposures that were substantially lower than the 0.04 µg kg -1 d -1 that is set by the World Health Organization (WHO web site) for chronic exposure based on a meal size of 300 g. The reason for the low values was thought to result from the absence of a Microcystis bloom during the summer of 2005. The liver concentrations in fish were much higher (4 33 ng g -1) wet weight suggesting that the fish do get exposed to the microcystin toxin. The sampling this year has been more extensive covering Lake Erie, Saginaw Bay (Lake Huron) and three inland lakes (Gull Lake, Spring Lake, and Muskegon Lake) during June thru September to help insure that fish would be collected from areas with high Microcystis blooms. The inland lakes exhibited relatively high concentrations of microcystin toxin in July. The concentrations in the fish are currently undergoing analysis.
GLERL Research Biologist Juli Dyble samples an algal bloom in Lake Erie.
Project Rationale
Blooms of cyanobacteria specifically Microcystis variants lead to exposures that can induce toxicity from the associated microcystin toxin to a wide range of animals including humans (de Figueiredo et al. 2004). These blooms occur from the increased nutrient loads to aquatic systems and can be exacerbated by the presence of the zebra mussel, Dreissena polymorpha (Vanderploeg et al. 2001). The microcystis threshold for human health is 1 ug L-1 in drinking water (WHO 1998) and 20 ug L-1 in water for recreation (WHO 2003). Microcystin in mammals is selective for hepatocytes and inhibits serine/theonine protein phosphatases (Dawson 1998). This inhibition causes disintegration of the liver structure, liver necrosis, and internal hemorrhage in the liver that can lead to death (Dow and Swoboda 2000). The LD50 for microcystin-LR in mice is about 50 ug kg-1 (Dawson 1998, WHO 1998). Microcystins have also been shown to lead to promotion of liver cancer in chronic administration (Ito et al. 1997). Thus, the recent increases in Microcystin blooms in the Great Lakes (Babcock-Jackson 2000, Murphy et al. 2003) leads directly to the need for assessment for human and ecological health investigations.
Most
of the exposures of concern to humans occur through exposure to contaminated
drinking water and to inhaled/ingested micorcystin in aquatic recreation.
There is circumstantial evidence of exposure and toxicity to humans consuming
contaminated fish (Dawson 1998) and measured concentrations that would
exceed acceptable daily intake levels based on fish tissue concentrations
(De Margalćes et al. 2001, 2003). Thus, the potential of fish in the Great
Lakes to serve as a source of contamination to humans should be evaluated.
To date, only one study has investigated fish concentrations in Great
Lakes fish and that study only reported concentrations in liver and intestine
content for field collected fish (Babcock-Jackson 2003). In this study,
the concentrations in liver are sufficient to show that the microcystin
is available to fish but the question remains on the potential for human
health issues. To make an estimate of the potential for exceeding the
acceptable daily intake of 0.04 ug kg-1 d-1 (WHO
1998), the following analysis was made: Using the consumption and weight
estimates in de Margalćes et al. (2001) of an average weight of an individual
is 60 kg yielding the total tolerable intake of 2.4 ug with a 300 g intake
for fish the fish concentration would be 8 ng g-1 wetweight in muscle tissue. Because
the concentration in fish muscle was not provided for Great Lakes fish
and estimate of potential concentrations was made from the ratio of liver
to muscle concentrations for rainbow trout (Burry et al. 1998) and applied
to the fish liver concentrations from the Great Lakes (Babcock-Jackson
2000). The ratio for the liver to muscle for rainbow trout after 24 h
exposure was 0.397 ± 0.24 (note the lowest value measured was 0.225, Burry
et al. 1998). If this ratio is applied to fish collected from Lake Erie
(Babcock-Jackson 2000) for yellow perch the concentrations during a bloom
in fish muscle would be estimated to range from about 37 to 91 ng g-1
and for walleye the concentration would be not detectable. Other fish
species are reported for Lake Erie but they do not represent species consumed
by humans although the concentration expected in these organisms would
be estimated to be as high as 118 ng g-1. Comparing these estimated
values with that estimated for a tolerable daily intake, the estimated
concentrations in fish would be about 5 to 11 times greater and thus represent
a potential risk to humans consuming fish during periods of blooms. Despite
the above estimates, the actual concentrations in fish muscle tissue are
not known and may be substantially different from that represented by
the estimate because the actual ratio for between liver and muscle tissue
for perch is not known. In fact in flounder, microcystins can be accumulated
in the liver with no detectable concentrations in the muscle (Sipiä et
al. 2002). Also, in feeding studies with gobies feeding on zebra mussels,
there was a correlation between liver and gut concentrations and the amount
of microcystin ingested but not muscle (Babcock-Jackson 2000). In this
same report, the feeding study was complicated because of background concentrations
of microcystin in the fish prior to the feeding experiment. However, the
concentrations in the muscle did range from non-detectable to greater
than 100 ng g-1 in this feeding study. Overall, the relationship
between fish exposure and muscle concentrations remains in question. This
question was not well addressed in the first year of this study because
of the limited exposure of the fish to Microcystis based on liver
concentrations below 36 ng g-1. Thus, it is important to secure
fish samples from populations that have higher levels of exposure.
Project Accomplishments
2006
Cyanobacterial blooms pose serious threats to food-webs in the Great Lakes basin. The purpose of this work is to establish the potential hazard associated with humans consuming fish tainted with the hepatotoxin, microcystin. Many ubiquitous cyanobacterial genera found in the Great Lakes, such as Microcystis and Anabaena, can produce microcystins and other known toxic secondary metabolites. Evidence exists which suggests that microcystins can accumulate in fish tissue, particularly livers and somewhat in the muscle tissue, from Great Lakes fishes, however, the data are limited.
The work from last year provided the limited data on accumulation of microcystins in fish muscle and live tissue (Tables 1 and 2). Despite finding that fish are exposed to liver toxin and that some of the material is accumulated,the concentrations were well below concentrations that are considered of concern, 8 ng g -1, as calculated from the WHO limit of 0.04 0.04 µg kg -1 d -1 considering a 60 kg individual and a 300 g meal. The reason for the low concentrations observed in fish could have been due to limited uptake efficiency for the toxin or to limited exposure. The exposure in 2005 was considered low as no major Microcystin bloom was observed in Lake Erie. Thus, determine whether the low concentrations in fish were due to low absorption efficiency or to limited exposure, the sampling parameters were expanded for the summer of 2006.
Samples of Microcystis, water, zooplankton, and fish were collected in collaboration with scientists from the Ohio DNR and Michigan DNR (MI DNR web site), from Lake Erie and Saginaw Bay during June 2006 to September 2006. We also have sampled three inland lakes, Gull, Spring, and Muskegon, that vary in productivity, have frequent and extreme cyanobacterial blooms, and are heavily used for recreation from June 2006 to October 2006. Algal samples from June and July 2006 from Lake Erie and the inland lakes show large variation in toxin levels from June (none existent in Lake Erie to 500-4,000 ng toxin (g dry mass) -1 in the inland lakes) to very high toxin levels in July (700-7,500 ng toxin (g dry mass) -1 in Lake Erie to 3,500-10,000 ng toxin (g dry mass) -1 in the inland lakes). Relative changes in toxin levels from June to July 2006 in the inland lakes varied from 21% to over 500%. Fish livers from Lake Erie yellow perch and walleye collected in July 2006 contained 807 ng toxin (g dry mass) -1 and 143 ng toxin (g dry mass) -1, respectively. The toxin levels we observed in the yellow perch livers were more than an order of magnitude greater than levels we found in 2005 and more than twice that observed for yellow perch livers collected during a Microcystis bloom in Lake Erie in year 1998 (297 ng toxin (g wet weight) -1 or about 74 ng g -1 dry weight; Babcock-Jackson 2000 thesis). Large cyanobacterial blooms were observed from all sites during later collections in 2006, and consequently, even higher toxin levels are expected in samples collected from these time periods. The remaining phytoplankton, fish, zooplankton, and water samples from our collections will be analyzed for microcystin concentration later this year. Field sampling will be conducted through October 2006.
2005
The purpose of this work is to establish the potential hazard associated with fish consumption due to potential accumulation of microcystin. Bluegreen algal blooms in the Great Lakes have increased particularly since the invasion of the zebra mussel. Several of the species in the lake, including Microcystis and Anabaena, have the potential to produce the algal toxin microcystin a known hepatotoxin. The potential for accumulation of microcystin in the food chain to edible portions of fish is not known for the Great Lakes but for planktivores such as Tilapia. Methods for the measurement of microcystin in fish were established and recovery of spiked samples was 90.7 ± 17.6%. For this first year, fish of opportunity were collected by the Ohio Deppartment of Natural Resources during their monthly fish collections. The fish were collected in May (pre bloom), July, August and September. The concentrations in the May fish were essentially at background (0.27 ± 0.09 ng g-1). The Fish from the other collections will be completed this next year.
Presentations
Landrum, P.F. and D.C. Gossiaux. Evaluation of the hazard of Microcystis blooms for human health through fish consumption. Ocean and Human Health All PI Meeting, January 17-20, 2006, Charleston, SC.
Sedgman, E. 2006. Evaluation of the Hazard of Microcystis Blooms for Human Health through Fish Consumption. NOAA Hollings Fellow Conference. Silver Springs, Maryland.
References
Babcock-Jackson, L. 2000. Toxic microcystis in western Lake Erie: Ecotoxicological relationships with three non-indigenous species increase risks to the aquatic community. Dissertation, The Ohio State University, Columbus, OH.
Burry, N.R., Newlands, A.D., Eddy, F.B., Codd, G.A. 1998. Invivo and in vitro intestinal transport of 3H-microcystin-LR, a cyanobacterial toxin, in rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 42:139-148.
Dawson, R.M. 1998. The toxicology of microcystins. Toxicon 36:953-962.
De Figueiredo, D.R., Azeiteiro, U.M., Seteves, S.M., Goncalves, F.J.M., Pereira, M.J. 2004. Micorcystin-producing blooms - a serious global public health issue. Ecotoxicol. Environ. Safety 59:151-163.
De Magalćes, V.F., Soares, R.M., Azevedo, S.M.F.O. 2001. Microcystin contamination in fish from Jacarepaguį Lagoon (Rio de Janeiro, Brazil): ecological implication and human health risk. Toxicon 39:1077-1085.
De Magalćes, V.F., Marinho, M.M., Domingos, P., Oliveira A.C., Costa, S.M., Azevedo, L.O., Azevedo, S.M.F.O. 2003. Microcystins (cyanobacteria hepatotoxins) bioaccumulation in fish and crustaceans from Sepetiba Bay (Brasil, RJ). Toxicon 42:289-295.
Dow, C.S., Swoboda, U.K. 2000. Cyanotoxins. In Whitton, B.A., Potts, M. (Eds.) The Ecology of Cyanobacteria. Kluwer Academic Publishers, The Netherlands, pp. 613-632.
Ito, E., Kondo, F., Terao, K., Harada, K.I., 1997. Neoplastic nodular formation in mouse liver induced by repeated intraperitoneal injections of microcystin-LR. Toxicon 35:1453-1457.
Murphy, T.P., Irvine, K., Guo, J., Davies, J., Murkin, H., Charlton, M., Watson, S.B. 2003. New microcystin concerns in the lower Great Lakes. Water Qual. Res. J. Canada 38:127-140.
Sipiä, V.O., Kankaanpää, H.T.,Pflugmacher, S., Flinkman, J., Furey, A. James, K.J. 2002. Bioaccumulation and detoxication of nodularin in tissues of flounder (Platichthys flesus), mussels (Mytilus edulis, Dreissena polymorpha), and clams (Macoma galthica) from the Northern Baltic Sea. Ecotoxicol. Environ. Safety 53:305-311.
Vanderploeg, H. A., J. R. Liebig, W. W. Carmichael, M. A. Agy, T. H. Johengen, G. L. Fahnenstiel, and T. F. Nalepa. 2001. Zebra mussel (Dreissena polymorpha) selective filtration promoted toxic Microcystis blooms in Saginaw Bay (Lake Huron) and Lake Erie. Can J. Fish. Aquat. Sci. 58: 1208-1221.
WHO, 1998. Cyanobacterial toxins: microcystin-LR. In: Guidelines for drinking water quality. 2nd Edition, Addendum to Vol 2. Health criteria and other supporting information. World Health Organization, Geneva, Switzerlan, pp. 95-110.
WHO. 2003. Algae and cyanobacteria in fresh water. In Guidelines for safe recreational water environments. Vol. 1: Coastal and fresh waters. World Health Organization, Geneva, Switzerland, pp. 136-158.
Last updated: 2007-03-22 mbl