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Animal Science Journal (2015) 86, 120–124

doi: 10.1111/asj.12301

R A P I D C O M M U N I C AT I O N Cesium radioactivity in peripheral blood is linearly correlated to that in skeletal muscle: Analyses of cattle within the evacuation zone of the Fukushima Daiichi Nuclear Power Plant Tomokazu FUKUDA,1 Yasushi KINO,2 Yasuyuki ABE,3 Hideaki YAMASHIRO,4 Jin KOBAYASHI,5 Yoshinaka SHIMIZU,6 Atsushi TAKAHASHI,7 Toshihiko SUZUKI,6 Mirei CHIBA,6 Shintaro TAKAHASHI,8 Kazuya INOUE,8 Yoshikazu KUWAHARA,8 Motoko MORIMOTO,5 Hisashi SHINODA,6 Masahiro HIJI,9 Tsutomu SEKINE,10 Manabu FUKUMOTO8 and Emiko ISOGAI1 1

Graduate School of Agricultural Sciences, Tohoku University, Sendai, Miyagi, Japan 2Department of Chemistry, Tohoku University, Sendai, Miyagi, Japan 3National Research Center for Protozoa Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido, Japan 4Faculty of Agriculture, Niigata University, Niigata, Niigata, Japan 5Miyagi University, School of Food, Agricultural and Environmental Sciences, Miyagi, Japan 6Graduate School of Dentistry, Tohoku University, Sendai, Miyagi, Japan 7Tohoku University Hospital, Sendai, Miyagi, Japan 8Department of Pathology, Institute of Development, Aging and Cancer, Tohoku University, Sendai, Miyagi, Japan 9Hitachi Solutions East Japan, Ltd, Sendai, Miyagi, Japan 10Center for the Advancement of Higher Education, Tohoku University, Sendai, Miyagi, Japan

ABSTRACT The accident at the Fukushima Daiichi Nuclear Power Plant (FNPP) released a large amount of radioactive substances into the environment. Furthermore, beef contaminated with radioactive cesium above the 500 Bq/kg safety standard was circulated in the food chain in 2011. Japanese consumers remain concerned about the safety of radioactively contaminated food. In our previous study, we detected a linear correlation between radioactive cesium (137Cs) activity in blood and muscle around 500 to 2500 Bq/kg in cattle. However, it was unclear whether the correlation was maintained at a lower radioactivity close to the current safety standard of 100 Bq/kg. In this study, we evaluated 17 cattle in the FNPP evacuation zone that had a 137Cs blood level less than 10 Bq/kg. The results showed a linear correlation between blood 137Cs and muscle 137Cs (Y = 28.0X, R2 = 0.590) at low radioactivity concentration, indicating that cesium radioactivity in the muscle can be estimated from blood radioactivity. This technique would be useful in detecting high-risk cattle before they enter the market, and will contribute to food safety.

Key words: food safety, Fukushima Daiichi Nuclear Power Plant, radioactive cesium, radioactive substances.

INTRODUCTION The accident at the Fukushima Daiichi Nuclear Power Plant (FNPP) released a large amount of artificial radioactive substances into the environment (Bowyer et al. 2011; Kinoshita et al. 2011; Sinclair et al. 2011; Yasunari et al. 2011). In particular, the release of radioactive cesium (137Cs and 134Cs) is a safety concern (Calabrese 2011). We previously reported a correlation between 137Cs radioactivity in whole peripheral blood and in the organs of cattle (Fukuda et al. 2013). This finding led us to the hypothesis that muscle cesium radioactivity could be estimated from blood radioactivity, and may serve as an indicator for evaluating food safety. However, this correlation was evaluated in © 2014 Japanese Society of Animal Science

cattle with a high radioactivity, around 500 to 2500 Bq/kg of skeletal muscle (Fukuda et al. 2013), and the relationship at lower radioactivity levels is not well understood. Since April 2012, the safe standard allowed in Japan for radioactive cesium has decreased from 500 Bq/kg to 100 Bq/kq (Okada et al. 2013). Therefore, it is important to study any potential correlation between blood Cs and organ Cs radioactivity at the new 100 Bq/kg standard. Correspondence: Emiko Isogai, Graduate School of Agricultural Sciences, Tohoku University, Tsutsumidori, Amamiyamachi, Aoba, Sendai 981-8555, Japan. (Email: [email protected]) Received 20 May 2014; accepted for publication 2 July 2014.

BLOOD AND MUSCLE CESIUM LEVELS IN CATTLE

Table 1

121

The details of the analyzed cattle

Date of sampling

Sampling location

Sex

Date of birth

Strain

2011.8.31 2011.8.31 2011.9.6 2011.10.20 2011.11.15. 2011.12.27. 2011.12.27. 2011.12.27. 2011.3.8 2011.3.8 2012.3.14. 2012.3.15. 2012.3.15. 2012.3.15. 2012.3.15. 2013.1.17. 2013.1.17.

Fukushima, Minami-Soma city Fukushima, Minami-Soma city Fukushima, Kawauchii village Fukushima, Kawauchii village Fukushima, Kawauchii village Fukushima, Naraha town Fukushima, Naraha town Fukushima, Naraha town Fukushima, Naraha town Fukushima, Naraha town Fukushima, Naraha town Iwate, Ichinoseki city Iwate, Ichinoseki city Iwate, Ichinoseki city Iwate, Ichinoseki city Tochigi, Nasu-shiobara city† Tochigi, Nasu-shiobara city†

Heifer Heifer Heifer Heifer Heifer Heifer Heifer Heifer Heifer NA Heifer Steer Steer Steer Steer Heifer Heifer

2010.08.04 2011.01.18 1994.12.05 NA 2005.09.18 2005.09.18 2006.02.23 2007.02.05 2000.12.12 NA 2005.12.15 2009.04.10 2009.03.20 2009.03.03 2009.05.20 2006.01.23 2008.11.25

Japanese Japanese Japanese Japanese Holstein Holstein Holstein Holstein Japanese Japanese Holstein Japanese Japanese Japanese Japanese Japanese Japanese

Black Black Black Black

Black Black Black Black Black Black Black Black

†Samples were obtained from the radiocontamination feeding test. NA, not available.

In this study, we evaluated the correlation of cesium radioactivity between blood and skeletal muscle with the goal of estimating muscle cesium radioactivity from peripheral blood, which can provide useful information on food safety.

MATERIALS AND METHODS Sample collection and radioactivity measurement We collected peripheral blood and muscle samples from 223 cattle in the FNPP evacuation zone between August 29, 2011 and September 12, 2012. Skeletal muscle samples were obtained from three representative positions, that is, the Longissimus, Bicep femoris and Masseter muscles. The sample radioactivity was determined by gamma-ray spectrometry using high-purity Germanium (HPGe) detectors (Ortec Co., Oak Ridge, TN, USA), as described previously (Fukuda et al. 2013). All measurements were decaycorrected to the day of major release, March 15, 2011. Cattle with a blood cesium activity lower than 10 Bq/kg were selected for further analyses (n = 17). In 17 cattle, 11 were abandoned cattle in the evacuation zone. The blood and muscle samples from four steers in Iwate prefecture, and two cattle in Tochigi prefecture, which were used for radiocontaminated feed testing at Nasu-shiobara city, were also analyzed. The feeding condition of testing is described below. The cattle were kept in grassland, on free access to the contaminated grass (around 3000 Bq/kg) from March to October in 2011. After that, the cattle were kept in barns and received radio-contaminated feeding (around 2000 Bq/kg) from November 2011 to March 2012. From April to June 2012, the cattle were provided with radio-contamination free feeding (0 Bq/kg). Furthermore, cattle were kept on grassland, and free access to the contaminated grass (around 2000 Bq/kg) from August to October in 2012. From November 2012 to January 2013, cattle were kept in barns and obtained contaminated feeding (around 100 Bq/kg) until being sacrificed. Animal Science Journal (2015) 86, 120–124

Ethics This study was performed as one of the national studies associated with the Great East Japan Earthquake and supported by the Japanese government through the Ministry of Education, Culture, Sports, Science and Technology, Japan. A detailed description of the animal care and protocol is described in a previous study (Fukuda et al. 2013). In brief, organs and blood from euthanized cattle were collected by veterinarians at the Livestock Hygiene Service Center (LHSC) of Fukushima prefecture. Cattle were sacrificed by the veterinarians using the method detailed in our previous publication (Fukuda et al. 2013).

RESULTS To elucidate the relationship between radioactive cesium in blood and that of muscle, we analyzed the radioactivities in muscle samples. In the abandoned cattle, we analyzed the samples, which showed lower than 10 Bq/kg in the blood 137Cs concentration. In total, 17 animals were analyzed to evaluate the correlation. Information on the cattle are summarized and shown in Table 1. We confirmed that any photopeaks of 134Cs and 137Cs (data not shown) were not detectable in the control animals, which were housed in Hokkaido prefecture in northern Japan, 630 km from the FNPP (Fukuda et al. 2013). We confirmed that all cattle which had more than 100 Bq/kg in their meat were all derived from the evacuation zone. In total, the number of analyzed blood sample was 17, the number of analyzed muscle sample was 34 from the 17 cattle. Therefore, 34 measuring points were plotted on the graph, as shown in Figure 1. The lowest level of the detected radioactive cesium was 0.48 Bq/kg (137Cs) in the blood sample. The lowest limit of the quantitation is dependent on the volume of the sample and measurement background. Therefore, we calcu© 2014 Japanese Society of Animal Science

122 T. FUKUDA et al.

Figure 1 Cesium radioactivity in skeletal muscle and blood samples from cattle in the Fukushima Daiichi evacuation zone. A positive correlation was observed between blood and muscle radioactivity of 137Cs (A), 134Cs (B) and total radioactive cesium (137Cs + 134Cs) (C).

lated the detection limit and determination limit of 70 g of sample, which is the identical condition with the lowest detected sample. As shown in supplemental Figure 1, the detection limit of radioactive cesium was 0.023 to 0.037 Bq/kg (it depended on the background measurements). Furthermore, we calculated the determination limit was 0.257–0.411 Bq/kg. In this study, all of the detected samples for 137Cs and 134Cs were more than the determination limit. Based on these data, we concluded that our detection condition is enough to obtain the quantitative results. A regression analysis between blood and muscle 137 Cs activity showed a linear correlation (Y = 28.0X, R2 = 0.590) at low radioactivity, shown in Figure 1A. A similar correlation was also observed in the activity of 134 Cs (Fig. 1B) and total radioactive cesium (137Cs and 134 Cs, Fig. 1C) in the corresponding animals. Furthermore, we showed the correlation with average and standard deviation in Figure 2. The R2 value with average and standard deviation becomes higher than that with all measuring points (R2 = 0.742 in 137Cs). © 2014 Japanese Society of Animal Science

DISCUSSION Radioactive cesium contamination has been reported in various types of food and water sources, including vegetables, fruit, milk and tea leaves, in May 2011, beef in July, and rice in September 2011. The beef contamination was caused by the delayed announcement from the Ministry of Agriculture, Forestry, and Fisheries of Japan to farmers on the risk of feeding dry rice straw to cattle. With the deposit of radioactive cesium into muscle, contaminated beef has circulated within the marketplace, resulting in safety concerns for consumers. Radioactive cesium has been reported in several types of meat (Isogai et al. 2013), and the need to access the risk of chronic exposure to radioactive cesium has been raised by scientists (Calabrese 2011). Based on these concerns, we analyzed the relationship between blood and muscle cesium radioactivity. There was a variation of the radioconcentration of cecium dependent on the cattle even in the same Animal Science Journal (2015) 86, 120–124

BLOOD AND MUSCLE CESIUM LEVELS IN CATTLE

123

Figure 2 Cesium radioactivity in skeletal muscle and blood samples from cattle. The measuring points were summarized into average and standard deviation for each cattle. A positive correlation was observed between blood and muscle radioactivity of 137Cs (A), 134Cs (B) and total radioactive cesium (137Cs + 134Cs) (C).

location. In brief, Holstein cattle, which were sampled on December 27 in 2011, showed relatively lower radioconcentrations both in blood and muscle, when they were compared with other sampling days. The lower value of December 27 would be due to the feeding history of the cattle. According to infomation from the owner, the cattle were released to the outside of the barn (evaluation zone) within 2 days period, and they could access the radiocontaminated grass outside within 2 days. In the rest of the period, non-radiocontaminated grass were accessed, based on the backgound history obtained from the owner. From these situations, the difference in radioconcentration of cesium might come from the time period staying in the evacucation zone and history of the cattle. A previous regression analysis of multiple organs in cattle showed that the skeletal muscle has the highest deposition of radioactive cesium (Fukuda et al. 2013). A strong correlation was established between blood Animal Science Journal (2015) 86, 120–124

and organ cesium radioactivity around 500–2500 Bq/kg in skeletal muscle, but it was unclear whether this relationship was maintained at lower skeletal muscle radioactivity levels, such as 100 Bq/kg, until this study. Our findings show that cesium concentration in skeletal muscle can be estimated from the measured cesium radio-concentration in blood, even at low concentrations. The regression analysis also showed that the total cesium radioactivity in skeletal muscle was 27.0 times higher than in blood. Based on the present analysis, an approximately 4 Bq/kg blood concentration is the threshold corresponding to the safe regulated level in muscle. Our previous results showed that concentration of radioactive cesium in skeletal muscle was 21.3 times higher (137Cs) than that in blood, indicating the slope of the regression line is higher in the current study, which was relatively lower than that in this study. A potential explanation for this difference may be measuring or sampling error. In the relatively low radioactivity area, the measuring results © 2014 Japanese Society of Animal Science

124 T. FUKUDA et al.

are more sensitive for these errors. The measurements in high radioactivity area can be finished in a relatively shorter time period. However, the measurement of 2–3 Bq/kg takes around 24 h. The improvement of the sensitivity on radioactivity measurement would reduce the effect of the error. Our result in this study indicate that this technique could prove useful in screening high-risk cattle beyond the radioactivity regulation for meat (100 Bq/kg), and in preventing the circulation of contaminated meat. We intend to build on the current findings by designing software that can estimate the muscle radioactive cesium concentration from blood cesium concentration. Japanese consumers are still have safety concerns about livestock products from Fukushima. Therefore, the establishment of more sensitive methods to measure radioactive cesium in lower radio-concentration levels, such as 50 Bq/kg, may help the recovery of livestock production in Fukushima. For more efficient estimation, the collection of larger numbers of samples, and improvement of detection devices are essential. Future applications of the present findings could increase food safety of meat, and contribute to the recovery of the livestock industry in the area affected by the Great East Japan Earthquake.

Conclusion Radioactive cesium in blood is a useful marker to estimate levels in muscle, even in lower radioactivity areas. The measurement of radioactive cesium in blood would contribute to food safety in livestock production.

ACKNOWLEDGMENTS This study was funded by the Emergency Budget for the Reconstruction of Northeastern Japan, MEXT, Japan; Discretionary Expense of the President of Tohoku University; the Research and Development Projects for Application in Promoting New Policy of

© 2014 Japanese Society of Animal Science

Agriculture, Forestry and Fishers, MAFF, Japan; and the Program for Promotion of Basic and Applied Research for Innovations in Bio-oriented Industry, BRAIN, Japan. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

REFERENCES Bowyer TW, Biegalski SR, Cooper M, Eslinger PW, Haas D, Hayes JC, et al. 2011. Elevated radioxenon detected remotely following the Fukushima nuclear accident. Journal of Environmental Radioactivity 102, 681–687. Calabrese E. 2011. Improving the scientific foundations for estimating health risks from the Fukushima incident. Proceedings of the National Academy of Sciences of the United States of America 108, 19447–19448. Fukuda T, Kino Y, Abe Y, Yamashiro H, Kuwahara Y, Nihei H, et al. 2013. Distribution of artificial radionuclides in abandoned cattle in the evacuation zone of the Fukushima Daiichi nuclear power plant. PLoS ONE 8, e54312. Isogai E, Kino Y, Abe Y, Yamashiro H, Shinoda H, Fukuda T, et al. 2013. Distribution of radioactive cesium in ostrich (Struthio camelus) after the Fukushima Daiichi nuclear power plant accident. Radiation Emergency Medicine 2, 68–71. Kinoshita N, Sueki K, Sasa K, Kitagawa J, Ikarashi S, Nishimura T, et al. 2011. Assessment of individual radionuclide distributions from the Fukushima nuclear accident covering central-east Japan. Proceedings of the National Academy of Sciences of the United States of America 108, 19526–19529. Okada K, Sato I, Deguchi Y, Morita S, Yasue T, Yayota M, et al. 2013. Distribution of radioactive cesium in edible parts of cattle. Animal Science Journal 84, 798–801. Sinclair LE, Seywerd HCJ, Fortin R, Carson JM, Saull PRB, Coyle MJ, et al. 2011. Aerial measurement of radioxenon concentration off the west coast of Vancouver Island following the Fukushima reactor accident. Journal of Environmental Radioactivity 102, 1018–1023. Yasunari TJ, Stohl A, Hayano RS, Burkhart JF, Eckhardt S, Yasunari T. 2011. Cesium-137 deposition and contamination of Japanese soils due to the Fukushima nuclear accident. Proceedings of the National Academy of Sciences of the United States of America 108, 19530–19534.

Animal Science Journal (2015) 86, 120–124

Cesium radioactivity in peripheral blood is linearly correlated to that in skeletal muscle: analyses of cattle within the evacuation zone of the Fukushima Daiichi Nuclear Power Plant.

The accident at the Fukushima Daiichi Nuclear Power Plant (FNPP) released a large amount of radioactive substances into the environment. Furthermore, ...
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