Concentrations of 137Cs radiocaesium in the organs and tissues of low-dose-exposed wild Japanese monkeys

Objectives Following the massive earthquake that struck eastern Japan on March 11, 2011, a large amount of radioactive material was released into the environment from the damaged reactor of the Fukushima Daiichi Nuclear Power Plant (FDNPP). After the FDNPP accident, radiocaesium was first detected in muscle samples from wild Japanese monkeys exposed to radioactive materials, and haematologic effects, changes in head size, and delayed body weight gain were also reported, but little is known about the distribution of 137Cs in the organs and tissues of wild Japanese monkeys. Results We detected the 137Cs in various organ and tissue samples of 10 wild Japanese monkeys inhabiting the forested areas of Fukushima City that were captured between July and August 2012. Among muscle, brain, heart, kidney, liver, lung, and spleen, muscle exhibited the highest and the brain the lowest 137Cs concentration. The concentration (mean ± SD) of 137Cs in muscle, brain, heart, kidney, liver, lung, and spleen was 77 ± 66, 26 ± 22, 41 ± 35, 49 ± 41, 41 ± 38, 53 ± 41, and 53 ± 51 Bq/kg, respectively. These results can help us understand the biological effects of long-term internal radiation exposure in non-human primates.

The Japanese monkey, one of the world's northernmost wild primates, is endemic to Japan and has a life span of more than 20 years [18]. Japanese monkeys usually form troops consisting of 50-100 individuals of one maternal lineage, and each troop occupies a home range spanning approximately 4-27 km 2 in snowy areas [19][20][21]. The monkeys feed primarily on plant leaves and fruits but also eat insects and other small animals [22]. We began a research project in 2011 to examine the health effects of long-term radiation exposure on wild Japanese monkeys inhabiting the forested areas surrounding Fukushima City, which is located 70 km from the FDNPP, and we anticipate that our findings will provide valuable data and insights. In addition, data from non-human primatesthe closest taxonomic relatives to humans-should make

BMC Research Notes
*Correspondence: toshinoriomi@gmail.com 1 Nippon Veterinary and Life Science University, 1-7-1 Kyonancho, Musashino City, Tokyo 180-8602, Japan Full list of author information is available at the end of the article a notable contribution to future research examining the health effects of radiation exposure in humans. In our previous study, we detected high levels of radiocaesium in muscle [10] and reported haematologic effects [11] as well as changes in head size and delayed body weight gain in wild Japanese monkeys [12] after the FDNPP disaster. In the present study, we determined the distribution of 137 Cs in various organs and tissues of wild Japanese monkeys inhabiting the forested areas surrounding Fukushima City that were captured between July and August 2012.

Materials and methods Animals
Samples of muscle, brain, heart, kidney, liver, lung, and spleen were collected from 10 Japanese monkeys (Macaca fuscata) captured between July and August 2012 from the forested areas around Fukushima City. These monkeys were used in a previously reported study to determine the concentrations of 134 Cs and 137 Cs in the muscles and characterize the changes in concentration over time as well as their relationship with soil contamination levels [12]. Organ and tissue samples were stored frozen at − 30 °C after 2012 until they were used in the present study. The age of each animal was estimated from the status of tooth eruption, as described by Iwamoto et al. [23], to divide the animals into the following age groups: juveniles (0-3 years), subadults (4-5 years), and adults (≥ 6 years).

Radioactivity measurements
Samples of skeletal muscle, brain, heart, kidney, liver, lung, and spleen were analysed using a germanium semiconductor spectrometer (Canberra, GC2020-7500SL-2002CSL, Meriden, CT) in Food Allergy Research Laboratories FARL (Maebashi, Gunma, Japan). Data were corrected to the background radiation dose of the measurement environment on an as-needed basis. 137 Cs was detected based on 661.6-keV gamma-ray energy. Collected samples were stored frozen at − 30 °C until radioactivity measurements. This method of measurement is the same as that used in our previous study [12]. The radiocaesium radioactivity level was adjusted to the value on the day of capture based on physical halflife. The limit of detection was 5 Bq/kg.

Statistical analysis
Differences in mean 137 Cs concentration between groups were analysed by one-way ANOVA using SPSS, ver. 19 (IBM Corp., Armonk, NY, USA). Table 1 and Fig. 1 show the concentrations of 137 Cs in skeletal muscle and various organ samples obtained from 10 Japanese monkeys captured between July and August 2012. The monkeys inhabited the forested areas surrounding Fukushima City, which is located 70 km from the FDNPP. The average 137 Cs concentration in the skeletal muscles and internal organs ranged from 26 to 77 Bq/kg. Among the skeletal muscle, brain, heart, kidney, liver, lung, and spleen, muscle exhibited the highest and the brain the lowest 137 Cs concentration. The mean (± SD) 137 Cs concentration in the muscle, brain, heart, kidney, liver, lung, and spleen was 77 ± 66, 26 ± 22, 41 ± 35, 49 ± 41, 41 ± 38, 53 ± 41, and 53 ± 51 Bq/kg, respectively. There were no significant differences in mean 137 Cs concentration between groups, as determined by one-way ANOVA. The ratio of the concentration of 137 Cs in each organ to that in muscle ( 137 Cs in each organ/ 137 Cs in muscle) was 0.34 ± 0.06, 0.53 ± 0.13, 0.64 ± 0.14, 0.52 ± 0.14, 0.70 ± 0.26, and 0.66 ± 0.15 for the brain, heart, kidney, liver, lung, and spleen, respectively. In this study, we found the highest concentration of radiocaesium in the skeletal muscle and lowest concentration in the brain of Japanese wild monkeys inhabiting forested areas surrounding Fukushima City. These findings agree with those of previous studies in cattle [8,9] and wild boar [17]. Similar results in wild Japanese monkeys were recently reported by Urushibara et al. [26]. However, the order of the relative 137 Cs concentration of the internal organs seemed to be slightly different between species. In particular, the lung and spleen showed high 137 Cs concentrations in Japanese monkeys.

Results and discussion
The muscle radiocaesium concentration in the monkeys correlated significantly with the level of soil contamination at each capture location [12]. The 137 Cs concentration in organs of two individuals, labelled FF-890 and FF-904, was higher than that in other individuals, which was related to the soil concentration of radiocaesium.
These data regarding the distribution of 137 Cs in the organs and tissues of Japanese monkeys captured in the areas surrounding Fukushima City will enhance our understanding of the biological effects of long-term internal radiation exposure. Continued monitoring of Japanese wild monkeys exposed to radioactive materials following the FDNPP accident would help in understanding the biological effects of long-term internal radiation exposure to the natural world.

Limitations
Continued monitoring of Japanese wild monkeys exposed to radioactive materials following the FDNPP accident would help in understanding the variation of the 137 Cs concentration among the organs of the body and its biological effects under long-term internal exposure.