To evaluate the biological effect of the Fukushima Daiichi nuclear disaster, relative differences in the growth of wild Japanese monkeys (Macaca fuscata) were measured before and after the disaster of 2011 in Fukushima City, which is approximately 70 km from the nuclear power plant, by performing external measurements on fetuses collected from 2008 to 2016. Comparing the relative growth of 31 fetuses conceived prior to the disaster and 31 fetuses conceived after the disaster in terms of body weight and head size (product of the occipital frontal diameter and biparietal diameter) to crown-rump length ratio revealed that body weight growth rate and proportional head size were significantly lower in fetuses conceived after the disaster. No significant difference was observed in nutritional indicators for the fetuses’ mothers. Accordingly, radiation exposure could be one factor contributed to the observed growth delay in this study.
The Fukushima Daiichi nuclear power plant (NPP) disaster that occurred in March 2011 exposed a large number of humans and wild animals to radioactive substances. Several studies of wild animals in Fukushima investigated health effects of the disaster, such as morphological abnormalities in gall-forming aphids (Tetraneura sorini, T. nigriabdominalis)1 and pale grass blue butterfly (Zizeeria maha)2, hematological abnormalities in carp (Cyprinus carpio)3, and chromosomal aberrations in wild mice (Apodemus argenteus, Mus musculus)4. However, there is no research investigating long-term exposure to radiation on mammals that typically have long life-span to date. This study is the first report to observe long-term biological effects of the pre- and post-NPP disaster on non-human primates in Fukushima.
We previously studied radioactive exposure and its effect on health of Japanese monkeys (Macaca fuscata) inhabiting Fukushima City, which is located approximately 70 km from the Fukushima Daiichi NPP5, 6. After the NPP disaster, the range of radiocesium soil concentrations in Fukushima City was 10,000–300,000 Bq/m2. Hayama et al.5 investigated chronological changes in muscle radiocesium concentrations in monkeys inhabiting Fukushima City from April 2011 to June 2012. The cesium concentration in monkeys’ muscle captured at locations with 100,000–300,000 Bq/m2 was 6000–25,000 Bq/kg in April 2011 and decreased over 3 months to approximately 1000 Bq/kg. However, the concentration increased again to 2000–3000 Bq/kg in some animals during and after December 2011, before returning to 1000 Bq/kg in April 2012, after which it remained constant.
Fukushima monkeys had significantly lower white and red blood cell counts, hemoglobin, and hematocrit, and the white blood cell count in immature monkeys showed a significant negative correlation with muscle cesium concentration6. These results suggested that the short-term exposure to some form of radioactive material resulted in hematological changes in Fukushima monkey
The effects associated with long-term low-dose radiation exposure on fetuses are among the many health concerns. Children born to atomic bomb survivors from Hiroshima and Nagasaki showed low birth weight, high rates of microcephaly7, and reduced intelligence due to abnormal brain development8. Experiments with pregnant mice or rats and radiation exposure had been reported to cause low birth weight9, 10, microcephaly11,12,13, or both14, 15. We identified one similar study on wild animals16, which reported that the brains of birds captured in the vicinity of the Chernobyl NPP weighted lower compared to those of birds captured elsewhere.
The population of Japanese monkeys in Fukushima City had been systematically managed since 2008 according to a management plan based on law and regulated by Fukushima Prefecture to reduce damage to agricultural crops. Our research group studied the reproductive and nutritional status of the Japanese monkey population by performing autopsies on individuals captured and euthanized by Fukushima City17. These Japanese monkeys were the first wild primate population exposed to radiation as result of nuclear disaster. However, there was no other study either in Chernobyl or Fukushima that followed fetal development over time or compared fetal development before and after long-term radiation exposure in the same wild animal populations.
The objectives of this study were to compare changes in the fetal development of Japanese monkeys in Fukushima City before and after the NPP disaster to determine evidence of developmental delay in Japanese monkey fetuses.
Radiocesium was detected in mothers’ muscle that had conceived after the NPP disaster (Table 1). Mean muscle radiocesium concentration was 1059 Bq/kg for mothers that mated in 2011 and gave birth in 2012 (n = 14), although the concentration decreased gradually in subsequent years up to 22 Bq/kg for mothers that gave birth in 2016 (n = 3). Because muscle tissue was not available prior to the NPP disaster, muscle radiocesium concentrations for individuals captured pre-disaster could not be measured. However, muscle radiocesium concentrations in wild Japanese monkeys captured in 2012 in Aomori Prefecture, which is also located in the Tōhoku region 400 km north from the NPP, were below the detection limit2, therefore, we assumed that the muscle radiocesium concentrations in the Japanese monkeys in Fukushima City prior to the disaster were also below the detection limit.
Similarly, although the air dose in the area of Fukushima City inhabited by the Japanese monkeys was 1.1 to 1.2 µSv/h in April, 2011, it has decreased, reaching 0.10 to 0.13 µSv/h in May, 2016 (Table 2). Based on these measurements, it is estimated that monkeys in this area received accumulated air doses of at least 12 mSv over the five years since the NPP disaster.
The descriptive statistics for Japanese monkey fetuses in Fukushima were shown in Table 3. The median body weight (g) and median body weight growth rate (g/mm) were significantly different between pre- and post-disaster groups (p = 0.032 and 0.0083, respectively). The mean biparietal diameter (mm), occipital frontal diameter (mm), head size (mm2), and proportional head size (mm) were significantly different between pre- and post-disaster groups (p = 0.046, 0.018, 0.014, and 0.0002, respectively). CRL was not significantly different between the two groups. Regression lines describing association of body weight and CRL in pre- and post-disaster groups were described in Fig. 1. Post-disaster regression line was significantly lower than pre-disaster regression line (p < 0.0001) (Table 4). Regression lines describing association of head size and CRL in pre- and post-disaster groups were described in Fig. 2. Post-disaster regression line was significantly lower than pre-disaster regression line (p < 0.0001) (Table 5).
The body fat index for the mothers of these fetuses was not significantly different before and after the NPP disaster (Z = 1.213; P = 0.219).
Body weight and head size relative to the CRL were lower in fetuses conceived after the NPP disaster compared with fetuses conceived prior to the NPP disaster. Japanese monkeys in Fukushima City first conceive in fall when they were five years old and gave birth in spring when they were six years old17. Thus, we assumed that all the mothers we examined that conceived babies after the NPP disaster were continuously exposed to radiation from at the time of the disaster in 2011.
Growth retardation of the fetuses could be caused by the deterioration of the mothers’ nutritional status. However, we did not observe any difference in the body fat index of mothers pre- and post-NPP disaster. Therefore, the growth retardation of the fetuses was unlikely to be associated with to the mothers’ nutritional status. Other factors such as climate changes or food nutrient components might have affected the growth of fetuses. The limitations of this study were that we were not able to obtain samples to look at histological change that might have contributed to the cause of delayed fatal growth and the sample size were relatively small because of the nature of the sampling collection. It might have been ideal to compare monkeys from the evacuation order area to monkeys from the non-contaminated area of Fukushima; however, there was no other area such besides the one in this study that performed systematic large-scale capturing aimed at seizing hundreds of monkeys. In addition, there had been access limitations beyond the evacuation order area. For these reasons, it is impossible to replicate an equivalent study elsewhere at this time.
In experiments using mice and rats, radiation exposure has been reported to cause reduced fetal weight, microcephaly, and reduced brain mass9,10,11,12,13,14,15. However, most of these experiments involved exposing the mother to a single radiation dose at a fetal age of 10 days or later when the brain undergoes development. Such exposure may be qualitatively different from the low-dose, long-term exposure following an NPP disaster. The radiation doses in these experiments varied substantially. Hande et al.9 exposed mice to 9 mGy of 70 kilo-Volt peak X-rays at fetal ages of 3.5, 6.5, and 11.5 days, and found that birth weight was reduced relative to the control mice in all cases. Uma Devi et al.15 exposed mice to 0.25 Gy at a fetal age of 11.5 days and observed reduced head size at birth. In addition, they observed negative correlation between radiation dose and head size in fetuses exposed to 0.05 to 0.15 Gy.
The number of low birthweight children born to residents of some highly contaminated areas of Belarus increased between 1982 and 1990, after the Chernobyl NPP disaster18. Hujuel et al.19 conducted a longitudinal survey of women exposed to radiation through dental treatment who subsequently gave birth. They reported that women exposed to 0.4 mGy or more had increased risk (odds ratio 2.27) of giving birth to a child weighing 2500 g or less. Goldberg et al.20 elucidated the relationship between the level of radiation exposure as a result of medical exams prior to conception and birthweight, and found that birthweight decreased by 37.6 g for every cGy of exposure. Such medical exposure is believed to affect the mother’s gonads and endocrine glands rather than the fetus itself. There is still uncertainly to determine whether the retarded growth we observed was a direct effect of the radiation exposure.
Otake and Schull8 conducted a temporal variation study of mothers exposed to radiation by the atomic bombs in Hiroshima and Nagasaki. They did not observe any effect in newborns that had been exposed between fetal ages of 0 to 8 weeks, and the highest rates of microcephaly and other brain damage occurred in newborns exposed between fetal ages of 8 to 15 weeks. Given that the latter period was when the human brain undergoes rapid development, damage due to radiation exposure during this period might cause severe effect on fetuses.
The previous research suggested that the low birthweight and small head sizes observed in fetuses conceived after the NPP disaster were result of radiation exposure. However, we were not able to quantify the external and internal radiation dose in individual wild animals. Although radiocesium was detected in the muscles of all individuals captured after the NPP disaster, the cumulative exposure was unclear since the biological half-life of radiocesium in monkeys was approximately 3 weeks5. Furthermore, because of the small sample size, it was difficult to determine the causal relationship of exposure dosage and the effect on fetuses.
Although we showed that fetal proportional head size reduced after the NPP disaster, it was not possible to identify anatomically which part of the brain was developmentally retarded. Hossain et al.12 studied the brains of 6- to 12-month-old mice that were exposed to cobalt 60 at a fetal age of 14 days. Brain weight decreased at exposure rates of 0.5 to 1.5 Gy and the number of neurons in the hypothalamus in the CA3 region decreased significantly. We started to perform histological examination brain of fetuses and juvenile monkeys conceived after the NPP disaster to identify the regions of the brain that were developmentally retarded and the effect of retarded growth on post-natal development for further study.
1, Akimoto, S. I. Morphological abnormalities in gall-forming aphids in a radiation-contaminated area near Fukushima Daiichi: selective impact of fallout? Ecology and Evolution. 4, 355–369 (2014).
2, Hiyama, A. et al. The biological impacts of the Fukushima nuclear accident on the pale grass blue butterfly. Scientific Reports. 2, 570, doi:10.1038/srep00570 (2012).
3, Suzuki, Y. Influences of radiation on carp from farm ponds in Fukushima. Journal of Radiation Research. 56, i19–23, doi:10.1093/jrr/rrv076 (2015).
4, Kubota, Y. et al. Chromosomal aberrations in wild mice captured in areas differentially contaminated by the Fukushima Dai-Ichi nuclear power plant accident. Environ. Sci. Technol. 49, 10074–10083 (2015).
6, Ochiai, K. et al. Low blood cell counts in wild Japanese monkeys after the Fukushima Daiichi nuclear disaster. Scientific Reports. 4, 5793, doi:10.1038/srep05793 (2014).
21, Goldberg, M. S., Mayo, N. E., Levy, A. R., Scott, S. C. & Poitras, B. Adverse reproductive outcomes among women exposed to low levels of ionizing radiation from diagnostic radiography for adolescent idiopathic scoliosis. Epidemiology. 9, 271–278 (1998).
22, Primate Research Institute, Kyoto University Guideline for fieled reserch for non–human primates. http://www.pri.kyoto-u.ac.jp/research/guide-e2008.html Accessed 28 January, 2017.
23, Japanese Ministry of Environment. 2012 Japanese Red List. http://www.env.go.jp/en/nature/biodiv/reddata.html Accessed 28 January, 2017.
26, Fukushima Prefecture website. Available: Results of air dose rate monitoring survey by Fukushima Prefecture. https://www.pref.fukushima.lg.jp/sec/16025d/monitaring-mesh.html Accessed 20 January, 2017.