Radiocesium concentrations in mushrooms collected in Kawauchi Village five to eight years after the Fukushima Daiichi Nuclear Power Plant accident.

Following the Fukushima Daiichi Nuclear Power Plant accident in March 2011, radionuclides such as iodine-131, cesium-134 and cesium-137 were released into environment. In this study, we collected wild mushrooms from the Kawauchi Village of Fukushima Prefecture, located less than 30 km southwest of the Fukushima nuclear power plant, to evaluate their radiocesium (134Cs+137Cs) concentrations and the risk of internal radiation exposure in local residents. 342 mushroom samples were collected from 2016 to 2019. All samples were analysed for radiocesium content by a high-purity germanium detector. Among 342 mushroom samples, 260 mushroom samples (76%) were detected the radiocesium exceeding the regulatory limit of radiocesium (100 Bq/kg for general foods in Japan). The median of committed effective dose from ingestion of wild mushrooms was in the range of 0.015-0.053 mSv in 2016, 0.0025-0.0087 mSv in 2017, 0.029-0.110 mSv in 2018 and 0.011-0.036 mSv in 2019 based on the assumption that Japanese citizens consumed wild mushrooms for 1 year. Thus, our study showed that although radiocesium is still detected in mushrooms collected in Kawauchi village even after 5 to 9 years later, the committed effective dose due to consuming mushrooms was lower than 1 mSv per year. Long-term comprehensive follow-up should monitor radiocesium concentrations in wild mushrooms to support the recovery of the community after the nuclear disaster.

Introduction

After the Fukushima Daiichi Nuclear Power Plant (FDNPP) accident occurred in March 2011, huge amounts of radionuclides, such as iodine-131 (131I), cesium-134 (134Cs) and cesium-137 (137Cs), were released into the environment. The United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR) estimated that the total releases of 131I (8 days of half-life), 134Cs (2 years of half-life) and 137Cs (30 years of half-life) were 120.0, 9.0 and 8.8 petabecquerels (PBq), respectively [1].

After the Chernobyl Nuclear Power Plant (CNPP) accident, it has been confirmed that radiocesium tends to concentrate in wild mushrooms [2-9]. Travnikova, et al. found that the average 137Cs activity in Boletus luteus, B. chanteral, and B. russula wild mushroom samples collected in Veprin village of Russia from 1994 to 1998 were 14,500, 2,550 and 8,980 Bq/kg, respectively [10]. At 30 years after the accident, the median of radiocesium concentrations of Boletus edulis, Leccinum aurantiacum and L. scabrum mushroom samples collected 120 km away from the CNPP were 580, 250 and 290 Bq/kg, respectively [9]. Thus, human consumption of wild mushrooms has contributed greatly to the internal radiocesium body burden around the CNPP [11, 12].

Kawauchi village is located within a 30 km radius from southwest of the FDNPP, and it was the first local authority to have residents return following evacuations after the accident [13]. Currently, almost 80% of residents have returned to the village and restarted their lives. It is customary for residents of some areas of Fukushima Prefecture to eat home-grown plants, such as vegetables, edible wild plants, and mushrooms [14]. Residents living in mountainous areas are more likely to eat home-grown foods than are urban residents. In particular, a common pastime for older adults in the area is to forage for edible wild plants in the mountains or to hunt for wild animals [14]. Before the accident, the village was also famous for collecting wild mushrooms, including Sarcodon aspratus and Tricholoma matsutake. Because collection and consumption of wild mushrooms is part of the food culture of this village, residents want to know radiocesium levels in the wild mushrooms [15, 16]. National and local governments implemented monitoring of radioactive concentrations over a wide area of Japan in fiscal year (FY) 2016, and 23 out of 2084 wild mushrooms (not mushrooms purchased at the market) tested were found to contain radiocesium that exceeded the standard values [17]. Since 2013, we have evaluated the activity concentration of artificial radiocesium in wild mushrooms collected in Kawauchi village [15, 18]. To support the recovery efforts of the community after nuclear disaster and conduct continuous risk communication with residents, it is important to monitor the radiocesium concentrations in mushrooms not only for regions of Japan, but also in limited areas, such as municipal units, and to minimise internal radiation exposure of residents due to consumption of contaminated foods. The aims of this study were to evaluate the follow-up radiocesium contamination in wild mushrooms collected from 2016 to 2019, which is 5 to 8 years after the accident.

Materials & methods

Sampling information

The sampling sites for mushroom collection were in Kawauchi village (the village government office, 37° 20′ 15.5″ N, 140° 48′ 33.5″ E), 22 km southwest of the FDNPP. After we obtained approval from the Kawauchi Village Office, 342 samples were collected in Autumn from 2016 to 2019. Only approximated locations were recorded because of mushroom points usually kept by villagers as secret for future collection. All samples were classified as saprophytic or symbiotic. Samples of fresh mushroom (14–108 g fresh weight (FW)) were washed and minced and then enclosed in 100 mL plastic containers made of polypropylene for the radionuclide measurements.

γ–spectrometric measurements

All samples were measured fresh and analyzed for 3,600 s (real time) with a high-purity germanium detector (ORTEC, GMX30–70, ORTEC INTERNATIONAL Inc., Oak Ridge, TN, USA) coupled with a multi-channel analyzer (MCA7600, SEIKO EG&G Co., Ltd., Chiba, Japan). Decay corrections were made based on the sampling date, and detector efficiency calibration was performed for different measurement geometries using mixed-activity standard volume sources (Japan Radioisotope Association, Tokyo, Japan). The relative efficiency was 31%, and energy resolution of the spectrometer was 1.85 keV for 60Co. The correction factor of the sum-peak effect of 134Cs and 137Cs were almost 1, respectively. Activity concentrations of radiocesium were automatically adjusted based on the date of collection, and the data were defined as the activity concentrations at the collection date. The detection limit of about 11 Bq/kg for 134Cs and 9 Bq/kg for 137Cs, the counting errors were ± 6 Bq/kg for 134Cs (median) and ± 13 Bq/kg for 137Cs (median), respectively. The radioactivity measurements were performed at Nagasaki University (Nagasaki, Japan). The limit for radiocesium is 100 Bq/kg for general foods. Typically, after the Fukushima Daiichi Nuclear accident, food samples without drying were used for measuring radioactivity.

Committed effective dose

Internal effective doses from wild mushroom samples were estimated using equation: where C is the activity concentration of detected artificial radiocesium (Bq/kg FW). Here, D represents the age-dependent dose conversion coefficients presented in International Commission on Radiological Protection (ICRP), Publication 119 [19] for 134Cs (age 1 years, 1.6E–08 Sv/Bq; age 5 years, 1.3E–08 Sv/Bq; 10 years 1.4E-08 Sv/Bq and age 15–70 years, 1.9E–08 Sv/Bq) and 137Cs: (age 1 years, 1.2E–08 Sv/Bq; age 5 years, 9.6E-09, age 10 years, 1.0E–08 Sv/Bq; and age 15–70 years, 1.3E–08 Sv/Bq). The value for e was determined from the mean value of daily intake for age and sex which was obtained from the Ministry of Health, Labour, and Welfare, Japan in 2016: males, 2.8–7.3 kg/year; females, 2.5–7.3 kg/year) [20].

Statistical analysis

Radiocesium concentrations were presented as median, minimum and maximum. Normality was checked by Kolmogorov–Smirnov test. The Jonckheere–Terpstra test was performed to compare radiocesium concentrations in Sarcodon aspratus collected during 2016–2019. The Mann–Whitney test was conducted to determine variability between symbiotic and saprophytic species. Data were statistically analyzed using SPSS statistics 25.0 (IBM Corp., Armonk, NY, USA). A p-value less than 0.05 was considered statistically significant. The raw measurement data are provided in S1 File.

Results

Fig 1 shows the distribution of radiocesium concentrations in wild mushrooms broken down by year and according to concentration distribution. The numbers of wild mushroom samples that exceeded 100 Bq/kg of radiocesium by year were 144 of 192 (75%) in 2016, 10 of 21 (48%) in 2017, 64 of 76 (84%) in 2018 and 42 of 53 (79%) in 2019. Activity concentrations of radiocesium in representative species are shown in Table 1 and activity concentration results for all other species are shown in Supplementary file 2. The median concentrations of 134Cs were 75 Bq/kg in 2016, n.d. (not detected) in 2017, 92 Bq/kg in 2018 and 25 Bq/kg in 2019, and those of 137Cs were 454 Bq/kg in 2016, 80 Bq/kg in 2017, 1,006 Bq/kg in 2018 and 339 Bq/kg in 2019, respectively. In addition, the average 134Cs/137Cs ratios were 0.171 in 2016, 0.126 in 2017, 0.091 in 2018 and 0.068 in 2019. Radiocesium concentrations were significantly higher in symbiotic species, such as Sarcodon aspratus and Suillus bovinus, than saprophytic species, such as Albatrellus confluens and Lyophyllum fumosum (p<0.05).

Fig 1

Distribution of concentrations of radiocesium (134Cs+137Cs) in wild mushroom samples collected in Kawauchi village (2016–2019).

n.d.: could not be determined.

Table 1

Activity concentrations of radiocesium (Bq/kg) in mushroom samples (5 species) collected in Kawauchi village from 2016 to 2019.

Species	Sample year	n	134Cs (Bq/kg)	137Cs (Bq/kg)
			Median (Min-Max) *	Median (Min-Max)
Sarcodon aspratus	2016	73	136 (12–1,079)	759 (86–6,350)
“Kotake” in Japanese	2017	8	177 (73–711)	1,059 (562–1,838)
(symbiotic)	2018	40	138 (n.d.–1,572)	1,524 (60–17,155)
	2019	21	92 (24–1,075)	1,290 (339–15,867)
Suillus bovinus	2016	28	48 (n.d.–289)	307 (21–1,774)
“Amitake” in Japanese	2017	2	15 (n.d.–127)	74 (21–127)
(symbiotic)	2018	3	94 (26–219)	962 (326–2,457)
	2019	3	27 (n.d.–128)	336 (53–1,837)
Albatrellus confluens	2016	20	n.d. (n.d.–48)	24 (n.d.–258)
“Ningyotake” in Japanese	2017	5	n.d.	24 (n.d.–80)
(saprophytic)	2018	6	n.d.	50 (44–85)
	2019	5	n.d.	16 (12–55)
Lyophyllum fumosum	2016	5	n.d. (n.d.–23)	39 (27–119)
“Shakashimeji” in Japanese	2017	2	n.d.	44 (34–53)
(saprophytic)	2018	1	n.d.	60
	2019	4	n.d.	104 (45–158)
Armillaria tabescens	2016	3	n.d.	n.d.
“Naratake” in Japanese	2017	1	n.d.	23
(saprophytic)	2018	1	n.d.	n.d.
	2019	1	n.d.	16

*Min: minimum; Max: maximum; n.d.: not detected.

We also compared the activity concentrations of radiocesium in Sarcodon aspratus samples collected each year (Fig 2). No significant differences were found in 134Cs activity concentrations (p>0.05). While the activity concentration of 137Cs in 2018 was significantly higher than that in 2016 (p = 0.004), no significant differences were observed between other years.

Fig 2

Boxplots of radiocesium concentrations (a) 134Cs and (b) 137Cs in Sarcodon aspratus collected from 2016 to 2019.

Significance determined by the Jonckheere–Terpstra test.

Internal committed effective dose for residents were shown in Table 2. The median of committed effective dose from ingestion of wild mushrooms was in the range of 0.015–0.053 mSv in 2016, 0.0025–0.0087 mSv in 2017, 0.029–0.110 mSv in 2018 and 0.011–0.036 mSv in 2019.

Table 2

Internal committed effective dose calculated with the assumption that residents consume wild mushrooms collected in Kawauchi village for 1 year.

Age (y)	Intake (kg/y)*	Median (minimum—maximum) committed effective dose (mSv/year)
		Female				Male
		2016	2017	2018	2019	2016	2017	2018	2019
1–6	F: 2.5; M: 2.8	0.015 (0.00055–0.31)	0.0025 (0.00057–0.065)	0.029 (0.00057–0.58)	0.011 (0.00061–0.52	0.016 (0.00062–0.35)	0.0027 (0.00063–0.073)	0.033 (0.00063–0.65)	0.012 (0.00068–0.58)
7–14	F: 4.3; M: 4.7	0.026 (0.001–0.59)	0.0039 (0.001–0.12)	0.052 (0.001–1.1)	0.019 (0.0011–0.97)	0.028 (0.0011–0.65)	0.0043 (0.0011–0.13)	0.056 (0.001–1.2)	0.021 (0.0012–1.1)
15–19	F: 4.2; M: 5.4	0.030 (0.0013–0.58)	0.005 (0.0013–0.12)	0.063 (0.0013–1.06)	0.020 (0.0014–0.95)	0.039 (0.0017–0.75)	0.0064 (0.0017–0.15)	0.081 (0.0013–1.3)	0.026 (0.0018–1.2)
20–29	F: 5.1; M: 5.1	0.037 (0.0016–0.7)	0.0061(0.0016–0.14)	0.076 (0.0013–1.3)	0.025 (0.0018–1.2)	0.037 (0.0016–0.70)	0.0061 (0.0016–0.14)	0.076 (0.0013–1.3)	0.025 (0.0018–1.2)
30–39	F: 5.2; M: 4.9	0.038 (0.0016–0.72)	0.0062 (0.0017–0.15)	0.078 (0.0013–1.3)	0.025 (0.0018–1.2)	0.036 (0.0015–0.68)	0.0058 (0.0016–0.14)	0.073 (0.0012–1.2)	0.024 (0.0017–1.1)
40–49	F: 5.0; M: 5.0	0.036 (0.0016–0.69)	0.006 (0.0016–0.14)	0.075 (0.0012–1.3)	0.024 (0.0017–1.1)	0.036 (0.0016–0.69)	0.006 (0.0016–0.14)	0.075 (0.0012–1.3)	0.024 (0.0017–1.1)
50–59	F: 6.5; M: 6.7	0.047 (0.002–0.9)	0.0078 (0.0021–0.18)	0.097 (0.0016–1.6)	0.032 (0.0022–1.5)	0.049 (0.0021–0.92)	0.008 (0.0021–0.19)	0.1 (0.0017–1.7)	0.033 (0.0023–1.5)
60–69	F: 7.3; M: 7.3	0.053 (0.0023–1.0)	0.0087 (0.0023–0.21)	0.11 (0.0018–1.8)	0.036 (0.0025–1.7)	0.053 (0.0023–1.0)	0.0087 (0.0023–0.21)	0.11 (0.0023–1.8)	0.036 (0.0025–1.7)
>70	F: 6.6; M: 6.6	0.048 (0.002–0.91)	0.0079 (0.0021–0.19)	0.099 (0.0016–1.7)	0.032 (0.0023–1.5)	0.048 (0.0021–0.91)	0.0079 (0.0021–0.19)	0.099 (0.0021–1.7)	0.032 (0.0023–1.5)

* The mean value of daily intake for age and sex from the MHLW. F: Female; M: Male.

Discussion

After the FDNPP accident, the Fukushima Prefecture governmental office reported monitoring results for radiocesium concentration for agricultural, forestry and fishery products from Fukushima Prefecture. The number of cases exceeding the standard value (100 Bq/kg for general foods) was 419 cases (1.5% of total) in FY2013, 113 cases (0.4% of total) in FY2014, 18 cases (0.08% of total) in FY2015, 6 cases (0.03% of total) in FY2016 and 10 cases (0.05% of total) in FY2017 [21]. We also evaluated radiocesium concentrations in local foods collected in Kawauchi Village. The number of samples exceeding the regulatory radiocesium limit was five out of 4,080 vegetables (0.1%), 652 of 1,986 edible wild plants and fungi (32.8%), and eight of 647 fruits (1.2%). Overall, the concentration of radionuclides in food has decreased with the passage of time [22]. However, radiocesium concentrations in edible wild plants and mushrooms were comparatively higher, while radiocesium was at or near the detection limit for vegetables and fruits.

After the FDNPP accident, several studies have been reported concentrations of radiocesium in wild mushrooms [23-25]. In Namie town, Fukushima Prefecture, the median concentrations of radiocesium in shiitake mushroom in each year from fiscal 2012 to fiscal 2015 were 4,070, 973, 2,269 and 742 Bq/kg [25]. Previously, we evaluated radiocesium concentration in wild mushroom samples collected in Kawauchi village and found that radiocesium exceeding 100 Bq/kg was detected in 125 of 154 samples (81%) in 2013, and in 123 of 159 samples (77%) in 2015 [15, 18]. In the present study, the percentage of radiocesium in samples exceeding 100 Bq/kg was 75%, 45%, 84% and 79% from 2016 to 2019, respectively. The median concentration of radiocesium in all mushroom species was 526 Bq/kg in 2016, 88 Bq/kg in 2017, 1,106 Bq/kg in 2018 and 362 Bq/kg in 2019. These results suggest that the proportion of mushroom samples with radiocesium concentrations above 100 Bq/kg did not dramatically change in Fukushima over 8 years. Radiocesium concentrations in mushrooms can be affected by many factors of forest, such as species, mycelium habitat and depth, minerals in the soil and contamination level of soil [6, 26–28]. Long-term comprehensive follow-up should be conducted because the existing data is insufficient to characterize risk.

Sarcodon aspratus has long been widely collected and consumed in Fukushima. In our previous study, we reported that the median concentration of 134Cs decreased from 291 Bq/kg in 2013 to 150 Bq/kg in 2015, whereas that of 137Cs did not decrease (668 Bq/kg in 2013 and 620 Bq/kg in 2015) [15, 18]. In the present study, 134Cs concentrations of Sarcodon aspratus did not significantly decrease from 2016 to 2019. Furthermore, while the activity concentration of 137Cs in 2018 was significantly higher than that in 2016, no significant differences were observed between other years. The radioactivity of 134Cs in mushrooms collected in Kawauchi village have reached to relatively low levels and hard to find statistically significant differences from 2016 to 2019, these inconsistencies in changes in 137Cs concentrations can be considered to be largely due to the relatively long effective half-life of 137Cs. In the study after the Chernobyl accident, the radiocesium concentrations in mushrooms also showed fluctuation [29, 30]. In Poland, no clear decreasing trend in C. cibarius was observed from 1998 to 2013 [29]. In Sweden, the overall concentrations of 137Cs in mushrooms did not decrease from 1986 to 2007 and increased in Cantharellus spp. [30]. In addition, previous studies have made significant contributions to addressing the reasons for the lack of activity reductions over time [28, 31]. Hashimoto S, et al. [31] investigated whether the 137Cs concentration of wild mushrooms would be spatially biased or influenced by the 137Cs or exchangeable potassium concentrations in soils because the concentration fluctuates among the same species growing within a given area.

We estimated the committed effective dose based on the average annual intake of mushrooms by Japanese citizens. We showed that the estimated committed effective dose from the only ingestion of wild mushrooms collected in 2016 was 0.015–0.053 mSv, 0.0025–0.0087 mSv in 2017, 0.029–0.110 mSv in 2018 and 0.011–0.036 mSv in 2019 (female and male, median). Previously, we reported that the calculated effective dose ranged from 0.1–1.6 mSv in 2013 [15] and from <0.001 to 0.6 mSv in 2015 [18]. These findings suggest that internal radiation exposure due to the consumption of wild mushrooms remained lower than 1 mSv per year in Kawauchi village. The current reference level (≤1 mSv/year), which was established by the national government, is set at an adequate level such that effects of continued consumption of radioactive material found in agricultural products remain small and safe. The value 1 mSv/year is in accordance with the guidelines set by the Codex Alimentarius Commission, which sets international standards for food [32]. On the basis of food intake according to age group and the effects of radioactive materials on health, the values are set such that the annual additional radiation dose does not exceed approximately 0.9 mSv, even if 50% of foods contain that level of radioactive materials and are ingested continuously. The “limit of 100 Bq kg” for general foods was determined by choosing the most rigorous limits among the calculated values [32]. Our results suggest that the proportion of mushroom samples with radiocesium concentrations above 100 Bq/kg did not dramatically change, but the committed effective dose by consuming mushrooms is estimated to be relatively limited. Experts need to provide careful explanation of the concepts of radiation protection such as the concept of standard values for food.

After the Fukushima accident, we have been cooperating with Kawauchi stakeholders and dialogue with them regarding radiological risk [33]. Our samples were collected in autumn and measured in winter. During regular group meeting in March, we shared results of radioactivity of mushrooms and the committed effective dose by using understandable terms and figures. For the recovery of the community after the nuclear disaster, we suggested that implementing the health promotion of the residents by using the objective data obtained from the local area can contribute to support the decision making of the residents.

Several limitations of this study should be explored. First, sample size was small in 2017. Secondly, although all samples were collected in Kawauchi village, sampling sites were not recorded precisely. Additionally, transfer factors among mushrooms, host plant, soil, organic matter and animals could not be estimated. Uncertainties arise because the committed effective dose from dietary intake of mushrooms does not capture day-to-day variation in individuals. Further, we did not evaluate the potential loss of radiocesium upon cooking in mushrooms. Finally, there is variation in individual consumption of wild mushrooms in Fukushima, and the population has been repeatedly advised not to eat them. It is likely that these are large overestimates for the majority of the population, and underestimates for a small number of individuals who consume large quantities of the most contaminated varieties.

We suggest that providing the basic radioisotope monitoring for wild mushrooms or other foods for human consumption is important for addressing residents’ anxiety and for the reduction of future risks of internal exposure.

Conclusion

We showed that radiocesium in mushrooms collected in Kawauchi village is still detected even 5 to 9 years after the accident and the proportion of mushroom samples with radiocesium concentrations above 100 Bq/kg did not dramatically change, but the median committed effective dose by consuming mushrooms was found to be lower than 1 mSv per year. We suggest that providing basic radioisotope monitoring inspection for wild mushrooms and other foods for human consumption is important for addressing residents’ anxiety and for the reduction of future risks of internal exposure. Long-term comprehensive follow-up should be conducted to clarify the radiocesium concentrations in wild mushrooms in order to support the recovery of the community after the nuclear disaster.

The original dataset of this study.

(XLSX)

Click here for additional data file.

Radiocesium concentration in mushrooms collected in in Kawauchi village from 2016 to 2019.

(DOCX)

Click here for additional data file.

23 Jul 2020

PONE-D-20-19962

Radiocesium concentrations in mushrooms collected in Kawauchi Village five to eight years after the Fukushima Daiichi nuclear power plant accident

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Manuscript Title: Radiocesium concentrations in mushrooms collected in Kawauchi Village five to eight years after the Fukushima Daiichi nuclear power plant accident

Overall comments:

This manuscript describes interesting new research that is an important part of the continuing understanding of recovery from the Fukushima meltdowns. This reviewer strongly recommends publication but with minor revisions below.

This work would be improved by adding data for pre-meltdown activities of these same species, as well as control samples of mushrooms from areas not affected by this contamination event. The lack of control and background samples is a notable ommission. Likewise, there is no comparison to other locally-grown or regionally-available foods or edible plants, or even staples such as rice and grains. This deficiency applies equally to activity and committed effective dose data.

Specific comments

L21-28: Quantitative data supports that 76% of samples exceed the allowable limit of 100 Bq/kg. By comparison the committed effective dose is described as relatively low but is not compared to a regulatory limit nor is there a comparison to other parts of the diet of returned residents of Kawauchi Village.

Do wild mushrooms have more or less activity compared to other local foods?

If all foods in the villagers’ diet had the same activity as these mushrooms, is that acceptable based on human health considerations?

Which conclusion is dominant – should mushrooms be avoided because they exceed 100 Bq/kg or can they be eaten because effective committed doses are relatively low?

L17 and also L44: Authors give distances from Fukushima, but should give direction as well. Replace “X km from nuclear plant” with “X km south of nuclear plant” as appropriate.

L41: Replace “concentration” with “activity” wherever appropriate in the manuscript. Remove unnecessary “of” from this line as well.

L61: The introduction ends abruptly, without giving much context or discussion of prior work with this study. Has this author or any other researcher also studied edible mushrooms in the region? How common is wild mushroom consumption?

L72: Samples were analyzed by wet weight, without drying. Is the general food standard of 100 Bq/kg also a wet weight standard or a dry weight standard? The authors should clarify this in the text.

L158: What is the purpose of the proposed long-term follow-up? Is it because the existing data is insufficient to characterize risk, or is it because there is not yet a documented reduction in percentage of mushrooms exceeding the general food standard?

L162 to 173: The authors imply that the only removal mechanism for Cs-137 and Cs-134 from village soils is radioactive decay. The authors should explicitly state whether this is the only removal mechanism, and that erosion, remediation, infiltration to lower soil depths and so on do (or do not) take place. The authors correctly note that other researchers have done significant work to address these questions, and readers would be interested if other researchers investigated the reasons for the lack of activity reductions over time.

L176: The committed effective dose from mushrooms is important data, but it needs context. What is the committed effective dose (on average) from the whole diet? What would be the committed effective dose if all foods eaten were at 100 Bq/kg? Are these doses higher or lower than for other foods? How do mushrooms compare to the activity of other local foods?

L180: The overall quality of the written text is excellent, but errors of tense (‘has’ used instead of the correct ‘have’) mar the otherwise logical and readable nature of this manuscript.

L181: Including the authors’ communications with stakeholders is something that is not done nearly enough by other researchers. This is a commendable effort by the authors and I applaud them for it.

L198: Again, the use of nonquantitative terms such as ‘relatively-limited’ should be buttressed with quantitative data. The previous comments for L21-28 should also be reflected in the conclusions.

Reviewer #2: This is a useful paper which updates findings from a long-term study reported in previous papers, such as Nakashima et al, 2015, Orita et al 2017, Tsuchiya et al 2017. The data is clearly presented overall. Some pertinent background information that would give useful context, and was generally included in the earlier papers, is absent. Specifically, it would be helpful to note relevant aspects of food testing policy in Fukushima overall, such as the fact that wild gathered food items such as these mushrooms are rarely included in official testing. The range of Cs activities reported by official testing for agriculturally grown and commercially distributed mushrooms could be given for context. Also, it is important to note that although the Fukushima public has been repeatedly advised since 2011 to avoid eating wild mushrooms because of contamination risk, many people, particularly elderly, do in fact continue to eat them. Helping to clarify the risks to such people is, I believe, the underlying motivation for this ongoing study in Kawauchi.

Comments regarding specific sections are listed below by text line number:

50) “Before the accident, the village was famous for collecting wild mushrooms, including Sarcodon aspratus and Tricholoma matsutake.”

Comment: In Tsuchiya et al, 2017, you provided common Japanese names for the mushrooms in addition to Latin names. This is helpful for non-botanists as well as researchers in the social sciences and others who may find interest in this study.

+++++

93) “The value for e was determined from the mean value of daily intake for age and sex which was obtained from the Ministry of Health, Labour, and Welfare, Japan in 2016: males, 2.8–7.3 kg/year; females, 2.5–7.3 kg/year) [18].”

Comment: There are a few issues that should be clarified regarding these estimates and how they are derived:

— From the citation [18] it appears that the reference document is: The National Health and Nutrition Survey in Japan, 2016 (direct link https://www.mhlw.go.jp/bunya/kenkou/eiyou/dl/h28-houkoku.pdf). If this is the case, then it should be cited directly, and relevant pages should be cited as well.

— It is not clear that all of the mushroom varieties examined in this study are included in this MHLW document. Further, it is not clear that “wild” versus “commercially distributed” mushrooms are categorized separately by MHLW.

— MHLW gives fairly detailed breakdown of consumption quantity estimates by age. It is not clear how this is factored into the value of e obtained, in conjunction with the age-dependent dose conversion coefficients. Is only the mean of all age groups used?

— The larger question is whether or not MHLW’s estimates for typical mushroom consumption are accurate in the case of wild mushrooms gathered and eaten in Fukushima.

++++

119) "Fig 1. Distribution of concentrations of radiocesium(134Cs+137Cs) in wild mushroom samples collected in Kawauchi village (2016–2019)."

Comment: The activities are separated into only four bins: n.d; n.d.-100Bq; 100-1000Bq; >1000Bq. This appears consistent with the earlier papers, although Nakashima et al, 2015, uses five bins. It would be helpful to include more granular histogram for each year, with at least ten bins each, so the actual activity distributions could be better grasped.

++++

141) "Table 2. Internal committed effective dose calculated with the assumption that residents consume wild mushrooms collected in Kawauchi village for 1 year."

Comment: Related to the above comment. It would be helpful to add the estimated quantity consumed for each age group to the table.

++++

152) "The median concentration of radiocesium in all mushroom species was 526 Bq/kg in 2016, 88 Bq/kg in 2017, 1,106 Bq/kg in 2018 and 362 Bq/kg in 2019."

Comment: These are very wide fluctuations. You touch on some of the reasons for this later. Perhaps one finding is that the sampling methodology reported in this study is unable to provide representative measurements of the overall change in radiocesium levels in wild mushrooms in general in Fukushima. However, it can provide a good indication of typical intake of radiocesium from consumption of gathered wild mushrooms.

++++

154) "These results suggest that the proportion of mushroom samples with radiocesium concentrations above 100 Bq/kg did not dramatically change in Fukushima over 8 years."

Comment: This is a key finding, and consistent with the literature regarding Chernobyl.

++++

75) "We showed that the estimated committed effective dose from the ingestion of wild mushrooms collected in 2016 was 0.017 – 0.054 mSv, 0.0028 – 0.0087 mSv in 2017, 0.034 – 0.110 mSv in 2018 and 0.011 – 0.036 mSv in 2019. Previously, we reported that the calculated effective dose ranged from 0.1 – 1.6 mSv in 2013 [14] and from <0.001 to 0.6 mSv in 2015 [16]. These findings suggest that internal radiation exposure due to the consumption of wild mushrooms remained relatively limited in Kawauchi village."

Comment: These points as stated appear to be valid. However, as noted later, there is great variation in individual consumption of wild mushrooms in Fukushima, and the population has been repeatedly advised not to eat them. It is likely that these are large overestimates for the majority of the population, and underestimates for a small number of individuals who consume large quantities of the most contaminated varieties.

++++

190) "Uncertainties arise because the committed effective dose from dietary intake of mushrooms does not capture day-to-day variation in individuals."

Comment: As noted above.

**********

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31 Aug 2020

Reviewer #1:

Overall comments:

This manuscript describes interesting new research that is an important part of the continuing understanding of recovery from the Fukushima meltdowns. This reviewer strongly recommends publication but with minor revisions below. This work would be improved by adding data for pre-meltdown activities of these same species, as well as control samples of mushrooms from areas not affected by this contamination event. The lack of control and background samples is a notable ommission. Likewise, there is no comparison to other locally-grown or regionally-available foods or edible plants, or even staples such as rice and grains. This deficiency applies equally to activity and committed effective dose data.

We greatly appreciate your comments on our manuscript. We have revised some sections and added more information on comparison values. Although we could not obtain data on the radioactive material concentration in mushrooms in Kawauchi Village before the accident, we added the food monitoring data in other regions and other food products after the Fukushima accident for comparison in Discussion section. (Page 10, lines 159-169)

Specific comments

L21-28: Quantitative data supports that 76% of samples exceed the allowable limit of 100 Bq/kg. By comparison the committed effective dose is described as relatively low but is not compared to a regulatory limit nor is there a comparison to other parts of the diet of returned residents of Kawauchi Village.

According to your suggestion, we revised the Discussion section as follows; “These findings suggest that internal radiation exposure due to the consumption of wild mushrooms remained lower than 1 mSv per year in Kawauchi village. The current reference level (1 mSv/year), which was established by the national government, is set at an adequate level such that effects of continued consumption of radioactive material found in agricultural products remain small and safe. The value 1 mSv/year is in accordance with the guidelines set by the Codex Alimentarius Commission, which sets international standards for food [32]. On the basis of food intake according to age group and the effects of radioactive materials on health, the values are set such that the annual additional radiation dose does not exceed approximately 0.9 mSv, even if 50% of foods contain that level of radioactive materials and are ingested continuously. The “limit of 100 Bq kg” for general foods was determined by choosing the most rigorous limits among the calculated values [32]. Our results suggest that the proportion of mushroom samples with radiocesium concentrations above 100 Bq/kg did not dramatically change, but the committed effective dose by consuming mushrooms is estimated to be relatively limited. Experts need to provide careful explanation of the concepts of radiation protection such as the concept of standard values for food.” (Page 12, Line 208-222.)

Do wild mushrooms have more or less activity compared to other local foods?

If all foods in the villagers’ diet had the same activity as these mushrooms, is that acceptable based on human health considerations?

We added food monitoring data from other regions and for other food products after the Fukushima accident for comparison in the Discussion section. In addition, we considered concepts of radiation protection, especially for consideration of the standard values for food products. (Page 10, Lines 159-169 and Page 12, Lines 208-222)

Which conclusion is dominant – should mushrooms be avoided because they exceed 100 Bq/kg or can they be eaten because effective committed doses are relatively low?

There is variability in individual consumption of wild mushrooms in Fukushima, and the population has been repeatedly advised not to eat them. It is likely that these values are greatly overestimated for the majority of the population and underestimated for a small number of individuals who consume large quantities of the most contaminated varieties. We suggest that providing basic radioisotope monitoring inspection for wild mushrooms and other foods for human consumption is important. We revised the limitation of this study and Conclusion section. (Pages 13, Lines 235-242, and 245-253.)

L17 and also L44: Authors give distances from Fukushima, but should give direction as well. Replace “X km from nuclear plant” with “X km south of nuclear plant” as appropriate.

According to your suggestion, we added the direction from the Fukushima daiichi nuclear power plant in the Abstract and Introduction section. We also describe the location as being within a set radius of the plant (Lines 17 and 49.)

L41: Replace “concentration” with “activity” wherever appropriate in the manuscript. Remove unnecessary “of” from this line as well.

We replace “concentration of” with “activity” on Page 3, Line 42.

L61: The introduction ends abruptly, without giving much context or discussion of prior work with this study. Has this author or any other researcher also studied edible mushrooms in the region? How common is wild mushroom consumption?

We added this information in Introduction session as follows; “It is customary for residents of some areas of Fukushima Prefecture to eat home-grown plants, such as vegetables, edible wild plants, and mushrooms [14]. Residents living in mountainous areas are more likely to eat home-grown foods than are urban residents. In particular, a common pastime for older adults in the area is to forage for edible wild plants in the mountains or to hunt for wild animals [14]. Before the accident, the village was also famous for collecting wild mushrooms, including Sarcodon aspratus and Tricholoma matsutake. Because collection and consumption of wild mushrooms is part of the food culture of this village, residents want to know radiocesium levels in the wild mushrooms [15, 16]. National and local governments implemented monitoring of radioactive concentrations over a wide area of Japan in fiscal year (FY) 2016, and 23 out of 2084 wild mushrooms (not mushrooms purchased at the market) tested were found to contain radiocesium that exceeded the standard values [17]. Since 2013, we have evaluated the activity concentration of artificial radiocesium in wild mushrooms collected in Kawauchi village [15, 18]. To support the recovery efforts of the community after nuclear disaster and conduct continuous risk communication with residents, it is important to monitor the radiocesium concentrations in mushrooms not only for regions of Japan, but also in limited areas, such as municipal units, and to minimise internal radiation exposure of residents due to consumption of contaminated foods. The aims of this study were to evaluate the follow-up radiocesium contamination in wild mushrooms collected from 2016 to 2019, which is 5 to 8 years after the accident.” (Page 2 and 3, Lines 51-69.)

L72: Samples were analyzed by wet weight, without drying. Is the general food standard of 100 Bq/kg also a wet weight standard or a dry weight standard? The authors should clarify this in the text.

According to your suggestion, we added this clarification to the Materials and methods as follows: “The limit for radiocesium is 100 Bq/kg for general foods. Typically, after the Fukushima Daiichi Nuclear accident, food samples without drying were used for measuring radioactivity.” (Page 5, Line 94-95.)

L158: What is the purpose of the proposed long-term follow-up? Is it because the existing data is insufficient to characterize risk, or is it because there is not yet a documented reduction in percentage of mushrooms exceeding the general food standard?

According to your suggestion, we revised the sentence as follows, “Long-term comprehensive follow-up should be conducted because the existing data is insufficient to characterize risk.” (Pages 11, Lines 183-184.)

L162 to 173: The authors imply that the only removal mechanism for Cs-137 and Cs-134 from village soils is radioactive decay. The authors should explicitly state whether this is the only removal mechanism, and that erosion, remediation, infiltration to lower soil depths and so on do (or do not) take place. The authors correctly note that other researchers have done significant work to address these questions, and readers would be interested if other researchers investigated the reasons for the lack of activity reductions over time.

We added the following explanation to the Discussion section: “previous studies have made significant contributions to addressing the reasons for the lack of activity reductions over time [28, 31]. Hashimoto S, et al. [31] investigated whether the 137Cs concentration of wild mushrooms would be spatially biased or influenced by the 137Cs or exchangeable potassium concentrations in soils because the concentration fluctuates among the same species growing within a given area.” (Page 11, Lines 198-202.)

L176: The committed effective dose from mushrooms is important data, but it needs context. What is the committed effective dose (on average) from the whole diet? What would be the committed effective dose if all foods eaten were at 100 Bq/kg? Are these doses higher or lower than for other foods? How do mushrooms compare to the activity of other local foods?

We estimated the committed effective dose from the ingestion of wild mushrooms alone. According to your suggestion, we revised the Discussion section including the concepts of radiation protection, especially, and the standard values for food and comparison with the activity of other local foods.

L180: The overall quality of the written text is excellent, but errors of tense (‘has’ used instead of the correct ‘have’) mar the otherwise logical and readable nature of this manuscript.

We replace “has” with “have” on Page 12, Line 223.

L181: Including the authors’ communications with stakeholders is something that is not done nearly enough by other researchers. This is a commendable effort by the authors and I applaud them for it.

Thank you for your comment.

L198: Again, the use of nonquantitative terms such as ‘relatively-limited’ should be buttressed with quantitative data. The previous comments for L21-28 should also be reflected in the conclusions.

According to your suggestion, we added specific values in the Conclusion as follows: “the median committed effective dose by consuming mushrooms was found to be lower than 1 mSv per year.” (Page 13, Line 248-249)

Reviewer #2:

This is a useful paper which updates findings from a long-term study reported in previous papers, such as Nakashima et al, 2015, Orita et al 2017, Tsuchiya et al 2017. The data is clearly presented overall. Some pertinent background information that would give useful context, and was generally included in the earlier papers, is absent. Specifically, it would be helpful to note relevant aspects of food testing policy in Fukushima overall, such as the fact that wild gathered food items such as these mushrooms are rarely included in official testing. The range of Cs activities reported by official testing for agriculturally grown and commercially distributed mushrooms could be given for context. Also, it is important to note that although the Fukushima public has been repeatedly advised since 2011 to avoid eating wild mushrooms because of contamination risk, many people, particularly elderly, do in fact continue to eat them. Helping to clarify the risks to such people is, I believe, the underlying motivation for this ongoing study in Kawauchi.

We greatly appreciate your comments on our manuscript. We have changed some sections and added more information.

0) “Before the accident, the village was famous for collecting wild mushrooms, including Sarcodon aspratus and Tricholoma matsutake.”

Comment: In Tsuchiya et al, 2017, you provided common Japanese names for the mushrooms in addition to Latin names. This is helpful for non-botanists as well as researchers in the social sciences and others who may find interest in this study.

According to your suggestion, we added Japanese names of mushrooms in Table 1. (Page 7)

93) “The value for e was determined from the mean value of daily intake for age and sex which was obtained from the Ministry of Health, Labour, and Welfare, Japan in 2016: males, 2.8–7.3 kg/year; females, 2.5–7.3 kg/year) [18].”

Comment: There are a few issues that should be clarified regarding these estimates and how they are derived:

— From the citation [18] it appears that the reference document is: The National Health and Nutrition Survey in Japan, 2016 (direct link https://www.mhlw.go.jp/bunya/kenkou/eiyou/dl/h28-houkoku.pdf). If this is the case, then it should be cited directly, and relevant pages should be cited as well.

We revised reference 20 for research the quoted the part directly, “Ministry of Health, Labour and Welfare, Japan. Report on National Health and Nutrition Survey, pages 72-73 and 76-77. (in Japanese) [cited August 31, 2020]. In: https://www.mhlw.go.jp/bunya/kenkou/eiyou/dl/h28-houkoku-04.pdf”. (Page 20)

— It is not clear that all of the mushroom varieties examined in this study are included in this MHLW document. Further, it is not clear that “wild” versus “commercially distributed” mushrooms are categorized separately by MHLW.

The MHLW results show the total mushroom intake in the population. The MHLW data contains all kinds of mushrooms (both wild and commercially distributed). We added this as one of the limitations of this study. (Page 13, Line 235-242).

— MHLW gives fairly detailed breakdown of consumption quantity estimates by age. It is not clear how this is factored into the value of e obtained, in conjunction with the age-dependent dose conversion coefficients. Is only the mean of all age groups used?

We calculated the internal effective doses using the median intake of each age group and the age-dependent dose conversion coefficients. We added the mushroom intake information for each age group in Table 2.

— The larger question is whether or not MHLW’s estimates for typical mushroom consumption are accurate in the case of wild mushrooms gathered and eaten in Fukushima.

As you pointed out, we are not sure whether the typical MHLW estimates of mushroom consumption are accurate for the quantity of wild mushrooms consumed in Fukushima or not, and we added this as one of the limitations. (Page 13, Line 235-242).

119) "Fig 1. Distribution of concentrations of radiocesium(134Cs+137Cs) in wild mushroom samples collected in Kawauchi village (2016–2019)."

Comment: The activities are separated into only four bins: n.d; n.d.-100Bq; 100-1000Bq; >1000Bq. This appears consistent with the earlier papers, although Nakashima et al, 2015, uses five bins. It would be helpful to include more granular histogram for each year, with at least ten bins each, so the actual activity distributions could be better grasped.

According to your suggestion, we added more bins and replaced Fig 1.

141) "Table 2. Internal committed effective dose calculated with the assumption that residents consume wild mushrooms collected in Kawauchi village for 1 year."

Comment: Related to the above comment. It would be helpful to add the estimated quantity consumed for each age group to the table.

According to your suggestion, we added the mushroom intake information for each age group in the Table 2.

152) "The median concentration of radiocesium in all mushroom species was 526 Bq/kg in 2016, 88 Bq/kg in 2017, 1,106 Bq/kg in 2018 and 362 Bq/kg in 2019."

Comment: These are very wide fluctuations. You touch on some of the reasons for this later. Perhaps one finding is that the sampling methodology reported in this study is unable to provide representative measurements of the overall change in radiocesium levels in wild mushrooms in general in Fukushima. However, it can provide a good indication of typical intake of radiocesium from consumption of gathered wild mushrooms.

As you describe, we also think that this is a key point.

154) "These results suggest that the proportion of mushroom samples with radiocesium concentrations above 100 Bq/kg did not dramatically change in Fukushima over 8 years."

Comment: This is a key finding, and consistent with the literature regarding Chernobyl.

Thank you for your comments.

75) "We showed that the estimated committed effective dose from the ingestion of wild mushrooms collected in 2016 was 0.017 – 0.054 mSv, 0.0028 – 0.0087 mSv in 2017, 0.034 – 0.110 mSv in 2018 and 0.011 – 0.036 mSv in 2019. Previously, we reported that the calculated effective dose ranged from 0.1 – 1.6 mSv in 2013 [14] and from <0.001 to 0.6 mSv in 2015 [16]. These findings suggest that internal radiation exposure due to the consumption of wild mushrooms remained relatively limited in Kawauchi village."

Comment: These points as stated appear to be valid. However, as noted later, there is great variation in individual consumption of wild mushrooms in Fukushima, and the population has been repeatedly advised not to eat them. It is likely that these are large overestimates for the majority of the population, and underestimates for a small number of individuals who consume large quantities of the most contaminated varieties.

According to your comment, we added the sentence you mentioned above as a limitation of this study. (Page 13, Line 235-242.)

190) "Uncertainties arise because the committed effective dose from dietary intake of mushrooms does not capture day-to-day variation in individuals."

Comment: As noted above.

According to your comment, we added the sentence you propose as a limitation of this study. Thank you for your suggestions. (Page 11, Line 235-242.)

Submitted filename: ResponseToReviewers.docx

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3 Sep 2020

Radiocesium concentrations in mushrooms collected in Kawauchi Village five to eight years after the Fukushima Daiichi nuclear power plant accident

PONE-D-20-19962R1

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7 Sep 2020

PONE-D-20-19962R1

Radiocesium concentrations in mushrooms collected in Kawauchi Village five to eight years after the Fukushima Daiichi nuclear power plant accident

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