137Cesium (137Cs) assessment in wild boars from northwestern Italy

Daniele Pattono; Alessandro Mannelli; Alessandra Dalmasso; Riccardo Orusa; Massimo Faure Ragani; Maria Teresa Bottero

doi:10.1371/journal.pone.0303093

. 2024 May 9;19(5):e0303093. doi: 10.1371/journal.pone.0303093

¹³⁷Cesium (¹³⁷Cs) assessment in wild boars from northwestern Italy

Daniele Pattono ^1,^*, Alessandro Mannelli ¹, Alessandra Dalmasso ¹, Riccardo Orusa ², Massimo Faure Ragani ³, Maria Teresa Bottero ¹

Editor: Mohamad Syazwan Mohd Sanusi⁴

PMCID: PMC11081301 PMID: 38722996

Abstract

Radionuclide contamination is a serious health issue caused by nuclear experiments and plant accidents, as seen for the Chernobyl and Fukushima nuclear plants. Italy has been especially interested in northwestern alpine regions, as have several other nations. The aim of this work was to indagate ¹³⁴Cs and ¹³⁷Cs contamination in wild boars, which were considered bioindicators sampled in the Chisone/Germanasca Valley and the Pellice Valley districts (Piedmont, Italy) in two hunting seasons (2014 and 2016). In the 2014 season, only the livers of the animals (n = 48) were sampled, whereas in 2016, five different anatomical sampling sites were sampled for each animal (n = 16). The analyses were conducted in an accredited laboratory (Agenzia Regionale per la Protezione dell’Ambiente–ARPA) by the aid of an HPGe detector (Ortec) with a relative efficiency of 50%. In general, the contamination levels registered in 2014 were under the detection limit for ¹³⁴Cs and low for ¹³⁷Cs (Chisone/Germanasca valley: min: 0.0, max: 23.9 median 11.0 Bq/kg vs Pellice valley: min 0, max: 31.7, median: 9.6 Bq/kg) and no health concern can be supposed. In the first-year samples, the liver showed a negative correlation between age and contamination level. In the second year of sampling, low levels were confirmed (min: 3.1 Bq/kg, max: 113.3; median 17.7 Bq/kg). Multiple sampling from the same animal showed that the diaphragm (median = 27.7 Bq/kg) kidney (27.4) and tongue (27.6) were more contaminated than the liver (17.7) and spleen (15.3). Moreover, a linear mixed model revealed a negative organ-by-age interaction, meaning that interorgan differences in contamination level were greater in younger (5–11 months) than in older (18–36 months) animals. Different feeding habits can be the explanation. Our paper shows that muscle sites (diaphragm and tongue) can be useful for radionuclide pollution surveillance in wild boar populations and that younger animals show more interorgan variability in contamination levels than older animals. More investigations are needed to confirm this correlation and to fulfill the request for more data to achieve better risk assessment.

Introduction

Radionuclide contamination as a threat to human health is receiving growing attention from the scientific community [1]. Sources of radionuclides may be natural, as in the case of radioactive minerals and sediments, or anthropogenic, such as the pollution derived from nuclear weapon experiments performed in the 1950s and 1960s and nuclear power plant accidents [2, 3]. Of the various anthropogenic radionuclides, the most frequently detected are ¹³⁴Cesium (¹³⁴Cs) (T_1/2 = 2.06 years) and ¹³⁷Cesium (¹³⁷Cs) (T_1/2 ranging from 30.17 to 69.3 years) [3–5]. Cs is generally found in the top few centimeters of the soil, with different vertical profiles for the different isotopes [6, 7]. In the soil environment, it can create bioavailable complexes and be absorbed by plants and mushrooms (secondary reservoirs) in the same way as potassium ions, thus becoming soil-independent sources of radionuclides and prolonging the contamination of sites [5, 8].

Anthropogenic sources of radionuclide contamination became the primary source in the second half of the twentieth century [2, 4, 6].

Considering the health consequences of anthropogenic radionuclide pollution, in 1957, the European Union (EU) set up regulations that were recently updated. The maximum level of ¹³⁴Cs + ¹³⁷Cs radioactivity in food products considered acceptable for consumption is 100 Bq/kg [6]. In addition, the new basic safety standard directives stated that environmental monitoring must be performed as an essential part of the management of emergency exposure and risk assessment, as in other fields [2, 9].

Moreover, assessing the effects of radionuclides on natural flora and fauna is important not only because of the potential impact of contamination on forest ecosystems but also because of their possible consumption by humans in the form of fruit, mushrooms, wild game meat and meat products [1, 4, 10]. In fact, it has been demonstrated that exposure to radionuclides through the consumption of contaminated food has the potential to affect a large part of the population and poses the most relevant radiological risk of chronic accumulation once measures have been taken [6, 7].

Within the biota of the forest ecosystem, wild boar (Sus scrofa) and earthworms are considered among the most reliable bioindicators for the study of these radionuclides [11–14]. Indeed, wild boars are considered hyperaccumulators of radionuclides [8]. There are many reasons for this; first, their diet is based on fungi and plants or insects in which radionuclides become bioavailable and that act as “secondary reservoirs”. In addition, wild boars themselves can accumulate radionuclides, and their resorption rate is close to 100% [6, 15–17].

In the context of food safety, wild boars are regularly hunted for human consumption by the hunters themselves or sold on the national and international market. Moreover, these animals have the capability to travel long distances [13, 18–20] with a consequent propagation of risk; in fact, animals living in contaminated zones can be hunted far from the original zones. Furthermore, their meat can be sold in different areas. This fact means that hunter families and a wide number of consumers can be at risk of exposure to radionuclide contamination, and health problems must be considered a consequence of this environmental pollution. For these reasons, testing wild boars is essential to assess the potential for radionuclides to enter the food chain [1, 6, 10].

Muscle is the most common sampling site, but many authors have stressed that more data are needed on the distribution of radionuclides in the whole body to define safety limits more accurately, taking into account the distribution in the different anatomical systems and that some of the radionuclides are normally consumed [1, 6]. This is an important aspect if we consider that biodistribution and biological half-life depend on the organ [21].

In all Europe the attention on radionuclides contamination raised after two main nuclear plant accidents: Chernobyl and Fukushima nuclear plants accidents. Both nuclear plants accidents lead to a severe contamination across Europe of Cs isotope, ¹³⁴Cesium (¹³⁴Cs) and ¹³⁷Cesium (¹³⁷Cs) even if the contamination levels varied among regions [21]. With regard to Italy, considerable levels of ¹³⁷Cs contamination were detected in the northwestern alpine region, in addition to natural sources of radionuclides. The region of Piedmont was affected; in particular, certain valleys, such as the Sesia Valley District [22, 23]. Some initial investigations to ascertain radionuclide contamination were conducted in Piedmont [22], but this was not followed up by detailed studies to assess radioactive contamination levels for the monitoring of contamination, and these data are still missing. In addition, evaluating the contamination of wild boar in these valleys provides us with valuable information for assessing the risk associated with the consumption of contaminated wild boar meat products, as well as data about radionuclide risk assessments requested by EU Regulations [9, 18, 24]. The output of this study will be useful for future sampling campaigns by helping to optimize the collection of data and to establish safe hunting management strategies [2, 13, 18].

The aim of this work was to determine the radioactive contamination of wild boar regularly hunted in the districts of the Pellice and Chisone/Germanasca Valleys in Piedmont, Northwest Italy (Fig 1), within the Western Alps. In the 2014 hunting season, we collected data on ¹³⁴Cs and ¹³⁷Cs contamination of the liver, whereas in the 2016 season, we collected data on the distribution of ¹³⁷Cs in five different anatomical systems to study the distribution of radionuclide contamination in wild boar.

Material and methods

All samples came from wild boars killed during two hunting seasons (2014 and 2016). The hunters were responsible for providing the anatomical samples collected at the slaughterhouse for the surveillance campaign carried out over these years.

In the first year (2014), liver samples (20–25 gr each sample) were collected in plastic bags by hunters from 48 wild boars (25 males and 23 females). The samples came from two valley districts in the Piedmont: the Chisone/Germanasca Valley (20 samples) and the Pellice Valley (28 samples). The ages were > 17 months (21 samples) and < 12 months (27 samples).

Two years later (2016), we obtained samples (10–100 gr depending on the anatomical site) from five different anatomical sites derived from 16 wild boars (6 males and 10 females) hunted in Pellice Valley District within the same hunting period. The sites comprised two muscular sites (diaphragm and tongue), kidney, spleen and liver. These sites of interest were chosen in light of the literature on radiocaesium contamination [1, 16] and to cover the main body systems, namely, the emunctory, digestive and hematopoietic systems.

¹³⁴Cs and ¹³⁷Cs radioactivity was determined by gamma-spectrometric measurements performed by an accredited laboratory using an HPGe detector (Ortec) with a relative efficiency of 50%.

Tissue samples were stored at -20°C until the time of assay. Individual samples were dried at 105 ºC to constant weight, then crushed in a cross-beater mill, and thoroughly mixed until homogeneous. Then the samples were placed in 20 cc to 100 cc polyethylene cups in contact with the detector End-Cap. The counting time was 60000 sec. The minimum detectable activity (MDA) was 1 Bq/kg (fresh weight) for both radionuclides. The calibration of the instrument/geometry was performed with a 100 cc certified multigamma source, and the Monte Carlo software EFFTRAN was used to evaluate the efficiency transfer due to the density and volume differences between the calibration source and the samples. All contributions to the uncertainty were considered: counting, gamma emission, efficiency, efficiency transfer, repeatability, and instrumental stability.

Statistical analysis

The concentrations of ¹³⁷Cs in wild boars’ livers (2014) and in in five different anatomical sites (2016) were analyzed by the UNIVARIATE procedure in SAS System ver. 9.4 [25]. The Shapiro‒Wilk test was used to check normality. The FREQ procedure was used to generate a distribution of the age of wild boars. Subsequently, individuals were divided into two age groups: 5 to 11, and 18 to 90 months of age. We used the MEANS procedure to calculate median, first and third quartiles (Q1, Q3) of the concentrations of ¹³⁷Cs, since these statistics are not affected by the distribution of the data [25]. Furthermore, for descriptive purposes, we calculated minimum and maximum, mean, standard error and 95% confidence limits of the mean, after dividing the data by year, age group and sex of wild boars. For the second year of the study, descriptive statistics were obtained for each tested organ.

Wilcoxon two-sample tests were used to compare median concentrations from boars hunted in 2014, in the Chisone Germanasca Valley District with those hunted in the Pellice Valley Districts (PROC NPAR1WAY) and females vs. males. The correlation between the concentrations of ¹³⁷Cs in the liver and wild boar age was tested using the nonparametric correlation coefficient Kendall’s tau (PROC CORR).

For data obtained in 2016, a linear mixed statistical model (PROC MIXED) was used to estimate the association between the tested organ, age group, and sex of wild boar and the natural log transformation of the concentrations of ¹³⁷Cs (log¹³⁷Cs). The effects of these predictors were included in the model as fixed, as in a linear regression. We also considered that there might be variations in log¹³⁷Cs across wild boars. Furthermore, measurements, which we made on different organs belonging to the same 16 animals, were not independent. This needs to be taken into account in the statistical analysis. Since there was no interest in comparing specific individuals, between-wild boar variation was included in the model as a random effect [26]. Age group by tested organ interaction terms was included to test whether the association between organs and log¹³⁷Cs differed across age groups. Statistical significance was fixed at the 0.05 level.

Results

As stated in the introduction, the sampling carried out in the 2014 hunting season was to obtain information on ¹³⁴Cs and ¹³⁷Cs levels in wild boars caught in two distinct mountain districts: the Chisone/Germanasca Valley and the Pellice Valley (Fig 1).

In 2014, ¹³⁴Cs levels were always below the sensitivity threshold of the gamma-spectrometer, in agreement with a report from the national control authority in which levels of this contaminant in the soil were also below the sensitivity threshold for this method [27].

In the same year the median (first, third quartiles) level of ¹³⁷Cs (Table 1 and S1 Table) in wild boar liver samples from the Chisone/Germanasca Valley was 11.05 Bq/kg (6.3, 15.7) vs. 9.6 (7.1, 17.8) for the Pellice Valley. This difference was not statistically significant (P = 0.98). Moreover, there was no significant difference between the liver ¹³⁷Cs contamination levels in male vs. female boars hunted in 2014 (P = 0.46, Table 1). On the other hand, in 2014, we found a negative correlation between animal age and ¹³⁷Cs liver contamination levels (Kendall’s tau = -0.21, P < 0.05).

Table 1. Radioactivity levels of ¹³⁷Cesium (¹³⁷Cs, Bq/kg) in liver of 48 wild boars during the first sampling season (2014) in Chisone/Germanasca and Pellice Valleys, by age class and sex.

n = sample size; Q1: first quartile; Q3: third quartile; se: standard error; CL’s: confidence limits of the mean.

Age class, months (n)	Median value (Q1, Q3)	Minimum, maximum	Mean (se)	95% CL’s
5, 11 (27)	11.8 (7.7, 18.2)	0.0, 39.7	13.3 (1.7)	9.8, 16.8
> 11 (21)	9.0 (5.8, 14.2)	0.0, 22.8	9.7 (1.4)	6.8, 12.7
Sex (n)
Female (23)	9.1 (6.6, 14.2)	0, 39.7	11.2 (1.7)	7.7, 14.6
Male (25)	11.1 (6.9, 18.1)	0, 31.7	12.3 (1.6)	8.9, 15.6

Open in a new tab

In the second year (2016), considering the results of the previous sampling, we focused only on ¹³⁷Cs. Multiple anatomical sites were sampled to permit a comparison between three physiological systems, namely, the emunctory, digestive and hematopoietic systems. The results are summarized in Tables 2 and 3 and S2 Table. In general, the levels were very low for all the sampling sites.

Table 2. Radioactivity levels of ¹³⁷Cesium (¹³⁷Cs, Bq/kg) in 16 wild boars, in tongue, diaphragm, liver, spleen (results from all organs combined), during the second sampling season in Pellice Valley, 2016 by age class and sex.

n = number of observations; Q1: first quartile; Q3: third quartile; se: standard error; CL’s: confidence limits of the mean.

Age class, months (n)	Median value (Q1, Q3)	Minimum, maximum	Mean (se)	95% CL’s
5, 11 (45)	29.0 (18.9, 96.4)	2.4, 279.1	62.1 (9.8)	42.3, 81.8
> 11 (35)	15.0 (8.3, 27.2)	3.1, 83.0	21.6 (3.3)	14.9, 28.3
Sex (n)
Female (50)	27.9 (16.5, 61.5)	2.4, 279.1	50.3 (8.1)	33.9, 66.6
Male (30)	15.6 (8.3, 27.2)	3.1, 199.6	34.5 (8.9)	16.3, 52.7

Open in a new tab

Table 3. Radioactivity levels of ¹³⁷Cesium (¹³⁷Cs, Bq/kg) in different anatomical sites of 16 wild boars during the second sampling season in Pellice Valley, 2016.

Q1: first quartile; Q3: third quartile; se: standard error; CL’s: confidence limits of the mean.

Tested organ	Median value (Q1, Q3)	Minimum, maximum	Mean (se)	95% CL’s
Tongue	27.4 (16.1, 40.7)	3.4, 144.6	43.5 (11.5)	19.0, 68.0
Diaphragm	27.7 (12.7, 52.9)	4.2, 279.1	60.7 (20.0)	18.2, 103.3
Liver	17.7 (10.3, 41.4)	3.1. 113.3	32.9 (8.8)	14.2, 51.6
Spleen	15.3 (8.2, 30.4)	2.4, 109.1	29.4 (8.3)	11.7, 47.1
Kidney	27.6 (17.1, 50.0)	4.5, 192.0	55.2 (16.0)	21.0, 89.4

Open in a new tab

The contamination with ¹³⁷Cs (Fig 2) was greatest in organs from three wild boars of seven months of age (id = 5, 6, 7), with a maximum value of 279.1 Bg/kg in a diaphragm. Relatively high ¹³⁷Cs levels were detected in only one animal of the older age group (≥ 18 months; id = 10). Differences in ¹³⁷Cs among organs were particularly wide in the three most contaminated, young wild boars. However, in relative terms, ¹³⁷Cs in the diaphragm of another young wild boar (id = 2) was 5.6 times greater than in the spleen of the same animal (46.1 vas 8.2 Bq/kg).

The Shapiro–Wilk test indicated a departure from normality (W = 0.71) of the distribution of ¹³⁷CS in 2016, which justified the natural log transformation (log¹³⁷Cs) to fit a normal distribution (W = 0.98) to be used in the linear mixed model. The spleen, which was characterized by the lowest contamination levels (Table 3), was used as the reference organ in the analysis. The final model successfully converged, and the results, which are shown in Table 4, indicated that differences between log¹³⁷Cs across organs were greatest in younger wild boars. This was demonstrated by significant, negative diaphragm-by-age, and kidney-by-age interaction terms. There was also a negative tongue-by-age interaction, although it was not significant at the 0.05 level. There was no significant association between wild boar sex and log¹³⁷Cs (Table 4). There was no significant interaction between sex and organ or between sex and wild boar age; therefore, the corresponding terms were not retained in the final model.

Table 4. Results of a mixed linear statistical model of the association between tested organ, age group, and the natural log of ¹³⁷Cs (log¹³⁷Cs), in wild boars in Italy, in 2016.

The spleen was used as the reference organ. Individuals were divided into two age groups: > 18 months and < 11 months as the reference group. Consequently, the negative interaction sign indicates that the increased log¹³⁷Cs levels in certain organs, in comparison with the spleen, were greatest in young wild boars.

Fixed effect	Estimate	Standard Error	P
Intercept	2.87	0.60	0.00
Diaphragm	0.82	0.10	< .0001
Liver	0.25	0.10	0.02
Tongue	0.58	0.10	< .0001
Kidney	0.74	0.10	< .0001
Spleen	0	.	.
Female	0.23	0.61	0.70
Male	0	.	.
Age	-0.46	0.60	0.44
*Diaphragm Age**	-0.51	0.15	0.002
*Liver Age**	-0.21	0.15	0.19
*Tongue Age**	-0.29	0.15	0.07
*Kidney Age**	-0.30	0.15	0.05
*Spleen Age**	0	.	.

Open in a new tab

Discussion

The aim of this paper was to determinate Cs contamination in two Valleys of Piedmont region several years after Chernobyl and Fukushima nuclear plants accidents. At the time of the Chernobyl accident, the Agenzia Regionale per la Protezione dell’Ambiente of the Piedmont region (ARPA), a public agency for environmental protection, evaluated a radioactive fallout of ¹³⁷Cs ranging from 31500 (north alpine valleys of the Piedmont) to values lower than 4000 Bq/m² in the southern valley. In the investigated valleys, values were between 4000 and 7800 Bq/m² [27]. Even if in food of animal origin, relatively low values were registered (farm Milk in 1990 value approximately 1.2 Bq/l and values lower than 0.2 Bq/l in 2011) in particular situations (milk produced from highland pastures), values of approximately 20–30 Bq/l were still found at the time of the investigation [27].

The results concerning ¹³⁴Cs levels show in our opinion that the nuclear power accidents did not result in the contamination of these two valleys. These findings are in agreement with a report from the national control authority in which levels of this contaminant in the soil were also below the sensitivity threshold for this method [27].

The contamination levels of ¹³⁷Cs in 2014 are similar to values reported for ¹³⁷Cs in wild boar meat from Piedmont in 2012 (approximately 10 Bg/kg) [27] but very different from findings for other European countries in the same period. For example, the mean contamination level reported for wild boar hunted in Switzerland was 1084 Bq/kg, and the maximum was 2420 Bq/kg [16], while another study reported mean values eightfold higher for central Europe, in the range of 20 kBq/kg [8]. In Bavaria wild boar, meats exceeded the regulatory limit by 1–2 orders of magnitude. High contamination values (min 0.37 kBq/kg max 14 kBq/kg–median 1.7 kBq/kg) were still registered several years later (fall 2019 –spring 2020) in the tongue [28].

Thus, the range of values for animals across Europe is extremely wide [5, 8]. The contamination was widely spread across Europe and in agreement with other sites showed a slower decline than what could be expected considering the half-life of ¹³⁷Cs in wild boar meat. This phenomenon is called the “wild boar paradox” [28]. In addition, it was demonstrated also in a retrospective study for vegetables, water and soils [29]. Recently, Saito et al. [30] explained that the mechanical action of wild boar rooting behavior is responsible for longer persistence. In fact, this peculiar feeding behavior is responsible for changing the depth of ¹³⁷Cs and chemical or biological interactions with the organic layer and mineral soil components. The consequences are changes in bioavailability and vertical and horizontal/surface distributions in contaminated areas.

In relation to the consumption of wild boar meat, considering the statutory limit of 600 Bq/kg for ¹³⁷Cs [7], the low contamination levels detected in samples collected in 2014 confirm the lack of any health concerns related to wild boar hunted in the two valleys studied. Moreover, the risks associated with eating this meat are reduced considering that levels can be lower because the boars were hunted in the autumn when levels are higher [13, 17, 20]. This means that in other periods, the contamination can be lower. Another recommendation to decrease the rate of consumption and consequently the health-related risk is to eat cooked meat instead of raw meat preparations (salami or raw meat dishes) because the cooking process appears to decrease the effects of radionuclide contamination in food [11].

Other considerations can be done comparing different classes, e.g. male vs. female, different sampling sites or different ages. Comparing the liver ¹³⁷Cs contamination levels in male vs. female boars hunted in 2014, no significant differences were found (P = 0.46). While this confirms the finding of some authors [15], it does not agree with those of others [31]; however, this result remains controversial because few data are available in the literature about comparisons between male and female subjects. The same consideration must be made in relation to the provenience of the animals (in 2014).

A negative correlation between animal age and ¹³⁷Cs liver contamination levels, in 2014, indicated that samples from younger animals tend to be more contaminated than those from older animals, as described for other species [19]. Differences in feeding habits in quality and quantity (younger animals consume higher quantities of contaminated feed) may explain this finding [7, 13, 18, 29, 32]. If this is so, a new approach to risk assessment should be devised, with younger animals being considered the preferred target for the sampling campaigns.

In general, the diaphragm, kidney, and tongue were the most heavily contaminated organs, whereas the spleen and liver were characterized by lower values (Table 3; Fig 2). The interorgan differences in contamination levels were most evident in young animals. There is no literature available with which to compare these findings, and more studies are needed.

If we consider the distribution in the literature, a similar distribution was described by other authors for these organs. Gulakov [16] found that muscles and kidneys were more contaminated than the liver and spleen, but no information was provided about animal age. In another study looking at bovine samples, mean values varied greatly between muscle sites (e.g., contamination levels in the tongue were twice those of the diaphragm), with the highest found in the liver and the lowest in the kidney [33]. In Bavarian wild boar samples, the contamination of tongue and other unspecified muscles was higher than our findings (min 0.37 kBq/kg, max 14 kBq/kg–median 1.7 kBq/kg) [28]. From our point of view, the different contamination levels among anatomical sites found can be ascribed to a variety of factors [34–36]. The first one can be the different equilibrium times for ¹³⁷Cs. The higher contamination of muscles can also be explained considering the different chemical composition of this specific anatomical site. It is a tissue with high Potassium (K) content and Cs shows similar biodynamic patterns being in the same group of the periodic table (Group 1 alkali metals). This is in accordance with other papers [37, 38].

Explanations for the different contamination levels among the papers can be differences between monogastric vs. poligastric animals, differences in feeding habits, differences in the levels of feed contamination, and the heterogeneous deposition of radionuclide fallout within contaminated areas [7, 13, 17, 18, 27]. The results also indicate that the muscles sites are associated with the highest level of contamination considering edible tissues [1].

Also, the kidney seems to show higher contamination. This issue is interesting because distribution has been studied in several animals and insects but not in wild boar [21, 34, 36].

Several final considerations can be summarized from the discussion. New insight into contamination levels, food safety and distribution among organs can be used for the risk assessment of radionuclide contamination in wild boar. First, in these valleys, contamination levels seem to be low, which confirms the lower fallout of Cs in the southern parts of the Piedmont [27]. Moreover, it has been proven that muscular site sampling can be considered a reliable site for checking contamination in the case of ordinary and extraordinary surveillance. The advantage is that muscles are already considered a routine sampling site for hunters for trichinellosis surveillance programs, and for this reason, there is no need for training [39].

The comparison among different organs confirms that the kidney can also be useful [1, 13, 18]. Unfortunately, few other studies are available in the present literature for other organs in field surveillance with which to compare our results, a problem also highlighted by Saito et al. [17].

Finally, our data show that organs from certain younger animals were the most contaminated, so we can suggest that younger animals are more useful for risk assessment. This can be useful for surveillance campaigns.

Conclusions

Radionuclides are gaining attention for their importance and potential consequences for public health. The pollution resulting from nuclear power plant accidents (e.g., Chernobyl) is still present and continues to cause a small increased risk of stochastic radiation effects (cancer and heritable effects) [7]. To provide a high level of protection from this risk, mandatory risk assessments must be performed using reliable data [4, 18] and in a regular manner due to the very long half-lives of certain radionuclides, such as ¹³⁷Cs [8].

Wild boars are considered to be valuable bioindicators and a significant source of contamination for people consuming their meat products [7, 10]. At the present time, the request for data is only partially fulfilled [1].

Our research shows that in these valleys, the situation is good with low contamination levels. An important finding of our research indicates that juvenile animals have slightly higher contamination and that variations between sampling points are more detectable in these individuals. In accordance with recent legislation [9], more work is needed to extend monitoring activities to other radionuclides to a greater number of animals, and different matrices such soil, food material and feces are needed to study the phenomenon more thoroughly to confirm the statistically significant correlations found here. The analysis should also be extended to cover additional edible animal parts and other species for a more complete evaluation of game meat safety for human consumption, thus raising the level of food safety associated with game meat and game meat products [16, 33]. In addition, hunters might have available safer and more reliable instructions given by authorities for hunting campaigns (e.g., young animals can be more useful for assessment and surveillance). At present, the information gathered about ¹³⁷Cs contamination helps consumers and producers to a safer consumption of this kind of meat by cooking it or using it for cooked products instead of raw fermented products such as salami, raw ham or tartare or suggests the exclusion of some edible organs.

Supporting information

S1 Table. First-year sampling data.

(XLS)

pone.0303093.s001.xls^{(45KB, xls)}

S2 Table. Second-year sampling data.

(XLS)

pone.0303093.s002.xls^{(62.5KB, xls)}

Acknowledgments

We would like to thank Mr. Marco Giovo and Dr. Elisa Dalmas for their help during the sampling phase.

Data Availability

All relevant data are within the paper and its Supporting information files.

Funding Statement

The author(s) received no specific funding for this work.

References

1.Ferri M, Baldi L, Cavallo S, Pellicanò R, Brambilla G. (2017). Wild game consumption habits among Italian shooters: relevance for intakes of cadmium, perfluorooctanesulphonic acid and ¹³⁷Cesium as priority contaminants. Food Addit Contam Part A, 34 (5), 832–841, doi: 10.1080/19440049.2017.1293303 [DOI] [PubMed] [Google Scholar]
2.Aliyu AS, Evangeliou N, Mousseau TA, Wu J, Ramli AT. (2015). An overview of current knowledge concerning the health and environmental consequences of the Fukushima Daiichi Nuclear Power Plant (FDNPP) accident. Environ Internat 85, 213–228. doi: 10.1016/j.envint.2015.09.020 [DOI] [PubMed] [Google Scholar]
3.Vetikko V, Kostantiainen E. (2013). Assessment of doses to game animals in Finland. J Enviro Radioact, 125, 69–73. doi: 10.1016/j.jenvrad.2013.01.014 [DOI] [PubMed] [Google Scholar]
4.Nakamura K, Chiba S, Kiuchi T, Nabeshi H, Tsutsumi T, Akiyama H, et al. (2022). Comprehensive analysis of a decade of cumulative radiocesium testing data for foodstuff throughout Japan after the 2011 Fukushima Daiichi Nuclear Power Plant accident. PloS one 17(9): e0274070. doi: 10.1371/journal.pone.0274070 [DOI] [PMC free article] [PubMed] [Google Scholar]
5.Oloś G, Dolhańczuk-Śródka A. (2022) Effective and environmental half-lives of radiocesium in game from Poland. Journal of Environmental radioactivity, 248, 106870. doi: 10.1016/j.jenvrad.2022.106870 [DOI] [PubMed] [Google Scholar]
6.Merz S, Shozugawa K, Steinhauser S. (2015). Analysis of Japanese Radionuclide Monitoring Data of Food Before and After the Fukushima Nuclear Accident. Environ Sci Technol, 49, 2875–2855. doi: 10.1021/es5057648 [DOI] [PMC free article] [PubMed] [Google Scholar]
7.Janssens A, Necheva C, Tanner V, Turai I. (2013). The New Basic Standards Directive and its implications for environmental monitoring. J Environ Radioact, 125, 99–104. [DOI] [PubMed] [Google Scholar]
8.Piñero-García F, Thomas R, Mantero J, Forssell-Aronsson E, Isaksson M. (2022). Concentration of radionuclides in Swedish market basket and its radiological implications. Food Control, 133, 108658. doi: 10.1016/j.foodcont.2021.108658 [DOI] [Google Scholar]
9.Meisenberg O, Gerstmann UC. (2021). Exposure of german hunters and their family members to the radioactive nuclide ¹³⁷Cs due to their eating habits. Sci Total Environ, 798, 149264. doi: 10.1016/j.scitotenv.2021.149264 [DOI] [PubMed] [Google Scholar]
10.Aono T, Yoshida S, Akashi M. (2016). Initial and present situation of food contamination in Japan after the accident at the Fukushima Dai-Chi nuclear power plant. Radiat Prot Dosimetry 171, 14–19. [DOI] [PubMed] [Google Scholar]
11.Caridi F, D’Agostino M, Belvedere A. (2020). Radioactivity in Calabrian (Southern Italy) Wild Boar Meat. Appl Sci, 10, 3580, doi: 10.3390/app10103580 [DOI] [Google Scholar]
12.Nemoto Y, Saito R, Oomachi H. (2018). Seasonal variation of Cesium -137 concentration in Asian black bear (Ursus thibetanus and wild boar (Sus scrofa) in Fukushima Prefecture, Japan. PLoS ONE 13(7): e0200797. doi: 10.1371/journal.pone.0200797 [DOI] [PMC free article] [PubMed] [Google Scholar]
13.Noelia Barros-Garcia M, Ballari SA. (2012). Impact of wild boar (Sus scrofa) in its introduced and native range: a review. Biol Invasions 14, 2283–2300. [Google Scholar]
14.Steinhauser G, Saey PRJ. (2016). ¹³⁷Cs in the meat of wild boars. A comparison of the impacts of Chernobyl and Fukushima. J Radioanal Nucl Ch 307, 1801–1806. doi: 10.1007/s10967-015-4417-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
15.Dvořák P, Snášel P, Beňová K. (2010). Transfert of radiocesium into Wild Boar Meat. Acta Vet BRNO, 79, S85–S91. [Google Scholar]
16.Gulakov AV. (2014). Accumulation and distribution of ¹³⁷Cs and ⁹⁰Sr in the body of the wild boar (Sus scrofa) found on the territory with radioactive contamination. J Environ Radioact, 127, 171–175. [DOI] [PubMed] [Google Scholar]
17.Saito R, Nemoto Y, Tsukada H. (2020). Relationship between radiocaesium in muscle and physicochemical fractions of radiocaesium in the stomach of wild boar. Nature Sci Rep, 10:6796. doi: 10.1038/s41598-020-63507-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
18.Kouba F, Vernerová K, Šoch M, Hanzal V, Filásová L, Semerád Z, et al. (2022). Radiocaesium in wild boars in Novohradské (Gratzen) Mountains. Acta Vet BRNO, 91:087–097. doi: 10.2754/avb202291010087 [DOI] [Google Scholar]
19.Semizhon T, Putyrskaya V, Zibold G, Klemt E. (2009). Time-dependency of the ¹³⁷Cs contamination of wild boar from a region in Southern Germany in the years 1998 to 2008. J Environ Radioact, 100, 988–992. [DOI] [PubMed] [Google Scholar]
20.Tsukada H. (2021). Radiocaesium in the environment of Fukushima. Annals of the ICRP, 50 (1 suppl, 44–54. doi: 10.1177/01466453211006808 [DOI] [PubMed] [Google Scholar]
21.Endo S, Matsunami Y, Kajimoto T, Tanaka K, Suzuki M (2020). Internal exposure rate conversion coefficients and absorbed fractions of mouse for ¹³⁷Cs, ¹³⁴Cs and ⁹⁰Sr contamination in body. J Rad Res, 61 (4), 535–545. doi: 10.1093/jrr/rraa030 [DOI] [PMC free article] [PubMed] [Google Scholar]
22.VV AA. Il Monitoraggio Radiologico in Piemonte post Chernobyl (2013). ARPA PIEMONTE, pp. 13a.
23.http://www.arpa.piemonte.it/news/cinghiali-radioattivi-in-valsesia.-aggiornamento last accessed 29 april 2024.
24.Grande S, Risica S. (2015). Radionuclides in drinking water: the recent legislative requirements of the European Union. J Radiol Prot, 35, 1–19. doi: 10.1088/0952-4746/35/1/1 [DOI] [PubMed] [Google Scholar]
25.SAS Institute Inc. 2016. SAS/STAT^® 14.2 User’s Guide. Cary, NC: SAS Institute Inc.
26.Dohoo IR, Martin W, Stryhn H. 2012. Methods In Epidemiologic Research. Charlottetown, P.E.I.: VER, Inc., 890 pp. [Google Scholar]
27.VV AA. Monitoraggio straordinario dell’attività ambientale in Piemonte Anno 2013. ARPA PIEMONTE pp. 26b.
28.Stäger F, Zok D, Schiller AK, Feng B, Steinhauser G (2023). Disproportionately high contribution of 60 years old weapons-¹³⁷Cs explain the persistence of radioactive contamination in Bavarian wild boars. Environ Sci Technol 57, 13601–13611 doi: 10.1021/acs.est.3c03565 [DOI] [PMC free article] [PubMed] [Google Scholar]
29.Eissa F and E-Dein A (2023). Irradiated and radioactively contaminated foods: Analysis of EU RASFF notifications from 1997 to 2022. J Environ Radioact 270, 107315 doi: 10.1016/j.jenvrad.2023.107315 [DOI] [PubMed] [Google Scholar]
30.Saito R, Wakiyama Y, Bontrager H, Nanba K, Beasley JC (2023). Alteration of the Caesium-137 soil profile by wild boar rooting after the Fukushima Daiichi Nuclear Power Plant accident. Environmental Challenges 12, 100728 doi: 10.1016/j.envc.2023.100728 [DOI] [Google Scholar]
31.Yablokov A. (2013). A review and critical analysis of the “Effective Dose of radiation” concept. J Health Pollut, 3(5), 13–28. [Google Scholar]
32.Kocadag M, Exler V, Burger-Scheidlin C, Baumgartner A, Stietka M, Landstetter C, et al. (2017). Environmental radioactivity study of Austrian and Bavarian forest ecosystem: Long-term behavior of contamination of soil, vegetation and wild boar and its radioecological coherences. Appl Radiat Isot, 126, 106–111. [DOI] [PubMed] [Google Scholar]
33.Okada K, Sato I, Deguchi Y, Morita S, Yasue T, Yayota M, et al. (2013). Distribution of radioactive cesium in edible parts of cattle. Anim Sci J 84, 798–801. doi: 10.1111/asj.12075 [DOI] [PubMed] [Google Scholar]
34.Mamyrbayeva AS, Baigazinov ZA, Lukashenko SN, Panitskiy AV, Karatayev SS, Shatrov AN, et al. (2020). The trasfert of ²⁴¹Am and ¹³⁷Cs to the tissues of broilers’organs. PloS one, 15(7):e0235109. doi: 10.1371/journal.pone.0235109 [DOI] [PMC free article] [PubMed] [Google Scholar]
35.Isaksson M, Tondel M, Wålinder R, Rääf C (2021). Absorbed dose rate coefficients for ¹³⁴Cs and ¹³⁷Cs with steady-state distribution in the human body: S-coefficients revisited. J Rad Prot 41, 1213–1227 doi: 10.1088/1361-6498/ac2ec4 [DOI] [PubMed] [Google Scholar]
36.Baigazinov Z, Lukashenko S, Silybayeva B, Zharykbasova K, Bukabayeva Z, Muhamediarov N, et al. (2023). The transfer of ¹³⁷Cs and heavy metals to tissues within the organs of snails. Nature Scientific Reports 13:15690 doi: 10.1038/s41598-023-42580-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
37.VVAA (2010). Adult Reference Computational Phantoms, Annals of the International Commision on Radiological Protection, 39 (2), 170 pp. [Google Scholar]
38.Large MJ, Malaroda A, Petasecca M, Rosenfeld AB, Guatelli S (2020) Modelling ICRP110 Adult Reference Voxex Phantoms for dosimetric application: Development of a new Geant4 Advanced Example. J Pys: Conference Series 1662, 012021 doi: 10.1088/1742-6596/1662/1/012021 [DOI] [Google Scholar]
39.Reg CE 1375/2015 Commission Implementing Regulation (EU) 2015/1375 of 10 August 2015 laying down specific rules on official controls for Trichinella in meat. OJ L 212, 11.8.2015, p. 7–34 https://data.europa.eu/eli/reg_impl/2015/1375/oj. [Google Scholar]

PLoS One. 2024 May 9;19(5):e0303093. doi: 10.1371/journal.pone.0303093.r001

Author response to previous submission

8 Sep 2023

Attachment

Submitted filename: Answers To Reviewers 2023 09 07 variato.docx

pone.0303093.s003.docx^{(23KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0303093.r002

Decision Letter 0

Mohamad Syazwan Mohd Sanusi

20 Oct 2023

PONE-D-23-24864Radionuclide assessment in wild boars from Northwest Italy.PLOS ONE

Dear Dr. pattono,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Please submit your revised manuscript by Dec 04 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Mohamad Syazwan Mohd Sanusi

Academic Editor

PLOS ONE

Journal requirements:

When submitting your revision, we need you to address these additional requirements.

1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at

https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and

https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf

2. In your Data Availability statement, you have not specified where the minimal data set underlying the results described in your manuscript can be found. PLOS defines a study's minimal data set as the underlying data used to reach the conclusions drawn in the manuscript and any additional data required to replicate the reported study findings in their entirety. All PLOS journals require that the minimal data set be made fully available. For more information about our data policy, please see http://journals.plos.org/plosone/s/data-availability.

Upon re-submitting your revised manuscript, please upload your study’s minimal underlying data set as either Supporting Information files or to a stable, public repository and include the relevant URLs, DOIs, or accession numbers within your revised cover letter. For a list of acceptable repositories, please see http://journals.plos.org/plosone/s/data-availability#loc-recommended-repositories. Any potentially identifying patient information must be fully anonymized.

Important: If there are ethical or legal restrictions to sharing your data publicly, please explain these restrictions in detail. Please see our guidelines for more information on what we consider unacceptable restrictions to publicly sharing data: http://journals.plos.org/plosone/s/data-availability#loc-unacceptable-data-access-restrictions. Note that it is not acceptable for the authors to be the sole named individuals responsible for ensuring data access.

We will update your Data Availability statement to reflect the information you provide in your cover letter.

3. Please include a separate caption for each figure in your manuscript.

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

Reviewer #2: Yes

Reviewer #3: Yes

Reviewer #4: Partly

Reviewer #5: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: N/A

Reviewer #2: Yes

Reviewer #3: I Don't Know

Reviewer #4: I Don't Know

Reviewer #5: Yes

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

Reviewer #4: No

Reviewer #5: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

Reviewer #4: Yes

Reviewer #5: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Although the work is interesting, the manuscript requires serious modifications in several places before it can be recommended for publication in PLOS ONE.

• More investigations are needed to confirm the results and to fulfill the request for more data in order to achieve better 59 risk assessment.

• Language and sentence construction are another areas which need thorough improvement.

• The references cover the the past activities in the field. Particularly, results and discussion should be re-written in more details using current literatures.

• Figure 1 should be drawn as the graph linearly.

Reviewer #2: The manuscript titled "Radionuclide Assessment in Wild Boars from Northwest Italy" addresses the issue of radionuclide contamination in wild boars and its potential impact on human health. The study is conducted in the northwest regions of Italy, which have been affected by nuclear events, including the Chernobyl accident. Radionuclides, such as cesium-137 (137Cs), were detected in samples of wild boars hunted in the studied regions. The study highlights that radionuclide contamination can pose a threat to human health, whether from natural sources or anthropogenic sources like nuclear accidents. European Union regulations establish safe limits for radioactivity in food products, including wild boar meat, to ensure food safety. The manuscript examines the concentrations of 137Cs in the livers of wild boars collected from different regions and hunting seasons. The results reveal that, despite the detected contamination, the levels are below regulatory limits and therefore do not pose a significant concern for human health, especially considering the cooking of wild boar meat, which can reduce the effects of radionuclide contamination. Furthermore, the study emphasizes the importance of considering the age of the animals in contamination assessment, noting a negative correlation between the age of the animals and contamination levels.

This article provides a valuable contribution to the understanding of radionuclide contamination in wild boars in the northwest region of Italy. The results suggest that the contamination levels found are below established regulatory limits, which is reassuring from a food safety perspective. Additionally, the analysis of the correlation between age and contamination is an interesting and relevant finding for research. However, it is important to note that the sampling is limited in terms of sample size and the variety of organs analyzed. To obtain a more comprehensive and representative picture, further studies with larger samples and a comprehensive analysis of different organs would be beneficial. In summary, this article offers valuable insights into radionuclide contamination in wild boars, emphasizing the importance of food safety and the need to continue monitoring and assessing the risks associated with radioactive contamination in food.

After the review process that has already taken place, I am satisfied with the manuscript as it stands. My comments and suggestions have been addressed by the other reviewers, which has enriched the overall quality of the article. However, there are still some minor details that I would like to suggest the authors consider adding to make the study more comprehensive.

1) Firstly, it would be beneficial if the authors could provide a discussion of the practical implications of the findings (just one sentence). For example, they could discuss how the findings of this study may influence food safety policies related to wild boar meat in the northwest region of Italy and elsewhere. This would help readers better understand the real-world impact of these findings/importance of the study.

2) Furthermore, it would be helpful if the authors could briefly mention any limitations of the study, such as sampling constraints or uncertainties associated with radioactivity measurement methods (Methods section). Acknowledging these limitations would provide a more complete and honest view of the work.

3) In addiction, given the relevance of the results to food safety, the authors may want to highlight some practical guidelines or recommendations for hunters, regulators, or consumers based on the study's findings.

4) The sentence "In our opinion" appears three times in the text. One of those would be better replaced with "In our point of view". That would make the manuscript more clearear.

5)Lately, I suggest inserting an image/map of Italy and the two valleys of the sampling place (Chisone/Germanasca and the Pellice Valley). This would be great to localize the readers (Line 159-161).

These additional suggestions would further strengthen the article and make it more informative and applicable to the scientific community and those interested in food safety and the management of radionuclide contamination in game products.

Reviewer #3: This paper presents a critical evaluation of the article titled "Radionuclide assessment in wild boars from Northwest Italy". The article under scrutiny addresses a significant issue and offers valuable insights. Upon careful examination, it is determined that the overall assessment of this manuscript is accept, with only minor revisions required.

The abstract is excessively lengthy, comprising nearly 400 words and consisting of 24 lines in font size 11. It is advisable to condense and enhance its focus and precision on the study's outcomes.

The statistical analysis is perplexing, as I am unacquainted with the referenced statistical models. It would be advantageous to provide a concise explanation of the methodologies employed, in order to furnish the readers with insights into understanding the statistical analysis.

The presentation of the results lacks precision and should be more comprehensive. Additionally, if the authors opt to integrate the results with the discussion, it is imperative that they thoroughly analyze each result subsequent to its reporting.

The conclusion fails to effectively summarize the findings; rather, it appears to serve as a set of recommendations. Consequently, it is recommended that the conclusion be revised to recommendations. which are highly valuable and significant for future research endeavors.

Finally, the manuscript needs to be edited by a native English speaker to enhance its clarity and fluency.

Reviewer #4: The data presented in the article is interesting to read. However, I have some additional remarks and comments that are necessary:

1) Showing statistical analyses is important, but it is necessary to see the initial data as well. Please provide supplementary activity concentrations of Cs-137 in organs for both seasons. Additionally, please specify whether the data is for dry or fresh weight.

2) The paper would be more complete if data for activity concentrations in fecal samples were available. This would provide some idea of the activity concentration range in organs.

3) It would be interesting to see any data describing soil contamination or radioactive fallout in Northwest Italy.

4) High activity concentration can be simply described by considering different equilibrium times for Cs-137 in different organs. You can refer to any classical book for more information on this topic.

I hope you find these suggestions helpful for improving your article.

Best regards,

Reviewer #5: Dear Authors

Based on the replies to previous comments, the quality of the article has improved

The article contains interesting data for the scientific community.

however, the title of the article is misleading as only Cs-137 ( Cs-134) was measured in the publication and not the other radionuclides ( and the concentrations of the other radionuclides were not assessed) .

I suggest a clarification of the title of the article.

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: Yes: Sérgio José Gonçalves Jr.

Reviewer #3: No

Reviewer #4: No

Reviewer #5: No

**********

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

PLoS One. 2024 May 9;19(5):e0303093. doi: 10.1371/journal.pone.0303093.r003

Author response to Decision Letter 0

12 Dec 2023

Dear Editor and Reviewers,

thank you so much for the time you have dedicated to our manuscript. We agree that in the previous version of the manuscript, there were important concerns to resolve, and we truly thank you and the editorial office for the opportunity to answer to all the concerns raised by you and by the referees.

The answers are written in red, whereas the changes in the manuscript are highlighted in yellow Enclosed here, you find all the changes and the additions we made to answer the questions raised for the revision process.

We have revised our manuscript for English quality by a native English speaker. We attached here the certificate of the language revision.

Reviewer #1: Although the work is interesting, the manuscript requires serious modifications in several places before it can be recommended for publication in PLOS ONE.

• More investigations are needed to confirm the results and to fulfill the request for more data in order to achieve better 59 risk assessment.

Answer:

However, more sampling is needed for a complete risk assessment. Our data can be an objective starting point for a new sampling campaign. Data were not available for these valleys, especially liver samples, as stated by Ferri et al. (2017). In our opinion, our paper adds useful information to the current knowledge to improve more specific designs for risk assessment and therefore achieve better surveillance campaigns. Our intention is to continue to test for radionuclide pollution in wild species considering the important suggestion given by the reviewer

Language and sentence construction are other areas which need thorough improvement.

Answer:

The paper has been reviewed by a native English speaker, the certificate is attached.

From the revision agency “Your document was edited for correct English language, grammar, punctuation, and phrasing. In addition, we have made some changes to ensure consistency throughout the document. These changes are based on our extensive knowledge of what journals typically require.”

• The references cover the past activities in the field. Particularly, results and discussion should be re-written in more details using current literatures.

Answer:

New paragraphs and new considerations have been added to the sections (Page 6 from line 126 to line 127, from Page 11 line 251 to Page 12 line 272, Page 14 from line 311 to line 313, Page 16 from line 351 to line 357, Page 16 from line 364 to line 365, Page 16 from line 366 to Page 17 line 384).

Stäger F, Zok D, Schiller AK, Feng B, Steinhauser G (2023). Disproportionately high contribution of 60 years old weapons-137Cs explain the persistence of radioactive contamination in Bavarian wild boars. Environ Sci technol 57, 13601-13611 http://doi.org/10121/acs.est3c03565

Endo S, Matsunami Y, Kajimoto T, Tanaka K, Suzuki M (2020). Internal exposure rate conversion coefficients and absorbed fraciont of mouse for 137Cs, 134Cs and 90Sr contamination in body. J Rad Res, 61 (4), 535-545. Doi:10.1093/jrr/rraa030

Mamyrbayeva AS, Baigazinov ZA, Lukashenko SN, Panitskiy AV, Karatayev SS, Shatrov AN, et al (2020). The trasfert of 241Am and 137Cs to the tissues of broilers’organs. PloS ONE, 15(7):e0235109. https://doi.org/10.1371/journal.pone.0235109

Baigazinov Z, Lukashenko S, Silybayeva B, Zharykbasova K, Bukabayeva Z, Muhamediarov N, et al (2023). The transfer of 137Cs and heavy metals to tissues within the organs of snails. Nature 13:15690 https://doi.org/10.1038/s41598-023-42580-6

Eissa F and E-Dein A (2023). Irradiated and radioactively contaminated foods: Analysis of EU RASFF notifications from 10097 to 2022. J Environ Radioact 270, 107315 https://doi.org/10.1016/j.envrad.2023.107315

Saito R, Wakiyama Y, Bontrager H, Nanba K, Beasley JC (2023). Alteration of the Caesium-137 soil profile by wild boar rooting after the Fukushima Daiichi Nuclear Power Plant accident. Environmental Challenges 12, 100728 http://doi.org/10.1016/j.envc.2023.100728

Isaksson M, Tondel M, Wålinder R, Rääf C (2021). Absorbed dose rate coefficients for 134 Cs and 137Cs with steady-state distribution in the human body: S-coefficients revisited. J Rad Prot 41, 1213-1227 https://doi.org/10.1088/1361-6498/ac2ec4

• Figure 1 should be drawn as the graph linearly.

Answer:

Figure n. 1 has been revised, and a more linear order has been signed for the samples.

Answer:

Requested suggestions have been added to the text (Page 6 from line 115 to line 118 and Page 18 from line 400 to line 404).

This fact means that hunter families and a wide number of consumers can be at risk of exposure to radionuclide contamination, and health problems must be considered a consequence of this environmental pollution.

Answer:

We are aware of the limitation of the number of samples obtained and of the number of analyses conducted. The results support new sampling with a more specific design considering wild boars and other local wild species and can be useful for analyzing liver contamination (Ferri et al., 2017). The requested suggestions have been added to the text and more specific indications have been added to the methods section about measurements as requested by the reviewer (Page 8 from line 173 to line 175 and Page 8 from line 180 to Page 9 line 187, Page 17 from line 384 to line 385, Page 18 from line 406 to line 407).

134Cs and 137Cs radioactivity was determined by gamma-spectrometric measurements performed by an accredited laboratory using an HPGe detector (Ortec) with a relative efficiency of 50%.

The calibration of the instrument/geometry was performed with a 100 cc certified multigamma source, and the Monte Carlo software EFFTRAN was used to evaluate the efficiency transfer due to the density and volume differences between the calibration source and the samples. All contributions to the uncertainty were considered: counting, gamma emission, efficiency, efficiency transfer, repeatability, and instrumental stability.

different matrices such soil, food material and feces are needed

Answer:

Requested suggestions have been added to the text (Page 13 from line 281 to line 285, Page 17 from line 382 to line 385, Page 18 from line 400 to line 404 and Page 18 from line 413 to Page 19 line 420).

the rate of consumption and consequently the health-related risk is to eat cooked meat instead of raw meat preparations (salami or raw meat dishes) because meat is usually consumed cooked and the cooking process appears to decrease the effects of radionuclide contamination in food [11].

The information gathered about Cs 137 contamination can help consumers and producers to a safer consumption of this kind of meat (e.g., cooking it or using it for cooked products instead of raw fermented products such as salami, raw ham or tartare or exclusion of edible organs). Moreover, hunters might have available safer and more reliable instructions given by authorities for hunting campaigns (e.g., young animals can be more useful for assessment and surveillance).

4) The sentence "In our opinion" appears three times in the text. One of those would be better replaced with "In our point of view". That would make the manuscript clearer.

Answer:

The sentence has been rewritten as requested (Page 16 line 354).

From our point of view, this can

5)Lately, I suggest inserting an image/map of Italy and the two valleys of the sampling place (Chisone/Germanasca and the Pellice Valley). This would be great to localize the readers (Line 159-161).

Answer:

A map of Valleys and north Italy has been attached in the paper (Fig. n. 1 Page 7 line 148 and a new numeration for Fig. n. 2 at Page 14 line 315).

The abstract is excessively lengthy, comprising nearly 400 words and consisting of 24 lines in font size 11. It is advisable to condense and enhance its focus and precision on the study's outcomes.

Answer:

The abstract has been rewritten in a shorter way (from Page 2 line 23 to Page 3 line 50).

Answer:

An explanation has been added to help readers better comprehend the statistical methods used (Page 10 line 209 to line 222). A new reference has been added at Page 23 from line 526 to line 528.

A linear mixed statistical model [25] was used to estimate the association between the tested organ, age group, and sex of wild boar and logCs. The effects of these predictors were included in the model as fixed, as in a linear regression. We also considered that there might be variations in logCs across wild boars. Furthermore, measurements, which we made on different organs belonging to the same 16 animals, were not independent. This needs to be taken into account in the statistical analysis. Since there was no interest in comparing specific individuals, between-wild boar variation was included in the model as a random effect [26]. Age group by tested organ interaction terms was included to test whether the association between organs and logCs differed across age groups. Statistical significance was fixed at the 0.05 level.

Dohoo, Ian Robert, S. Wayne Martin, and Henrik Stryhn. 2012. Methods In Epidemiologic Research. Charlottetown, P.E.I.: VER, Inc.

Answer:

More parts have been added in order to be more precise and comprehensive (Page 11 line 245, Page 11 from line 251 to Page 12 line 272, Page 13 from line 281 to line 287, Page 13 from line 295 to line 298, Page 14 from line 304 to line 305, Page 14 from line 313 to Page 15 line 343).

Answer:

The conclusions have been rewritten following the suggestions of the reviewer. We added paragraphs to summarize the results of the present paper. In the conclusions Page 18 from line 400 to line 404.

Finally, the manuscript needs to be edited by a native English speaker to enhance its clarity and fluency.

Answer:

The paper has been reviewed by a native English speaker, the certificate is attached.

Reviewer #4: The data presen

Attachment

Submitted filename: Response to reviewers PONE-D-23-24864.doc

pone.0303093.s004.doc^{(192KB, doc)}

PLoS One. doi: 10.1371/journal.pone.0303093.r004

Decision Letter 1

Mohamad Syazwan Mohd Sanusi

6 Mar 2024

PONE-D-23-24864R1137Cesium (137Cs) assessment in wild boars from northwestern ItalyPLOS ONE

Dear Dr. pattono,

Please submit your revised manuscript by Apr 20 2024 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

We look forward to receiving your revised manuscript.

Kind regards,

Mohamad Syazwan Mohd Sanusi

Academic Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Additional Editor Comments:

Decision: Minor Revision

General Comments: The title of the work, "137Cesium (137Cs) assessment in wild boars from northwestern Italy," is worthy of study. The proposed method, with large samplings and targeted organ samples of the wild boars (48 for liver and 16 samples for each of the 5 types of samples), is technically sound. The method is sufficient, and the qualitative analysis approach investigating the correlation between Cs levels and age, and different types of tissue organs, seems appropriate in the field of radioecology. However, the manuscript's results and discussion are difficult to follow, especially when the author mixes up the results and discussion.

(1) Therefore, it is suggested that the author separate the results and discussion to make it easier and more comprehensible for readers to follow.

(2) The presentation of the results also seems insufficient. As most of the results are not directly presented in a table and mostly discussed in the text, I suggest the author add one table of descriptive statistics (n, mean +/- standard error, confidence intervals for mean, min-max) for each category (types of organs, year of collection, age, sex).

(3) In the discussion, I would like the author to add the point that Cs-137 tends to show high accumulation in muscle due to its high potassium K content. Cesium (Cs) and Potassium (K) have some similarities in their biodynamic patterns because they belong to the same group in the periodic table, Group 1 (alkali metals), and due to the fact that muscle tissue, such as skeletal muscles, contain significant amounts of potassium for metabolic functions. Similar to Sr-90 and calcium (Ca). This seems to correlate with the findings of the work where muscle (diaphragm and tongue) show high activities. Please cite this using appropriate references as well as ICRP Publication 110 Realistic reference phantoms.

Specific Comments:

Keywords: Keywords are crucial for increasing the visibility of the article and guiding readers. Consider including terms such as "Cesium 137-contaminated wild boar," "Cs-137 contaminated animal organ," "Cs-137 in Sus Scrofa," "wild boar radioactive bioindicator," and "North-western Italy Cesium-contamination."

Abstract: Limited values of results are given as most of the results are discussed. Add important values of the obtained results, e.g., mean, min-max based on different organ sites. This is important as the abstract needs to reflect the title, i.e., Cs in wild boar, but none of the Cs activity values are presented. Add a brief line about the main instrument used in this work. All approaches and methods are well described. Discussion and conclusion are sufficient.

Introduction: Revise the introduction to reflect the revised title and aim of the study.

Study Site: Revise the map in Fig. 1. Please title the countries in the map.

Line 177 - please elaborate on the process of homogenization. What matrix of the sample was obtained in this work? Is it in wet weight?

Line 229 - define ARPA, as it is missing in affiliation and not all readers recognize Agenzia Regionale per la Protezione dell'Ambiente.

Line 252-258 - metric SI prefix for (10^3) k or K?

Line 233 - superscript m^2

Line 245 - "Bq/k" does not appear to be a standard unit for specific activity, and it may be a typographical error.

Line 296 - p significant symbol. Sometimes you use small "p" and sometimes you use capital "P." Please be consistent.

Line 319 - sometimes "137Cs," sometimes "137^Cs," be consistent.

Fig. 2 missing unit on the y-axis.

Supplementary materials 1 & 2 - revise the title of each column. Typos and capital/small letter issues. The symbol for kilogram is "kg," not "Kg."

That's all.

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #3: All comments have been addressed

Reviewer #5: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #3: Yes

Reviewer #5: (No Response)

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #3: I Don't Know

Reviewer #5: (No Response)

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #3: Yes

Reviewer #5: (No Response)

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #3: Yes

Reviewer #5: (No Response)

**********

6. Review Comments to the Author

Reviewer #3: (No Response)

Reviewer #5: (No Response)

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #3: No

Reviewer #5: Yes: Tibor Kovacs

**********

PLoS One. 2024 May 9;19(5):e0303093. doi: 10.1371/journal.pone.0303093.r005

Author response to Decision Letter 1

12 Apr 2024

Dear Editors and Reviewers,

We would like to submit the manuscript entitled “137Cesium (137Cs) assessment in wild boars from northwestern Italy.” Pattono, D., Mannelli, A., Dalmasso A., Orusa, R., Faure Ragani, M., & Bottero M.T. for possible publication in Plos ONE.

We believe that the paper fits the aims and scope of the Journal. Indeed, it is an original article based on a survey of radionuclide contamination in two valley districts in Piemonte (Italy) caused by the Chernobyl and Fukushima nuclear power plant accidents. In particular, the study supplies the data missing on wild boar contamination, as needed by EU directives, and provides some insights into the distribution of radionuclide contamination across different organs in the body.

Briefly, the aim of the study was to provide data on 137Cs contamination in two valley districts in the Piedmont by sampling wild boars hunted for human consumption in two different years (2014 and 2016). The results indicate very low contamination levels in the two valleys studied compared with other valleys in the Piedmont. Moreover, the distribution of 137Cs between organs obtained from the same animal differed according to the age of the animal, with greater differences in younger animals. The diaphragm was the organ showing the highest levels of Cs137.

In conclusion, our analysis shows the lack of any significant risk of radionuclide contamination associated with the consumption of wild boar meat hunted in these valley districts. Moreover, the data indicate muscle, specifically the diaphragm, to be the most useful and convenient for sampling considering that this organ is already routinely collected by hunters for trichinellosis surveillance. Last, samples from younger animals may be more indicative for assessing the risk of meat consumption to human health associated with nuclear accidents, although further data will be needed to confirm this finding.

We would like to thank the Editor and the Reviewers for their comments, which have helped us to elevate the quality of our work.

For us, it is a great opportunity to improve the content, clarity and style of our work according to the comments provided by them. We have answered every concern point by point, and the file is enclosed in the submission page.

We uploaded the revised version of the manuscript on the submission page of the journal.

In accordance with the suggestions and comments of the Reviewers, the main changes we have made are as follows:

- Results and Discussion have been separated in order to improve comprehension and make easier for the reader to follow as requested by Reviewer 3;

- Tables of descriptive statistics has been added (Table n. 2 and n. 3) or modified (Table n. 1) as requested by reviewer 3;

- In the discussion we added a point stressing that 137Cesium belongs to the same periodic table’s group of potassium (K). This fact, as suggested by reviewer 3, can easily explain why muscle sites show high accumulation rates. For this reason, two more references have been cited in the text and added in the reference list. We thank the reviewer for this important suggestion;

- The keywords have been replaced with the suggested ones;

- Abstract: The abstract has been rewritten. We added more results and a new line about the instruments used for the cesium quantification as requested by Reviewer 3;

- Introduction: a paragraph has been added, as suggested by the reviewer 3, to improve the quality of the section and to be more linked to the aim of the work;

- The map has been revised and we added the name of the countries;

- The homogenization process was rewritten accordingly to the reviewer’s 3 suggestion;

- Here and in other parts of the paper we reported ARPA as Agenzia Regionale per la Protezione dell’Ambiente;

- We revised the metric prefix- We wrote in the corrected form the m^2;

- We wrote in the correct form “Bq/kg”;

- P symbol was corrected and unified throughout all the text

- 137Cesium was unified throughout all the text

- Fig. 2 unit was added on the y-axis

- In Supplementary Material 1 & 2 the titles have been corrected.

We confirm that neither the manuscript nor any parts of its content are currently under consideration or published in another journal. All authors have approved the manuscript and agree with its submission to Plos ONE. All figures and tables were produced by the authors. Last, all authors declare no conflicting interests.

In the hope that the manuscript fulfils the scientific standards of Plos ONE all the requests of the reviewers,

yours sincerely,

Daniele Pattono and coauthors

Attachment

Submitted filename: Manuscript PONE-D-23-24864R Response to reviewers 2024 04 11.doc

pone.0303093.s005.doc^{(185.5KB, doc)}

PLoS One. doi: 10.1371/journal.pone.0303093.r006

Decision Letter 2

Mohamad Syazwan Mohd Sanusi

18 Apr 2024

137Cesium (137Cs) assessment in wild boars from northwestern Italy

PONE-D-23-24864R2

Dear Dr. Pattono,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice will be generated when your article is formally accepted. Please note, if your institution has a publishing partnership with PLOS and your article meets the relevant criteria, all or part of your publication costs will be covered. Please make sure your user information is up-to-date by logging into Editorial Manager at Editorial Manager® and clicking the ‘Update My Information' link at the top of the page. If you have any questions relating to publication charges, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Mohamad Syazwan Mohd Sanusi

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

PLoS One. doi: 10.1371/journal.pone.0303093.r007

Acceptance letter

Mohamad Syazwan Mohd Sanusi

25 Apr 2024

PONE-D-23-24864R2

PLOS ONE

Dear Dr. pattono,

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team.

At this stage, our production department will prepare your paper for publication. This includes ensuring the following:

* All references, tables, and figures are properly cited

* All relevant supporting information is included in the manuscript submission,

* There are no issues that prevent the paper from being properly typeset

If revisions are needed, the production department will contact you directly to resolve them. If no revisions are needed, you will receive an email when the publication date has been set. At this time, we do not offer pre-publication proofs to authors during production of the accepted work. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few weeks to review your paper and let you know the next and final steps.

Lastly, if your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

If we can help with anything else, please email us at customercare@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Mohamad Syazwan Mohd Sanusi

Academic Editor

PLOS ONE

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 Table. First-year sampling data.

(XLS)

pone.0303093.s001.xls^{(45KB, xls)}

S2 Table. Second-year sampling data.

(XLS)

pone.0303093.s002.xls^{(62.5KB, xls)}

Attachment

Submitted filename: Answers To Reviewers 2023 09 07 variato.docx

pone.0303093.s003.docx^{(23KB, docx)}

Attachment

Submitted filename: Response to reviewers PONE-D-23-24864.doc

pone.0303093.s004.doc^{(192KB, doc)}

Attachment

Submitted filename: Manuscript PONE-D-23-24864R Response to reviewers 2024 04 11.doc

pone.0303093.s005.doc^{(185.5KB, doc)}

Data Availability Statement

All relevant data are within the paper and its Supporting information files.

[pone.0303093.ref001] 1.Ferri M, Baldi L, Cavallo S, Pellicanò R, Brambilla G. (2017). Wild game consumption habits among Italian shooters: relevance for intakes of cadmium, perfluorooctanesulphonic acid and ¹³⁷Cesium as priority contaminants. Food Addit Contam Part A, 34 (5), 832–841, doi: 10.1080/19440049.2017.1293303 [DOI] [PubMed] [Google Scholar]

[pone.0303093.ref002] 2.Aliyu AS, Evangeliou N, Mousseau TA, Wu J, Ramli AT. (2015). An overview of current knowledge concerning the health and environmental consequences of the Fukushima Daiichi Nuclear Power Plant (FDNPP) accident. Environ Internat 85, 213–228. doi: 10.1016/j.envint.2015.09.020 [DOI] [PubMed] [Google Scholar]

[pone.0303093.ref003] 3.Vetikko V, Kostantiainen E. (2013). Assessment of doses to game animals in Finland. J Enviro Radioact, 125, 69–73. doi: 10.1016/j.jenvrad.2013.01.014 [DOI] [PubMed] [Google Scholar]

[pone.0303093.ref004] 4.Nakamura K, Chiba S, Kiuchi T, Nabeshi H, Tsutsumi T, Akiyama H, et al. (2022). Comprehensive analysis of a decade of cumulative radiocesium testing data for foodstuff throughout Japan after the 2011 Fukushima Daiichi Nuclear Power Plant accident. PloS one 17(9): e0274070. doi: 10.1371/journal.pone.0274070 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0303093.ref005] 5.Oloś G, Dolhańczuk-Śródka A. (2022) Effective and environmental half-lives of radiocesium in game from Poland. Journal of Environmental radioactivity, 248, 106870. doi: 10.1016/j.jenvrad.2022.106870 [DOI] [PubMed] [Google Scholar]

[pone.0303093.ref006] 6.Merz S, Shozugawa K, Steinhauser S. (2015). Analysis of Japanese Radionuclide Monitoring Data of Food Before and After the Fukushima Nuclear Accident. Environ Sci Technol, 49, 2875–2855. doi: 10.1021/es5057648 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0303093.ref007] 7.Janssens A, Necheva C, Tanner V, Turai I. (2013). The New Basic Standards Directive and its implications for environmental monitoring. J Environ Radioact, 125, 99–104. [DOI] [PubMed] [Google Scholar]

[pone.0303093.ref008] 8.Piñero-García F, Thomas R, Mantero J, Forssell-Aronsson E, Isaksson M. (2022). Concentration of radionuclides in Swedish market basket and its radiological implications. Food Control, 133, 108658. doi: 10.1016/j.foodcont.2021.108658 [DOI] [Google Scholar]

[pone.0303093.ref009] 9.Meisenberg O, Gerstmann UC. (2021). Exposure of german hunters and their family members to the radioactive nuclide ¹³⁷Cs due to their eating habits. Sci Total Environ, 798, 149264. doi: 10.1016/j.scitotenv.2021.149264 [DOI] [PubMed] [Google Scholar]

[pone.0303093.ref010] 10.Aono T, Yoshida S, Akashi M. (2016). Initial and present situation of food contamination in Japan after the accident at the Fukushima Dai-Chi nuclear power plant. Radiat Prot Dosimetry 171, 14–19. [DOI] [PubMed] [Google Scholar]

[pone.0303093.ref011] 11.Caridi F, D’Agostino M, Belvedere A. (2020). Radioactivity in Calabrian (Southern Italy) Wild Boar Meat. Appl Sci, 10, 3580, doi: 10.3390/app10103580 [DOI] [Google Scholar]

[pone.0303093.ref012] 12.Nemoto Y, Saito R, Oomachi H. (2018). Seasonal variation of Cesium -137 concentration in Asian black bear (Ursus thibetanus and wild boar (Sus scrofa) in Fukushima Prefecture, Japan. PLoS ONE 13(7): e0200797. doi: 10.1371/journal.pone.0200797 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0303093.ref013] 13.Noelia Barros-Garcia M, Ballari SA. (2012). Impact of wild boar (Sus scrofa) in its introduced and native range: a review. Biol Invasions 14, 2283–2300. [Google Scholar]

[pone.0303093.ref014] 14.Steinhauser G, Saey PRJ. (2016). ¹³⁷Cs in the meat of wild boars. A comparison of the impacts of Chernobyl and Fukushima. J Radioanal Nucl Ch 307, 1801–1806. doi: 10.1007/s10967-015-4417-6 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0303093.ref015] 15.Dvořák P, Snášel P, Beňová K. (2010). Transfert of radiocesium into Wild Boar Meat. Acta Vet BRNO, 79, S85–S91. [Google Scholar]

[pone.0303093.ref016] 16.Gulakov AV. (2014). Accumulation and distribution of ¹³⁷Cs and ⁹⁰Sr in the body of the wild boar (Sus scrofa) found on the territory with radioactive contamination. J Environ Radioact, 127, 171–175. [DOI] [PubMed] [Google Scholar]

[pone.0303093.ref017] 17.Saito R, Nemoto Y, Tsukada H. (2020). Relationship between radiocaesium in muscle and physicochemical fractions of radiocaesium in the stomach of wild boar. Nature Sci Rep, 10:6796. doi: 10.1038/s41598-020-63507-5 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0303093.ref018] 18.Kouba F, Vernerová K, Šoch M, Hanzal V, Filásová L, Semerád Z, et al. (2022). Radiocaesium in wild boars in Novohradské (Gratzen) Mountains. Acta Vet BRNO, 91:087–097. doi: 10.2754/avb202291010087 [DOI] [Google Scholar]

[pone.0303093.ref019] 19.Semizhon T, Putyrskaya V, Zibold G, Klemt E. (2009). Time-dependency of the ¹³⁷Cs contamination of wild boar from a region in Southern Germany in the years 1998 to 2008. J Environ Radioact, 100, 988–992. [DOI] [PubMed] [Google Scholar]

[pone.0303093.ref020] 20.Tsukada H. (2021). Radiocaesium in the environment of Fukushima. Annals of the ICRP, 50 (1 suppl, 44–54. doi: 10.1177/01466453211006808 [DOI] [PubMed] [Google Scholar]

[pone.0303093.ref021] 21.Endo S, Matsunami Y, Kajimoto T, Tanaka K, Suzuki M (2020). Internal exposure rate conversion coefficients and absorbed fractions of mouse for ¹³⁷Cs, ¹³⁴Cs and ⁹⁰Sr contamination in body. J Rad Res, 61 (4), 535–545. doi: 10.1093/jrr/rraa030 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0303093.ref022] 22.VV AA. Il Monitoraggio Radiologico in Piemonte post Chernobyl (2013). ARPA PIEMONTE, pp. 13a.

[pone.0303093.ref023] 23.http://www.arpa.piemonte.it/news/cinghiali-radioattivi-in-valsesia.-aggiornamento last accessed 29 april 2024.

[pone.0303093.ref024] 24.Grande S, Risica S. (2015). Radionuclides in drinking water: the recent legislative requirements of the European Union. J Radiol Prot, 35, 1–19. doi: 10.1088/0952-4746/35/1/1 [DOI] [PubMed] [Google Scholar]

[pone.0303093.ref025] 25.SAS Institute Inc. 2016. SAS/STAT^® 14.2 User’s Guide. Cary, NC: SAS Institute Inc.

[pone.0303093.ref026] 26.Dohoo IR, Martin W, Stryhn H. 2012. Methods In Epidemiologic Research. Charlottetown, P.E.I.: VER, Inc., 890 pp. [Google Scholar]

[pone.0303093.ref027] 27.VV AA. Monitoraggio straordinario dell’attività ambientale in Piemonte Anno 2013. ARPA PIEMONTE pp. 26b.

[pone.0303093.ref028] 28.Stäger F, Zok D, Schiller AK, Feng B, Steinhauser G (2023). Disproportionately high contribution of 60 years old weapons-¹³⁷Cs explain the persistence of radioactive contamination in Bavarian wild boars. Environ Sci Technol 57, 13601–13611 doi: 10.1021/acs.est.3c03565 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0303093.ref029] 29.Eissa F and E-Dein A (2023). Irradiated and radioactively contaminated foods: Analysis of EU RASFF notifications from 1997 to 2022. J Environ Radioact 270, 107315 doi: 10.1016/j.jenvrad.2023.107315 [DOI] [PubMed] [Google Scholar]

[pone.0303093.ref030] 30.Saito R, Wakiyama Y, Bontrager H, Nanba K, Beasley JC (2023). Alteration of the Caesium-137 soil profile by wild boar rooting after the Fukushima Daiichi Nuclear Power Plant accident. Environmental Challenges 12, 100728 doi: 10.1016/j.envc.2023.100728 [DOI] [Google Scholar]

[pone.0303093.ref031] 31.Yablokov A. (2013). A review and critical analysis of the “Effective Dose of radiation” concept. J Health Pollut, 3(5), 13–28. [Google Scholar]

[pone.0303093.ref032] 32.Kocadag M, Exler V, Burger-Scheidlin C, Baumgartner A, Stietka M, Landstetter C, et al. (2017). Environmental radioactivity study of Austrian and Bavarian forest ecosystem: Long-term behavior of contamination of soil, vegetation and wild boar and its radioecological coherences. Appl Radiat Isot, 126, 106–111. [DOI] [PubMed] [Google Scholar]

[pone.0303093.ref033] 33.Okada K, Sato I, Deguchi Y, Morita S, Yasue T, Yayota M, et al. (2013). Distribution of radioactive cesium in edible parts of cattle. Anim Sci J 84, 798–801. doi: 10.1111/asj.12075 [DOI] [PubMed] [Google Scholar]

[pone.0303093.ref034] 34.Mamyrbayeva AS, Baigazinov ZA, Lukashenko SN, Panitskiy AV, Karatayev SS, Shatrov AN, et al. (2020). The trasfert of ²⁴¹Am and ¹³⁷Cs to the tissues of broilers’organs. PloS one, 15(7):e0235109. doi: 10.1371/journal.pone.0235109 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0303093.ref035] 35.Isaksson M, Tondel M, Wålinder R, Rääf C (2021). Absorbed dose rate coefficients for ¹³⁴Cs and ¹³⁷Cs with steady-state distribution in the human body: S-coefficients revisited. J Rad Prot 41, 1213–1227 doi: 10.1088/1361-6498/ac2ec4 [DOI] [PubMed] [Google Scholar]

[pone.0303093.ref036] 36.Baigazinov Z, Lukashenko S, Silybayeva B, Zharykbasova K, Bukabayeva Z, Muhamediarov N, et al. (2023). The transfer of ¹³⁷Cs and heavy metals to tissues within the organs of snails. Nature Scientific Reports 13:15690 doi: 10.1038/s41598-023-42580-6 [DOI] [PMC free article] [PubMed] [Google Scholar]

[pone.0303093.ref037] 37.VVAA (2010). Adult Reference Computational Phantoms, Annals of the International Commision on Radiological Protection, 39 (2), 170 pp. [Google Scholar]

[pone.0303093.ref038] 38.Large MJ, Malaroda A, Petasecca M, Rosenfeld AB, Guatelli S (2020) Modelling ICRP110 Adult Reference Voxex Phantoms for dosimetric application: Development of a new Geant4 Advanced Example. J Pys: Conference Series 1662, 012021 doi: 10.1088/1742-6596/1662/1/012021 [DOI] [Google Scholar]

[pone.0303093.ref039] 39.Reg CE 1375/2015 Commission Implementing Regulation (EU) 2015/1375 of 10 August 2015 laying down specific rules on official controls for Trichinella in meat. OJ L 212, 11.8.2015, p. 7–34 https://data.europa.eu/eli/reg_impl/2015/1375/oj. [Google Scholar]

PERMALINK

137Cesium (137Cs) assessment in wild boars from northwestern Italy

Daniele Pattono

Alessandro Mannelli

Alessandra Dalmasso

Riccardo Orusa

Massimo Faure Ragani

Maria Teresa Bottero

Roles

Abstract

Introduction

Fig 1. Map of Chisone/Gremanasca and Pellice Valleys (Northwest Italy).

Material and methods

Statistical analysis

Results

Table 1. Radioactivity levels of 137Cesium (137Cs, Bq/kg) in liver of 48 wild boars during the first sampling season (2014) in Chisone/Germanasca and Pellice Valleys, by age class and sex.

Table 2. Radioactivity levels of 137Cesium (137Cs, Bq/kg) in 16 wild boars, in tongue, diaphragm, liver, spleen (results from all organs combined), during the second sampling season in Pellice Valley, 2016 by age class and sex.

Table 3. Radioactivity levels of 137Cesium (137Cs, Bq/kg) in different anatomical sites of 16 wild boars during the second sampling season in Pellice Valley, 2016.

Fig 2. Concentration of 137Cesium (137Cs) in different organs from wild boars in northern Italy in 2016.

Table 4. Results of a mixed linear statistical model of the association between tested organ, age group, and the natural log of 137Cs (log137Cs), in wild boars in Italy, in 2016.

Discussion

Conclusions

Supporting information

Acknowledgments

Data Availability

Funding Statement

References

Author response to previous submission

Decision Letter 0

Mohamad Syazwan Mohd Sanusi

Roles

Author response to Decision Letter 0

Decision Letter 1

Mohamad Syazwan Mohd Sanusi

Roles

Author response to Decision Letter 1

Decision Letter 2

Mohamad Syazwan Mohd Sanusi

Roles

Acceptance letter

Mohamad Syazwan Mohd Sanusi

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

Similar articles

Cited by other articles

Links to NCBI Databases

¹³⁷Cesium (¹³⁷Cs) assessment in wild boars from northwestern Italy

Table 1. Radioactivity levels of ¹³⁷Cesium (¹³⁷Cs, Bq/kg) in liver of 48 wild boars during the first sampling season (2014) in Chisone/Germanasca and Pellice Valleys, by age class and sex.

Table 2. Radioactivity levels of ¹³⁷Cesium (¹³⁷Cs, Bq/kg) in 16 wild boars, in tongue, diaphragm, liver, spleen (results from all organs combined), during the second sampling season in Pellice Valley, 2016 by age class and sex.

Table 3. Radioactivity levels of ¹³⁷Cesium (¹³⁷Cs, Bq/kg) in different anatomical sites of 16 wild boars during the second sampling season in Pellice Valley, 2016.

Fig 2. Concentration of ¹³⁷Cesium (¹³⁷Cs) in different organs from wild boars in northern Italy in 2016.

Table 4. Results of a mixed linear statistical model of the association between tested organ, age group, and the natural log of ¹³⁷Cs (log¹³⁷Cs), in wild boars in Italy, in 2016.