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Article

Bee Products as a Bioindicator of Radionuclide Contamination: Environmental Approach and Health Risk Evaluation

Faculty of Energy and Fuels, AGH University of Krakow, Al. Mickiewicza 30, 30-059 Krakow, Poland
*
Author to whom correspondence should be addressed.
Sustainability 2025, 17(15), 6798; https://doi.org/10.3390/su17156798
Submission received: 2 July 2025 / Revised: 23 July 2025 / Accepted: 24 July 2025 / Published: 26 July 2025

Abstract

This study evaluated the activity concentrations of radionuclides in honey, bee pollen, bee bread, and propolis from multiple regions in Poland (Europe) to assess the levels of radiological contamination and their implications for public health. Furthermore, the work considers the use of bee products as bioindicators of the state of environmental contamination with radionuclides. The apiaries from which the samples were collected were selected in eight provinces in Poland, and are also complemented by reference data from soil contamination monitoring. Radionuclide measurements included both natural (e.g., 40K, 226Ra) and anthropogenic isotopes (e.g., 137Cs). The results show that although the overall activity concentrations were generally low, certain locations exhibited elevated levels of 137Cs in bee products, likely reflecting historical deposition in soils. Propolis was best correlated with 137Cs deposited in soil compared to the other products studied. The patterns observed substantiate the hypothesis that bee products, predominantly propolis, accurately reflect local radiological conditions, thereby providing a practical and non-intrusive approach to monitoring radionuclide contamination and informing risk management strategies. An assessment of potential health risks indicates that the effective dose is safe and ranges from 0.02 to 10.3 µSv per year, depending on the type of product and consumption.

Graphical Abstract

1. Introduction

Bees are indispensable to biodiversity—which constitutes the foundation of human existence—and also function as significant contributors to the advancement of sustainability. As pollinators, they play an essential role in plant reproduction, which subsequently supports agricultural systems, food security, and ecosystem equilibrium. Their activities imitate the principles of sustainability by fostering ecological resilience and sustaining natural cycles. Beyond their ecological functions, bees offer valuable nutritional and medicinal resources such as honey, royal jelly, bee pollen, and bee bread. Products like beeswax, propolis, and apitoxin (bee venom) additionally contribute to various sectors, including food, medicine, cosmetics, and pharmaceuticals [1]. Honey, a sweet substance produced by bees of the Apis mellifera species from flower nectar, is categorized as either blossom honey or honeydew honey. In Europe, over 100 plant species contribute to the production of unifloral honeys, many of which are associated with local biodiversity and regional traditions [2].
Importantly, various bee products exhibit unique therapeutic properties and high nutritional value. For instance, bee bread, a fermented blend of pollen, honey, and enzymes, is rich in proteins, B-complex vitamins, and bioactive compounds. Bee pollen contains essential amino acids, vitamins (especially C and E), and antioxidants. Propolis, known for its antimicrobial and anti-inflammatory qualities, varies by region due to its botanical origins. Beeswax, produced by worker bees, is widely used in sustainable manufacturing, highlighting the ecological and economic importance of bee-derived materials.
The health and productivity of bee populations are significantly affected by environmental conditions. Bees forage within areas extending up to 10 km2, collecting nectar and pollen that may be contaminated by pollutants including heavy metals, pesticides, and radioisotopes [3,4,5]. These contaminants not only jeopardize bee health, but can also accumulate in hive products, which are subsequently consumed by humans. As a result, bees and their products have proven to be effective biomonitoring instruments in the assessment of environmental sustainability [6,7,8,9,10,11].
Recent studies have identified the presence of hazardous substances such as lead, cadmium, and pesticide residues in honey and other apicultural products. Radioisotopes also play a crucial role in the environmental context. Naturally occurring radionuclides constitute an inherent component of the environment; however, radioisotopes derived from anthropogenic activities can be found and may pose contamination risks. The environmental behavior of radionuclides includes both deposition—influenced by atmospheric conditions and surface characteristics—and migration, governed by soil properties, hydrology, and biological uptake. These processes affect the availability of radionuclides for uptake by plants and their subsequent transfer through the food chain, including into bee products.
Furthermore, radioisotopes, particularly (137Cs), have been found, notably in areas impacted by nuclear incidents such as Chernobyl [12,13,14] and Fukushima [15]. These discoveries highlight the extensive environmental consequences of unsustainable practices and emphasize the interconnected nature of human, animal, and ecological health. Essential for agricultural productivity and ecosystem sustainability, pollination also contributes to the dissemination of environmental contaminants. This dual function underscores the necessity for integrated, sustainable strategies in land use, pollution control, and agriculture. By examining how environmental variables—such as soil composition and land management—impact contaminant concentrations in bee products, targeted approaches can be developed to mitigate ecological harm [11].
The primary aim of this research was to evaluate the concentrations of radionuclides in honey and other bee-derived products sourced from diverse regions within Poland. This investigation sought to assess their potential utility as indicators of radioactive contamination and environmental health. The present study is concerned with existing exposure, which refers to prolonged exposure resulting from long-lived radionuclides in the environment and, in this case, through consumer products such as honey and other bee-derived substances.
In addition, this study aimed to identify geographical patterns in radionuclide levels and examine how factors such as local soil characteristics influence the contamination.
In the sustainability context, this research provides crucial insights that can inform public health policy, foster ecological agriculture, and safeguard both pollinators and humans. The central hypothesis posits that bee products not only serve as reflections of environmental quality, but also provide a sustainable and natural methodology for monitoring ecological disturbances, thus supporting a circular, nature-based approach to environmental stewardship.

2. Materials and Methods

2.1. Study Area

The samples under examination originate from selected counties across eight voivodeships in Poland (Europe), namely Lubelskie, Małopolskie, Podkarpackie, Mazowieckie, Opolskie, Śląskie, Warmińsko-Mazurskie, and Wielkopolskie. The study included material obtained from 57 beehives across the sampling area. All sampling sites were in agricultural areas, typically situated near small urban centers (with populations below 100,000), allowing for potential influence from surrounding urban environments. The sites of these plots varied, encompassing forested regions, agricultural fields, and urban areas. The study focuses on products such as honey, bee bread, propolis, and bee pollen, with their availability differing among the locations (Figure 1).

2.2. Sampling and Measurements

Honey samples were collected from apiaries. Following the extraction of honeycombs from the hive, the beekeeper employed a specialized comb to remove the wax covering. Subsequently, the combs were positioned in a honey extractor to initiate the centrifugation process. The honey extracted was then passed through sieves to eliminate impurities, and the clarified honey was subsequently dispensed into packaging. The beekeeper extracted the bee bread from the patch with a special mechanical mining technique. Then, it was dried. Propolis was collected mechanically by scraping from the hive frames. Bee pollen was collected by using special traps, then freeze-dried and sifted through sieves. The honey samples were placed directly into the measuring containers. Other bee products (bee bread, propolis, and pollen) were freeze-dried and homogenized prior to analysis. The entire surface of the vessel was filled so that there were no free spaces, and sealed with parafilm. The measuring geometry consisted of a cylindrical vessel with a capacity of 63 mL made of polyethylene. After a period of one month, to achieve equilibrium between 226Ra and its short-lived progeny, gamma spectrometry measurements were conducted. For these measurements, a Canberra (USA) spectrometer equipped with a BE 3830 detector with an efficiency of 34% was utilized. The measurement process spanned a minimum of 3 days, and the resultant spectra were analyzed using the Genie-2000 software (V3.4.1).
Specific radionuclides such as 40K, 137Cs, and 210Pb were determined directly by their respective energies of 1460 keV, 661.6 keV, and 46.5 keV. The assumption of equilibrium was considered to calculate the concentrations of 226Ra, which enabled the indirect measurement, required due to weak gamma radiation emission and interferences. The radioactivity of 226Ra was ascertained by counting the radioactivity of its progeny radionuclides 214Bi using the following energy lines: 1764.5 keV, 1120.3 keV, and 609.3 keV, as well as 214Pb via the following energy lines: 351.9 keV and 295.2 keV. Prior to gamma measurements, the detector was efficiency-calibrated using three distinct reference materials: IAEA-447, IAEA-RGU-1 (uranium series), and IAEA-RGTh-1 (thorium series). The activity concentration (A) was computed following the specified formula
A = N s L T N b L T · 1000 m · ε · p ( E ) ·   T z
where Ns is the number of sample counts, Nb is the number of background counts, LT is the measurement time (s), m is the mass of the sample (g), p(E) is the probability of emission (E)–peak efficiency, ɛ—detector efficiency, and Tz is the self-absorption coefficient.
Due to the physical differences between the samples of the analyzed bee product samples and the reference material used for detector calibration, particularly in terms of density and composition, self-absorption corrections were applied. The correction procedure was based on the methodology described by Misiak et al. (2011), which accounts for the attenuation of gamma radiation as a function of both the sample density and the photon energy [16]. For each type of bee product, individual correction factors were determined using point sources of radionuclides, and the sample matrices reflected the density ranges of the analysed materials. The resulting data were used to construct empirical correction curves that allowed for the accurate compensation for self-absorption effects.
The uncertainty associated with the radionuclide concentration was determined by employing the total differential methodology. The expanded uncertainty in the results comprised the following components: the uncertainty in the radioactivity of the reference material, the uncertainty in the background measurement, the uncertainty in the efficiency measurement, and the standard efficiency pertinent to the sample measurement [17]. The minimum detectable activity (MDA) was calculated with Currie’s formula [17] for each measurement individually because it depends on the sample’s bulk density.

2.3. Reference Soil Data

Reference data for activity concentration in soil was provided by a report published by the Central Laboratory for Radiation Protection (CLOR) [18]. To assign relevant reference values to each sampling location used in this study, a geospatial proximity analysis was performed. Specifically, each beehive site was matched with the nearest CLOR monitoring point based on straight-line distance, calculated from geographic coordinates.

2.4. Health Risk Calculation

To assess the health risk, the effective dose and risk coefficients, which quantify the likelihood of cancer mortality or morbidity per unit intake of a radionuclide, were computed. The effective dose was determined in accordance with [11,19].
D = Ai·I·Q
where D is the annual effective dose µSv y−1, Ai is the activity concentration of radionuclide [Bq kg−1], I is the average annual consumption of product [kg·y−1], and Q is the conversion factor [µSv Bq−1] [19].
For the average annual consumption of the product, the recommended prophylactic values were adopted for propolis, bee bread, and bee pollen, while for honey, the average consumption in Poland for 2023 was used, as well as an increased value of 15 kg y−1.
Lifetime cancer risk was calculated according to the following formula:
CR = Ci·I·Ei·f
where CR is the lifetime cancer risk, Ci is the activity concentration of radionuclide [Bq kg−1], I is the annual food intake [kg y−1], Ei is the exposure duration of life [y] (50 years for adults), and f is the risk coefficient [20,21,22,23,24].

3. Results and Discussion

3.1. General Radioisotopic Characterization of Bee Products

Radionuclides such as 137Cs, 40K, 226Ra, and 210Pb were detected in four different bee-derived products: bee bread, propolis, bee pollen, and honey. The range and level of activity concentrations (in Bq kg−1) is presented in Figure 2.
Regarding 137Cs, bee bread reached the highest level of activity concentration for cesium. For this product, the range was 0.537 ± 0.079 to 7.06 ± 0.47 Bq kg−1, with an average value of 3.67 Bq kg −1. The second product that showed a measurable value of the cesium radioisotope was propolis. 137Cs in this product ranged from 0.469 ± 0.054 to 5.60 ± 0.57 Bq kg−1, with an average value of 2.49 Bq kg−1. Furthermore, both products of bees, taken from one apiary, showed a similar degree of concentration. The highest and lowest 137Cs concentrations for both products were sampled from the same apiaries, e.g., sample of bee bread IWO2401 and propolis IWO2402. For these two products, measurable cesium activity concentration was observed for almost all samples, while for the other products, most were below the detection limits. For honey and bee pollen, 68% and 79%, respectively, were below the minimum detectable activity. Our observations are in good agreement with others authors [9,25,26]. The concentration of cesium in honey is relatively low, which can be attributed to the multiple purification stages that nectar undergoes within the bee’s honeydew crop during its transformation into honey. This process visibly results in the accumulation of heavy metals within the bee’s body as noted by Roman (2003), and a similar mechanism is likely applicable to cesium [27,28,29].
Propolis and bee bread are fundamentally different in origin and function in the hive, but both are produced by mixing with salivary enzymes [30]. Secondly, both propolis and bee bread are rich in phenolic compounds, flavonoids, and other antioxidant substances [31]. Therefore, the increased activity concentration for cesium may be the result of either increased accumulation or contact with saliva. A comparable mechanism was observed by Borsuk et al., whose work focused on heavy metals [32]. Among other things, the authors observed 40-times-lower concentrations of iron in honey than in nectar, which is the raw material for its production. The bees absorbed the metals into their bodies, which were then removed with their secretions [32]. A similar mechanism could be possible for cesium. Propolis exhibited a comparable activity concentration of 137Cs, likely attributable to the significantly higher contribution of 137Cs within its constituents. It is assumed that the mixing of resin from tree buds and bark by bees may play a substantial role in this composition.
The activity concentration for 40K in bee products emerged as the highest among the natural radionuclides analyzed, a finding that aligns with earlier reports that highlighted potassium radioisotope as dominant. The highest activity concentrations were observed in the bee pollen samples, the content of which ranges from 16.5 ± 1.5 to 233 ± 12 Bq kg−1, and the average value was 174 Bq kg−1. Comparing the average values for the other products, the activity concentration of the 40K radioisotope was 50.3 Bq kg−1 and 43.0 Bq kg−1 for propolis and honey, respectively. However, the range for propolis was much wider, and in comparison, this product may be more dependent on environmental conditions. The activity concentration for 40K in bee bread was below the detection limit, with one exception. Similar relationships to the results presented can be found in the literature, where the highest average potassium content was observed in bee products for bee pollen and the lowest for honey. On the other hand, the widest range of activity concentration for 40K was observed for propolis [33,34,35]. The measured activity concentration levels are substantiated by the fact that the presence of 40K, as a natural radionuclide, in the environment significantly exceeded that of artificial radioactive contamination. Moreover, potassium uptake by plants from the soil, its presence in airborne particulates, and its direct deposition on flowers further contribute to its concentrations [36,37].
The 226Ra concentration was at a similar level when comparing mean values, with the exception of bee bread. It was 2.3 Bq kg−1, 2.0 Bq kg−1, 1.8 Bq kg−1, and 0.9 Bq kg−1, respectively, for bee pollen, propolis, honey, and bee bread. The occurrence of 226Ra in plants predominantly arises from its inherent presence in soil and water, along with the application of phosphate fertilizers and contamination resulting from mining activities [38,39]. This radionuclide can be taken up by the plant mainly from the soil if its soluble chemical forms are available to the root system [40]. Despite the spread of 226Ra in the environment, its concentration in bee products is at low levels. Based on the publication of Gheorghe Bulubas, where a comparison was made of activity concentration in honeys in nine countries, it was above the detection level only in three [41]. In Europe, the average content of 226Ra was 4.16 Bq kg−1 (Romania) and 0.49 Bq kg−1 (Kosovo) [41,42].
The radioactivity of 210Pb in propolis samples was comparatively high relative to other bee products. The mean activity concentration for propolis was 8.9 Bq kg−1, with values ranging from 5.9 ± 1.1 to 10.8 ± 1.2 Bq kg−1. Bee pollen demonstrated moderate concentrations, with a median value of 1.4 Bq kg−1. Bee bread demonstrated the lowest activity concentration levels, remaining below the minimum detectable activity (MDA) threshold. A comparable trend was identified in honey, aside from a singular sample that measured 1.85 ± 0.86 Bq kg−1. Moreover, the presence of 210Pb in the atmosphere as particulate matter, originating from the decay of 222Rn [43], is likely a significant contributor to its incidence in both propolis and bee pollen.
Overall, these results indicate that the propolis samples were the most diverse in terms of the activity concentration of the listed isotopes. One reasonable explanation is that environmental conditions are more likely to affect the activity concentration in this particular product. Propolis is a resinous product that is collected from plant resin and exudates [44]. These environmental elements may be characterised by a higher accumulation of radioisotopes.
To evaluate whether propolis can reflect the radiological condition of the environment, the activity concentrations of individual radionuclides were compared with the reference values obtained from national monitoring.

3.2. Principal Component Analysis for Environmental Radioisotopic Correlations

Principal component analysis (PCA) was performed to quantify how radionuclide concentrations in samples reflect those observed in reference environmental data and to assess the underlying correlation structure among variables. Although correlation analyses were conducted for all analyzed bee products, statistically significant relationships between radionuclide concentrations in the products and corresponding soil data were limited. Honey samples, in particular, exhibited consistently low activity concentrations, indicating minimal accumulation of environmental radionuclides and, therefore, limited potential as environmental indicators. Bee bread showed a weak correlation for cesium isotopes; however, this relationship was neither strong nor consistent across regions. In contrast, propolis demonstrated the most pronounced and interpretable correlation with soil radioactivity, particularly for specific isotopes, supporting its potential as a bioindicator. Given the primary objective of the study, i.e., to assess the indicative potential of bee products, the presented analysis focused on propolis, as other matrices provided limited additional insight.
Figure 3 shows the PCA loading plot for propolis samples. The first two components, accounting for 40.70% and 34.55% of the total variance, respectively, reveal distinct groupings for most radionuclides in propolis (red) relative to their reference counterparts (green). In particular, 137Cs in propolis aligns closely with reference 137Cs deposition levels, indicating a strong relationship between environmental contamination and its bioaccumulation in propolis. What is noticeable here is that 137Cs in propolis is not likely correlated to cesium mass concentration in soil. One of the likely causes of this phenomenon may be the additional link to soil density in the case of mass concentration. Therefore, the variability in the soil type (including bulk density) will be an additional factor that may disrupt the correlation between the values. The vector for 226Ra in propolis differs from the reference data, suggesting that factors beyond simple soil availability may regulate the uptake of 226Ra. Similarly, the vector separation between 40K in propolis and 40K reference suggests a differentiated impact of the soil content compared to product-specific pathways. On the contrary, the reference variables for 226Ra, 40K, and the absorbed dose rate (ADR) are grouped together, emphasizing their mutual correlation. Overall, the analysis confirms that propolis concentrations reflect certain ambient conditions, but mostly for 137Cs deposited in square meters, while also highlighting unique patterns driven by the composition and biochemical processes associated with propolis.
The comparison was conducted with data from monitoring sites [18] characterized by higher deposition, which generally present elevated concentrations of 137Cs in propolis. This is consistent with previous statistical findings. Such concordance implies that propolis, primarily derived from plant resins, may serve as a reliable indicator of local radiological conditions, while emphasizing the regional variation in 137Cs contamination.

3.3. Health Risk Assessment

In evaluating the average honey consumption in Poland across various age demographics, the effective dose was ascertained. Additionally, utilizing data from interviews and practical observations, consumption estimates were determined for an annual intake of 15 kg of honey, as this level of consumption is frequently observed (Table 1). The radionuclides assessed include 137Cs, 40K, and 226Ra, for which the range of values were delineated.
The dose contribution from 137Cs remained relatively low across all age categories. Adults consuming 15 kg of honey annually exhibited the highest doses. The presence of 40K, a naturally occurring radionuclide, resulted in higher dose values in comparison to 137Cs. Among the radionuclides measured, 226Ra exhibited the most significant variability, with maximum doses reaching 91.36 µSv·y−1 for adults consuming 15 kg of honey annually. Although 226Ra is a recognized contributor to internal radiation exposure, the computed doses remained within acceptable safety thresholds for food consumption [45]. For younger individuals, the values were lower but remained significant compared to other radionuclides.
In Poland, similar to other parts of the world, the consumption of honey and bee products is prevalent from a medical perspective. Consequently, it is pertinent to present the estimated effective dose for these products. Calculations were conducted for three age groups: adults, as well as children aged 10 and 15 years. The results are detailed in Table 1. In bee products, the minimal dose values were ascertained for 137Cs. The effective dose of 137Cs across distinct age groups displayed a comparable magnitude. Among the evaluated levels, bee bread demonstrated the highest levels of 137Cs, whereas propolis exhibited the lowest. The doses associated with 40K and 226Ra were elevated and displayed variability across diverse products. Regarding natural radionuclides, the most pronounced dose levels were identified for 40K in bee bread, whilst the lowest were observed in propolis. This variation in dose distribution within the assessed products, including the minimal values for propolis, is significantly influenced by its low recommended intake.
Research on the total annual effective dose of radionuclides (137Cs, 226Ra, 40K) in honey, bee bread, propolis, and bee pollen reveals significant differences between these products and their consumption by different age groups. The results are shown in Table 2.
Honey exhibited a wide range of radiation doses. This indicates a substantial variation in consumption. Among bee products, propolis was characterized by the lowest total dose. Even though this product was characterized by one of the highest concentrations of radionuclides in these studies, due to the low consumption, the dose was also low. The calculated doses were low and comparable to the doses found in honey in Romania [41], which is one of the most important European honey producers. Data confirm that the total effective dose was far below the reference value of 1 mSv y−1 recommended by the WHO and ICRP for radiological safety for all sources of exposure (except natural radioactivity and medical exposure) [45].
The evaluation of lifetime cancer risk (CR) associated with honey consumption over a 50-year period for an adult individual consuming 15 kg y−1 and 0.83 kg y−1 demonstrated significant variability contingent on the radionuclide present. The results illustrate that the estimated cancer risks vary considerably among the radionuclides examined (137Cs, 40K, 226Ra,), with 40K presenting the highest risks (Table 3).
The lifetime cancer risk levels identified in honey, bee bread, propolis, and bee pollen display substantial variation based on radionuclide concentration, yet they remained comparatively low in relation to international safety thresholds. In general, a lifetime cancer risk exceeding 10−4 (1 in 10,000) is deemed a significant concern, while risks below 10−6 (1 in 1,000,000) are frequently considered negligible in radiological risk assessments [46]. The greatest risks were associated with 226Ra in honey, where the maximum mortality CR attained 156 × 10−6 (156 in 100,000); this was for the highest estimated consumption. Bee bread showed elevated risks for 137Cs and 40K, yet these were within levels not deemed critical. Propolis possessed the lowest cancer risk values, indicating minimal radiological concern. Bee pollen was positioned within an intermediate risk range, generally lower than honey and bee bread, but higher than propolis.

4. Conclusions

Based on the research findings, it can be concluded that the proposed method of analysis was efficient, enabling the examination of radionuclides in honey and other bee products. Both the accumulation of natural radionuclides and radioactive contamination in these products were observed at very low levels. The concentrations of radionuclides vary and depend on the levels of radioisotopes in nectar or pollen, which are influenced by background radiation, meteorological conditions, agricultural practices, and metabolic processes. Among bee products, those other than honey—particularly propolis—appeared more sensitive to environmental contaminants. The effective doses calculated for the analyzed products are considered safe, and although the lifetime cancer risk showed some variability, it remains within acceptable safety limits.
In summary, bee products can serve as significant markers reflecting environmental pollution levels. Propolis, in particular, is an excellent bioindicator. Regarding health risk, it should be stressed that both honey and bee products are considered radiologically safe. Although honeys were characterized by a low radionuclide content, the significance of their large consumption in contaminated areas should not be overlooked. It is also important to note that the cancer risk (CR) will similarly be characterized by a higher value. The same scenario may apply to bee products. Therefore, the detected elevated levels of radionuclides in individuals are not unfounded, but instead reflect the prevailing environmental conditions in which bees forage.
It is crucial to emphasize that research should prioritize examining regional disparities in radionuclide concentrations and the potential implications for long-term accumulation in scenarios of high consumption. Additionally, conducting comparative analyses with honey produced in other countries could provide substantial insights into global disparities in both natural and anthropogenic radionuclide contents.

Author Contributions

Conceptualization, K.S. and F.J.; methodology, K.S. and F.J.; validation, K.S., F.J. and J.N.; formal analysis, J.N.; investigation, K.S. and F.J.; resources, K.S.; data curation, J.N.; writing—original draft preparation, K.S., F.J. and J.N.; writing—review and editing, K.S., F.J. and J.N.; visualization, F.J.; supervision, K.S.; project administration, K.S.; funding acquisition, K.S. All authors have read and agreed to the published version of the manuscript.

Funding

This work was financially supported by the Polish Ministry of Education and Science, grant number 16.16.210.476.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The raw data are available in the repository under the Creative Commons BY 4.0 licence: https://doi.org/10.58032/AGH/I9J5B8 [47].

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

The following abbreviations are used in this manuscript:
ADRAbsorbed dose rate
CRCancer risk
MDAMinimum detectable activity
PCAPrincipal component analysis
WHOWorld Health Organization

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Figure 1. Study area with the type of bee products analyzed.
Figure 1. Study area with the type of bee products analyzed.
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Figure 2. Activity concentration of 137Cs, 40K, 226Ra, and 210Pb in bee products.
Figure 2. Activity concentration of 137Cs, 40K, 226Ra, and 210Pb in bee products.
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Figure 3. Propolis PCA loading plot.
Figure 3. Propolis PCA loading plot.
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Table 1. Annual effective dose of radionuclides (137Cs, 226Ra, 40K) from honey, bee bread, propolis, and bee pollen in adults and children (aged 10 and 15 years).
Table 1. Annual effective dose of radionuclides (137Cs, 226Ra, 40K) from honey, bee bread, propolis, and bee pollen in adults and children (aged 10 and 15 years).
Element
(Age)
Dose for Honey
[µSv y−1]
(15 kg y−1) 1
Dose for Honey
[µSv y−1]
(0.83 kg y−1) 1
Dose for Bee Bread
[µSv y−1]
(7.3 kg y−1) 1
Dose for
Propolis
[µSv y−1]
(0.05 kg y−1) 1
Dose for
Bee Pollen
[µSv y−1]
(1.8 kg y−1) 1
137Cs (adult)0.031–0.2770.002–0.0150.05–0.670.0003–0.00360.006–0.023
137Cs (10 y)-0.001–0.0120.04–0.520.0002–0.00280.005–0.018
137Cs (15 y)-0.002–0.0150.05–0.670.0003–0.00360.006–0.023
40K (adult)0.354–16.0920.020–0.890~7.670.002–0.0400.185–2.605
40K (10 y)-0.041–1.867l~16.080.005–0.0830.388–5.461
40K (15 y)-0.024–1.092~9.400.003–0.0490.227–3.193
226Ra (adult)1.23–91.360.068–5.0551.27–1.750.012–0.0350.635–1.455
226Ra (10 y)-0.195–14.4443.62–5.000.035–0.1011.814–4.158
226Ra (15 y)-0.365–27.0826.78–9.380.066–0.1893.402–7.797
1 Amount of prophylactic consumption.
Table 2. Total annual effective dose of radionuclides (137Cs, 226Ra, 40K) in honey, bee bread, propolis, and bee pollen for adults, 10-year-old children, and 15-year-old children.
Table 2. Total annual effective dose of radionuclides (137Cs, 226Ra, 40K) in honey, bee bread, propolis, and bee pollen for adults, 10-year-old children, and 15-year-old children.
Product
(Consumption)
Mean Total Dose
[µSv y−1]
(Adult)
Mean Total Dose [µSv y−1]
(10 y)
Mean Total
Dose [µSv y−1]
(15 y)
Honey (15 kg y−1)10.28--
Honey (0.83 kg y−1)0.571.462.16
Bee bread (7.3 kg y−1)2.164.815.95
Propolis (0.05 kg y−1)0.0250.0600.086
Bee pollen (1.8 kg y−1)2.686.166.27
Table 3. Calculated cancer risk for adults for the examined radionuclides (137Cs, 40K, 226Ra) in terms of mortality and morbidity for the tested products.
Table 3. Calculated cancer risk for adults for the examined radionuclides (137Cs, 40K, 226Ra) in terms of mortality and morbidity for the tested products.
ProductCR for
137Cs
Mortality
[10−8]
Mean (Range)
CR for
137Cs
Morbidity [10−8]
Mean
(Range)
CR for
40K
Mortality
[10−6]
Mean
(Range)
CR for
40K
Morbidity [10−6]
Mean
(Range)
CR for
226Ra
Mortality
[10−6]
Mean
(Range)
CR for
226Ra
Morbidity [10−6]
Mean
(Range)
Honey for consumption
15 kg y−1
16.6
(8.3–73.4)
24.4
(12.2–107.7)
19.0
(1.7–76.4)
29.8
(2.6–120.2)
12.4
(2.1–156.0)
18.0
(3.1–226.8)
Honey for consumption
0.83 kg y−1
0.9
(0.5–4.1)
1.4
(0.7–6.0)
1.1
(0.1–4.2)
1.7
(0.1–6.6)
0.7
(0.1–8.6)
1.0
(0.2–12.5)
Bee bread for consumption
7.3 kg y−1
92.1
(13.5–177.4)
135.1
(19.8–260.4)
~36.4~57.32.4
(2.2–3.0)
3.5
(3.1–4.3)
Propolis for consumption 0.05 kg y−10.43
(0.08–0.96)
0.63
(0.11–1.41)
0.07
(0.01–0.19)
0.12
(0.02–0.30)
0.04
(0.02–0.06)
0.06
(0.03–0.09)
Bee pollen for consumption
1.8 kg y−1
5.0
(1.6–6.2)
7.3
(2.3–9.1)
9.2
(0.9–12.4)
14.5
(1.4–19.5)
1.6
(1.1–2.5)
2.3
(1.6–3.6)
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Szarłowicz, K.; Jędrzejek, F.; Najman, J. Bee Products as a Bioindicator of Radionuclide Contamination: Environmental Approach and Health Risk Evaluation. Sustainability 2025, 17, 6798. https://doi.org/10.3390/su17156798

AMA Style

Szarłowicz K, Jędrzejek F, Najman J. Bee Products as a Bioindicator of Radionuclide Contamination: Environmental Approach and Health Risk Evaluation. Sustainability. 2025; 17(15):6798. https://doi.org/10.3390/su17156798

Chicago/Turabian Style

Szarłowicz, Katarzyna, Filip Jędrzejek, and Joanna Najman. 2025. "Bee Products as a Bioindicator of Radionuclide Contamination: Environmental Approach and Health Risk Evaluation" Sustainability 17, no. 15: 6798. https://doi.org/10.3390/su17156798

APA Style

Szarłowicz, K., Jędrzejek, F., & Najman, J. (2025). Bee Products as a Bioindicator of Radionuclide Contamination: Environmental Approach and Health Risk Evaluation. Sustainability, 17(15), 6798. https://doi.org/10.3390/su17156798

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