As, Cr, Cd, and Pb in Bee Products from a Polish Industrialized Region

Adam Roman; Ewa Popiela-Pleban; Paweł Migdał; Wojciech Kruszyński

doi:10.1515/chem-2016-0007

Article Open Access

As, Cr, Cd, and Pb in Bee Products from a Polish Industrialized Region

Adam Roman , Ewa Popiela-Pleban , Paweł Migdał and Wojciech Kruszyński

Published/Copyright: March 12, 2016

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From the journal Open Chemistry Volume 14 Issue 1

Abstract

Bee pollen and bee bread from stationary apiaries in the southwest Polish Legnica-Glogow copper district (LGOM) were analyzed for Cr, Pb, Cd and As by ICP-AES. Their concentrations in both products were As > Cr > Pb > Cd. Concentrations in bee pollen were higher than in bee bread. Average Cr, Pb, As and Cd concentrations in bee products were 0.138, 0.093, 0.325, and 0.019 mg kg⁻¹, respectively. Chromium was the most problematic element in bee pollen because its concentration limit was exceeded in more than 50% of the samples. Differences in Cd level between bee pollen and bread were significant (p ≤ 0.05)

Keywords: bee bread; bee pollen; toxic metals; industrialized region

1 Introduction

Industry, road traffic, and agriculture have increased environmental pollution [1,2]. High Cr, Pb, As, and Cd concentrations – metals widely used in industry - cause many types of disease. In the environment these metals may occur at greater than the maximum allowable concentrations. This is important because they have been detected in pollen, plant nectar, and water – the raw material collected by honeybees. The metals then accumulate in bee pollen and bee bread which are consumed for api-therapeutical purposes. Bees and their products have been used to monitor environmental contamination [3–9]. There are significant correlations between the level of toxic metals in soil and plants and their content in bee products [10].

The aim of this study was to determine Cr, Pb, Cd and As in bee pollen (pollen loads) and bee bread from bee colonies in industrialized southwest Poland.

2 Experimental procedure

2.1 Material

The research material consisted of bee pollen (pollen loads) and bee bread from stationary apiaries in the Legnica-Glogow copper district (LGOM). LGOM is an industrial area in Lower Silesia consisting of five counties with ~0.5 million inhabitants. It is the main center of the copper industry in Poland and one of the largest in the world.

Samples were collected from June to September 2012. The study included 25 apiaries (N=25). Both products were collected from 3 colonies in each apiary (bee pollen – n = 3 × 25 = 75, bee bread – n = 3 × 25 = 75). Bee bread was collected directly from honeycombs using a ceramic knife to avoid contamination. Pollen was collected directly from the hive using bee pollen traps. Individual samples were combined into one pooled bee pollen or bee bread sample per apiary.

2.2 Methods

All samples were dried at 120°C, homogenized in an A-11 laboratory mill (IKA GMBH, Germany) and digested in spectrally pure concentrated nitric acid (Merck, Darmstadt, Germany) using an MD-2000 digestion system (CEM, USA). They were then cooled and diluted to final volume with Milli-Q^TM water. Quantitative ICP-AES analyses for Cr, Pb, As and Cd were performed on a PU-7000 spectrometer (Phillips-Unicam, Cambridge, U.K.) with a 5000uAT ultrasonic nebulizer (CETAC, USA) [11]. The limit of detection (LOD) was 1 ppb.

2.3 Data analysis

Statistical analysis was performed using SAS 9.1.3 software (SAS Institute, 2004). Because the Shapiro-Wilk test showed the distributions were not normal, Kruskal-Wallis and Wilcox tests were applied to verify the significance of differences between metal levels in bee pollen and bee bread. The Spearman rank correlation coefficient was used to verify correlations among element concentrations.

3 Results and Discussion

Bee pollen (pollen loads) contained the highest concentrations of As, Cr, Cd, and Pb (Tables 1,3). Others have also found elevated toxic metals in bee pollen [12–15], but there have been few publications dealing with bee bread contamination. Our results showed that in both bee products As was present in highest concentration. Although more was found in bee bread (avg. 0.325 mg kg⁻¹) than in pollen (0.290 mg kg⁻¹), the differences were not significant (Tables 1, 2). Both averages exceed the allowable 0.20 mg kg⁻¹ [16,17]. Much lower As content was observed by Roman [18] in pollen loads from two different industrial regions. Similarly, Falco et al. [19] found a mean As content of 0.04 mg kg⁻¹ in Polish pollen, with a maximum of 0.19 mg kg⁻¹.

The average pollen Cr level was 0.230 mg kg⁻¹ (Table 1), above the permissible limit (0.14 mg kg⁻¹) [16,17]. More than 50% of bee pollen samples contained excessive Cr. There was less in bee bread (0.138 mg kg⁻¹). Values ranged from 0.038 to 0.251 mg kg⁻¹; the limit was exceeded in 40% of the samples (Table 3). Differences between Cr concentrations in the bee products were not significant (Table 3). Conti and Bortè [13] found less Cr in all bee pollen samples from areas of varied contamination. Morgano et al. [20] observed varied Cr levels in samples from southeastern Brazil, depending on collection time. They found higher levels of Pb (0.147 mg kg⁻¹) and Cd (0.033 mg kg⁻¹) in bee loads.

Table 1

Toxic elements in bee pollen loads from Lower Silesia.

Apiary	Concentration (mg kg⁻¹)
	Cr	Pb	Cd	As
1	0.087	0.025	0.015	0.142
2	0.127	0.101	0.020	0.097
3	0.115	0.025	0.020	0.225
4	0.079	0.284	0.090	0.275
5	0.107	0.250	0.001	0.475
6	0.407	0.327	0.066	0.758
7	0.095	0.025	0.001	0.245
8	0.110	0.043	0.003	0.312
9	0.945	0.25	0.047	0.135
10	0.227	0.142	0.031	0.299
11	0.613	0.321	0.009	0.523
12	0.089	0.032	0.024	0.121
13	0.265	0.103	0.056	0.228
14	0.078	0.219	0.072	0.107
15	0.131	0.022	0.095	0.782
16	0.439	0.128	0.012	0.126
17	0.099	0.113	0.092	0.252
18	0.176	0.038	0.023	0.199
19	0.312	0.341	0.011	0.338
20	0.145	0.181	0.007	0.089
21	0.201	0.218	0.003	0.225
22	0.236	0.066	0.029	0.111
23	0.184	0.169	0.044	0.406
24	0.155	0.098	0.021	0.377
25	0.334	0.159	0.030	0.392
Median	0.155^[a]	0.128^[a]	0.023^[b]	0.245^[a]
Mean ± SD	0.230 ± 0.200	0.147 ± 0.105	0.033 ± 0.030	0.290 ± 0.188

SD – standard deviation

Table 2

Toxic elements in bee bread from Lower Silesia.

Apiary	Concentration (mg kg⁻¹)
	Cr	Pb	Cd	As
1	0.061	0.025	0.001	0.062
2	0.110	0.029	0.009	0.066
3	0.157	0.103	0.001	0.061
4	0.251	0.198	0.045	0.062
5	0.126	0.025	0.010	0.625
6	0.127	0.137	0.001	0.627
7	0.142	0.129	0.017	0.892
8	0.078	0.029	0.012	0.198
9	0.129	0.101	0.008	0.081
10	0.216	0.154	0.034	0.242
11	0.038	0.122	0.003	0.033
12	0.132	0.104	0.077	0.012
13	0.098	0.118	0.003	0.554
14	0.202	0.177	0.021	0.085
15	0.084	0.099	0.026	0.191
16	0.221	0.083	0.005	0.332
17	0.179	0.102	0.012	0.667
18	0.138	0.091	0.002	0.839
19	0.125	0.032	0.065	0.062
20	0.219	0.047	0.001	0.049
21	0.078	0.028	0.080	0.731
22	0.133	0.094	0.001	0.338
23	0.152	0.130	0.009	0.672
24	0.094	0.065	0.001	0.342
25	0.148	0.103	0.031	0.299
Median	0.132^[A]	0.101^[AB]^[a]	0.009^[C]	0.242^[A]^[b]
Mean ± SD	0.138 ± 0.054	0.093 ± 0.049	0.019 ± 0.024	0.325 ± 0.288

SD – standard deviation

Table 3

Comparison of concentrations in pollen loads and bee bread from Lower Silesia.

		Concentration (mg kg⁻¹)
		Cr	Pb	Cd	As
Pollen loads	Minimum	0.078	0.022	0.001	0.089
	Median	0.155	0.128	0.023	0.245
	Maximum	0.945	0.341	0.095	0.782
	Mean	0.230	0.147	0.033	0.290
Bee bread	Minimum	0.038	0.025	0.001	0.012
	Median	0.132	0.101	0.090	0.242
	Maximum	0.251	0.198	0.08	0.892
	Mean	0.138	0.093	0.019	0.325
Kruskal-Walis test testtest	p-value	0.1277	0.1092	0.0365	0.5802
Wilcox test	p-value	0.1301	0.1114	0.0374	0.5869

The Pb concentration in bee pollen was higher than in bee bread. The pollen maximum was 0.341 mg kg⁻¹ and the average 0.147 mg kg⁻¹. The mean in bee bread was 0.093 mg kg⁻¹ (Table 3). The highest content in either product did not exceed the allowed maximum of 0.50 mg kg⁻¹) [16,17]. Statistical analysis showed no significant differences in lead concentration between pollen and bread (Table 3). Our results for bee bread were lower than those of Madras-Majewska et al. [21], and our results for bee loads were lower than those reported by Szczęsna et al. [5] (0.45−0.98 mg kg⁻¹).

Generally, Cd occurred at the lowest concentration. Its mean was higher in bee pollen (0.033 mg kg⁻¹) with a maximum about 3-fold higher than the average (0.095 mg kg⁻¹). In bee bread the average was 0.019 mg kg⁻¹ (Table 3). The levels in pollen and bee bread differed significantly (Table 3). Cd in bee pollen from most controlled apiaries has been found to exceed acceptable levels [22–24]. Our results agree; Cd exceeded the standards (0.05 mg kg⁻¹) by 8% and 20% for bee bread and bee loads.

Table 4

Correlation coefficients (r) between element concentrations.

Elements	Correlation coefficient (r)
	pollen loads	bee bread
Cr-Pb	0.402^p=0,0464	0.487^p=0,0134
Cr-Cd	-0.004	0.089
Cr-As	0.226	0.025
Pb-Cd	0.043	0.163
Pb-As	0.228	0.006
Cd-As	0.106	-0.014

However, Szczęsna et al. [5] found 0.032 to 0.154 mg kg⁻¹ Cd in pollen; only 9% of their samples exceeded the accepted limit.

4 Conclusion

Arsenic and chromium are the most problematic toxic elements in bee pollen and bee bread, since these elements’ mean concentrations exceeded the limits. The concentrations were As>Cr>Pb>Cd. Significant inter element correlations were found for Cr and Pb in both bee products (Table 4). Most metal levels were higher in pollen loads than in bee bread. Metal loss may occur during processing pollen loads to bee bread.

As bee products are considered beneficial supplements, consumers may consider their contamination important. Additionally, these products are valuable indicators of environmental pollution.

Acknowledgments

This work was authorized (No. Z4/S/2011) by the Department of Environment, Animal Hygiene and Welfare, Wroclaw University of Environmental and Life Sciences. Publication was supported by the Wrocław Center of Biotechnology, Leading National Research Centre Program (KNOW) for 2014–2018.

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Received: 2015-5-18

Accepted: 2016-1-26

Published Online: 2016-3-12

Published in Print: 2016-1-1

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