Article pubs.acs.org/JAFC
Absorption, Distribution, Metabolism, and in Vitro Digestion of BetaCypermethrin in Laying Hens Xueke Liu, Peng Wang, Chang Liu, Yiran Liang, Zhiqiang Zhou, and Donghui Liu* Beijing Advanced Innovation Center for Food Nutrition and Human Health, Department of Applied Chemistry, China Agricultural University, Beijing, 100193, P. R. China S Supporting Information *
ABSTRACT: Beta-cypermethrin (beta-CP), an important pyrethroid insecticide, and its main acid metabolites are frequently detected in human samples. Because beta-CP may pose some risk to human health, we studied dynamics and residues of beta-CP and its metabolites in hen egg, droppings, blood, and 15 other tissues after continuous exposure. A digestive model was then used to study beta-CP’s digestive fate. Beta-CP and its metabolites significantly accumulated in tissues with high lipid contents and were readily transferred to eggs. Beta-CP was mainly metabolized into acid metabolites that accumulated in egg and edible tissues of laying hens, suggesting that humans may be exposed to beta-CP acid metabolites through food. KEYWORDS: beta-cypermethrin, metabolites, laying hens, residue, digestion
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INTRODUCTION
Chemicals and Animals. Beta-CP and trans/cis-DCCA standards were obtained from Jiangsu Yangnong Chemical Group Co., Ltd. Chlorpyrifos, 3-PBA, 1,1,1,3,3,3-hexafluoroisopropanol (HFIP, 99.5%), N,N-diisopropylcarbodiimide (DIC, 98%), lipase (L3126), pancreatin (P7545), and pepsin (P7125) were obtained from SigmaAldrich. Cholic acid and chenodeoxycholic acid were purchased from Aladdin Industrial Inc. Water was from a Milli-Q purification system. All other reagents were chromatography-grade. The chemical structures of beta-CP, trans/cis-DCCA, and 3-PBA are shown in Figure S1. Laying hens, weighing 1.8 kg, were purchased from Fujia Poultry Center (Beijing, China); they were 35 weeks of age and caged individually with drinking water and fed ad libitum. Hens were acclimated to laboratory conditions for 1 week prior to experiments. Laboratory conditions were 22 ± 2 °C with a 16/8 (light/dark) cycle. Animal experiments were carried out in accordance with the guidelines of Institutional Animal Care and Use Committee of China Agricultural University. Exposure Experiment and Sample Collection. Treated feed contained 1 mg/kg of beta-CP. Based on daily feed intake of hens, the daily intake of beta-CP was approximately 0.07 mg/kg body weight. In addition, the LD50 for cypermethrin for chickens exceeds 2000 mg/ kg,21 so daily exposure concentration was less than 0.01% of the LD50. Treated feed was prepared by dissolving beta-CP in n-hexane, adding this solution to feed, then homogeneously mixing and removing nhexane. After 7 days of adaptation, 13 laying hens were randomly assigned to treatment group (N = 9) or control group (N = 4). All animals were individually caged with monitoring feed intake as well as collecting egg and droppings. The treated hens were fed the treated feed for 10 days and then the control feed for 5 days. Three hens of the treatment group and three of the control group were sacrificed after 10 days, and then all other hens were sacrificed at the 15th day. The eggs and droppings were collected and weighed daily, and the egg yolks and whites were separately weighed and stored. Hen blood
Pyrethroid insecticides have a broad spectrum and are used widely for vegetable and crop pest control, as well as human health pest control. It has been regarded to be low toxic to humans, because it can be quickly metabolized to nontoxic metabolites.1−3 However, recent studies suggest that it might not be as safe as previously thought; for example: a correlation between sperm concentration/sperm DNA fragmentation and urinary pyrethroid metabolites, 4−6 a potential positive correlation between heart disease risk and pyrethroid exposure,2 and a possible association between urinary pyrethroid metabolites and risk of childhood acute lymphocytic leukemia.7 The pyrethroid beta-cypermethrin (beta-CP) has been extensively used to control various pests in agricultural and residential areas for more than 30 years, and China is the greatest consumer of this product.8 Beta-CP’s major animal metabolites are 3-phenoxybenzoic acid (3-PBA) and cis/trans3-(2,2-dichloroethenyl)-2,2-dimethylcyclopropanecarboxylic acid (cis/trans-DCCA),9−11 and these have been identified in human urine,12−14 breast milk,15,16 and other human samples.17 Also, animals may be contaminated by beta-CP or its metabolites via direct contact or feed. Therefore, beta-CP and its metabolites in the human food chain are worthy of study. Studies show that humans can derive pesticide residues from food consumption,18 and some CP and its metabolites have been reported in some animal products.19,20 Because humans consume chickens and eggs, the residues of cypermethrin and its metabolites are worthy of study in these foods. Thus, we investigated the metabolic behavior, excretion ratio, tissue residues, and characteristics of maternal transfer of beta-CP and its metabolites in laying hens after continuous exposure. We also established a digestive model to further study the trend of beta-CP in the hen digestive system. © 2017 American Chemical Society
MATERIALS AND METHODS
Received: Revised: Accepted: Published: 7647
June 3, 2017 August 2, 2017 August 10, 2017 August 10, 2017 DOI: 10.1021/acs.jafc.7b02581 J. Agric. Food Chem. 2017, 65, 7647−7652
Article
Journal of Agricultural and Food Chemistry
Figure 1. Dynamics of beta-CP and its metabolites in blood (A), egg yolks (B), egg whites (C), and droppings (D). reconstituted in 250 μL of acetonitrile, and combined with 30 μL of HFIP and 10 μL of DIC for reaction. After reaction for 10 min, 0.5 mL of water and 0.5 mL of n-hexane were added followed by vortexing. After centrifugation, 150 μL of n-hexane was transferred and mixed with 50 μL of chlorpyrifos n-hexane solution (0.2 mg/kg, as an internal standard), and the mixture was analyzed by GC-MS/MS. A Thermo Scientific TSQ Quantum XLS system was used to assess beta-CP and three acid metabolites. A HP-5 MS column (30 m × 0.25 mm × 0.25 μm) was used for chromatographic separation, and helium (99.999%) was the carrier gas with a flow rate of 1.0 mL/min. The splitless mode was used during the injection process, and the inlet temperature was 270 °C. The oven temperature program was as follows: 60 °C (1 min hold), 5 °C/min to 110 °C (2 min hold), 20 °C/min to 270 °C (1 min hold), and 10 °C/min to 290 °C (10 min hold). Tandem mass spectrometry was used with an electron impact (EI) ion source. The ionization voltage and ion source temperature were set at 70 eV and 290 °C, respectively. The scan mode used the selected reaction monitoring (SRM). Other parameters are listed in Table S1. To evaluate the sample analysis methods, recovery and precision were assessed by spiking the samples with analytes at three concentrations (n = 3). Table S2 shows that the recoveries of betaCP and its three metabolites were in the range 70.0−120.6% with relative standard deviations (RSDs) of 0.2−14.9%. LOQs of different samples, based on the signal-to-noise ratio (S/N) of 10, range from 0.1 to 0.6 ng/g, which is listed in Table S3. The linearity of beta-CP and its three metabolites were good with correction coefficients (r) of 0.9950−0.9998. Sample results were not corrected for recoveries less than 100%. Determination of Antioxidant Enzymes Activities and Lipid Peroxidation. Antioxidant enzymes, such as superoxide dismutase (SOD) and catalase (CAT), reduce reactive oxygen species (ROS), which results in the oxidative stress.26 Malondialdehyde (MDA), a product of lipid peroxidation, may be an indicator of oxidative stress.27 Thus, SOD, CAT, and MDA were measured. First, 0.15 g samples of
was collected at days 1, 3, 5, 7, 10, 11, 13, and 15. In addition, heart, liver, spleen, lung, kidney, brain, thigh muscle, breast muscle, muscular stomach, glandular stomach, ovary, chest skin, intestine, ovum, and abdominal fat were collected and weighed. Prior to analysis, samples were stored at −20 °C. Digestive Model. The digestive model was designed to simulate three digestion stages (crop, stomach, and small intestine).22,23 The digestion process included 5 min of crop (pH = 4.3), 70 min of stomach (pH = 3.0), and 150 min of small intestinal digestion (pH = 6.3). In addition, digestion was maintained at 41 °C, and 120 rpm. Feed (1 g, 1 mg/kg beta-CP) was mixed with 1.6 mL of 0.012 M HCl for 5 min in an incubation tube. Then, 0.5 mL of stomach fluid (1.25 mg/mL pepsin in 0.4 M HCl) was added and incubated for 70 min. Then, 0.8 mL of 0.54 M NaHCO3 solution was added to adjust the pH, and chyme was transferred to a dialysis bag (8000−10000 Da). Finally, 5 mL of bile (5.48 mg/L chenodeoxycholic acid and 5.65 mg/ L cholic acid in 0.2 M phosphate buffer at pH 6.3) and 0.5 mL of intestinal fluid (2.60 mg/mL lipase and 17.34 mg/mL pancreatin in 0.2 M phosphate buffer at pH 6.3) were added, and the dialysis bag was sealed and immersed in 100 mL of 0.2 M phosphate buffer at pH 6.3 for 150 min. After incubation, chyme was centrifuged and separated into digestive fluid and digestion residue. Beta-CP and its metabolites in dialysate, digestive fluid, and digestion residue were extracted and analyzed. Sample Preparation and Analysis. First, 1 g of homogenized sample (expected 0.5 g of fat) was extracted twice with 9 mL of ethyl acetate for 5 min each using a vortex mixer. Extracts were concentrated to dryness under nitrogen at 30 °C. To remove lipids, the remaining extracts were dissolved in 1 mL of acetonitrile (fat, intestine, ovum, and egg yolk were dissolved in 2 mL of acetonitrile) and purified twice with 2 mL of n-hexane (fat, intestine, ovum, and egg yolk were purified twice with 4 mL of n-hexane). When n-hexane was removed, the acetonitrile was concentrated to dryness. Derivatization of metabolites was based on previously published mehtods.24,25 Briefly, extracts were 7648
DOI: 10.1021/acs.jafc.7b02581 J. Agric. Food Chem. 2017, 65, 7647−7652
Article
Journal of Agricultural and Food Chemistry Table 1. Residues of Beta-CP and Its Three Metabolites in Tissues at the 10th Day and the 15th Day cis-DCCA (ng/g)
beta-CP (ng/g) tissues heart liver spleen lung kidney brain thigh muscle breast muscle muscular stomach glandular stomach ovary skin intestine ovum fat a
10 d 1.12 0.80 0.49 0.55 0.64 1.67 0.45 0.51 1.42 1.41 1.45 2.49 2.26 3.88 5.07
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.34 0.31 0.09 0.03 0.26 0.55 0.19 0.20 0.29 0.46 0.32 0.72 0.23 0.87 1.12
15 d 0.36 0.40 0.35 0.31 0.35 0.35 0.42 0.38 0.61 0.47 1.09 1.28 0.69 0.41 5.65
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.10 0.01 0.06 0.08 0.04 0.10 0.03 0.11 0.19 0.05 0.24 0.51 0.30 0.14 1.97
10 d 1.46 2.59 1.18 2.74 1.66 2.27 7.36 3.72 14.35 10.55 2.19 16.75 13.22 16.01 24.08
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.36 1.10 0.68 1.61 0.74 1.44 5.04 0.13 6.43 7.25 1.34 11.64 9.11 6.74 14.75
trans-DCCA (ng/g)
15 d 0.10 0.14 0.15 0.23 0.32 0.21 0.55 1.17 1.75 1.11 0.98 2.41 2.25 6.60 13.88
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
10 d 0.03 0.05 0.06 0.04 0.07 0.01 0.25 0.61 0.91 0.55 0.46 1.22 1.18 3.72 2.98
4.08 3.85 6.53 3.73 13.66 14.86 36.00 6.15 12.58 6.61 37.11 26.15 26.77 7.90 82.41
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
1.71 2.44 4.37 1.94 0.41 10.17 25.09 1.87 8.43 3.70 25.67 18.02 14.37 5.31 2.48
3-PBA (ng/g)
15 d 0.16 0.15 0.28 0.39 0.48 0.36 0.22 0.21 3.25 2.57 5.36 3.60 20.74 3.89 51.94
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
10 d
0.06 0.05 0.09 0.06 0.13 0.04 0.12 0.10 1.73 1.33 2.93 1.83 11.83 2.13 2.22
0.17 0.20 ND 0.13 0.16 0.76 1.23 0.69 1.61 1.73 3.83 1.96 1.10 1.06 0.85
± 0.01 ± 0.05 ± ± ± ± ± ± ± ± ± ± ± ±
0.01 0.03 0.30 0.03 0.16 0.89 0.03 2.16 0.15 0.52 0.26 0.56
15 d NDa ND ND ND ND ND ND ND ND ND ND ND ND ND ND
ND < LOQ.
because 3-PBA was more easily metabolized.21 Thus, trans/cisDCCA were more likely to be transferred to egg yolks, and this may have implications for food safety. The concentrations of beta-CP and its three metabolites (trans/cis-DCCA and 3-PBA) in egg whites were plotted over time in Figure 1C, and trends of beta-CP and trans/cis-DCCA were similar; they did not have significant change throughout the experiment. The concentration of 3-PBA was less than LOQ. The concentrations of beta-CP and trans/cis-DCCA were not significantly different, but were significantly greater than that of 3-PBA in egg whites. Dynamics in Droppings and Excretion Rate of BetaCP. Excretion is an important pathway in reducing xenobiotics. As shown in Figure 1D and Figure S2, the concentrations of beta-CP in droppings were in a relatively steady state during exposure, and rapidly decreased during depuration. The depuration t1/2 of beta-CP in droppings was only 1.20 days, and this may be due to incomplete absorption from the feed during exposure, or uptake into hen tissues of higher lipid contents during depuration,29,33 such as fat and skin.9,10 After the exposure ended, concentrations of 3-PBA rapidly decreased, and trans/cis-DCCA were continuously excreted. 3-PBA was most readily metabolized and excreted, and this was also observed in egg and tissues. For further insight into excretion characteristics by dropping, excretion rate was introduced. Excretion rates were calculated by dividing the mass of beta-CP in droppings by that in ingested feed, and the results are presented in Figure S3. Excretion rates of beta-CP increased and then decreased, ranging from 6.9% to 9.3%. Under the exposure, the average excretion rate was 8.0%. In previous investigation, the excretion rate of chlordane was only 1.1%.34 In comparison, excretion is an important pathway for beta-CP elimination in laying hens. Residues in Tissues and Distribution Characteristics. Residues of beta-CP and its three metabolites in tissues at days 10 and 15 appear in Table 1. The highest concentration of betaCP at the 10th day was observed in fat, followed by ovum, skin, intestine, brain, ovary, and other tissues. Similar to organochlorine pesticides,34 beta-CP is lipophilic and concentrates in lipid tissues. Similar results have been reported for beta-CP in mice9 and bovines.10 Compared to concentrations of beta-CP in tissues at the10th day, beta-CP at the 15th day decreased
brain, ovary, liver, and kidney were homogenized in 1 mL of phosphate buffer (0.05 M, pH 7.0, 4 °C) and then centrifuged at 12000g for 10 min (4 °C). The enzyme solution (supernatant) was first used to measure enzyme activity. Then, the reasonable enzyme concentrations were used to measure SOD, MDA, and CAT. Methods of these indicators were the same as with the previous method.28 Statistical Analysis. A first-order kinetics model was used to evaluate the elimination of beta-CP in blood, egg yolks, and droppings. Charts were created using OriginPro 8.0 (OriginLab Corporation). Antioxidant data were statistically analyzed with SPSS Statistics 19.0 (IBM SPSS Inc.). Significant differences between groups were analyzed using an independent sample Student’s t test (p < 0.05).
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RESULTS AND DISCUSSION Dynamics in Blood. The dynamics of beta-CP in blood is presented in Figure 1A. During the 10 days of exposure, the concentrations of beta-CP in blood slowly increased, and the increment was small. During depuration with untreated feed, it quickly decreased. Metabolites (trans/cis-DCCA and 3-PBA) were lower than LOQ. The data of beta-CP during depuration were adjusted to the first-order kinetics equation, and R2 and the half-life (t1/2) were 0.9885 and 4.42 days, respectively. BetaCP was metabolized more slowly in our experiments than in previous investigations,29 perhaps because more beta-CP in other tissues was redistributed to the blood. Dynamics in Egg Whites and Egg Yolks. Concentration trends of beta-CP and its three metabolites (trans/cis-DCCA and 3-PBA) in egg whites and egg yolks are depicted in Figure 1B. Unlike persistent organochlorine pesticide30 and other chemicals,31,32 concentrations of beta-CP in egg yolks rapidly achieved a balanced state at the fifth day. During depuration, t1/2 of beta-CP in egg yolks was only 3.56 days compared with t1/2 of α-hexabromocyclododecane (17.4 days)32 and αhexachlorocyclohexane (6.71 days).30 This revealed that betaCP was not persistent in egg yolks, while beta-CP was more slowly depurated after continuous exposure than after single exposure.29 The maximum concentration of beta-CP was 4.8 ng/g in egg yolks on the 10th day, below the maximum residue limit (MRL, 50 ng/g) allowed in eggs for the European Union and the United States. Concentrations of trans/cis-DCCA increased over time during the 10 days of exposure and declined during the 5 days of depuration. Concentrations of trans/cis-DCCA were greater than concentrations of 3-PBA, 7649
DOI: 10.1021/acs.jafc.7b02581 J. Agric. Food Chem. 2017, 65, 7647−7652
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Journal of Agricultural and Food Chemistry
Figure 2. Mass distribution of beta-CP and its three metabolites (trans/cis-DCCA and 3-PBA) in tissues at 10 d (A) and 15 d (B).
Figure 3. Influences of beta-CP on SOD (A), CAT (B), and MDA (C) of four tissues of laying hens after 10 d exposure; asterisks indicate significant differences (p < 0.05).
Figure 4. Mass distribution of beta-CP and its three metabolites (trans/cis-DCCA and 3-PBA) in three digestive samples (A) and the main form of beta-CP in three digestive samples (B).
except in fat, likely because fat is chiefly composed of triglycerides, which accumulate lipophilic xenobiotics. However, the brain and ovum have more phospholipids and cholesterol but fewer triglycerides. In addition, the concentrations of betaCP were less than MRLs (50 ng/g) in the United States for fat and muscle, and MRL (50 ng/g) in the European Union for edible offal. trans/cis-DCCA and beta-CP were similarly distributed in most tissues, but trans/cis-DCCA were significantly higher than beta-CP in thigh muscle. Concentrations of 3-PBA in the main detoxification organs, such as liver and kidney, were
significantly lower than in other tissues. Meanwhile, three metabolites were found in all tissues in the decreasing order trans-DCCA > cis-DCCA > 3-PBA. This indicated that transDCCA was more stable. Comparing three metabolites at the 10th day and the 15th day indicated that trans/cis-DCCA greatly decreased except in fat, and 3-PBA was reduced in all tissues. The concentrations of 3-PBA were lower than LOQ in all tissues at the 15th day, indicating that 3-PBA could be more readily further metabolized. The masses of beta-CP and its three metabolites in tissues were calculated by multiplying their concentrations in tissues by 7650
DOI: 10.1021/acs.jafc.7b02581 J. Agric. Food Chem. 2017, 65, 7647−7652
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Journal of Agricultural and Food Chemistry Notes
masses of tissues, and the results appear in Figure 2. The majority of beta-CP and its three metabolites were distributed in fat, ovum, intestine, thigh muscle, and breast muscle at the 10th day. The mass of beta-CP was the highest in fat, while its three metabolites were most abundant in thigh muscle at the 10th day, because beta-CP was more lipophilic than the metabolites, and mass of thigh muscle had absolute advantage. Subsequently, fat and intestine became the main storage tissues of trans/cis-DCCA. Thus, trans/cis-DCCA were partially lipophilic, and 3-PBA was not lipophilic. Activity of Antioxidant Enzymes and Content of MDA. Because xenobiotics may break the balance of an antioxidant system, we measured SOD activity and MDA in brain (nerve center), ovary (reproductive organ), liver, and kidney (main detoxification organ) at the 10th day. These data appear in Figure 3. The SOD activity was significantly increased in ovary, but was not significantly changed in other tissues. Significant enhancement of the SOD activity with low-dose xenobiotics was observed in previous investigation.28 There were no differences between treatment group and control group for CAT in four tissues (Figure 3). MDA was decreased in the kidney and ovary but unchanged in the liver and brain. Thus, oxidative stress induced by beta-CP was not significant at this dose. In turn, there might be only slight stimulation for antioxidant system. Digestive Model. To obtain further insight into the fate of beta-CP in the digestive system, a digestive model was utilized to observe the possible degradation behavior. As shown in Figure 4, trans/cis-DCCA and 3-PBA appeared in the digestive process, and mainly they existed in dialysate. However, beta-CP was mainly retained in the digestion residue, and it was degraded about 20% after digestion, perhaps due to the greater water solubility of three metabolites, along with the passive diffusion of absorption.23 Although the digestive model did not explain all aspects of the digestive process and absorption, we did note that the beta-CP was metabolized and that its metabolites were absorbed. Beta-CP and its metabolites (cis/trans-DCCA and 3-PBA) were transferred to egg yolk, and they accumulated in tissues with high lipid contents. Meanwhile, beta-CP was found as metabolites in the eggs and edible tissues of laying hens, which may be transferred to humans via food consumption.
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The authors declare no competing financial interest.
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ASSOCIATED CONTENT
* Supporting Information S
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.7b02581. Analyte chemical structures, MS parameters, recovery and LOQ of analytes in samples, excretion rate of betaCP, and chromatograms of analytes (PDF)
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REFERENCES
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AUTHOR INFORMATION
Corresponding Author
*Tel: +86 010-62731294. Fax: +86 010-62732937. E-mail:
[email protected]. ORCID
Zhiqiang Zhou: 0000-0002-0816-6203 Donghui Liu: 0000-0002-7121-2364 Funding
This work was supported by the National Natural Science Foundation of China (Contract Grants 21307155, 21337005, 21677175). 7651
DOI: 10.1021/acs.jafc.7b02581 J. Agric. Food Chem. 2017, 65, 7647−7652
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DOI: 10.1021/acs.jafc.7b02581 J. Agric. Food Chem. 2017, 65, 7647−7652
