Pesticide Contamination in Central Kentucky Urban Honey: A Pilot Study.
Honey has increased in popularity among shoppers at chain and local marketplaces. The increased popularity has led to small-scale urban beekeeping becoming an attractive practice, coinciding with the local food movement and concern over the decreasing honeybee population (Peters, 2012). Concerning to the producers of honey, and ultimately the end market, are the potential contaminants that can result in a toxic hive product or hive collapse. During foraging, honeybees are exposed to pollutants deposited on plants and from systemic pesticides. Most honeybees and their food are contaminated by spray applications that bees fly through or by residual pesticide left on foliage or floral parts (especially pollen).
Honeybees can bring these pollutants into their hive via collected nectar or pollutants that attach to the pollen-collecting hairs on their body; the aforementioned modes of pollutant transport yields the possibility of pesticide contamination in honey and other bee products, including the honeycomb (Mussen & Brandi, 2010). Pesticide contamination could weaken the beneficial properties of honey and, if present in hazardous amounts, pose a threat to human health (Peters, 2012).
Assessment of environmental diffusion of pesticides can be accomplished via matrix analyses of hive products, such as beeswax or honey (Chauzat et al., 2006). Monitoring pesticide residues in honey is also critical for assessing potential risk to consumer health and health of the hive, and can provide information on the pesticide treatments that have been used in areas surrounding hives (Peters, 2012). Researchers have used bees and bee products as biomonitoring agents for environmental contamination (Badiou-Beneteau et al., 2013; Barganska, Slebioda, & Namiesnik, 2016; Chauzat et al., 2011; de Oliveira, Queiroz, da Luz, Porto, & Rath, 2016; Malhat, Haggag, Loutfy, Osman, & Ahmed, 2015; Perez et al., 2016), to assess heavy metal environmental contamination (Giglio et al., 2017; Matin, Kargar, & Buyukisik, 2016), and to analytically document chemicals used in agricultural settings (Irungu et al., 2016; Niell et al., 2015). Monitoring research suggests that urban bees are exposed to even higher levels of pesticides than rural bees. Approved pesticide-use levels often are much higher for home and garden use than the levels permitted in commercial agriculture (Peters, 2012).
The rising fear of potential diseases transmitted via mosquito bites has sparked increased mosquito abatement through commercial pesticide application, homeowner pesticide application, and public health programming. Pyrethroids are an extensively used class of insecticides with acute toxicity to insects governed by toxicological actions upon the central nervous system. Humans are less sensitive to pyrethroids than are insects, due to a combination of faster metabolic disposal, higher body temperature, and an inherently lower sensitivity of the similar human ion channel target sites. These features led to pyrethroids becoming the major pesticide class for agricultural and public health applications (Ray & Fry, 2006). As an insecticide with both repellent and killing functions, pyrethroids are the mainstay of current mosquito management. Insecticide use in the U.S. accounted for 40% of total world use by volume in 2006, and at least 9% or 70 million pounds of these insecticides were applied in urban settings (Zhu et al., 2016).
Due to extensive use of pesticides on food, escalated commercial pesticide use, and easy unsupervised access to pesticides by the general public, the public likely is facing higher risks from pesticide exposure than currently acknowledged. Unfortunately, the Food and Drug Administration has no regulations or definition for honey, so approximately 70% of the honey on U.S. grocery store shelves is adulterated. Adulterated honey can contain cheaper sweeteners, illegally trafficked honey, and/or chemicals. U.S. honey companies can dilute honey with other sweeteners to save money. Some companies receive imported honey, which can come from countries with negligent environmental safety regulations (The Honeybee Conservancy, 2017).
The best way to avoid adulterated honey is to buy local honey from a source that you can trust such as from farmers markets, coops, or local apiaries. The Kentucky State Beekeepers Association (2018) launched the Kentucky Certified Honey Program in summer 2018 as a new marketing program. This certification signifies that the producers' beehives are being managed within the state, the bees have collected nectar and pollen within the area immediately surrounding their beehives, and the honey is processed and bottled in Kentucky.
Organochlorine Pesticides and Heavy Metals
Organochlorine pesticides are chlorinated hydrocarbons used extensively from the 1940s through the 1960s in agriculture and mosquito control. These compounds are lipophilic pesticides known for their high toxicity, slow degradation, and bioaccumulation in lipid-rich tissue such as body fat. As a result, most living organisms now contain organochlorine residues, with the highest concentrations generally occurring in carnivorous species. These chemicals belong to the class of persistent organic pollutants, with high persistence in the environment through large reservoirs that remain in soils, sediments, and other environmental compartments (Huang et al., 2018).
Among environmental contaminants found on honeybees and in bee products, the most commonly studied are heavy metals. Honeybees are good biological indicators of anthropogenic pollution because they can indicate the chemical damage of their environment through high bee mortality and the residues present on their bodies or in beehive products. Honeybees sample most environmental sectors (i.e., soil, vegetation, water, air) through foraging (Abrol, 2013).
Ecosystem pollution from chemicals and heavy metals have greatly accelerated during the last few decades due to mining, smelting, manufacturing, use of agricultural fertilizers, pesticides, municipal wastes, traffic emissions, industrial emissions, and industrial chemicals (Bogdanov, 2006). The primary characteristic that distinguishes heavy metals from other pollutants, such as pesticides, is their introduction into an area and their environmental outcome. Pesticides are scattered both in time and space and deteriorate by means of various environmental factors over differing periods of time. Heavy metals are discharged in a continuous manner by various natural and human sources to continuously enter the physical and biological cycles (Porrini et al., 2003).
The main sources for contamination of honey with heavy metals result from placing hives near urban areas with heavy car traffic or near industrialized areas, or from storing honey in objects or containers made of materials that are unsuitable (Ciobanu & R dulescu, 2016). A number of variables have to be considered when using bees, or beehive products such as honey, to monitor heavy metals in the environment: the weather (rain and wind can reduce air pollution or transfer heavy metals to other environmental areas); the season (the nectar flow, which is usually more prominent in spring than in summer and autumn, could dilute the pollutant); and the botanical origin of the honey (flowers with an open morphology are more vulnerable to pollutants) (Porrini et al., 2003).
Pesticides and Heavy Metal Health Issues
Several studies have cited the human health hazards concerning honey contamination by pesticides (Al-Waili, Salom, Al-Ghamdi, & Ansari, 2012; Amendola, Pelosi, & Dommarco, 2011; Celli & Maccagnani, 2003; Chauzat et al., 2006; Chen, Tao, McLean, & Lu, 2014; Chiesa et al., 2016; Frazier, Mullin, Frazier, & Ashcraft, 2008; Long & Krupke, 2016; Mukherjee, 2009; Porrini et al., 2003; Sanchez-Bayo & Goka, 2014). The research done by Mahmoudi and coauthors (2016) found that floral sources can create a significant influence on honey safety and contamination. Rissato and coauthors (2007) showed that honey could contain a low level of contamination from pesticide residues with a much higher concentration of pesticide used for controlling dengue mosquitos. Mullin and coauthors (2010) conducted the most extensive North American survey of pesticide residues in managed honeybee colonies to date in 23 states and 1 Canadian province during the 2007-2008 growing season. Pyrethroids were the dominant class of insecticides detected in all samples. A study done by Stahl (2002) indicated that all pesticides are associated with some risk of harm to human health and the environment.
This pilot study examined two research questions:
1. Are residues from pyrethroid pesticide present in urban honeybee hive products (i.e., honey, honeycombs, and beeswax)?
2. Are organochlorine pesticides and heavy metals present in urban honeybee hive products (i.e., honey, honeycombs, and beeswax)?
Materials and Methods
To determine if pyrethroid pesticide residues were present in urban honeybee hive products, a total of 20 1-lb honey samples were collected from beekeepers located in urban areas (i.e., cities or towns) in Central Kentucky. This pilot study included cities or towns within McLean, Hardin, Bullitt, Jefferson, Nelson, Shelby, Oldham, Franklin, Woodford, Fayette, Madison, and Menifee counties. Inclusion criteria were urban beekeepers or amateur beekeepers who maintained hives within 4 miles of their residence or 4 miles from a park, campground, or recreational area. Exclusion criteria included commercial beekeepers or those beekeepers who lived in rural areas that would not be involved in mosquito abatement spraying.
Each 1-lb honey sample was placed in a 1-lb BPA-free plastic jar and then shipped to the U.S. Department of Agriculture (USDA) Agricultural Marketing Service's National Science Laboratories in Gastonia, North Carolina, which was contracted to perform pesticide analysis for the presence of d-phenothrin, prallethrin, and piperonyl butoxide. The National Science Laboratories performed a pesticide residue analysis (method AOAC OMA 2007.01) referred to as QuEChERS, which stands for Quick-Easy-Cheap-Effective-Rugged-Safe. The honeybee product method uses the QuEChERS approach with a cleanup step to help overcome the added complexities and interferences associated with residue testing of honeybee products.
Sample extracts were analyzed for pesticide residues by gas chromatography (GC) and/or liquid chromatography (LC) using mass selective detection systems. Using both LC with tandem mass spectrometry (LC/MS/ MS) and GC approaches allow for a faster, more complete picture of pesticide residues. The use of tandem mass spectrometry also permits identification of the target pesticides through the selection of specific multiple reaction monitoring (MRM) transitions for each compound.
To determine if organochlorine pesticide residues and heavy metals were present in urban honeybee hive products, 10-50 mL beeswax honeycomb samples and 8-50 mL honey samples were collected during the months of May-December 2017 for pesticide residue analysis. In brief, 10 g of sample material was mixed with acetonitrile and agitated. Additions of sodium chloride, magnesium sulfate, and buffering salts were used for phase separation and pH adjustment. Intensive agitation and spinning in a centrifuge produced a raw extract. Using dispersive solid phase extraction cleanup (d-SPE) to remove water and undesired co-extractives produced the final extract that was analyzed by GC/LC techniques.
Wax honeycomb analysis consisted of adding 15 mL methanol to each tube and sonicating for 1 hr, then centrifuging at 2,000 rpm for 20 min. Tubes were then frozen at -20 [degrees]C for 2 hr. The supernatant methanol was passed through cellulose extraction thimbles to collect the filtered separated solvent. A second extraction was performed with the extracts transferred to evaporation tubes and placed in a 75 [degrees]C water bath. Once the extracts were nearly dry, they were moved to 1 mL volumetric tubes and brought to volume with methanol. The analysis was done by both LC/MS/ MS and GC approaches.
We looked for the following pesticides: alpha-cyclohexane, 1,2,3,4; beta-cyclohexane, 1,2,3,4; gamma-cyclohexane, 1,2,3,4; delta-cyclohexane, 1,2,3,4; heptachlor; 1,4:5,8-dimethanonaphthale; epoxyheptachlor; endosulfan I; p,p'-dichlorodiphenyldichloroethylene (p,p'-DDE); dieldrin; endrin; p,p'-DDD; endosulfan II; endrin aldehyde; p,p'-DDD+DDT; endosulfan sulfate; and methoxychlor.
Honey was prepared prior to the digestion procedure by placement in a desiccator under vacuum until dry. Once dry, the samples were ground using a mortar and put through a 2 mm sieve. We placed 0.2 g of solid sample into a preweighed digestion vessel, then added 5 mL of trace metal grade nitric acid and left the sample at room temperature overnight. We then closed and tightened the digestion vessels using a specialized wrench. Next we placed the vessels in the microwave for two consecutive cycles: once at power level 3 for 30 min, then at power level 2 for 30 min.
Once cooled, we opened the vessels and added 20 mL of deionized water. Then the vessels were shaken. We recorded the full vessel weight and collected sample aliquots in centrifuge tubes. Prior to inductively coupled plasma mass spectrometry (ICP/ MS) analysis, we diluted the samples 1:10. Note: the dilution factor was calculated by subtracting the weight of the empty vessel before analysis from that of the loaded vessel at the end, then dividing by the mass of the samples used. Using mass instead of volume for this calculation increases the accuracy of the results. The results of the ICP/MS analysis were multiplied by this calculated dilution factor as well as by the 1:10 dilution factor.
We tested a total of 20 raw unfiltered honey samples from urban hives for Duet pesticide containing d-phenothrin, prallethrin, and piperonyl butoxide by the USDA National Science Laboratories using GC/ LC analysis. The report of analytical test results showed that samples were below the detectable limit for d-phenothrin, prallethrin, and piperonyl butoxide.
As seen in Table 1, we tested a total of 6 honeycomb samples and 12 honey samples by GC/MS for organochlorine pesticides and 72% exceeded one or more U.S. Environmental Protection Agency (U.S. EPA) tolerable daily intake (TDI) values. Results are based on U.S. EPA (2018) noncarcinogen TDI values:
* 1,4:5,8-dimethanonaphthale (CAS 309002): U.S. EPA limits daily oral intake to 0.00003 (mg/kg/d); honey samples FA2 and JE1 exceeded daily oral intake.
* Heptachlor (CAS 76448): U.S. EPA limits daily oral intake to 0.0005 (mg/kg/d); honey sample MA1 exceeded daily oral intake.
* Dieldrin (CAS 60571): U.S. EPA limits daily oral intake to 0.00005 (mg/kg/d); honey samples NI1 and PO1 exceeded daily oral intake.
* p,p'-DDD+DDT (CAS 50293): U.S. EPA limits daily oral intake to 0.0005 (mg/kg/d); honeycomb samples BU1 and JE1 and honey samples CS1, FA1, FA3, LR1, MA1, NI1, and RO1 exceeded daily oral intake.
* Endrin (CAS 72208): U.S. EPA limits daily oral intake to 0.0003 (mg/kg/d); honey samples FA2 and FA3 exceeded daily oral intake.
* Endrin aldehyde (CAS 72208): U.S. EPA limits daily oral intake to 0.0004 (mg/kg/d); honey samples FA3 and PO1 exceeded daily oral intake.
* Methoxychlor (CAS 72435): U.S. EPA limits daily oral intake to 0.005 (mg/kg/d); honey samples FA2 and MA1 and honeycomb samples JE1 and LM1 exceeded daily oral intake.
Additionally, we analyzed these honey and honeycomb samples for heavy metal content. Some lead contamination was apparent, but results were below the tolerable upper intake level (UL) guidelines (6 [micro]g/day) set by U.S. EPA, which is the maximum usual daily intake level at which no risk of adverse health effects is expected for most individuals in a specific group based on stage of life.
As seen in Table 2, 56% of the 18 samples tested for lead exceeded the World Health Organization/Food and Agriculture Organization (WHO/FAO) limit of 50 ppb, the Joint FAO/WHO Expert Committee on Food Additives (JECFA) provisional tolerable weekly intake of 0.025 mg/kg/bw, and the California Proposition 65 Safe Drinking Water and Toxic Enforcement Act of 1986 acceptable intake level of 0.0005 mg/day.
The detection of pesticide residues in honey is essential for determining that human exposure to contaminants through dietary intake does not exceed acceptable levels. With the local honey market strong and demand for honey on the rise (especially for locally produced honey and specialty honey), the bioaccumulation and short-term environmental uptake of insecticides can cause not only mass poisoning of bees but also a health threat to humans as pesticides are transferred to consumable bee products, affecting their quality and properties.
Honey typically is extracted by means of a centrifugal honey extractor, which makes it achievable to remove the honey without causing damage to the honeycomb. Empty honeycombs are replaced back into the hive for the bees to refill. Bees are attracted to older honeycombs because these combs are rich in the scent of bees, honeybee pheromones, beeswax, pollen, and honey. Unfortunately, though, old honeycombs can be a source of health problems for bees and contamination of bee products. Beeswax readily retains chemical contaminants such as miticides to control parasitic mites as well as fungal and bacterial spores inside the hive. Beeswax also retains agricultural or urban insecticides and pesticides. Beekeepers generally are taught to reuse honeycombs to reduce the workload on their bees and to facilitate honey production. There is a need for education, especially for amateur apiarists, on the practice of replacing old honeycombs to reduce the risk of bee product contamination.
Risk assessment of the impact of pesticides on human health differs in the periods and levels of exposure, the types of pesticides used (regarding toxicity and persistence), and the environmental characteristics of the areas where pesticides are applied. Risk assessments, however, fail to look at chemical mixtures, synergistic effects, myriad health endpoints (such as endocrine disruption), disproportionate effects to vulnerable population groups, and regular noncompliance with product label directions. These inadequacies contribute to severe limitations in defining real-world poisoning as captured by epidemiologic studies.
This study begins to establish a baseline of exposure from honey and honeybee products from one state's urban hives. Upon further examination of different regions, policy makers can be better informed about any necessary regulatory reactions to this unregulated industry. In addition, informed apiarists can protect their honeybees and hives by locating them away from areas contaminated by the pesticides and metals.
The overall goal of this research was to protect consumer health by addressing the need for regular monitoring programs for pesticide residues and heavy metal con taminants in honey and consumable bee products. Regional studies show that the statistically significant results concerning p,p'-DDD+DDT contamination in Kentucky is on the high end of the continuum and warrants further investigation to see if there are areas of higher concentrations that might pose risks to consumers.
Limitations of this study included the small sampling size and a short time period in which the sampling was conducted. With further research and analysis during an extended time period, a more comprehensive determination of contaminants and residues in honey and other bee products can help to assess the potential risk to consumer health. Pesticide treatments that have been used in areas surrounding the hives can also be evaluated, thereby offering a more realistic picture of possible health risks to consumers and honeybees.
Acknowledgement: This work was supported by a University-Funded Major Project Award from Eastern Kentucky University. The funders had no role in study design, data collection, analysis, decision to publish, or preparation of the manuscript. AM
Corresponding Author: Clint Pinion, Jr., Assistant Professor, Department of Environmental Health Science, College of Health Science, Eastern Kentucky University, 521 Lancaster Avenue, Dizney 220, Richmond, KY 40475. E-mail: email@example.com.
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Mary Sheldon, MPH
Clint Pinion, Jr., DrPH, RS
James Klyza, PhD, CIH
Eastern Kentucky University
Anne Marie Zimeri, PhD
University of Georgia, Athens
TABLE 1 Organochlorine Pesticide Testing Analysis Results Sample Target Compounds Heptachlor 1,4:5,8- Dieldrin Endrin (ppb) Dimethano- (ppb) (ppb) naphthale (ppb) BL1 (C) BDL BDL BDL BDL BU1 (C) BDL BDL BDL BDL CS1 (H) BDL BDL BDL BDL FA1 (H) BDL BDL BDL BDL FA2 (H) BDL 0.72# BDL 56.12# FA2 (C) BDL BDL BDL BDL FA3 (H) BDL BDL BDL 158.86# FA4 (H) BDL BDL BDL BDL JE1 (H) BDL 0.34# BDL BDL JE1 (C) BDL BDL BDL BDL LM1 (C) BDL BDL BDL BDL LR1 (H) BDL BDL BDL BDL MA1 (H) 2.50# BDL BDL BDL NI1 (H) BDL BDL 638.60# BDL PO1 (H) BDL BDL 98.96# BDL RO1 (H) BDL BDL BDL BDL SH1 (H) BDL BDL BDL BDL SH2 (C) BDL BDL BDL BDL Tolerable daily intake (TDI) TDI 0.0005 0.00003 0.00005 0.0003 (mg/kg/day) Sample Target Compounds p,p'- Endrin Methoxychlor DDD+DDT Aldehyde (ppb) (ppb) (ppb) BL1 (C) BDL BDL BDL BU1 (C) 225.72# BDL BDL CS1 (H) 28.31# BDL BDL FA1 (H) 145.02# BDL BDL FA2 (H) BDL BDL 38.97# FA2 (C) BDL BDL BDL FA3 (H) 137.28# 5.56# BDL FA4 (H) BDL BDL BDL JE1 (H) BDL BDL BDL JE1 (C) 294.07# BDL 622.02# LM1 (C) BDL BDL 158.10# LR1 (H) 55.33# BDL BDL MA1 (H) 207.43# BDL 516.31# NI1 (H) 26.75# BDL BDL PO1 (H) BDL 29.69# BDL RO1 (H) 29.61# BDL BDL SH1 (H) BDL BDL BDL SH2 (C) BDL BDL BDL Tolerable daily intake (TDI) TDI 0.0005 0.0004 0.005 (mg/kg/day) BDL = below detection limit; C = honeycomb sample, H = honey sample. Note. Bolded numbers indicate that results exceed TDI. Note: Results exceed TDI indicated with #. TABLE 2 Heavy Metal Testing Analysis Results Sample Lead (ppm) Exceeds Daily Intake Limits * BL1 (C) 1.297 Yes BU1 (C) 0.070 Yes CS1 (H) BDL No FA1 (H) BDL No FA2 (H) BDL No FA2 (C) BDL No FA3 (H) BDL No FA4 (H) 3.240 Yes JE1 (H) BDL No JE1 (C) 0.230 Yes LM1 (C) 0.127 Yes LR1 (H) 0.176 Yes MA1 (H) BDL No NI1 (H) 5.653 Yes PO1 (H) BDL No RO1 (H) 0.192 Yes SH1 (H) 1.104 Yes SH2 (C) 0.210 Yes BDL = below detection limit; C = honeycomb sample; H = honey sample. * WHO/FAO = 50 ppb; JECFA0.025 mg/kg/ bw; California Proposition 65 = 0.0005 mg/day.
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|Title Annotation:||ADVANCEMENT OF THE SCIENCE|
|Author:||Sheldon, Mary; Pinion, Clint, Jr.; Klyza, James; Zimeri, Anne Marie|
|Publication:||Journal of Environmental Health|
|Article Type:||Cover story|
|Date:||Jul 1, 2019|
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