Abstract
With thousands of pesticides registered by the United States Environmental Protection Agency, it not feasible to sample for all pesticides applied in agricultural communities. Hazard-ranking pesticides based on use, toxicity, and exposure potential can help prioritize community-specific pesticide hazards. This study applied hazard-ranking schemes for cancer, endocrine disruption, and reproductive/developmental toxicity in Yuma County, Arizona. An existing cancer hazard-ranking scheme was modified, and novel schemes for endocrine disruption and reproductive/developmental toxicity were developed to rank pesticide hazards. The hazard-ranking schemes accounted for pesticide use, toxicity, and exposure potential based on chemical properties of each pesticide. Pesticides were ranked as hazards with respect to each health effect, as well as overall chronic health effects. The highest hazard-ranked pesticides for overall chronic health effects were maneb, metam sodium, trifluralin, pronamide, and bifenthrin. The relative pesticide rankings were unique for each health effect. The highest hazard-ranked pesticides differed from those most heavily applied, as well as from those previously detected in Yuma homes over a decade ago. The most hazardous pesticides for cancer in Yuma County, Arizona were also different from a previous hazard-ranking applied in California. Hazard-ranking schemes that take into account pesticide use, toxicity, and exposure potential can help prioritize pesticides of greatest health risk in agricultural communities. This study is the first to provide pesticide hazard-rankings for endocrine disruption and reproductive/developmental toxicity based on use, toxicity, and exposure potential. These hazard-ranking schemes can be applied to other agricultural communities for prioritizing community-specific pesticide hazards to target decreasing health risk.
Keywords: pesticide prioritization, hazard-ranking, community health, chronic health effects
1. INTRODUCTION
Pesticide exposure is a major environmental health issue in agricultural communities (Arcury et al., 2006; Coronado et al., 2011; Liebman et al., 2007; Simcox et al., 1995). Cancer, endocrine disruption, and reproductive/developmental toxicity are among the health effects associated with chronic exposure to pesticides (Baldi et al., 2001; Garry et al., 2002; Oliva et al., 2001; Zheng et al., 2001). Children are particularly vulnerable to these health effects due to their less-developed metabolism and the on-going maturation of their organ systems (Anderson et al., 2000; Faustman et al., 2000; Ribas-Fito et al., 2006).
The ever-increasing and ever-changing use of pesticides has made it unfeasible to rely on environmental and biological sampling for all pesticides to assess health risk in communities (Blasco and Picó, 2009). Hazard-ranking schemes have long been used to rank and prioritize chemicals of greatest health concern (Bro-Rasmussen and Christiansen, 1984; Schmidt-Bleek et al., 1982). Previous approaches to hazard-ranking environmental contaminants have often been limited by incomplete databases, requiring researchers to base hazard-rankings on “likely present contaminants” rather than on quantified levels of identified contaminants (Baun et al., 2006; Mitchell et al., 2002; Siljeholm, 1997). Another common approach has used toxicity to assess known chemical releases; however, consideration of exposure potential has often been lacking (Dix et al., 2007; Neumann et al., 1998). Finally, other hazard-rankings have focused on acute toxicity, neglecting chronic exposure and its associated health effects (Swanson et al., 1997; USEPA, 1992). Identifying and prioritizing pesticides with hazard-ranking schemes that consider pesticide use, toxicity for chronic health effects, and exposure potential is necessary for a more accurate assessment of health risk in agricultural communities.
Gunier (2001) has been a leader in the effort to improve pesticide hazard assessments by developing a pesticide hazard-ranking scheme applied to California for the cancer endpoint. Pesticide use was quantified in California between 1991 and 1994 from the Pesticide Use Report (PUR) system provided by the California Department of Pesticide Regulation. The method developed by Gunier (2001) incorporated exposure potential and cancer toxicity to calculate hazard factors, which were in turn used to calculate hazard-adjusted use for each pesticide. The top hazard-adjusted use pesticides in California from 1991 through 1994 were propargite, methyl bromide, trifluralin, simazine, and molinate (Gunier et al., 2001). On the other hand, the top pesticides used in California in 1994, based solely on weight, were sulfur, unclassified petroleum oil, methyl bromide, metam sodium, and copper hydroxide (CDPR, 2010). The differences between the top hazard-ranked and top applied pesticides by weight underscores how consideration of toxicity and exposure potential, in addition to pesticide use, can improve pesticide hazard prioritization in agricultural communities.
The current study applies a modified and expanded version of the Gunier et al. (2001) hazard-ranking scheme to prioritize pesticide hazards in Yuma County, Arizona from January 2006 through June 2011. It focuses specifically on Yuma County rather than the entire state of Arizona because pesticide use may vary spatially based on crops grown, pests targeted, and local climate (Aspelin and Grube, 1999). With improved specificity, it is possible to identify and prioritize community-specific pesticide hazards. In addition to ranking pesticide hazards for cancer, the scope has been widened with this study to include hazard-ranking schemes for endocrine disruption and reproductive/developmental toxicity, both notable health effects associated with chronic pesticide exposure. This study is one of the first to provide pesticide hazard-rankings for endocrine disruption and reproductive/developmental toxicity. The most significant pesticide hazards in Yuma County, Arizona, with respect to cancer, endocrine disruption, reproductive/developmental toxicity, and overall chronic health risk are reported.
2. METHODS
2.1 Pesticide Use Data
Pesticide use in Yuma County for January 2006 to June 2011 was obtained from the Arizona Department of Agriculture Pesticide Application Database, referred to as the “1080 Database”. The Arizona Department of Agriculture, Department of Environmental Quality (2011) requires all regulated growers or pesticide control advisors to submit a “1080” form for all pesticides applications containing an active ingredient listed on the Arizona Department of Environmental Quality Groundwater Protection List. The “1080” database includes application date, application location, crop to which the pesticide was applied, total acreage covered, chemical active ingredient, and chemical trade name. Only high-use pesticides in the hazard-ranking assessments that had a minimum annual average application of 1 pound/square mile of total land in Yuma County (5,519 pounds/year) were included (Gunier et al., 2001).
2.2 Determination of Associated Health Effects
Using a wide range of established criteria lists for cancer, endocrine disruption, and reproductive/developmental toxicity, each high-use pesticide was assessed for association with each health effect. The following cancer criteria lists were considered: Report on Carcinogens from the National Toxicology Program (NTP, 2011), Proposition 65 from the California EPA (CalEPA, 2011), Chemicals evaluated for carcinogenic potential: Corrected Annual Cancer Report from the USEPA (USEPA, 2010) and Agents classified by the IARC Monographs Volumes 1–104 from the International Agency for Research on Cancer (IARC, 2011).
For endocrine disruption, the criteria lists considered were the Initial List of Chemicals for Screening (USEPA, 2009) and Second List of Chemicals for Screening (USEPA, 2011b) from the USEPA Endocrine Disruptor Screening Program, Study on Enhancing the Endocrine Disruptor Priority List with a Focus on Low Production Volume Chemicals from the European Commission (Petersen et al., 2007), List of Potential Endocrine Disruptors from The Endocrine Disruption Exchange (Colborn et al., 1993), Endocrine Disruptors Strategy from the Illinois EPA (IEPA, 1997), Environmental Endocrine Disruptors: A Handbook of Property Data by Lawrence Keith (Keith, 1997), and Growing Doubt: A Primer on Pesticides Identified as Endocrine Disruptors and/or Reproductive Toxicants by Charles Benbrook (Benbrook, 1996).
For reproductive/developmental toxicity, the criteria list from Proposition 65 from the California EPA (CalEPA, 2011) and the USEPA Chronic (Non-Cancer) Toxicity Data for Chemicals Listed under the Emergency Planning and Community Right-to-Know Act, Section 313 (USEPA, 2000) were considered. See Supplementary Material p. 2–4 for more detailed information on each criteria list.
2.3 Hazard Factor Variables
Toxicity for each health effect and exposure potential based on chemical properties were used to calculate the hazard factor for each pesticide. Toxicity was assessed based on the following variables: “class” and “potency.” Exposure potential was also based on two variables, “volatilization flux” and “soil persistence.”
The class weight characterizes how strongly each pesticide is associated with each health effect based on the criteria lists on a scale of 1–10 from low to high. Consideration of multiple cancer criteria lists is an expansion of the Gunier et al. (2001) cancer “class” weighting system, which was limited to the cancer list provided by the USEPA. The cancer “class” weights in this study took into account the number of criteria lists in which the pesticide appeared and the level of the cancer-causing potential (e.g., USEPA “known” carcinogen versus “probable” carcinogen). See Supplementary Material, Table S1 for more detailed information on the cancer “class” weighting system. To assign a “class” weight for endocrine disruption, consideration was given to each criteria list’s publication date and whether it was based on peer-reviewed literature, in addition to the number of criteria lists in which the pesticide appeared and the reported level of endocrine disrupting potential. These extra considerations were given to compensate for the fact that endocrine disruption in humans is generally less understood than cancer, and its relationship with environmental exposures is more scientifically controversial (Daston et al., 2003; Fenner-Crisp et al., 2000). See Supplementary Material, Table S2 for the endocrine disruption “class” weighting system.
In the case that multiple class ratings could be applied, the higher rating was used because this is a more conservative assumption. Pesticides that did not appear on any of the criteria lists were given a class weight of 0 for that health effect, removing the pesticide from that hazard-ranking scheme. Formal “class” weights for reproductive/developmental toxicity were not applied because only 7 high-use pesticides were found on these criteria lists.
“Potency,” the second variable of toxicity, was also weighed on a scale of 1–10 from low to high. The cancer slope factor was used to assign a cancer “potency” weight. For endocrine disruption and reproductive/developmental toxicity “potency” weights, the reference dose (RfD) was used. Cancer slope factors and RfD values were preferentially taken from the Integrated Risk Information System (IRIS) (USEPA, 1993; USEPA, 2011a). When information was not available through IRIS, other official USEPA documents, such as Registration Eligibility Decisions, were used to determine the cancer slope factor or reference dose (RfD). In the case that no cancer slope factor/RfD exists for the pesticide, a potency weight of “1” was applied. See the Supplementary Material for more information on the “potency” weighting systems.
To assess exposure potential of each pesticide, volatilization flux and soil persistence were both weighted on a scale of 1–10 from low to high. Volatilization flux is the pesticide’s tendency to be transferred to the air from the ground. The “flux” weight is calculated using vapor pressure, soil adsorption, and aqueous solubility according to Glotfelty et al. (1989). The “persistence” weight was based on the pesticide’s sandy-loam soil half-life because nearly 80% of Yuma, Arizona’s soil is loam or sandy-loam (Holmes et al., 1905). See Supplementary Material, Table S3 for more information on how “potency,” “flux,” and “persistence” values were weighted.
2.4 Hazard Factor Calculation
Hazard factor values for each pesticide were calculated separately for cancer and endocrine disruption by multiplying the “class,” “potency”, “flux”, and “persistence” weights and dividing by 1,000 to normalize hazard factors to values from 1 to 10 (Gunier et al., 2001). Since no “class” weight was assigned for reproductive/developmental toxicity, the hazard factor was computed as the product of the “potency,” “flux,” and “persistence” ratings divided by 100.
2.5 Hazard-Adjusted Pesticide Use
Hazard-adjusted pesticide use was computed by multiplying the computed hazard factors by the pesticide use (total weight applied) over the 4.5-year time period, as reported in the “1080” database provided by the Arizona Department of Agriculture. Pesticides were ranked for cancer, endocrine disruption, and reproductive/developmental toxicity according to their hazard-adjusted pesticide use for each health effect.
Pesticides were also ranked for overall chronic health effects, incorporating cancer, endocrine disruption and reproductive/developmental toxicity together. For the top 10 hazard-ranked pesticides for each health effect, the overall chronic health effects hazard for each pesticide was computed by dividing the “number of associated chronic health effects” by the “average hazard-ranked position.” The “number of associated chronic health effects” refers to how many of the chronic health effects in which the pesticide was ranked in the top 10. The “average hazard-ranked position” was computed by dividing the pesticide’s placement on each specific chronic health effect endpoint hazard-ranking list by 3. The highest potential average hazard-ranking placement was 1.
3. RESULTS
3.1 Pesticide Use Data
From January 2006 to June 2011, 25.5 million pounds of active ingredients of pounds were applied in Yuma County, with an annual average application of 5.7 million pounds. A total of 223 different pesticide types were used throughout Yuma during this time period. After applying the minimum use criteria, 74 pesticides were considered high-use and thus, further assessed by the hazard-ranking schemes. Despite the relatively small number of pesticides evaluated, these 74 pesticides represented 98% of total applications, by weight, in Yuma County. The highest applied pesticides by weight were Aspergillus flavus 36 colonized wheat seed, bensulide, metam-sodium, trifluralin, and sethoxydim.
3.2 Pesticide Health Effects
Of the 74 pesticides considered for the hazard-rankings, 43 were associated with cancer, endocrine disruption, and/or reproductive/developmental toxicity (Table 1). Many of the pesticides were associated with more than one health effect. Approximately 80% of pesticide pounds applied in Yuma County during this time-period was associated with the chronic health effects of cancer, endocrine disruption, and/or reproductive/developmental toxicity.
Table 1.
Health Effect | Total Application (lbs) | Annual Average Application (lbs) | Pesticides |
---|---|---|---|
Cancer | 6,612,173 | 1,469,372 | 1,3-Dichloropropene, Acephate, Benefin, Bifenthrin, Boscalid, Carbaryl, Cypermethrin, Dimethoate, Iprodione, Malathion, Mandipropamid, Maneb, MCPA, Metam-sodium, Mineral oil, Oxyfluorfen, Pendimethalin, Permethrin, Pronamide, Tribufos, Trifluralin |
Endocrine Disruption | 10,887,689 | 2,419,487 | Abamectin, Acephate, Benefin, Bensulide, Benzoic acid, Bifenthrin, Carbaryl, Chlorpyrifos, Clethodim, Cyfluthrin, Cypermethrin, DCPA, Diazinon, Dimethoate, Endosulfan, EPTC, Esfenvalerate, Fosetyl-Al, Glyphosate, Imidacloprid, Iprodione, lambda- Cyhalothrin, Malathion, Maneb, MCPA, Metam sodium, Oxyfluorfen, Paraquat dichloride, Pendimethalin, Permethrin, Pronamide, Pyrethrins, Trifluralin |
Developmental/Reproductive Toxicity | 2,968,723 | 659,717 | Bifenthrin, Bromoxynil octanoate, Carbaryl, EPTC, Maneb, Metam-sodium, Streptomycin sesquisulfate |
Total | 20,468,585 | 4,548,576 |
3.3 Cancer Hazard-Ranking
The top 5 pesticides by cancer hazard factor out of the 21 pesticides associated with cancer were pronamide, maneb, metam-sodium, oxyfluorfen, and permethrin. The cancer hazard factors ranged across 2 orders of magnitude from 0.01–2.00 (Table 2). The hazard-ranking differed slightly once the pesticide use was adjusted by the cancer hazard factor. The top 5 pesticides by cancer hazard-adjusted use were metam-sodium, maneb, pronamide, mineral oil, and permethrin (Table 2).
Table 2.
Pesticide | Class | Potency | Flux | Persistence | Hazard Factor | 4.5-Year Use | Hazard-Adjusted Use |
---|---|---|---|---|---|---|---|
Metam-sodium | 8 | 8 | 10 | 1 | 0.64 | 1,638,025 | 1,048,336 |
Maneb | 8 | 5 | 5 | 5 | 1.00 | 775,567 | 775,567 |
Pronamide | 8 | 5 | 10 | 5 | 2.00 | 313,257 | 626,514 |
Mineral oil | 8 | 1 | 10 | 3 | 0.24 | 476,065 | 114,256 |
Permethrin | 5 | 5 | 8 | 3 | 0.6 | 158,998 | 95,399 |
Iprodione | 8 | 5 | 5 | 1 | 0.2 | 351,466 | 70,293 |
Bifenthrin | 3 | 5 | 5 | 3 | 0.23 | 220,270 | 50,662 |
Cypermethrin | 3 | 1 | 8 | 3 | 0.07 | 675,052 | 47,254 |
Trifluralin | 3 | 3 | 10 | 5 | 0.45 | 70,068 | 31,531 |
1,3-Dichloropropene | 3 | 5 | 10 | 1 | 0.15 | 205,955 | 30,893 |
Oxyfluorfen | 5 | 8 | 5 | 3 | 0.6 | 45,830 | 27,498 |
Tribufos | 5 | 1 | 8 | 1 | 0.04 | 559,475 | 22,379 |
Benefin | 3 | 1 | 10 | 3 | 0.09 | 233,240 | 20,992 |
Pendimethalin | 3 | 1 | 8 | 8 | 0.19 | 61,594 | 11,703 |
Carbaryl | 8 | 1 | 8 | 1 | 0.06 | 161,212 | 9,673 |
Dimethoate | 3 | 1 | 8 | 1 | 0.02 | 281,234 | 5,625 |
Boscalid | 3 | 1 | 5 | 10 | 0.15 | 36,681 | 5,502 |
Malathion | 3 | 1 | 8 | 1 | 0.02 | 201,252 | 4,025 |
Mandipropamid | 5 | 1 | 5 | 1 | 0.03 | 93,749 | 2,812 |
Acephate | 3 | 3 | 3 | 1 | 0.03 | 57,087 | 1,713 |
MCPA | 3 | 1 | 3 | 1 | 0.01 | 34,121 | 341 |
3.4 Endocrine Disruption Hazard-Ranking
The top 5 pesticides by endocrine disruption hazard factor out of the 32 pesticides associated with endocrine disruption were trifluralin, pendimethalin, bensulide, endosulfan, and maneb. The endocrine disruption hazard factors ranged across 4 orders of magnitude from 0.004–4.00 (Table 3). The top 5 pesticides by endocrine disruption hazard-adjusted use were trifluralin, bensulide, maneb, endosulfan, and chlorpyrifos (Table 3).
Table 3.
Pesticide | Class | Potency | Flux | Persistence | Hazard Factor | 4.5-Year Use | Hazard-Adjusted Use |
---|---|---|---|---|---|---|---|
Trifluralin | 10 | 8 | 5 | 10 | 4.00 | 1,200,000 | 4,800,000 |
Bensulide | 4 | 8 | 10 | 8 | 2.56 | 1,631,499 | 4,176,637 |
Maneb | 9 | 8 | 5 | 5 | 1.80 | 775,567 | 1,396,021 |
Endosulfan | 10 | 8 | 3 | 10 | 2.40 | 507,329 | 1,217,590 |
Chlorpyrifos | 7 | 8 | 3 | 10 | 1.68 | 552,526 | 928,244 |
Metam-sodium | 7 | 5 | 10 | 1 | 0.35 | 1,638,025 | 573,309 |
Pronamide | 7 | 5 | 5 | 10 | 1.75 | 313,257 | 548,200 |
DCPA | 7 | 3 | 8 | 8 | 1.34 | 166,527 | 223,146 |
Cypermethrin | 4 | 5 | 3 | 5 | 0.3 | 675,052 | 202,516 |
Pendimethalin | 7 | 5 | 8 | 10 | 2.80 | 61,594 | 172,463 |
Paraquat dichloride | 7 | 8 | 10 | 1 | 0.56 | 302,833 | 169,586 |
Diazinon | 7 | 10 | 3 | 5 | 1.05 | 151,503 | 159,078 |
Dimethoate | 7 | 10 | 1 | 8 | 0.56 | 281,234 | 157,491 |
Permethrin | 7 | 5 | 3 | 8 | 0.84 | 158,998 | 133,558 |
Imidacloprid | 4 | 5 | 10 | 5 | 1.00 | 131,163 | 131,163 |
Bifenthrin | 9 | 3 | 3 | 5 | 0.41 | 220,270 | 90,311 |
Benefin | 4 | 3 | 3 | 10 | 0.36 | 233,240 | 83,966 |
Malathion | 10 | 5 | 1 | 8 | 0.4 | 201,252 | 80,501 |
Abamectin | 7 | 10 | 3 | 5 | 1.05 | 70,278 | 73,792 |
Cyfluthrin | 7 | 5 | 3 | 8 | 0.84 | 85,769 | 72,046 |
Carbaryl | 10 | 5 | 1 | 8 | 0.4 | 161,212 | 64,485 |
Iprodione | 7 | 5 | 1 | 5 | 0.18 | 351,466 | 63,264 |
Esfenvalerate | 7 | 5 | 3 | 10 | 1.05 | 59,643 | 62,625 |
lambda-Cyhalothrin | 4 | 8 | 3 | 5 | 0.48 | 123,507 | 59,283 |
Glyphosate | 7 | 5 | 3 | 1 | 0.11 | 358,876 | 39,476 |
Oxyfluorfen | 7 | 8 | 3 | 5 | 0.84 | 45,829 | 38,496 |
Benzoic acid | 7 | 1 | 3 | 10 | 0.21 | 114,074 | 23,956 |
MCPA | 7 | 10 | 3 | 3 | 0.63 | 34,121 | 21,496 |
EPTC | 7 | 5 | 1 | 10 | 0.35 | 50,864 | 17,802 |
Clethodim | 4 | 8 | 1 | 5 | 0.16 | 63,473 | 10,156 |
Pyrethrins | 7 | 5 | 1 | 8 | 0.28 | 35,230 | 9,864 |
Acephate | 7 | 8 | 1 | 3 | 0.17 | 57,087 | 9,705 |
Fosetyl-Al | 4 | 1 | 1 | 1 | 0.004 | 143,913 | 576 |
3.5 Reproductive/Developmental Toxicity Hazard-Ranking
There were only 7 pesticides associated with reproductive/developmental toxicity. The ranking of pesticides according to reproductive/developmental toxicity hazard factor were maneb; metam-sodium, bromoxynil octanoate, and EPTC (all ranked the same); bifenthrin; carbaryl; and streptomycin sesquisulfate. The hazard factors ranged two orders of magnitude from 0.05 to 2.00 (Table 4). After the hazard factor was used to adjust pesticide use, the ranking changed to maneb, metam-sodium, bifenthrin, carbaryl, and bromoxynil octanoate, EPTC, and streptomycin sequisulfate (Table 4).
Table 4.
Pesticide | Potency | Flux | Persistence | Hazard Factor | 4.5-Year Use | Hazard-Adjusted Use |
---|---|---|---|---|---|---|
Maneb | 8 | 5 | 5 | 2.00 | 775,567 | 1,551,134 |
Metam-sodium | 5 | 10 | 1 | 0.50 | 1,638,025 | 819,013 |
Bifenthrin | 3 | 5 | 3 | 0.45 | 220,270 | 99,122 |
Carbaryl | 5 | 8 | 1 | 0.40 | 161,212 | 64,485 |
Bromoxynil octanoate | 5 | 10 | 1 | 0.50 | 59,231 | 29,616 |
EPTC | 5 | 10 | 1 | 0.50 | 50,864 | 25,432 |
Streptomycin sesquisulfate | 5 | 1 | 1 | 0.05 | 101,580 | 5,079 |
3.6 Specific and Overall Chronic Health Effect Rankings
Taking into account all 3 chronic health effects together (i.e., cancer, endocrine disruption, reproductive/developmental toxicity), the top-ranked pesticides were maneb, metam sodium, trifluralin, pronamide and bifenthrin (Table 5).
Table 5.
Pesticide | Number of Associated Health Effects | Average Hazard Ranking Placement | Overall Rank |
---|---|---|---|
Maneb | 3 | 2 | 1.50 |
Metam Sodium | 3 | 3 | 1.00 |
Trifluralin | 2 | 5 | 0.40 |
Pronamide | 2 | 5 | 0.40 |
Bifenthrin | 2 | 5 | 0.40 |
Bensulide | 1 | 2 | 0.50 |
Mineral oil | 1 | 4 | 0.25 |
Endosulfan | 1 | 4 | 0.25 |
Carbaryl | 1 | 4 | 0.25 |
Permethrin | 1 | 5 | 0.20 |
4. DISCUSSION
The cancer hazard-ranking scheme developed by Gunier et al. (2001) was modified and expanded to prioritize pesticide hazards in Yuma County, Arizona. This study also developed and applied the first hazard-ranking schemes for endocrine disruption and reproductive/developmental toxicity that take into account pesticide use, toxicity, and exposure potential.
The relative order of hazard-ranked pesticides in this study was different from pesticide application by weight alone in Yuma County. The top hazard-ranked pesticides appear at the intersection of pesticide use, toxicity, and exposure potential. For example, pronamide was ranked the 4th highest overall pesticide hazard in Yuma, but it ranked 12th by pesticide application weight. In fact, pronamide’s application was about 100,000 pounds/year less than maneb, the 4th highest applied pesticide by weight. Pronamide’s high exposure potential via volatilization largely influenced pronamide’s placement as the 4th highest overall hazard-ranked pesticide.
The hazard-ranking schemes effectively revealed pesticides of concern that might have gone unnoticed if pesticide application by weight was the only consideration. Most notably, pronamide and bifenthrin were the 4th and 5th highest overall hazard-ranked pesticides, despite the fact that neither pesticide appeared at all in the top 10 pesticides applied by weight for the same time period. The hazard-ranking schemes were similarly effective at de-prioritizing pesticides with no associated health effects, even if they were highly applied. This was the case with Aspergillus flavus 36 colonized wheat seed, which was applied in a much greater quantity than any other pesticide, yet did not appear on any final hazard-ranking list because it was not included on the pre-established criteria lists for the considered health effects.
As expected, the hazard-adjusted use rankings in Yuma County, Arizona differed from the rankings for California by Gunier et al. (2001). Only trifluralin and metam-sodium appeared in the top 10 hazard-ranked pesticides in both studies. A partial reason for these dissimilarities is likely to be because of the unique pesticide use patterns in the two different study sites during two different study periods. In fact, some of the top hazard-ranked pesticides in Gunier et al.’s (2001) ranking, which considered pesticides used from 1991 through 1994, may no longer be used in this updated study period of 2006–2011. This is exemplified by methyl bromide, the second highest cancer hazard in the California study by Gunier et al. (2001), which has since been phased out by the USEPA due to evidence that it depletes stratospheric ozone (USEPA, 2011c), although a few exemptions continue to be granted. While methyl bromide, unsurprisingly, did not appear in the hazard-ranking for this current study, one of its most common substitutes, metam sodium, is currently the number one pesticide hazard for cancer and number two hazard for overall chronic health effects. Additionally, since the current study focused on one agricultural community within the state of Arizona, while Gunier et al. (2001) assessed pesticide hazards throughout the entire state of California, the captured resolution of each study is distinctive. While the Gunier et al. (2001) study was able to provide a general hazard ranking during that time period for California, it was not intended to capture hazards that are relevant to the many specific agricultural communities within California. The approach of the current study is novel because it allows for agricultural communities to become informed specifically about the locally relevant hazards.
Carbaryl and permethrin are the only pesticides from the top 10 overall hazard-ranking from this study that were detected in Yuma’s most recently published pesticide sampling study (CDC, 2002). Five of the current hazard-ranked pesticides in Yuma County (maneb, metam sodium, pronamide, bifenthrin, and mineral oil) were not analyzed in the Yuma sampling study, which sampled house and school dust from 1999 through 2000. While some of the hazard-ranked pesticides may not have been analyzed in the pesticide sampling study because of changes in pesticide use trends over the years, there may also have been a lack of appropriate identification of the most locally relevant pesticides for analysis.
Additionally, several of the pesticides that were detected in homes in the Yuma sampling study were not listed as the top hazards in the current study. This may largely be due to the fact that different pesticides are currently being used in Yuma compared to when the previous pesticide sampling was conducted. Other possible reasons for detection of certain pesticides in the home may be because the sampling occurred shortly after that particular pesticide had been applied in a nearby field, or because of weather conditions, such as a high wind event that promoted increased levels of that pesticide in the home. These details exhibit the importance of understanding intricacies such as temporal trends of pesticide use and environmental conditions in the agricultural community along with the hazard ranking schemes presented in this study.
An additional reason for detection of pesticides in homes that were not listed as the top hazards is the fact that considered pesticides were limited to those on the pre-established criteria lists for association with health effects. It is possible that some pesticide hazards were overlooked because they were not on the criteria lists. For example, although studies in the peer-review literature have found an association between diazinon exposure and cancer risk (Beane Freeman et al., 2005; Zhang et al., 2012) it did not appear on any of the cancer criteria lists, and thus was not considered as a carcinogen in this study. In the future, it would be useful to incorporate peer-reviewed literature to improve the toxicity component of the hazard rankings. Finally, while the current study considered pesticides applied during a 4.5 year time period, this may not capture pesticides applied in prior years that continue to persist in homes (Bradman et al., 2007; Curl et al., 2002). For instance, DDT was detected in homes in the Yuma sampling study (CDC, 2002), despite having been banned in 1972 (USEPA, 1972); however, DDT would not appear up on the hazard rankings because it is no longer legally applied.
Understanding chemical properties of pesticides that are relevant to exposure potential may provide insight regarding pesticide pathways into homes. For instance, maneb, the highest hazard-ranked pesticide for overall chronic health effects, binds strongly to soil (USEPA, 2005) suggesting that track-in and air-infiltration of wind-driven resuspended particles are both probable pathways into the home. Measuring maneb concentrations in the home during high and low winds can be used to assess the effect of wind-driven resuspension of particles. On the other hand, metam sodium is more likely to contaminate homes by air infiltration from pesticide spray drift, due to its high vapor pressure and volatilization flux (Lee et al., 2002; Li et al., 2006). High levels of metam sodium’s toxic breakdown product, methyl isothiocyante (MITC), have been previously detected in air samples in an agricultural community (Merriman and Hebert, 2007). Metam sodium is thus a good candidate for future air sampling initiatives.
As research on the health effects of exposure to various pesticides accumulates, pesticide substitutions have become commonplace. In the early 2000s, organophosphate (OPs) pesticides were widely used in Yuma County, as well as throughout the United States (Epstein and Bassein, 2003; Jaga and Dharmani, 2003). Chemical laboratories worked to improve analytical capabilities for OPs in response to the high demand for these services by researchers and regulatory agencies. Yet the current hazard-rankings reveal that only two of the top hazard-ranked pesticides, bensulide and chlorpyrifos, are members of the OP chemical class. As such, it is not currently reasonable to focus primarily on OPs in Yuma County. The hazard-ranking schemes provide a method to periodically reassess pesticide hazards in agricultural communities so that analysis for less relevant pesticides can be avoided.
This study is limited by self-reporting errors in the “1080” pesticide application database. Various spelling errors indicate that there may be low accountability for inputting thorough and accurate information. Identical records inputted consecutively in the database were observed on several occasions. It is unknown whether this is a duplication error or whether the pesticide was truly applied twice. In this study, each recorded application was assumed to be real and thus considered for the hazard rankings.
As mentioned earlier, this study is also limited to consideration of pesticides that appeared on the pre-established criteria lists and pesticides that were highly applied during the study period. A final limitation of this study is the fact that some pesticides are also approved for residential use, along with agricultural use, as is the case for both permethrin and carbaryl.
In this study, the relative ranking of pesticide hazards are each unique for cancer, endocrine disruption, and reproductive/developmental toxicity. This exhibits the value of considering more than one health effect when assessing overall risk for chronic health effects. It is important to remain current with the advances in research that have added the understanding of pesticide toxicity and associated health effects. The Gunier et al. (2001) study only considered cancer as a health outcome, but considerable advances have been made in understanding endocrine disruption and reproductive/developmental toxicity as an outcomes for pesticide exposure since that study period of 1991–1994. Therefore, it was natural to expand the hazard ranking scheme to incorporate endocrine disruption and reproductive/developmental toxicity in the current study to more effectively assess health risk. Future studies could adapt and modify these hazard-ranking schemes to include other health effects, such a genotoxicity or neurodevelopment outcomes to continue this trajectory of improving assessments of health risks for agricultural communities.
5. CONCLUSIONS
Pesticide hazard-rankings schemes that consider exposure potential and association with various health effects, in addition to pesticide use, can help identify and prioritize pesticides of greatest health risk in agricultural communities. The highest hazard-ranked pesticides in this study were not necessarily the ones most applied by weight. Rather, the greatest pesticide hazards were occurred at the intersection of pesticide use, toxicity, and exposure potential. Mounting evidence of pesticide exposure being associated with a variety of health effects, along with the fact that the hazard-rankings were unique for each health effect, show the value of assessing pesticides for multiple health effects to better assess risk in agricultural communities. The current study has led the way in expanding hazard-ranking schemes to include endocrine disruption and reproductive/developmental toxicity, considering pesticide use, toxicity, and exposure potential. These pesticide hazard-ranking schemes can be applied in other agricultural communities as an effective tool to assess community-specific health risk for a variety of health effects.
Supplementary Material
HIGLIGHTS.
We apply pesticide hazard-ranking schemes for chronic health effects.
Our hazard-rankings consider pesticide use, toxicity, and exposure potential.
We show that the highest hazard-ranked pesticides can vary by health effect.
These schemes can be applied to communities to identify local pesticide hazards.
Acknowledgments
This study was funded by the Arizona Area Health Education Center, Yuma Friends of Arizona Health Sciences Center, the Arizona Delegation of the U.S.-Mexico Border Health Commission, NIEHS Superfund Research Program (Grant #P42 ES04940). Dr. Beamer was supported by K25HL103970 from NHLBI. These funding sources had no involvement in the study design, collection, analysis and interpretation of data, writing this report, and decision to submit the article for publication. We thank Gerald Poplin, PhD for his assistance in database management and valuable comments and Mary Kay O’Rourke, PhD for her insight into the intricacies of pesticides.
Acronyms
- ED
Endocrine Disruption
- IARC
International Agency for Research on Cancer
- IRIS
Integrated Risk Information System
- OP
Organophosphate
- RD
Reproductive/developmental toxicity
- RfD
Reference Dose
- USEPA
United States Environmental Protection Agency
Footnotes
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References
- Anderson LM, Diwan BA, Fear NT, Roman E. Critical windows of exposure for children’s health: cancer in human epidemiological studies and neoplasms in experimental animal models. Environ Health Perspect. 2000;108 (Suppl 3):573–94. doi: 10.1289/ehp.00108s3573. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Arcury TA, Quandt SA, Barr DB, Hoppin JA, McCauley L, Grzywacz JG, et al. Farmworker exposure to pesticides: methodologic issues for the collection of comparable data. Environ Health Perspect. 2006;114:923–8. doi: 10.1289/ehp.8531. [DOI] [PMC free article] [PubMed] [Google Scholar]
- AzDA (Arizona Department of Agriculture) [Accessed July 1, 2011];Environmental Services Portal: 1080 Investigative Search. 2011 Available: http://www.azda.gov/Search1080/search1080.aspx.
- Aspelin AL, Grube AH. Pesticides Industry Sales and Usage 1996 and 1997 Market Estimates. United States Environmental Protection Agency; Washington, DC: 1999. [Google Scholar]
- Baldi I, Filleul L, Mohammed-Brahim B, Fabrigoule C, Dartigues JF, Schwall S, et al. Neuropsychologic effects of long-term exposure to pesticides: results from the French Phytoner study. Environ Health Perspect. 109, United States. 2001:839–44. doi: 10.1289/ehp.01109839. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baun A, Eriksson E, Ledin A, Mikkelsen PS. A methodology for ranking and hazard identification of xenobiotic organic compounds in urban storm water. Sci Total Environ. 2006;370:29–38. doi: 10.1016/j.scitotenv.2006.05.017. [DOI] [PubMed] [Google Scholar]
- Beane Freeman LE, Bonner MR, Blair A, Hoppin JA, Sandler DP, Lubin JH, et al. Am J Epidemiol. Vol. 162. United States: 2005. Cancer incidence among male pesticide applicators in the Agricultural Health Study cohort exposed to diazinon; pp. 1070–9. [DOI] [PubMed] [Google Scholar]
- Benbrook C. Growing Doubt: A Primer on Pesticides Identified as Endocrine Disruptors and/or Reproductive Toxicants. Washington D.C: National Campaign for Pesticide Policy Reform; 1996. [Google Scholar]
- Blasco C, Picó Y. Prospects for combining chemical and biological methods for integrated environmental assessment. TrAC Trends in Analytical Chemistry. 2009;28:745–757. [Google Scholar]
- Bradman A, Whitaker D, Quirós L, Castorina R, Claus Henn B, Nishioka M, et al. Pesticides and their metabolites in the homes and urine of farmworker children living in the Salinas Valley, CA. J Expo Sci Environ Epidemiol. 2007;17:331–49. doi: 10.1038/sj.jes.7500507. [DOI] [PubMed] [Google Scholar]
- Bro-Rasmussen F, Christiansen K. Hazard assessment—a summary of analysis and integrated evaluation of exposure and potential effects from toxic environmental chemicals. Ecol Modell. 1984;22:67–84. [Google Scholar]
- CDPR (California Department of Pesticide Regulation) [Accessed July 1, 2011];Pesticide Use Reporting Database. 2010 Available: http://www.cdpr.ca.gov/docs/pur/purmain.htm.
- CalEPA (California Environmental Protection Agency) Chemicals Known to the State to Cause Cancer or Reproductive Toxicity: From the Safe Drinking Water and Toxic Enforcement Act of 1986. Office of Environmental Health Assessment; 2011. [Accessed July 1, 2011]. Available: http://oehha.ca.gov/prop65/prop65_list/files/P65single111811.pdf. [Google Scholar]
- CDC (Centers for Disease Control and Prevention) Pesticide Exposure in Children Living in Agricultural Areas along the United States- Mexico Border, Yuma County, Arizona. Office of Border Health, Arizona Department of Health Services; 2002. [Accessed October 15, 2011]. Available: http://www.epa.gov/icc/projects_publications/pdf/pesticide_exposure_yuma_arizona.pdf. [Google Scholar]
- Colborn T, vom Saal FS, Soto AM. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect. 1993;101:378–84. doi: 10.1289/ehp.93101378. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Coronado GD, Holte S, Vigoren E, Griffith WC, Barr DB, Faustman E, et al. Organophosphate pesticide exposure and residential proximity to nearby fields: evidence for the drift pathway. J Occup Environ Med. 2011;53:884–91. doi: 10.1097/JOM.0b013e318222f03a. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Curl CL, Fenske RA, Kissel JC, Shirai JH, Moate TF, Griffith W, et al. Environ Health Perspect. Vol. 110. United States: 2002. Evaluation of take-home organophosphorus pesticide exposure among agricultural workers and their children; pp. A787–92. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Daston GP, Cook JC, Kavlock RJ. Uncertainties for endocrine disrupters: our view on progress. Toxicological Sciences. 2003;74:245–252. doi: 10.1093/toxsci/kfg105. [DOI] [PubMed] [Google Scholar]
- Dix DJ, Houck KA, Martin MT, Richard AM, Setzer RW, Kavlock RJ. The ToxCast program for prioritizing toxicity testing of environmental chemicals. Toxicol Sci. 2007;95:5–12. doi: 10.1093/toxsci/kfl103. [DOI] [PubMed] [Google Scholar]
- Epstein L, Bassein S. Patterns of pesticide use in California and the implications for strategies for reduction of pesticides. Annu Rev Phytopathol. 2003;41:351–75. doi: 10.1146/annurev.phyto.41.052002.095612. [DOI] [PubMed] [Google Scholar]
- Faustman EM, Silbernagel SM, Fenske RA, Burbacher TM, Ponce RA. Mechanisms underlying children’s susceptibility to environmental toxicants. Environmental Health Perspectives. 2000;108:13. doi: 10.1289/ehp.00108s113. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fenner-Crisp PA, Maciorowski AF, Timm GE. The endocrine disruptor screening program developed by the US Environmental Protection Agency. Ecotoxicology. 2000;9:85–91. [Google Scholar]
- Garry VF, Harkins ME, Erickson LL, Long-Simpson LK, Holland SE, Burroughs BL. Birth defects, season of conception, and sex of children born to pesticide applicators living in the Red River Valley of Minnesota, USA. Environ Health Perspect. 2002;110 (Suppl 3):441–9. doi: 10.1289/ehp.02110s3441. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Glotfelty DE, Leech MM, Jersey J, Taylor AW. Volatilization and wind erosion of soil surface applied atrazine, simazine, alachlor, and toxaphene. Journal of agricultural and food chemistry. 1989;37:546–551. [Google Scholar]
- Gunier RB, Harnly ME, Reynolds P, Hertz A, Von Behren J. Agricultural pesticide use in California: pesticide prioritization, use densities, and population distributions for a childhood cancer study. Environ Health Perspect. 2001;109:1071–8. doi: 10.1289/ehp.011091071. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Holmes JG, Jensen C, Marean H, Neili NP, Root AS, McLendon WE, et al. United States Department of Agriculture BoS, editor. Soil Survey of the Yuma Area, Arizona-California. Government Printing Office; Washington: 1905. [Google Scholar]
- IEPA (Illinois Environmental Protection Agency) Endocrine Disruptors Strategy. Springfield; Illionis: 1997. [Accessed Sept 1, 2011]. Available: http://iledi.org/ppa/docs/00/00/00/01/01/82/EndocrineDisruptorsStrategy.pdf. [Google Scholar]
- IARC (International Agency for Research on Cancer) Agents Classified by the IARC Monographs. 1–104. World Health Organization; France: 2011. [Accessed July 1, 2011]. Available: http://monographs.iarc.fr/ENG/Classification/ClassificationsGroupOrder.pdf. [Google Scholar]
- Jaga K, Dharmani C. Sources of exposure to and public health implications of organophosphate pesticides. Rev Panam Salud Publica. 2003;14:171–85. doi: 10.1590/s1020-49892003000800004. [DOI] [PubMed] [Google Scholar]
- Keith L. Environmental Endocrine Disruptors: A Handbook of Property Data. New York: Wiley Interscience; 1997. [Google Scholar]
- Lee S, McLaughlin R, Harnly M, Gunier R, Kreutzer R. Environ Health Perspect. Vol. 110. United States: 2002. Community exposures to airborne agricultural pesticides in California: ranking of inhalation risks; pp. 1175–84. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li LY, Barry T, Mongar K, Wofford P. Modeling methyl isothiocyanate soil flux and emission ratio from a field following a chemigation of metam-sodium. J Environ Qual. 2006;35:707–13. doi: 10.2134/jeq2005.0216. [DOI] [PubMed] [Google Scholar]
- Liebman AK, Juarez PM, Leyva C, Corona A. A pilot program using promotoras de salud to educate farmworker families about the risk from pesticide exposure. J Agromedicine. 2007;12:33–43. doi: 10.1300/J096v12n02_04. [DOI] [PubMed] [Google Scholar]
- Merriman JH, Hebert VR. Methyl isothiocyanate residential community air assessment for South Franklin County, Washington. Bull Environ Contam Toxicol. 2007;78:19–23. doi: 10.1007/s00128-007-9009-x. [DOI] [PubMed] [Google Scholar]
- Mitchell RR, Summer CL, Blonde SA, Bush DM, Hurlburt GK, Snyder EM, et al. SCRAM: A scoring and ranking system for persistent, bioaccumulative, and toxic substances for the North American Great Lakes-resulting chemical scores and rankings. Human and Ecological Risk Assessment: An International Journal. 2002;8:537–557. [Google Scholar]
- NTP (National Toxicology Program) Report on Carcinogens. United States Department of Health and Human Services, Public Health Service; 2011. [Accessed July 1, 2011]. Available: http://ntp.niehs.nih.gov/ntp/roc/twelfth/roc12.pdf. [Google Scholar]
- Neumann CM, Forman DL, Rothlein JE. Hazard screening of chemical releases and environmental equity analysis of populations proximate to toxic release inventory facilities in Oregon. Environ Health Perspect. 1998;106:217–26. doi: 10.1289/ehp.98106217. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oliva A, Spira A, Multigner L. Contribution of environmental factors to the risk of male infertility. Hum Reprod. 2001;16:1768–76. doi: 10.1093/humrep/16.8.1768. [DOI] [PubMed] [Google Scholar]
- Petersen G, Rasmussen D, Gustavson K. Revised Report to DG Environment. European Commission; Horsholm, Denmark: 2007. Study on Enhancing the Endocrine Disruptor Priority List with a Focus on Low Production Volume Chemicals. [Google Scholar]
- Ribas-Fito N, Torrent M, Carrizo D, Munoz-Ortiz L, Julvez J, Grimalt JO, et al. In utero exposure to background concentrations of DDT and cognitive functioning among preschoolers. Am J Epidemiol. 2006;164:955–62. doi: 10.1093/aje/kwj299. [DOI] [PubMed] [Google Scholar]
- Schmidt-Bleek F, Haberland W, Klein A, Caroli S. Steps towards environmental hazard assessment of new chemicals (including a hazard ranking scheme, based upon Directive 79/831/EEC) Chemosphere. 1982;11:383–415. [Google Scholar]
- Siljeholm J. A hazard ranking of organic contaminants in refinery effluents. Toxicology and Industrial Health. 1997;13:527–551. doi: 10.1177/074823379701300405. [DOI] [PubMed] [Google Scholar]
- Simcox NJ, Fenske RA, Wolz SA, Lee IC, Kalman DA. Pesticides in household dust and soil: exposure pathways for children of agricultural families. Environ Health Perspect. 1995;103:1126–34. doi: 10.1289/ehp.951031126. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Swanson MB, Davis GA, Kincaid LE, Schultz TW, Bartmess JE, Jones SL, et al. A screening method for ranking and scoring chemicals by potential human health and environmental impacts. Environmental Toxicology and Chemistry. 1997;16:372–383. [Google Scholar]
- USEPA (United States Environmental Protectection Agency) [Accessed July 1, 2011];DDT Ban Takes Effect. 1972 Available: http://www.epa.gov/history/topics/ddt/01.html.
- USEPA (United States Environmental Protection Agency) The Hazard Ranking System Guidance Manual. National Service Center for Environmental Publications; 1992. [Accessed October 25, 2011]. pp. 1–509. Available: http://www.epa.gov/superfund/sites/npl/hrsres/hrsgm/ch1.pdf. [Google Scholar]
- USEPA (United States Environmental Protection Agency. Reference Dose) (Rfd) [Accessed Dec 8, 2011];Description and Usage in Health Risk Assessments. Integrated Risk Information System. 1993 Available: http://www.epa.gov/IRIS/rfd.htm.
- USEPA (United States Environmental Protection Agency) [Accessed July 1, 2011];TRI-Listed Chemicals. Toxic Release Inventory Program. 2000 Available: http://www.epa.gov/tri/trichemicals/hazardinfo/hazard_categories.pdf.
- USEPA (United States Environmental Protection Agency) Federal Register. Vol. 70. Washington D.C: 2005. [Accessed April 5, 2012]. Reregistration Eligibility Decision (RED) for Maneb. Available: http://www.epa.gov/oppsrrd1/REDs/maneb_red.pdf. [Google Scholar]
- USEPA (United States Environmental Protection Agency) [Accessed July 1, 2011];Final List of Chemicals for Initial Tier 1 Screening. Endocrine Disruptor Screening Program. 2009 Available: http://www.epa.gov/endo/pubs/prioritysetting/finallist.html.
- USEPA (United States Environmental Protection Agency) Chemicals Evaluated for Carcinogenic Potential: Corrected Annual Cancer Report. Office of Pesticide Programs; 2010. [Accessed July 1, 2011]. Print. [Google Scholar]
- USEPA (United States Environmental Protection Agency) Integrated Risk Information System A-Z List of Substances. [Accessed Sept 1, 2011];Integrated Risk Information System Program. 2011a Available: http://cfpub.epa.gov/ncea/iris/index.cfm?fuseaction=iris.showSubstanceList.
- USEPA (United States Environmental Protection Agency) Second List of Chemicals for Tier 1 Screening. [Accessed July 1, 2011];Endocrine Disruptor Screening Program. 2011b Available: http://www.epa.gov/endo/pubs/draftlist2.pdf.
- USEPA (United States Environmental Protection Agency) The Phaseout of Methyl Bromide. 2011. [Accessed Sept 1, 2011];Regulatory Programs. 2011c Available: http://www.epa.gov/ozone/mbr.
- Zhang X, Wallace AD, Du P, Lin S, Baccarelli AA, Jiang H, et al. Genome-wide study of DNA methylation alterations in response to diazinon exposure in vitro. Environ Toxicol Pharmacol. 2012;34:959–68. doi: 10.1016/j.etap.2012.07.012. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zheng T, Zahm SH, Cantor KP, Weisenburger DD, Zhang Y, Blair A. Agricultural exposure to carbamate pesticides and risk of non-Hodgkin lymphoma. J Occup Environ Med. 2001;43:641–9. doi: 10.1097/00043764-200107000-00012. [DOI] [PubMed] [Google Scholar]
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