Critical Review pubs.acs.org/est
Environmental Concerns of Roxarsone in Broiler Poultry Feed and Litter in Maryland, USA Daniel J. Fisher,*,†,‡ Lance T. Yonkos,‡ and Kenneth W. Staver† †
College of Agriculture and Natural Resources, Wye Research and Education Center, University of Maryland, Queenstown, Maryland 21658, United States ‡ Department of Environmental Science and Technology, College of Agriculture and Natural Resources, University of Maryland, College Park, Maryland 20740, United States ABSTRACT: Roxarsone has been used extensively in the broiler chicken industry. We reviewed the environmental concerns of this usage. To summarize, arsenic added to poultry feed as roxarsone ends up in poultry litter. Fresh litter contains predominately roxarsone, whereas aged litter contains predominately inorganic arsenic. Soil arsenic concentrations from long-term poultry litter applications can exceed Maryland arsenic soil background remediation standards. Due to continued soil accumulation, arsenic-amended litter use as fertilizer is thought to be unsustainable. Surface-applied roxarsone-amended litter does not influence deep aquifer arsenic concentrations but is transported as inorganic arsenic to receiving waters and very shallow groundwater after precipitation. Arsenic in some receiving waters and sediments from agriculturally dominated watersheds have levels above established criteria. Arsenic in fish and shellfish is mostly organic. Phosphorus-based nutrient management will tend to limit PL application rates in areas that have over-applied phosphorus relative to crop needs, resulting in decreased rates of arsenic application and accumulation. Despite most arsenic in surface soils being tightly bound, as surface soils become more enriched in arsenic, the potential for downward movement increases but is limited in most soils due to the high capacity for binding of arsenic to clay minerals and oxides of iron and aluminum in subsoil horizons. In 2012, Maryland passed a law banning the use of arsenic additives except nitarsone in poultry feed. In 2013, the USFDA withdrew approval of roxarsone, carbarsone, and arsanilic but is reviewing nitarsone.
1. INTRODUCTION The most commonly used arsenical in broiler poultry production is roxarsone (4-hydroxy-3-nitrobenzenearsonic acid) (CAS Registry No. 121-19-7). It is an organic arsenical compound containing arsenic and approved by the U.S. Food and Drug Administration (FDA) in 1944 for use in poultry feed for disease prevention, growth promotion, enhanced feed utilization, and improved meat pigmentation.1 Of the roughly 9 billion chickens raised for human consumption in the United States in 2010, 88% received roxarsone.2 In 2012, most of the poultry produced in Maryland were broiler chickens (approximately 305 million broiler chickens compared to 2.4 million layers and 154,000 turkeys).3 This review therefore deals specifically with roxarsone used in broiler chicken poultry production. Arsenic (As) is a metallic element in the earth’s crust mostly in inorganic form.4 Due to environmental and human health issues, arsenicals were discontinued as feed additives by the European Union (EU) in 1999. Although not banned, maximum permissible limits in feed were set sufficiently low that manufacturers stopped selling arsenical-amended feed. For example, the 1999 EU limits were set at 2 mg/kg for livestock and 4 mg/kg for fish (increased to 6 mg/kg in 2002).5,6 The roxarsone concentration in U.S. poultry feed is 25−50 mg/kg.7 Conditions for registration and use of animal drugs in Europe © XXXX American Chemical Society
are so rigorous that manufacturers have not sought authorizations for many animal drugs, including roxarsone.8 In 2007, Perdue Farms, Inc., discontinued the use of roxarsone or arsenic.9 Perdue Farms, Inc., is ranked as the third largest U.S. poultry producer.10 In 2006/2007, McDonald’s asked its dedicated poultry facilities not to use arsenic.11 In 2011, the USFDA released a study that found a higher incidence of carcinogenic inorganic arsenic in livers of roxarsone-treated chickens compared to controls.12 In 2010/ 2011 Nachman et al.2 analyzed edible chicken meat for arsenic from grocery stores in 10 metropolitan areas. Among cooked samples, inorganic arsenic concentrations were higher by greater than a factor of 2 in the conventional samples (1.8 μg/kg) than in the antibiotic-free or organic samples. Roxarsone was also detected in 50% of the conventional samples. In 2011, Nachman et al.13 found arsenic concentrations in poultry feather meal ranging from 44 to 4100 μg/kg. The majority of the arsenic was inorganic. Because feather meal is used as an animal feed product, there is concern that arsenic could accumulate in animals consumed by humans. In 2011, Received: September 15, 2014 Revised: January 16, 2015 Accepted: January 21, 2015
A
DOI: 10.1021/es504520w Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Critical Review
Environmental Science & Technology
The clarification requested was in the form of a series of eight questions as presented in section 2.
following release of the USFDA study, the manufacturer of roxarsone (Alpharma) suspended the sale of roxarsone in poultry feed (http://www.fda.gov/NewsEvents/Newsroom/ PressAnnouncements/ucm258342.htm). Inorganic arsenic is a human carcinogen.14 Low-level, longterm exposures to inorganic arsenic have been shown to cause cancers of the lung, bladder, kidney, and skin.15−17 Due to these concerns, the USEPA lowered the drinking water MCL for total arsenic to 10 μg/L.18 Chronic low-level arsenic exposure has been implicated in adverse health consequences including cardiovascular disease,19,20 type 2 diabetes,21 neurocognitive deficits,22 adverse birth outcomes,23 and endocrine disruption.24 Arsenate (As(V)) and arsenite (As(III)) are believed to be most potent in inducing toxic effects, although the toxic potential of organic arsenicals is less well studied.25,26 Basu et al.27 found angiogenesis associated with vascular disease as well as the growth of new tumors following exposure of human endothelial cell cultures to roxarsone and As(III). Roxarsone was a more potent inducer of angiogenesis than As(III). In 2010 the USEPA’s IRIS program released a draft reassessment of the carcinogenic potency of inorganic arsenic (http://cfpub.epa.gov/ncea/iris_drafts/recordisplay.cfm?deid= 219111). In this draft, the cancer slope factor, a key metric in cancer risk assessment, was changed from 1.5 to 25.7 per mg/ kg-day, making inorganic arsenic 17 times more potent a carcinogen than previously believed. Furthermore, IRIS is currently reviewing the literature examining the relationship between inorganic arsenic and noncancer health effects, especially cardiovascular disease. O’Connor et al.28 found that homes in Arkansas near fields amended with PL containing roxarsone had elevated arsenic concentrations in dust. Peak dust-associated total arsenic concentrations in the homes ranged from 0.95 to 86.6 mg/kg with the majority of arsenic being As(V) with smaller percentages of As(III) and roxarsone. The similarities in arsenic species between PL, ambient air particles, and household dust were strong evidence that arsenic was being transported from litter-amended fields through the air and could affect people in nearby areas. Roxarsone in house dusts was definitive evidence that broiler litter arsenicals are airborne contaminants in areas of high-density poultry operations. The authors recommended that arsenical feed additives should be abandoned due to human health concerns. The possibility of significant human health consequences drives the overall discussion about the risk of using arsenic feed amendments. This literature review, however, is concerned with the possible environmental consequences and sustainability of roxarsone use in broiler poultry feed in Maryland (MD). The majority of MD broiler production is on the Delmarva Peninsula (DP), which encompasses the parts of Delaware (DE), MD, and Virginia (VA) east of the Chesapeake Bay. As chickens grow in poultry houses their excreta is incorporated with bedding material (wood shavings, sawdust, etc.) to produce poultry litter (PL). When houses are cleared, PL is applied to agricultural fields as fertilizer. Because roxarsone is used extensively in broiler poultry feed, there is concern that arsenic will end up in PL and thus cause environmental problems. During the 2010 legislative session, the Maryland state legislature debated a bill to ban the use of arsenicals in poultry feed. The legislature requested this review concerning the environmental consequences and sustainability of applying PL containing arsenic, especially roxarsone, to agricultural fields.
2. POINTS OF CONCERN FOR THE MARYLAND STATE LEGISLATURE 2.1. Does Arsenic from Poultry Feed Amended with Roxarsone End up in Poultry Litter? Feed formulations of roxarsone for chickens range from 22.7 to 45.4 g/ton (25−50 mg/kg).7 As very little arsenic remains in the bird, by design, the majority is excreted. The mean total arsenic concentration in PL ranges from 2.93 to 47.8 mg/kg (Table 1),29−43 so it is Table 1. Concentration of Total Arsenic in Poultry Litter from Various Studies author and citation Ashjaei29 and Ashjaei et al.30 Garbarino et al.31 (Kansas) Garbarino et al.31 (Maryland) Sims and Wolf32a Moore et al.33a Jackson and Miller34 Jackson and Bertsch35 Sims and LukaMcCafferty36 Jackson et al.37 Toor et al.38 Han et al.39 Arai et al.40 Adeli et al.41 Denver et al.42a Codling et al.43 a
mean arsenic concn (mg/kg dry weight)
SD (mg/kg)
range (mg/kg)
29.8
13.89
14.9−53.4
28.7
0.5
29.0
3.0
43.0 35.1 16.8
4.0
0−77
45 15.7
9.57
26.9 47.8 29.0 27 2.93
7.8 2.3 4.41
1.2−39.4 24−43 11.1−36.1
0.59
Not reported whether dry weight or wet weight.
clear that poultry fed roxarsone produce PL containing arsenic. The total arsenic reported by Codling et al.43 is significantly lower in total arsenic than other PLs. In addition, litter phosphorus concentrations were lower than other reported values. The authors felt that the lower PL concentration may have resulted from the types of bedding material or differences in the feed composition used. Kawalek et al.12 measured poultry feed before and after the addition of roxarsone. Control poultry feed had background levels of total arsenic of 0.156 mg/kg (0.024 mg/kg As(III) and 0.032 mg/kg As(V)) and nondetectable roxarsone. After the addition of roxarsone, the feed had a total arsenic concentration of 11.3 mg/kg with roxarsone being the dominant arsenic species. The concentrations of As(III) and As(V) were similar to levels before roxarsone amendment. This indicates that the increase in arsenic content in the feed was due to roxarsone amendment. Thus, PL produced without the addition of roxarsone will have only trace levels of arsenic. For example, Morrison44 measured total arsenic of 29.8 mg/kg ± 13.89 standard deviation (SD) (11.8−29.6 mg/kg) in 11 PLs from roxarsone-treated chickens and 6 times higher in litter-amended soils C
DOI: 10.1021/es504520w Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Critical Review
Environmental Science & Technology
concentration of 2.6 mg/kg ± 1.8 SD (nondetectable−6.6 mg/ kg), whereas soils from New Castle county had a mean total arsenic concentration of 4.1 mg/kg ± 1.9 SD (2.1−9.2 mg/kg). Meanwhile, the three UDE Research and Education Center soils had higher mean total arsenic concentrations: (1) Sussex county, 4.3 mg/kg ± 2.51 SD (0.4−8.9 mg/kg); (2) New Castle county, 7.4 mg/kg ± 2.27 SD (3.8−11.7 mg/kg); (3) New Castle county, 8.7 mg/kg ± 4.75 SD (3.3−19.6 mg/kg). Because the history of PL application on these farms varied, it is difficult to establish what specific practice(s) produced the higher arsenic concentrations in UDE New Castle farms. The UDE farms had 4 total arsenic values above the DE SABRS and 35 values above the lower MD SABRS. Sparks et al.61 calculated future arsenic accumulation in DE soils on the basis of realistic arsenic application/loss scenarios. They assumed an average total arsenic concentration of 40 mg/ kg in PL and a litter application rate of 9 Mg/ha. PL application was assumed to be two of three years, and a loss of 10% added litter arsenic was assumed from topsoils though erosion, leaching, plant uptake, or volatilization. In this scenario, it would require 75 years before topsoil total arsenic would be greater than the DE SABRS. Much less time would be required to produce exceedances of the lower MD SABRS. The authors felt that this raised questions about the sustainability of arsenic use in poultry production. A sustainable practice is assumed to be one that can continue indefinitely without adverse environmental effects. In summary, soil arsenic levels (predominately inorganic) from PL-amended fields are statistically greater than levels from unamended soils. Soil arsenic concentrations on the DP in areas of long-term PL applications can exceed the MD and DE SABRS. The use of arsenic as a feed additive is not a sustainable practice because arsenic soil concentrations will eventually increase to concentrations above these SABRSs. Because arsenic’s soil half-life is 108 days, once in soil it will remain there.62 2.4. Does Arsenic Transport from Litter-Amended Surface Soils into Deep Aquifers, Shallow Groundwater, and Receiving Streams and, If So, Are Levels High Enough To Be of Concern to the Biota in These Ecosystems on the Basis of Existing Arsenic Criteria? USEPA, MD, and DE use the same drinking water MCL of 10 μg/L.18 The current USEPA63 inorganic arsenic water quality criteria (WQC) for the protection of aquatic life were first published in 1984 (Table 3). For comparison, Canada’s 2001 arsenic criteria for freshwater and marine are 5.0 and 12.5 μg/L, respectively64 (Table 3). MD65 and DE66 both use these USEPA arsenic criteria for the protection of aquatic life. For freshwater the acute and chronic criteria are 340 and 150 μg/L, respectively. Acute and chronic saltwater criteria are 69 and 36 μg/L, respectively. MD65 and DE66 arsenic WQC for protection of human health for fish consumption are 1.4 and 10 μg/L, respectively, whereas the USEPA67 criterion is significantly lower at 0.14 μg/L (Table 3). Focazio et al.68 reported on total arsenic in 298 well samples from DE and MD Eastern Shore counties. Approximately 200 of the wells sampled were from depths ≤100 ft (2−100 ft). The highest total arsenic concentration measured was 9 μg/L, slightly below the drinking water MCL. Total arsenic was ≤4 μg/L in 99.5% of the samples and ≤1 μg/L in 87%. Of 164 shallow groundwater wells sampled by the DE Department of Agriculture, 99% had arsenic concentrations 10 μg/L (23 μg/ L; depth = 6 ft). Twenty-nine deeper groundwater samples from major aquifers throughout the DP had measurable arsenic of MCL at 14 μg/L. Wells as shallow as 40 ft were sampled in this survey. Drummond and Bolton70 state that, “The lack of elevated arsenic concentrations in the shallow aquifers, the age of water in the Aquia and Piney Point aquifers, and the distribution of arsenic in the Aquia and Piney Point aquifers indicate that the overall arsenic occurrence in these aquifers is a natural phenomenon, and is not caused by anthropogenic contamination.” Five shallow wells (
