Subclinical Lead Exposure Among Backyard Chicken Flocks in Massachusetts.
Key words: lead toxicosis, lead, lead exposure, backyard chicken, poultry, avian, chicken
Ownership of backyard chickens (BYCs) is an increasingly popular trend seen across the United States. (1,2) Although reasons for owning chickens may vary among individuals, a recent US Department of Agriculture study showed that most owners felt that eggs obtained from BYCs were safer and healthier to eat than those purchased at the grocery store. (2) This indicates that egg production for personal consumption is a driving factor behind owning BYCs.
In the context of BYC ownership, in which poultry are both pets and production animals, several conditions commonly affect BYCs, such as coccidiosis, mites, Marek's disease, egg-binding, and crop stasis. (3,4) In addition, chickens are host to several diseases that have significant zoonotic potential, including avian influenza and infections with Salmonella, and Campylobacter species, among others. (4) One lesser-recognized threat to both BYCs and people who consume their products is exposure to the toxic heavy-metal lead. Lead toxicosis in poultry can result from acute ingestion of large quantities of lead (eg, lead paint chips, metal objects) or from chronic ingestion of lower lead levels such as those found in soil. (3,6-9) Clinical signs range from crop stasis to acute lethargy, diarrhea, ataxia, and marked weight loss, to more chronic progressive neurologic deficits due to axonal degeneration. (3,6,7,10) Even ingestion of small amounts of dietary lead (eg, 1 mg/kg feed) has been associated with decreased weight gains in poultry. (8)
The symptomatic threshold for lead toxicosis in chickens, however, is not well established. Although low levels of ingestion may lead to decreased weight gains, this sign may be too subtle for owners to detect, and overt clinical signs of toxicosis may not always be present. A survey of a small backyard flock in Iowa revealed that chickens with known exposure to lead paint chips had blood lead levels (BLLs) ranging from less than 5 to 76 ng/dL; none of the chickens in that study displayed clinical signs of lead toxicosis. (9) This indicates that chickens may be relatively resistant to developing acute signs of lead toxicosis, making it difficult for owners to know if their birds are exposed. The same study found a strong correlation between the BLL and yolk lead concentration in eggs, with yolk lead concentrations ranging from 20 to 400 ppb (0.02 to 0.4 mg/ kg). (9) Studies conducted in small poultry flocks or BYC flocks in California, New York City, Iowa, and Australia have detected lead in poultry eggs and the highest egg lead concentrations ranged from 330 ppb (0.33 mg/kg) in a sample of homogenized yolk and albumin to as high as 400 ppb (0.4 mg/kg) in a sample of egg yolk alone. (6,9,11-13) These findings indicate that lead exposure may be more common in urban flocks than is currently recognized. A recent report from urban flocks in Australia correlated the amount of soil lead contamination with that of lead levels found in the yolks of eggs. (13) Other tissues that accumulate lead in poultry are liver, kidneys, bones, and eggshells. However, the kinetics of lead dispersal in chickens, particularly concerning the half life of lead in the bloodstream and the degree and rate at which lead transfers between the blood and yolk, are not well understood. (7)
In the northeastern United States, soil contamination with lead is common, with Massachusetts having some of the highest reported mean soil lead levels in the United States. (14) In some towns neighboring Boston, MA, USA, soil lead concentrations above 1500 ppm are reported, and in New York City correlations between the amount of lead found in the soil and the amount of lead found in the eggs of laying hens has been documented in urban community garden flocks. (11,15) Current research has implicated high soil lead concentrations to be the primary factor driving continued lead toxicosis among children, despite aggressive prevention efforts. (16) Backyard chickens that are housed on lead-contaminated soil are also exposed to lead, and their behavioral characteristics, mainly scratching, feeding, and dust-bathing in the soil, may contribute to their level of exposure.
This study was designed to determine the prevalence of lead exposure among BYCs in Massachusetts based on analysis of BLL using a rapid, point-of-care blood lead analyzer. No data currently exist regarding lead in Massachusetts' BYCs; however, anecdotal evidence from local veterinarians who treat poultry led us to hypothesize that a large percentage of BYCs would screen positive for exposure to lead. The data generated from this study serve as a starting point upon which future research and interventional measures can be based.
Materials and Methods
Study design, recruitment, and location
This study was cross-sectional in design and used a convenience sample to maximize sample collection from BYCs in eastern Massachusetts from both urban and rural areas. To attract participants, flyers were distributed to local farm and feed stores, posted to urban farming Listservs and online social groups, and recruited via word of mouth as the BYC community is tightknit and communicative in the study area. Potential participants who reached out to study personnel via email or phone, who had BYCs on their residential property, and who did not keep chickens for commercial purposes were enrolled. This study was approved by and conducted in accordance with the Tufts University Institutional Animal Use and Care Committee and the Health Sciences Institutional Review Board. Owner consent was obtained prior to hen sampling and survey administration. Samples were collected from July to November of 2015.
Sample acquisition and survey administration
All blood samples acquired from participating BYCs were obtained at the owner's home. The owner was asked to catch 2 chickens for sampling; however, in some instances the owner was only able to catch 1 chicken. A maximum of 0.5 mL of blood was obtained through venipuncture of the ulnar or median metatarsal veins by using a 1-mL syringe with a sterile 25-gauge needle. Blood samples were then placed in a 2-mL EDTA collecting vial and stored in a cooler for transport.
Trained study personnel conducted a brief physical examination of the hens that were sampled, and each hen was observed for abnormalities of gait and mobility. Owners were asked if any abnormal symptoms had been observed in their flock in the 24 hours preceding the study visit.
Owners were asked to complete a brief standardized questionnaire regarding their BYC husbandry and management practices. Some owners volunteered additional information that was not covered in the questionnaire (eg, soil and egg lead levels, if known), in which case verbal consent was obtained for inclusion in the discussion of this paper. Following the questionnaire, participants were given a handout containing tips and information for pursuing further lead testing for their home as well as advice on how to reduce the risk of lead exposure in their chickens. Results from BLL testing were shared with the owner.
Sample processing and blood lead testing
Blood samples were stored upright in a standard refrigerator maintained at 1.5[degrees]C (34.7[degrees]F) until tested, which occurred within 24 hours of collection. Blood samples were analyzed at the Cummings School of Veterinary Medicine using a rapid point-of-care analyzer (LeadCare II Blood Lead Test Kit. Magellan Diagnostics, Inc., North Billerica, MA, USA) according to the manufacturer's instructions. The analyzer quantifies blood lead values between 3.3 [micro]g/dL and 65.0 [micro]g/dL. To convert the data to a continuous scale, all samples that were reported as higher than 65.0 [micro]g/dL were assigned the value of 65.0 [micro]g/dL, and all samples that were reported as lower than 3.3 [micro]g/dL were assigned the midpoint value between 0 and 3.3, of 1.65 [micro]g/dL, as previously described. (17)
Estimations of population density and map generation
Census data from the 2010 Summary File 1 (SF1) were used to determine the human population density in people per square mile by zip code.l ,x The count of flocks, total number of birds sampled, and the average BLLs were summarized by zip code because more granular location information (Global Positioning System coordinates or street addresses) for each flock were not available. The map of average BLL and total number of birds sampled per zip code, overlaid with population density per zip code, was created using a geospacial processing program (ArcMap 10.4, ESRI, Inc., Redlands, CA, USA)
Data were analyzed using standard statistical software packages (STATA IC version 14 Data Analysis and Statistical Software, StataCorp LLC, College Station, TX, USA). Descriptive statistics were used to summarize the distribution of BLLs and questionnaire responses. A priori univariate associations between BLL and predictor variables (location, hen access to property, proximity of coop to home, and previous steps taken by owners to reduce lead exposure in the flock) were determined using the nonparametric Mann-Whitney U test, and bivariate associations between flock and household characteristics stratified by population density were determined by using the Fisher exact test. Statistical significance was assigned to P values <.05. Soil and egg lead results that are included in this study were reported voluntarily by a subset of flock owners.
A total of 57 hens were sampled representing 30 flocks throughout eastern Massachusetts. Two birds were sampled from 27 flocks and 1 bird was sampled from 3 flocks. Survey data were obtained from 26 of the 30 flocks. Hens were all sampled in Massachusetts, from the towns of Boylston (n = 2), Brighton (n = 4), Chelmsford (n = 2), Framingham (n = 2), Grafton (n = 14), Lexington (n = 1), Lynnfield (n = 2), Roslindale (n = 4), Shrewsbury (n = 6), Somerville (n = 12), South Grafton (n = 6), and Walpole (n = 2; Fig 1).
The average flock size was 8 hens (range: 2-29). Out of 26 flocks, almost all flocks (96%, n = 25) had access to soil within their coop, and most (69%, n = 18) were allowed to freely range around the property for periods of time during the day (Table 1). Of the 18 flocks that were allowed to freely range around the property, 13 flocks (72%) were allowed to freely roam on the property on a daily basis, 2 flocks (11%) were allowed to roam on a weekly basis, and 2 flocks (11%) were allowed to roam less than once a week. One flock owner did not specify how frequently the flock was allowed to roam. Just under half (44%, n = 11) of 25 flocks had coops that were located within 9.1 m (30 ft) of the home, and just over half (56%, n = 14) were located more than 9.1 m (30 ft) from the home (Table 1). For 25 flocks for which information was available, coops were built on average 12.5 years ago but ranged from brand new construction to over 100 years old (ie, chickens were housed in an old barn). Coop distance to the home and year of coop construction was not recorded for 5 flocks. There were no significant differences in flock characteristics stratified by population density (Table 1). No abnormalities were detected in the physical examination of the hens that were tested, and no owners reported abnormal clinical signs or symptoms observed in their flock in the 24 hours preceding the time of sample collection.
Of the 26 owners who were surveyed, 100% of respondents reported regularly consuming eggs from their flock (Table 1), and 54% (n = 14) reported using other products from their chickens such as feathers (for decoration/adornment), feces/litter (for compost), and eggshells (for compost or as a calcium supplement for the flock; Table 1). Selling and/or trading eggs from the flock was reported by 46% (n = 12) of respondents (Table 1). No respondents reported slaughtering and eating hens from the flock. Adults reported handling their hens on a daily basis in 42% (n = 11) of the flocks and reported daily contact with soil around the coop in 58% (n = 15) of the households. Just over two-thirds (62%, n = 16) of households reported that children live on the property (Table 1), and all households with children reported that the children had some degree of contact with the hens. Of the 16 households that reported having children, 19% (n = 3) reported that the children had contact with the hens on a daily basis, 44% (n = 7) reported weekly contact between children and hens, and 37% (n = 6) reported contact between children and hens occurring less than once a week. Of the households with children (n = 16), 19% (n = 3) reported that the children had contact with the soil around the coop on a daily basis, 19% (n = 3) reported the children had weekly contact with soil around the coop, and 62% (n = 10) reported that the children had less than weekly contact with soil around the coop.
Regarding lead use on the property, 35% (n = 9) of the 26 respondents reported known history of use, and 42% (n = 11) reported an awareness of potential lead exposure in their flock (Table 1). Nineteen percent of the 26 respondents (n = 5) reported they had taken steps to reduce lead exposure in the flock before participation in this study (Table 1). The details of how owners were aware of known history of lead use on the property and the actual steps taken to reduce lead exposure in the flock before participation in this study were not probed.
When stratified by population density, known history of lead use on the property was significantly higher in more densely populated neighborhoods compared with less densely populated neighborhoods (89% versus 11 % respectively; P =.006; Table 1). There were no other significant differences between household characteristics when stratified by population density (Table 1).
Of the 57 hens from 30 flocks sampled in this study, 70% (n = 40) of hens had detectable levels of lead in their blood representing 80% (n = 24) of flocks that were included in the study. The average BLL was 12.49 [micro]g/dL and ranged from less than the reported limit of the test to over 65 [micro]g/dL (Fig 2A). When stratified by population density, the mean BLL was higher in chickens that lived in more densely populated neighborhoods (mean = 16.05 [micro]g/dL, median = 10.1 [micro]g/dL, interquartile range = 17.5 [micro]g/dL; Fig 2B) compared with those that lived in less densely populated areas (mean = 8.8 [micro]g/dL, median = 5.2 [micro]g/dL, interquartile range = 7.7 [micro]g/dL; Fig 2B), a finding that neared statistical significance (P = .05; Table 2).
No significant association was found between the mean BLL of hens and their property roaming habits, the proximity of the coop to the home, whether the owners had taken steps to reduce lead exposure, and whether they lived on a property with a history of known lead exposure (Table 2).
Of the 27 flocks from which 2 birds were sampled, BLLs were discordant in 78% (n = 21) of the pairs. The mean difference between pairs from one flock was 8.87 [micro]g/dL (standard deviation = 13.68, range = 0-57.7).
None of the hens that were sampled in this study displayed clinical symptoms consistent with lead toxicosis or any illness at the time of sampling.
To our knowledge, this is the first study to assess subclinical lead exposure in BYCs. As ownership of backyard poultry increases, there is a parallel increase in the need to ensure safe management practices that protect the health of the chickens, their human caretakers, and their shared environment. (2,19-21) Because oversight concerning the health status of backyard poultry is minimal and few urban veterinarians treat chickens, there is a lack of resources and available data that can be used to guide husbandry and management decisions. This study serves as a preliminary assessment of BLLs of backyard poultry in Massachusetts while also highlighting the need for further research to understand how environmental lead contamination may affect the health and productivity of poultry raised in urban centers and to better define health risks to people.
Most birds sampled in this study had measurable BLLs that ranged from less than the reported limit of the test to greater than 65 [micro]g/dL. The toxic but sublethal BLL in waterfowl is reported at [greater than or equal to] 50 [micro]g/dL; however, clinical signs may be seen beginning at 20 [micro]g/dL. (22,23) Adverse health effects of lead toxicosis in people, particularly among children, have been well documented, and the World Health Organization has retracted a clinically relevant cut off, now stating that there is no safe BLL in children. (24,27) The levels seen in the hens in this study demonstrate considerable exposure to lead among BYCs. This presents a challenge because none of the chickens sampled displayed clinical signs of lead toxicosis. In part because the kinetics of lead in chickens is poorly understood, and in part because longitudinal data describing lead toxicosis in poultry is not available, the long-term effects of chronic lead exposure in chickens is unknown. This finding suggests that BYCs would benefit from routine screening for lead as a means of early detection and prevention, because the presence of clinical signs are an unreliable indicator of exposure. (6,11,28) This becomes particularly important when considering consumption of products from BYCs that may contain lead. While there is a linear correlation between BLL and egg lead concentrations in hens that are laying, a reduction in egg production is also documented in poultry that are intoxicated with lead. (9,10,22,23) Thus while testing eggs from BYCs to determine their exposure to lead may be logistically easier than collecting a blood sample, this approach is hampered by hens that experience decreased egg production and by the ability to discern between eggs produced by various hens in the flock. Taken together, our results highlight a need for poultry-specific recommendations and guidelines regarding lead exposure and safety in this unique setting.
Aside from testing and treating BYCs with high levels of lead in their blood, determining the route of exposure is important to maintaining a lead-free flock. The prevailing notion is that BYCs are exposed to environmental contaminants such as lead in the soil. Chickens are foragers by nature and spend a great deal of time digging through and sampling items from their environment. They often consume worms and insects, which have been shown to bioaccumulate lead if they live in a contaminated environment. (29,30) The data from this study show that chickens living in more densely populated areas had higher BLLs than those living in less densely populated areas, a finding that neared statistical significance. The densely populated areas in this study consisted largely of Boston and the surrounding urban neighborhoods, where levels of lead in soil are known to be high. (15,16) In fact, many owners who practice urban agriculture in these municipalities use raised beds with fresh soil for vegetable gardening to avoid contamination with the surrounding natural soil. This suggests that awareness of environmental lead contamination may be greater in more densely populated urban areas than in rural locations, which is consistent with our finding that a known history of lead use on the property was significantly higher in more densely populated neighborhoods. However, similar precautions are not routinely taken for chickens in these neighborhoods. Additionally, although not statistically significant, flocks that were allowed to roam the property tended to have higher average BLL than flocks that were not allowed to roam (Table 2), suggesting that birds allowed to forage from larger environments may have higher exposure to lead. A larger study with more participants would help clarify the significance of these trends. These findings also suggest that further research into the impact of soil lead on chicken BLLs is warranted. In addition, these findings highlight the need for more research to determine the public health relevance of raising poultry in lead-contaminated environments, especially in the context of families with children who regularly consume the BYC eggs, since lead exposure is a known health hazard and is more readily absorbed by the gastrointestinal tract of children. (6,9,11-13,24,25,27)
In many of the flocks that were sampled, one bird would have a substantially elevated BLL while another member would test negative. This has also been observed in a previous case report of acute lead exposure in a poultry flock. (11) There are several possible explanations for this, including differences in breed metabolism of lead and differences in foraging behaviors among members of the same flock. Among BYC flocks, chickens may also come from different sources and thus could have been exposed to lead before joining the flock. In addition, lead can accumulate in other tissues and in bone and may be mobilized under certain metabolic conditions. (22) This highlights a need to improve our understanding of lead absorption and metabolism in poultry to optimize recommendations for the duration and frequency of medical or environmental interventions.
When poultry are exposed to lead, the heavy metal accumulates in tissues such as liver, kidneys, and bone marrow. (6,31) Additionally, recent studies have shown a linear correlation between BLL of hens and the levels of lead in their eggs. (9,11,12) Given that 100% of survey respondents report regularly consuming eggs from their chickens, this raises the concern that chronic consumption of eggs from BYCs with high BLL could pose a health risk to humans. Some debate exists as to whether the amount of lead transferred into eggs would be enough to cause clinical problems in a healthy adult person. (12,31) Given that both the World Health Organization and the Centers for Disease Control and Prevention consider any level of lead detected in children to be unsafe, and that data show associations between low levels of lead and long-term health problems in adults and children, our data support the need for more robust research to understand and model lead exposure via consumption of contaminated BYC eggs. (24,25,27) Anecdotal reports from participants revealed that 2 separate households in the Boston suburbs had at least 1 child who was currently receiving lead chelation to treat elevated BLL. Between both of these households, 3 of the 4 birds sampled had elevated BLLs as well (mean = 7.55 [micro]g/dL, range 0-8.2 [micro]g/dL). While the circumstances under which the children were exposed to lead was not detailed and thus direct conclusions cannot be drawn, our findings suggest that BYCs may serve as sentinels of environmental lead contamination, and regular screening could assist families in recognizing lead contamination on their property. (28)
Most owners who participated in this study were unaware that lead exposure was an issue in BYCs. Few (19%) had taken preventative measures to protect their flock from exposure to lead before participation in this study. This gap in knowledge highlights an area for greater veterinary involvement in educating the public and their clients. Veterinarians who regularly see BYCs should encourage owners to test soil on their property for lead and have their birds screened for lead, and they also should have conversations with owners regarding preventative measures to reduce lead exposure in their flock. Preventative measures that can help reduce lead exposure in this context include 1) inspecting coop materials and nearby buildings for lead paint, 2) testing and replacing soil with high lead levels in and around the coop, and 3) restricting flock access to areas with known high levels of lead. We recommend that veterinarians wishing to treat BYCs access the recommended up-to-date clinical text and review article for treatment recommendations. (4,32)
While there is not a significant body of research that addresses lead prevention and/or remediation in the context of BYC keeping, 1 study found that increased dietary calcium is correlated with lower liver and blood lead values, and 1 study found that supplementation with garlic reduces lead absorption. (8,33) Calcium requirements differ for pullets and for laying hens. Diets high in calcium offered at a young age can increase the incidence of urolithiasis, interfere with proper absorption of other nutrients, and be detrimental to the health of young birds; however, high-calcium diets that are started a few weeks before egg production and offered through the laying season do not appear to have adverse health effects. (34) While garlic supplementation has been associated with numerous potential beneficial health outcomes, the long-term safety is not well studied. (35) These findings illustrate that changes in dietary composition and/or supplementation may be a promising approach to reduce lead absorption in poultry living in lead-contaminated environments; however, further investigation is needed to draw conclusions and inform prevention strategies. Flock owners should consult veterinarians or other poultry nutrition experts when considering supplementation with calcium and/or garlic to ensure proper nutritional support for their flock's developmental stage.
There were several limitations to this study, including sample size, that may have contributed to the limited significant findings. Selection bias (via convenience sampling) may have skewed results in that concerned owners may have been more likely to participate in the study. Another limitation to this study was that only 1-2 birds per flock were tested, regardless of the size of the flock. This was done because of resource constraints; however, individual variations between BLL among chickens from the same flock suggest that 1-2 randomly tested hens may not be representative of the entire flock. Future studies that consider intraflock variability would be useful to identify poultry behaviors associated with lead exposure. Owners were asked to catch 2 birds if able for testing, which may have introduced selection bias if the owners were choosing birds about which they were concerned or birds that were easier to catch.
Another limitation is that the test results do not provide a truly continuous scale for BLL and the unknown values below and above the limit of detection were modeled for the analysis. Thus, assigning all BLL values over the limit of detection the value of 65 [micro]g/dL and all BLL values lower than the limit of detection the value of 1.65 [micro]g/dL may have skewed our results. Additionally, we were not able to interpolate BLL values because there was a great deal of geographic variation between the flocks, and neighborhood-level variations in environmental contamination may have skewed our results.
To our knowledge, this is the first study aimed at systemically assessing prevalence of lead exposure in BYCs across a geographic range. The data generated from this study indicate that lead exposure is prevalent among Massachusetts urban flocks, with greater than two-thirds (70.2%) of birds sampled having detectable levels of lead in their blood (mean BLL = 12.49 [micro]g/dL). These findings raise the concern that 1) many backyard birds may be chronically exposed to high levels of lead in their environment and may remain clinically asymptomatic; and 2) consumption of products from these birds may represent an emerging source of exposure to lead for people. Additional research aimed to better understand exposure, clinical outcomes in poultry, and treatment and prevention strategies are warranted. Veterinarians who treat BYCs can play an important role in addressing this issue by recommending regular blood lead screening for BYCs and by discussing this underrecognized risk with clients. Lead exposure, in addition to other public health risks associated with BYC ownership, should be considered by municipalities that develop and oversee regulations surrounding BYC ownership in urban centers and by agencies and organizations that develop educational materials and recommendations guiding safe BYC keeping practices. (19,21)
Acknowledgments: We thank the Tufts Institute for Human-Animal Interactions for their funding support to carry out this study. We also thank Amanda Nee, Khrysti Smyth, and Jana Thomas, DVM, for their assistance in completing the study. The authors have no financial or personal disclosures to make regarding this study.
Daniel C. Mordarski, DVM, MPH, Jessica H. Leibler, DrPH, MS, Carolyn C. Talmadge, MS, Gregory M. Wolfus, DVM, Mark A. Pokras, DVM, and Marieke H. Rosenbaum, DVM, MPH, MS
From The Cummings School of Veterinary Medicine at Tufts University, 200 Westboro Road, North Grafton. MA 01536, USA (Mordarski. Wolfus. Pokras, Rosenbaum): Boston University School of Public Health, 715 Albany Street. Boston, MA 02118. USA (Leibler); and Tufts University, 419 Boston Avenue. Medford. MA 02115, USA (Talmadge).
(1.) U.S. City Dwellers Flock to Raising Chickens. Worldwatch Institute Web Site. http://www. worldwatch.org/node/5900. Accessed September 15, 2015.
(2.) US Department of Agriculture. Poultry 2010. Urban Chicken Ownership in Four U.S. Cities. Fort Collins, CO: USDA-APHIS-VS, CEAH; 2012.
(3.) Crespo R, Senties-Cue G. Postmortem survey of disease conditions in backyard poultry. J Exot Pet Med. 2015;24(2): 156-163.
(4.) Greenacre CB, Morishita TY. Backyard Poultry Medicine and Surgery: A Guide for Veterinary Practitioners. Ames, I A: John Wiley & Sons; 2015.
(5.) Whitehead ML, Roberts V. Backyard poultry: legislation, zoonoses, and disease prevention. J Small Anim Pract. 2014;55(10):487-496.
(6.) Roegner A, Giannitti F, Woods LW, et al. Public health implications of lead poisoning in backyard chickens and cattle: four cases. Vet Med Res Rep. 2013;4:11-20.
(7.) Mazliah J, Barron S, Bental E, et al. The effects of long-term lead intoxication on the nervous system of the chicken. Neurosci Lett. 1989;101(3):253-257.
(8.) Bakalli RI, Pesti GM, Ragland WL. The magnitude of lead toxicity in broiler chickens. Vet Hum Toxicol. 1995;37(1): 15-19.
(9.) Trampel DW, Imerman PM, Carson TL, et al. Lead contamination of chicken eggs and tissues from a small farm flock. J Vet Diagn Invest. 2003; 15(5); 418-422.
(10.) Salisbury RM, Staples ELJ, Sutton M. Lead poisoning of chickens. New Zealand Vet J. 1958; 6(1):2-7.
(11.) Bautista AC, Puschner B, Poppenga RH. Lead exposure from backyard chicken eggs: a public health risk? J Med Toxicol. 2014; 10(3):311-315.
(12.) Spliethoff HM, Mitchell RG, Ribaudo LN, et al. Lead in New York City community garden chicken eggs: influential factors and health implications. Environ Geochem Health. 2014;36(4):633-649.
(13.) Grace EJ, MacFarlane GR. Assessment of the bioaccumulation of metals to chicken eggs from residential backyards. Sci Total Environ. 2016; 1: 563-564:256-260.
(14.) USGS Background soil-lead survey: state data-Massachusetts. US Environmental Protection Agency Web Site, https://www.epa.gov/superfund/usgs-background-soil-lead-survey-state-data#MA. Accessed February 12, 2017.
(15.) Hynes HP, Maxfield R, Carroll P, et al. Dorchester lead-safe yard project: a pilot program to demonstrate low-cost, on-site techniques to reduce exposure to lead-contaminated soil. J Urban Health. 2001;78(1): 199-211.
(16.) Filippelli GM, Laidlaw MAS. The elephant in the playground: confronting lead-contaminated soils as an important source of lead burdens to urban populations. Perspect Biol Med. 2010;53(1):31-45.
(17.) Kornetsky R, Rock M, Pokras M. A rapid postmortem screening test for lead toxicosis in common loons (Gavia immer) and bald eagles (Haliaeetus leucocephalus). J Wildi Dis. 2013;49(3): 723-727.
(18.) US Census Bureau. 2010 Census Summary File 1. Washington, DC: US Census Bureau; 2012.
(19.) Tobin MR, Goldshear JL, Price LB, et al. A framework to reduce infectious disease risk from urban poultry in the United States. Public Health Rep. 2015; 130(4):380-391.
(20.) Karabozhilo I, Wieland B, Alonso S, et al. Backyard chicken keeping in the Greater London urban area: welfare status, biosecurity, and disease control issues. Br Poult Sci. 2012:53(4):421-430.
(21.) Pollock SL, Stephen C, Skuridina N, Kosatsky T. Raising chickens in city backyards: the public health role. J Community Health. 2012;37(3):734-742.
(22.) De Francisco N, Troya JDR, Aguera EI. Lead and lead toxicity in domestic and free-living birds. Avian Pathol. 2003;32(1):3-13.
(23.) US Fish and Wildlife Service. Lead poisoning in waterfowl. Washington DC: US Fish and Wildlife Service; 1990.
(24.) Lead. Centers for Disease Control and Prevention Web Site, http://www.cdc.gov/nceh/lead/. Accessed September 15, 2015.
(25.) Childhood lead poisoning. World Health Organization Web Site, http://www.who.int/ceh/publications/childhoodpoisoning/en/. Accessed September 20, 2015.
(26.) Navas-Acien A, Guallar E, Silbergeld EK, Rothenberg SJ. Lead exposure and cardiovascular disease--a systematic review. Environ Health Perspect. 2007; 115(3):472-482.
(27.) Lead poisoning and health. World Health Organization Web Site, http://www.who.int/mediacentre/factsheets/fs379/en/. Accessed November 5, 2016.
(28.) Bischoff K, Priest H, Mount-Long A. Animals as sentinels for human lead exposure: a case report. J Med Toxicol. 2010;6(2): 185-189.
(29.) Zhuang P, Zou H, Shu WB. Biotransfer of heavy metals along a soil-plant-insect-chicken food chain: field study. J Environ Sci. 2009;21(6):849-853.
(30.) Morgan JE, Morgan AJ. Earthworms as biological monitors of cadmium, copper, lead and zinc in metalliferous soils. Environ Pollut. 1988;54(2): 123-138.
(31.) Yabe J, Nakayama SMM, Ikenaka Y, et al. Metal distribution in tissues of free-range chickens near a lead-zinc mine in Kabwe, Zambia. Environ Toxicol Chem. 2013;32(1): 189-192.
(32.) Gonzalez MS, Carrrasco DC. Emergencies and critical care of commonly kept fowl. Vet Clin North Am Exot Anim Pract. 2016; 19(2):543-565.
(33.) Hossain MA, Mostofa M, Alam MN, et al. Effects of garlic (Allium sativum) feed supplement on hemato-biochemical properties in broiler chickens with sub-clinical toxicity of lead. Res Agric Livest Fish. 2013;1(1):87-96.
(34.) National Research Council. Nutrient Requirements of Poultry. 9th revised ed. Washington, DC: National Academy Press; 1994.
(35.) Khan RU, Nikousefat Z, Tufarelli V, et al. Garlic (Allium sativum) supplementation in poultry diets: effect on production and physiology. Worlds Poult Sci J. 2012;68:417-424.
Caption: Figure 1. Map of central/eastern Massachusetts showing the total number of hens sampled and the average blood lead levels (BLLs) per US Postal Service zip code overlaid on to population density (people per square mile). Triangle size corresponds to the total number of hens sampled per zip code, and circle size corresponds to the average BLL of hens per zip code.
Caption: Figure 2. (A) Histogram of blood lead levels (BLLs) among 57 clinically healthy backyard chickens (BYCs) from 30 flocks sampled in urban and rural eastern Massachusetts demonstrates that subclincal lead exposure is common, and (B) box plot depicting median BLL (line) in 57 BYCs stratified by density, expressed as people per square mile (PPSM) demonstrates that BYCs in denser neighborhoods tended to have higher BLLs than those in less densely populated areas.
Table 1. Summary of flock and household characteristics among 26 flocks of backyard chickens in eastern Massachusetts, stratified by population density. <1500 PPSM n (%) Flock characteristics Coop within 9.1 m from house (n = 25) 3 (27) Flock has access to soil 13 (52) Flock has access to outdoor property 10 (56) Household characteristics Known history of lead use on property 1 (11) Child lives on property 9 (56) Regularly consume eggs from flock 13 (50) Use other products from flock 5 (36) Sell or trade products from flock 5 (42) Aware of potential for 4 (36) lead exposure in flock Steps taken to reduce lead 2 (40) exposure in flock [greater than or equal to] 1500 PPSM n (%) Flock characteristics Coop within 9.1 m from house (n = 25) 8 (73) Flock has access to soil 12 (48) Flock has access to outdoor property 8 (44) Household characteristics Known history of lead use on property 8 (89) Child lives on property 7 (44) Regularly consume eggs from flock 13 (50) Use other products from flock 9 (64) Sell or trade products from flock 7 (58) Aware of potential for 7 (64) lead exposure in flock Steps taken to reduce lead 3 (60) exposure in flock Total n (%) P value Flock characteristics Coop within 9.1 m from house (n = 25) 11 (44) .07 Flock has access to soil 25 (96) .5 Flock has access to outdoor property 18 (69) .34 Household characteristics Known history of lead use on property 9 (35) .006 Child lives on property 16 (62) .34 Regularly consume eggs from flock 26 (100) -- Use other products from flock 14 (54) .12 Sell or trade products from flock 12 (46) .35 Aware of potential for 11 (42) .21 lead exposure in flock Steps taken to reduce lead 5 (19) .5 exposure in flock Abbreviation: PPSM indicates people per square mile. Table 2. Average blood lead level (BLL) of backyard chickens stratified by population density (n = 57), access to property (n = 49), proximity of coop to home (n = 48), known history of lead use on property (n = 49), and steps taken to prevent the flocks exposure to lead (n = 49 Mean BLL Standard ([micro]g/dL) deviation P value Human population density .05 <1500 PPSM 8.8 12.69 [greater than or 16.05 17.12 equal to] 1500 PPSM Access to property .22 yes 15.86 18.65 no 8.28 7.96 Coop proximity to home .65 <9.1 m 13.68 16.52 [greater than or 13.59 16.53 equal to] 9.1 m Known history of lead use on property .14 yes 14.54 15.0 no 12.78 17.1 Steps taken to prevent flock exposure to lead .43 yes 9.89 11.18 no 14.17 17.22 Abbreviation: PPSM indicates people per square mile.
|Printer friendly Cite/link Email Feedback|
|Title Annotation:||Original Study|
|Author:||Mordarski, Daniel C.; Leibler, Jessica H.; Talmadge, Carolyn C.; Wolfus, Gregory M.; Pokras, Mark A.|
|Publication:||Journal of Avian Medicine and Surgery|
|Date:||Sep 1, 2018|
|Previous Article:||Preliminary Findings of Structure and Expression of Opioid Receptor Genes in a Peregrine Falcon (Falco pevegrinus), a Snowy Owl (Bubo scandiacus),...|
|Next Article:||Retrospective Evaluation of Clinical Signs and Gross Pathologic Findings in Birds Infected With Mycobacterium genavense.|