Abstract
Wild meat often retains metallic particles originating from the ammunition fired by hunters. Since ammunition are traditionally lead (Pb)-based, the consumption of game meat may entail the ingestion of Pb embedded in tissues. To assess the related risks to human health, information is needed on the number, dimension and spatial distribution of Pb particles embedded in popular quarry species. In this study, we focused on the Eurasian woodcock (Scolopax rusticola), a medium-sized bird intensively hunted across its range. We X-rayed 59 carcasses of woodcock shot by Italian hunters in Ukraine. To check the ammunition types and evaluate the mean weight of the embedded gunshot, we excised a sample of 62 whole pellets from 20 birds. Ammunition residues were found in 57 of the 59 woodcock (96.6%). Radiographs revealed 215 whole pellets and 125 fragmentation centres in 51 (mean = 3.64) and in 48 birds (mean = 2.14), respectively. Most fragmentation centres (75.7%) contained tiny particles (<1 mm). The overall estimated Pb load ranged from 45 to 52 mg/100 g wet weight, most of which (84.6%) in edible parts. The number of embedded pellets per unit of body mass (1.21/100 g of body weight) was higher in comparison with other bird species and also with woodcock shot in the UK, presumably owing to the hunting methods adopted by Italian hunters. The quantity and characteristics of ammunition residues we found suggest that game meat consumers are exposed to a relevant Pb assumption.
Introduction
Lead (Pb) is a toxic element whose effects on human health are well known (Landrigan & Todd Citation1994). In the last decades, we have become aware that adverse consequences to organisms may arise even at very low doses when clinical symptoms are not evident. Many epidemiological studies revealed that low Pb exposures (<10 μg/dl in the bloodstream) are especially detrimental to foetuses and children, hampering the development of the nervous system and causing permanent negative effects on cognitive function and behaviour (Canfield et al. Citation2003; CDC Citation2005; Lanphear et al. Citation2005; Chandramouli et al. Citation2009). In adults, Pb affects information processing and short-term verbal memory, causing psychiatric symptoms and impairment of manual dexterity (Weisskopf et al. Citation2007). Furthermore, relatively low exposures among adults have been associated with elevated systolic blood pressure, increased risk of myocardial and stroke mortality, cancer and nephropathies (Menke et al. Citation2006; Schober et al. Citation2006; EFSA CONTAM Citation2010; Huang et al. Citation2013).
These findings prompted international health authorities to reject a safe threshold for Pb exposure as inappropriate and to advocate strongly for reduced intake of Pb as far as possible especially for the most sensitive categories (infants, children and pregnant women) (EFSA CONTAM Citation2010; JECFA Citation2010).
Since ingestion is considered the major source of exposure to Pb in developed countries, the intake of Pb for the population of Europe was estimated by analysing Pb contamination in all food categories (EFSA Citation2012). According to EFSA (Citation2012), Pb levels in food have decreased recently, but the consumption of some food categories may remain a cause of concern. Particularly, high concentrations were recorded in wild boar and pheasant meat, well above the maximum levels admitted by the Commission Regulation No. 1881/2006 for the categories ‘meat (excluding offal) of bovine animals, sheep, pig and poultry’ (max Pb level: 100 μg/kg wet weight) and ‘offal of bovine animals, sheep, pig and poultry’ (max Pb level: 500 μg/kg wet weight) (Commission of the European Communities Citation2006). The EFSA food category ‘boar (wild pig)’ meat gave a mean of 1143 μg/kg, 100-fold higher than ‘pork/piglet’ meat (mean value 11 μg/kg). Furthermore, some boar samples peaked at 232000 μg/kg. Similarly, ‘pheasant’ meat reached Pb concentrations 28-fold higher than ‘chickens’ meat (344 μg/kg versus 12 μg/kg). Similar differences between the game and domestic animals were found in the UK (Pain et al. Citation2010).
These results are due to the use of Pb ammunition for hunting game animals. High Pb values have been frequently found both in venison and game birds shot by hunters and intended for human consumption (Tsuji et al. Citation1999; Johansen et al. Citation2004; Cornatzer et al. Citation2009; Pain et al. Citation2010). Soft tissues of large mammals often retain a high number of fragments up to more than 45 cm away from the wound channel, as a result of the frangibility of the various kinds of a rifle bullet. In most cases, fragments are too small and are hardly ever detected or removed during food preparation (Hunt et al. Citation2006, Citation2009; Tsuji et al. Citation2009; Grund et al. Citation2010; Knott et al. Citation2010; Lindboe et al. Citation2012). Contamination is even higher in birds because they are generally killed by several small gunshot pellets instead of a single bullet. Normally, pellets are so small that it is difficult to remove them from the flesh even if they remain whole. Furthermore, they do tend to fragment, creating a large amount of microscopic splinters and particles (Scheuhammer et al. Citation1998; Mateo et al. Citation2011; Andreotti & Borghesi Citation2013).
The typical practices employed to prepare game meat for consumption (dressing, marinating and cooking in wine, vinegar or in other acidic conditions) facilitate the conversion of metallic Pb into organic compounds, which are more easily absorbed by the digestive system (Mateo et al. Citation2007, Citation2011; Hunt et al. Citation2009). Several studies have revealed a significant association between Pb blood levels and wild game consumption in human populations, not only in arctic regions where wild game is a significant part of the diet (Hanning et al. Citation2003; Bjerregaard et al. Citation2004; Johansen et al. Citation2006) but also at mid-latitude regions (Iqbal et al. Citation2009). Such evidence has encouraged researchers and several national authorities for health and food safety to assess the risk of Pb poisoning through the consumption of game meat. The results of these assessments concluded that the risks posed by Pb ammunition on human health are not negligible and appropriate measures are needed to minimise those risks (AESAN Citation2012; Green & Pain Citation2012, Citation2015; VKM Citation2013).
In Europe, a rough estimation of the human population exposed to Pb through the consumption of game meat can be obtained through analysis of the number of hunters and their relatives. According to the European Federation of Associations for Hunting and Conservation, in Europe, there are seven million hunters, without including Russia and Turkey. Therefore, it can be assumed that several tens of millions of Europeans, corresponding to approximately 2–4% of the whole population, more or less regularly eat game meat. The amount of birds shot annually in Europe is estimated to be 101 million (Hirschfeld & Heyd Citation2005).
To assess the risk to the health of wild meat consumers, it is important to know the quantity and characteristics of the Pb embedded in the flesh of the most popular quarry species. In this study, we focused on Pb contamination in the Eurasian woodcock (Scolopax rusticola), a medium-sized bird intensively hunted across its range. We examined adults and juveniles separately since adults may retain Pb fragments in old wounds originating in previous hunting seasons (Falk et al. Citation2006; Newth et al. Citation2011; Holm & Madsen Citation2013). According to Annex II/A of the EU Directive 2009/147/CE, the woodcock can be hunted in all the states within the Union borders (European Parliament and Council of the European Union Citation2010). Furthermore, the species is intensively shot in the Balkans and in the European countries of the former USSR, both by resident and foreign hunters. Given the popularity of woodcock hunting in Europe, the consumption of its meat is widespread and considerable, but unfortunately, only rough estimates are available on the number of birds annually killed on the continent. Ferrand and Gossmann (Citation2009a) proposed an approximate figure of 3–4 million individuals while Hirschfeld and Heyd (Citation2005) suggested a minimum of 2730125 woodcock shot per year in the EC, Switzerland and Norway.
Specific objectives of our study were: i) to estimate the frequency of both whole pellets and fragments in shot woodcock; ii) to assess if any difference exists in pellet and fragment frequency between adults and juveniles; iii) to estimate the Pb burden embedded in the edible parts and iv) to evaluate implications for the human health.
Materials and methods
We examined a sample of 59 individuals (28 juveniles and 31 adults) selected from a stock of 485 Eurasian woodcock shot by Italian hunters during a hunting trip in Ukraine in October 2011 and seized by the Italian Custom Agency because they were imported without complying to sanitary regulations. No bird was expressly killed for this study. The birds were frozen whole and stored at −20 °C. On analysis, the woodcock were thawed, aged by plumage and moult status (Ferrand & Gossmann Citation2009b) and weighed to the nearest gram with a Pesola spring balance. Our sample of juveniles and adults was selected with their body weights within a range of ±15% the average weight of the whole seized stock. We considered both age and weight because: 1) old birds may have embedded pellets remaining from healed wounds in previous hunting seasons (Falk et al. Citation2006; Newth et al. Citation2011) and 2) weight is a reliable measure of body mass, that in turn affects the number of embedded pellets (Pain et al. Citation2010).
We X-rayed the birds with digital radiography equipment (Kodak DirectView CR 800 System, and Kodak DirectView CR cassette 35 × 43 cm with a matrix size of 2048 × 2500) (Eastman Kodak Company, Rochester, NY). Metal particles are easy to distinguish from bone and grit because they are clearly more radio-opaque (Knott et al. Citation2010). Radiographs were examined at full size to detect whole pellets and large fragments. Micro fragments were counted by zooming into 150%. We considered as ‘large’ those fragments exceeding 0.5 mm in diameter (Hunt et al. Citation2006).
Following Andreotti and Borghesi (Citation2013), we subdivided the body of each bird into seven sectors so that the anatomical parts normally consumed by humans could be easily considered separately (). We regarded sectors 3, 4, 5 and 6 as edible, i.e. those most commonly eaten by humans.
Figure 1. X-ray photograph of a woodcock, showing the body sectors where the position of each shot pellet and fragment was noted. 1, head and neck; 2, wings; 3, humerus and a pectoral girdle; 4, thorax; 5, abdomen; 6, femur and tibiotarsus and 7, tarsus and metatarsus. A whole pellet and six fragmentation centres can be recognised inside the grey circles.
We counted the number of whole shot pellets, single macro fragments and clusters of radiodense particles (fragmentation centres – FC) embedded in each body sector. The fragments were scored as follows: 0 = none visible; 1 = 1–2 macro fragments; 2 = 2–4 micro-fragments and 3= > 4 fragments, regardless of their size. We tested whether the number of pellets and fragments observed in the body varied among age classes and body sectors with a chi-square test of independence performed using the R software (R Foundation for Statistical Computing, Vienna, Austria) (R Core Team Citation2013).
To check the ammunition types used by hunters, we performed a necropsy on 20 woodcock and excised 62 whole pellets (2–4 from each bird). These pellets were accurately washed, dried and weighed by means of a Sartorius analytical balance (accuracy d = 0.1 mg) (A&D Laboratory Balances, Bradford, MA). Furthermore, each pellet was examined for colour, form and size, and tested to see whether they were attracted by a bar magnet.
To evaluate the Pb quantity embedded in our sample, we multiplied the number of whole pellets by the mean weight of the excised pellets. Since most pellets lose fragments under the impact, this estimation was repeated considering the mean weight of the heaviest pellets from each woodcock, except in the case of three woodcock with pellets of different sizes, for which the mean weight of the excised pellets was used. Finally, we related the estimated amounts of Pb to the overall weight of the whole woodcock sample to obtain the Pb burden in 100 g wet weight.
Results and discussion
Ammunition residues were found in 57 of the 59 carcasses (96.6%). We observed only whole pellets or fragments in 9 (15.8%) and 6 (10.5%) carcasses, respectively, while in 42 carcasses (73.7%) we found both. Pellets and fragments were embedded in all body sectors ( and ), but with significant differences in frequency (pellets: chi-square value = 77.17, df = 6, p<0.001; fragments: chi-square value = 79.9, df = 6, p<0.001). In the anatomical regions most commonly eaten by humans, we found Pb residues in 47 carcasses (79.7%). No significant difference was detected between age classes in frequencies of whole shot and fragments (pellets: chi-square value = 10.34, df = 6, p=0.11; fragments: chi-square value = 7.68, df = 6, p=0.26).
Table 1 (A). Distribution of pellets in different body sectors of juveniles and adults of Eurasian woodcock shot during hunting activity.
Table 1 (B). Distribution of fragments in different body sectors of juveniles and adults of Eurasian woodcock shot during hunting activity.
Shotgun pellets
Radiographs revealed 215 pellets in 51 woodcock (mean = 3.64, SD = 3.97, range = 0–17, n = 59). Most of the pellets (n=131, 60.9%) were located in sectors 3 and 4 while only a small fraction (n=15.7%) was found in the distal parts of the wings and legs (sector 2 and 7; and ). In the edible sectors, we counted 182 pieces of shot, corresponding to 84.6% of the total amount (mean = 3.08, SD = 3.64, range = 0–17, n=59). In three adults, we detected pellets of different size by examining the radiographs. We ascertained that they were whole pellets of different dimensions by examining them after excision. During the necropsy, we did not find any evidence of connective tissue encapsulation.
Fragments
A minimum of 125 FC were detected in 48 woodcock (mean = 2.14, SD = 2.28, range = 0–10, n = 59). FC were concentrated (n=93, 74.4%) in the head, neck, wings and the pectoral girdle (). In the edible sectors, we estimated 44 FC, representing 35.2% of the detected FC (mean = 0.75, SD = 1.32, range = 0–6, n = 59). In most cases, the fragments were assigned to score 2 (n=62, 49.6%) or score 3 (n=36%), revealing a prevalence of small tiny particles ( and ).
Table 2 (A). Distribution of different fragment classes in adults of Eurasian woodcock shot during hunting activity (score 0 = none visible; score 1 = 1–2 macro fragments; score 2 = 2–4 micro fragments; score 3= > 4 fragments, regardless of their size).
Table 2 (B). Distribution of different fragment classes in juveniles of Eurasian woodcock shot during hunting activity (score 0 = none visible; score 1 = 1–2 macro fragments; score 2 = 2–4 micro fragments; score 3= > 4 fragments, regardless of their size).
Pellet characteristics
All pellets were non-magnetic, dark, dull and deformed, and, therefore, were assumed to be Pb. Overall they weighed 2319.8 mg (mean = 37.4 mg, SD = 16.7, range = 13.1–76.7, n=62). When taking the heaviest pellets from each necropsied woodcock, we obtained a mean weight of 43.8 mg (SD = 16.7, range = 20.0–76.7 n=20).
Woodcock weights
The mean weight of the whole stock of seized woodcock did not differ significantly from the examined sample (whole stock: mean = 313.8 g, SD 30.1, n=403; examined woodcock: 304.0 g, SD = 1.7, n=59; t-test= −1.94, p=0.05). The mean weights of adults and juveniles did not differ (juveniles: mean = 304.0 g, SD = 15.4, n=28; adults: mean = 300.4 g, SD = 19.5, n=31; t-test= −0.18, p = 0.40).
Pb mass
On the basis of both the mean weight of the excised pellets and the heaviest pellet subset, we estimated the Pb burden embedded in woodcock ranging from 45 to 52 mg/100 g wet weight.
Comparison with previous studies
Our study revealed that the majority of the X-rayed carcasses contained visible particles of metallic Pb deriving from spent ammunition. In comparison with data collected in previous studies on different bird species, woodcock had a higher rate of embedded whole pellets per unit of body mass, i.e. 1.21 pellets/100 g of body weight, versus 0.93 in European starlings (Andreotti & Borghesi Citation2013), 0.73 in red-legged partridges (Mateo et al. Citation2011), 0.52 in common eiders (Johansen et al. Citation2004) and 0.41 in thick-billed murres (Johansen et al. Citation2001). Moreover, the frequency of pellets counted in our study is relatively high when compared to the figures reported by Pain et al. (Citation2010) for the Eurasian woodcock hunted in the UK. The authors X-rayed oven-ready carcasses (without feathers, viscera and heads) and recorded numbers of pellets and large radio-dense fragments. They found a mean of one pellet per woodcock, a low value with respect to the mean of 3.1 detected in our study considering edible sectors only.
These discrepancies in pellet frequency may be due to different hunting methods adopted with regard to the target species and traditional hunting practices. The low shot resistance of woodcock leads many hunters to prefer cartridges with numerous pellets of smaller size than those used to shoot game birds with a similar body mass. In addition, the hunting technique may influence the firing distance, which affects the spread pattern of projectiles hitting the prey. For example, in the UK, woodcock are often flushed towards the guns by a line of ‘beaters’ walking through the wood, while Italian hunters prefer to walk behind a pointing dog, shooting the woodcock at a shorter distance over the dog’s point (Spanò & Fadat Citation2014). Hence, the quantity of Pb embedded in quarry bird species appears to be related not only to the species but also to the hunting technique. These results should be borne in mind when assessing Pb contamination levels in game meat from different countries.
The concomitant presence of pellets of different size embedded in three adults might be explained by either the use of cartridges loaded with mixed grains or the existence of old wounds originating in previous hunting seasons. Since only slight changes occur in tissues surrounding Pb gunshot embedded in old wounds (Sanderson et al. Citation1998), the circumstance that we did not observe connective tissue encapsulation does not allow us to exclude the presence of pellets from previous hunting seasons.
We did not find a higher frequency of whole pellets in adults when compared to juveniles, as found in long-lived species such as sea ducks and geese that can accumulate pellets in subsequent hunting seasons (Falk et al. Citation2006; Newth et al. Citation2011; Holm & Madsen Citation2013). This result might be influenced by two factors: (i) woodcock have little or no resilience to the shot and hardly ever survive when injured and (ii) adults are more cautious than juveniles and flush earlier when stalked leading to them being shot at longer distances by a wider pellet spread. This latter factor is relevant in assessing the Pb load in woodcock meals because juveniles are generally far more abundant than adults in hunting bags (more than 65% juveniles in France (Boidot & Aurousseau Citation2013); 81.1% juveniles in our sample).
If we compare data on fragments recorded in starlings in a study carried out with a similar methodology (Andreotti & Borghesi Citation2013), we observe a higher density of FC in woodcock (0.72 FC per 100 g of body weight, versus 0.60 in starlings), even if the fragmentation rate of pellets, calculated as the ratio FC/whole pellets, appears to be slightly lower in woodcock than in starlings (0.58 versus 0.64). The difference in the fragmentation rate might be related to a higher frequency of pellets that have passed through the starlings leaving Pb particles in the tissues, but have not remained in the carcass due to the smaller body mass of this species. Fragment distribution in woodcock differs significantly from starlings when considering all body sectors (chi-square value = 27.7, df = 6 p<0.0001), but there is no difference when taking into account the edible parts only (chi-square value = 0.4, df = 3, p=0.9).
Levels of Pb contamination in woodcock meat found in our study are much higher than those reported for venison examined by X-ray. As far as we know, there is only one estimate of the total mass of bullet fragments left in carcasses of deer (Knott et al. Citation2010). This corresponds to 1.6 mg/100 g wet weight, 30-fold lower than the estimates of Pb embedded in woodcock. Pb concentrations determined through chemical analysis confirm a higher burden of Pb in birds than in ungulates, but these differences are less relevant. For example, in partridges values have been found 2–8-fold higher than in red deer or wild boar (Mateo et al. Citation2011; Sevillano Morales et al. Citation2011). This discrepancy can be explained considering that in birds there is a relatively higher amount of large Pb particles (essentially whole pellets) that are generally removed before performing chemical analyses.
Implication for the human health
Our findings reveal that woodcock meat derived from animals shot by traditional Pb ammunition retains a considerable quantity of metallic Pb in the form of both large particles (i.e. macro fragments and whole pellets) and tiny fragments. Even when substantial pieces of Pb are removed from game meat, the presence of Pb is still significant, especially where tiny fragments are spread widely. Chemical analyses have found high levels of Pb contamination in game tissue samples of quarry species where Pb particles were detected by X-ray (Tsuji et al. Citation1999, Citation2009; Johansen et al. Citation2001; Pain et al. Citation2010; Mateo et al. Citation2011). Furthermore, embedded Pb can be easily absorbed through the intestine by game meat consumers, given the amount of tiny fragments, easily attacked by the gastric acid, and the leaching processes during cooking treatments (Mateo et al. Citation2007, Citation2011; Hunt et al. Citation2009). Hence, regular woodcock meat consumers are exposed to real health risks.
Hunters are not usually woodcock specialists, killing both ungulates and small game during the same hunting season. This implies that people consuming woodcock often eat other game birds, small mammals and ungulates. It has been found that frequent consumption of big game meat alone is enough to expose the hunter population to the risk of Pb poisoning (Sevillano Morales et al. Citation2011; Lindboe et al. Citation2012). Consumption of contaminated woodcock meat will increase the intake of Pb in game consumers already exposed to the risk of Pb poisoning. In Italy, more than 230 000 ungulates are estimated to be shot annually, producing 6828.7 tons of game meat (Ramanzin et al. Citation2010), in addition to at least 17 million birds (Hirschfeld & Heyd Citation2005) and an unknown number of hares and rabbits. Since the use of Pb ammunition is banned exclusively in wetlands of special protection areas and in some hunting districts for the hunting of cloven-hoofed games, only a negligible fraction of game birds and mammals is killed with Pb-free shot or bullets. This means that the 750 000 licenced hunters in Italy and their relatives consume approximately tens of millions of meals derived from ungulates and no less than 5 million meals from game birds, killed with Pb ammunitions.
The high frequency of Pb pieces and, in particular, of tiny fragments recorded in this study reveals that precautions during the preparation for consumption of shot game birds are not enough to guarantee Pb-free meat. The removal of whole pellets before cooking is not easily achieved, given their small size and abundance, and does not prevent the ingestion of a significant quantity of the smallest particles. Additionally, Pb residues are almost uniformly distributed in game bird carcasses, making removal more difficult. It is a different case to ungulates, where fragments of ammunition are concentrated in a radial zone around the wound channel, allowing a small concentrated area of the carcass to be removed and disposed of. The distribution of Pb in bird carcasses makes it impossible to define handling procedures which reduce the risk for game bird consumers. The use of Pb-free pellets is the only effective solution to avoid the consumption of Pb when eating shot small game. It could also reduce the Pb pollution in the environment. Positive effects have been observed in wildlife and ecosystems, where Pb ammunition has been banned (Mateo et al. Citation2014).
Conclusions
The considerable amount of embedded particles of metallic Pb found in our study suggests that a significant risk to human health is associated with the frequent consumption of woodcock killed using traditional Italian hunting techniques. Therefore, a risk assessment is recommended.
To reduce the hazard of Pb poisoning on regular woodcock consumers and more in general on game meat consumers, actions should be promoted to raise awareness of the risks among exposed groups (hunters, gamekeeper, etc.). A mandatory Pb-free certification mark could be used to provide a guarantee of safety for game meat consumers. At the same time, the adoption of a total ban for the use of Pb ammunition in both aquatic and terrestrial ecosystems is strongly recommended (Group of Scientists Citation2014).
Funding information
The study was funded by the Ministry for the Environment and the Protection of the Land and the Sea (MATTM, Italy).
Acknowledgements
The authors thank Paolo Vigo and Livia Zamboni for supporting them in taking the radiographs, Adriano De Faveri for supporting them in performing the necropsies, Riccardo Santolini, Milena Libretto, Giancarlo Passaglini and AUSL Rimini for allowing them the acquisition of the carcasses. They also thank Mark W. Miller and Craig Brakes for their helpful comments.
Disclosure statement
The authors report no conflicts of interest. The authors alone are responsible for the content and writing of this article.
References
- AESAN. 2012. Report of the Scientific Committee of the Spanish Agency for Food Safety and Nutrition (AESAN) in relation to the risk associated with the presence of lead in wild game meat in Spain. Revista del Comité Científico de la AESAN. 15:131–159.
- Andreotti A, Borghesi F. 2013. Embedded lead shot in European starlings Sturnus vulgaris: an underestimated hazard for humans and birds of prey. Eur J Wildl Res. 59:705–712.
- Bjerregaard P, Johansen P, Mulvad G, Pedersen HS, Hansen JC. 2004. Lead sources in human diet in Greenland. Environ Health Perspect. 112:1496–1498.
- Boidot JP, Aurousseau G. 2013. Evaluation of the 2012-2013 Woodcock hunting season in France. IW/IUCN_WSSG Newslett. 39:29–30.
- Canfield RL, Henderson CR, Cory-Slechta DA, Cox C, Jusko TA, Lanphear BP. 2003. Intellectual impairment in children with blood lead concentrations below 10 μg per deciliter. N Engl J Med. 348:1517–1526.
- CDC Centers for Disease Control and Prevention. 2005. Preventing lead poisoning in young children. Atlanta, GA: U.S. Department of Health and Human Services – CDC.
- Chandramouli K, Steer CD, Ellis M, Emond AM. 2009. Effects of early childhood lead exposure on academic performance and behaviour of school age children. Arch Dis Child. 94:844–848.
- Commission of the European Communities. 2006. Commission Regulation (EC) No 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Off J Eur Union. L364:5–24.
- Cornatzer WE, Fogarty EF, Cornatzer EW. 2009. Qualitative and quantitative detection of lead bullet fragments in random venison packages donated to the community action food centers of North Dakota, 2007. In: Watson RT, Fuller M, Pokras M, Hunt WG, editors. Ingestion of lead from spent ammunition: implications for wildlife and humans. Boise, ID: The Peregrine Fund. p. 154–156.
- EFSA. 2012. Lead dietary exposure in the European population. EFSA J. 10:2831.
- EFSA CONTAM. 2010. Scientific opinion on lead in food. EFSA J. 8:1570.
- European Parliament, Council of the European Union. 2010. Directive No 2009/147/UE of 30 November 2009 on the conservation of wild birds. Off J Eur Union. L20:7–25.
- Falk K, Merkel F, Kampp K, Jamieson SE. 2006. Embedded lead shot and infliction rates in common eiders Somateria mollissima and king eiders S. spectabilis wintering in southwest Greenland. Wild Biol. 12:313–321.
- Ferrand Y, Gossmann F. 2009a. La Bécasse des bois. Histoire naturelle. Saint-Lucien, France: Effect de Lisière.
- Ferrand Y, Gossmann F. 2009b. Ageing and sexing series 5: ageing and sexing the Eurasian Woodcock Scolopax rusticola. Wader Study Group Bull. 113:75–79.
- Green RE, Pain DJ. 2012. Potential health risks to adults and children in the UK from exposure to dietary lead in gamebirds shot with lead ammunition. Food Chem Toxicol. 50:4180–4190.
- Green RE, Pain DJ. 2015. Risks of health effects to humans in the UK from ammunition-derived lead. In: Delahay RJ, Spray CJ, editors. Proceedings of the Oxford Lead Symposium. Lead Ammunition: understanding and minimising the risks to human and environmental health. The University of Oxford, UK: Edward Grey Institute. p. 27–43.
- Group of Scientists. 2014. Wildlife and human health risks from lead-based ammunition in europe: a consensus statement by scientists. Available from: http://www.zoo.cam.ac.uk/. Accessed on October 10, 2014.
- Grund MD, Cornicelli L, Carlson LT, Butler EA. 2010. Bullet fragmentation and lead deposition in white-tailed deer and domestic sheep. Human Wildlife Interact. 4:257–265.
- Hanning RM, Sandhu R, MacMillan A, Moss L, Tsuji LJS, Nieboer E. 2003. Impact on blood Pb levels of maternal and early infant feeding practices of First Nation Cree in the Mushkegowuk Territory of northern Ontario, Canada. J Environ Monit. 5:241–245.
- Hirschfeld A, Heyd A. 2005. Mortality of migratory birds caused by hunting in Europe: bag statistics and proposals for the conservation of birds and animal welfare. Ber Vogelschutz. 42:47–74.
- Holm TE, Madsen J. 2013. Incidence of embedded shotgun pellets and inferred hunting kill amongst Russian/Baltic barnacle geese Branta leucopsis. Eur J Wildl Res. 59:77–80.
- Huang WH, Lin JL, Lin-Tan DT, Hsu CW, Chen KH, Yen TH. 2013. Environmental lead exposure accelerates progressive diabetic nephropathy in type II diabetic patients. Biomed Res Int. vol. 2013, Article ID 742545, 9 pages. doi:10.1155/2013/742545.
- Hunt WG, Burnham W, Parish CN, Burnham KK, Mutch B, Oaks JL. 2006. Bullet fragments in deer remains: implications for lead exposure in avian scavengers. Wildl Soc Bull. 34:167–170.
- Hunt WG, Watson RT, Oaks JL, Parish CN, Burnham KK, Tucker RL, Belthoff JR, Hart G. 2009. Lead bullet fragments in venison from rifle-killed deer: potential for human dietary exposure. PLoS One. 4:e5330.
- Iqbal S, Blumenthal W, Kennedy C, Yip FY, Pickard S, Flanders WD, Loringer K, Kruger K, Caldwell KL, Brown MJ. 2009. Hunting with lead: association between blood lead levels and wild game consumption. Environ Res. 109:952–959.
- JECFA. 2010. Food and Agriculture Organization of the United Nations Joint FAO/WHO Expert Committee on Food Additives, 73rd meeting, Geneva, 8–17 June 2010. Summary and conclusions. Available from: http://www.who.int/. Accessed on February 20, 2011.
- Johansen P, Asmund G, Riget F. 2001. Lead contamination of seabirds harvested with lead shot - implications to human diet in Greenland. Environ Pollut. 112:501–504.
- Johansen P, Asmund G, Riget F. 2004. High human exposure to lead through consumption of birds hunted with lead shot. Environ Pollut. 127:125–129.
- Johansen P, Pedersen HS, Asmund G, Riget F. 2006. Lead shot from hunting as a source of lead in human blood. Environ Pollut. 142:93–97.
- Knott J, Gilbert J, Hoccom DG, Green RE. 2010. Implications for wildlife and humans of dietary exposure to lead from fragments of lead rifle bullets in deer shot in the UK. Sci Total Environ. 409:95–99.
- Landrigan J, Todd AC. 1994. Lead poisoning. West J Med. 161:153–159.
- Lanphear BP, Hornung R, Khoury J, Yolton K, Baghurst P, Bellinger DC, Canfield RL, Dietrich KN, Bornschein R, Greene T, et al. 2005. Low level environmental lead exposure and children’s intellectual function: an international pooled analysis. Environ Health Perspect. 113:894–899.
- Lindboe M, Henrichsen EN, Høgåsen HR, Bernhoft A. 2012. Lead concentration in meat from lead-killed moose and predicted human exposure using Monte Carlo simulation. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 7:1052–1057.
- Mateo R, Baos AR, Vidal D, Camarero PR, Martinez-Haro M, Taggart MA. 2011. Bioaccessibility of Pb from ammunition in game meat is affected by cooking treatment. PLoS One. 6:e15892.
- Mateo R, Rodríguez-de la Cruz M, Vidal D, Reglero M, Camarero P. 2007. Transfer of lead from shot pellets to game meat during cooking. Sci Total Environ. 372:480–485.
- Mateo R, Vallverdú-Coll N, López-Antia A, Taggart MA, Martínez-Haro M, Guitart R, Ortiz-Santaliestra ME. 2014. Reducing Pb poisoning in birds and Pb exposure in game meat consumers: The dual benefit of effective Pb shot regulation. Environ Int. 63:163–168.
- Menke A, Muntner P, Batuman V, Silbergald EK, Guallar E. 2006. Blood lead below 0.48 micromol/L (10 microg/dL) and mortality among US adults. Circulation. 114:1388–1394.
- Newth JL, Brown MJ, Rees EC. 2011. Incidence of embedded shotgun pellets in Bewick’s swans Cygnus columbianus bewickii and Whooper swans Cygnus cygnus wintering in the UK. Biol Conserv. 144:1630–1637.
- Pain DJ, Cromie RL, Newth J, Brown MJ, Crutcher E, Hardman P, Hurst L, Mateo R, Meharg AA, Moran AC, et al. 2010. Potential hazard to human health from exposure to fragments of lead bullets and shot in the tissues of game animals. PLoS One. 5:e10315.
- Ramanzin M, Amici A, Casoli C, Esposito L, Lupi P, Marsico G, Mattiello S, Olivieri O, Ponzetta MP, Russo C, et al. 2010. Meat from wild ungulates: ensuring quality and hygiene of an increasing resource. Ital J Anim Sci. 9:318–331.
- R Core Team. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing. Wien, Austria. Available from: http://www.R-project.org/. Accessed on March 1, 2013.
- Sanderson GC, Anderson WL, Foley GL, Havera SP, Skowron LM, Brawn JW, Taylor GD, Seets JW. 1998. Effects of lead, iron, and bismuth alloy shot embedded in the breast muscles of game-farm mallards. J Wildl Dis. 34:688–697.
- Scheuhammer AM, Perrault JA, Routhier E, Braune BM, Campbell GD. 1998. Elevated lead concentrations in edible portions of game birds harvested with lead shot. Environ Pollut. 102:251–257.
- Schober SE, Mirel Lisa B, Graubard BI, Brody DJ, Flegal KM. 2006. Blood lead levels and death from all causes, cardiovascular disease, and cancer: results from the NHANES III mortality study. Environ Health Perspect. 114:1538–1541.
- Sevillano Morales JS, Moreno Rojas R, Pérez-Rodríguez F, Arenas Casa AA, Amaro López MA. 2011. Risk assessment of the lead intake by consumption of red deer and wild boar meat in Southern Spain. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 28:1021–1033.
- Spanò S, Fadat C. 2014. La Beccaccia. Gavi, Italy: Editore Il Piviere.
- Tsuji LJS, Nieboer E, Karagatzides JD, Hanning RM, Katapatuk B. 1999. Lead shot contamination in edible portions of game birds and its dietary implications. Ecosys Health. 5:183–192.
- Tsuji LJS, Wainman BC, Jayasinghe RK, Van Spronsen EP, Liberda EN. 2009. Determining tissue-lead levels in large game mammals harvested with lead bullets: human health concerns. Bull Environ Contam Toxicol. 82:435–439.
- VKM. 2013. Risk assessment of lead exposure from cervid meat in Norwegian consumers and in hunting dogs. Opinion of the panel on contaminants of the Norwegian scientific committee for food safety. Final document 11-505. Available from: http://www.english.vkm.no/. Accessed on September 24, 2013.
- Weisskopf MG, Proctor SP, Wright RO, Schwartz J, Spiro A, Sparrow D, Nie H, Hu H. 2007. Cumulative lead exposure and cognitive performance among elderly men. Epidemiology. 18:59–66.