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HomeMy WebLinkAboutArticle – Laidlaw et al. – Lead exposure at firing ranges – a reviewLaidlaw et al. Environmental Health (2017) 16:34 DOI 10.1186/sl 2940-017-0246-0 Environmental Health REVIEW Open Lead exposure at firing ranges—a review (S CmssMark Mark A. S. Laidlaw'', Gabriel Filippelliz, Howard Mielke3, Brian Gulson4 and Andrew S. Ball' Abstract Background: Lead (Pb) is a toxic substance with well-known, multiple, long-term, adverse health outcomes. Shooting guns at firing ranges is an occupational necessity for security personnel, police officers, members of the military, and increasingly a recreational activity by the public. In the United States alone, an estimated 16,000-18;000 firing ranges exist. Discharge of Pb dust and gases is a consequence of shooting guns. Methods: The objectives of this study are to review the literature on blood lead levels (BILLS) and potential adverse health effects associated with the shooting population. The search terms "blood lead", 'lead poisoning", 'lead exposure', "marksmen", "firearms", "shooting", "guns", "rifles' and "firing ranges' were used in the search engines Google Scholar, PubMed and Science Direct to identify studies that described BLLS in association with firearm use and health effects associated with shooting activities. Results: Thirty-six articles were reviewed that included BILLS from shooters at firing ranges. In 31 studies BILLS > 10 µg/ dL were reported in some shooters, 18 studies reported BILLS > 20 pg/d L, 17 studies > 30 pg/d, and 15 studies BILLS > 40 pg/d L. The literature indicates that BLLs in shooters are associated with Pb aerosol discharge from guns and air Pb at firing ranges, number of bullets discharged, and the caliber of weapon fired. Conclusions: Shooting at firing ranges results in the discharge of Pb dust, elevated BILLS, and exposures that are associated with a variety of adverse health outcomes. Women and children are among recreational shooters at special risk and they do not receive the same health protections as occupational users of firing ranges. Nearly all BLL measurements compiled in the reviewed studies exceed the current reference level of 5 pg/dL recommended by the U.S. Centers for Disease Control and Prevention/National Institute of Occupational Safety and Health (CDC/NIOSH). Thus firing ranges, regardless of type and user classification, currently constitute a significant and unmanaged public health problem. Prevention includes clothing changed after shooting, behavioural modifications such as banning of smoking and eating at firing ranges, improved ventilation systems and oversight of indoor ranges, and development of airflow systems at outdoor ranges. Eliminating lead dust risk at firing ranges requires primary prevention and using lead-free primers and lead-free bullets. Keywords: Blood, Lead, Poisoning, Shooting, Range, Firearms, Health, Effects, Expert shooter, Guns Background Most attention in the area of human health and guns has been rightly placed on shooting injuries and deaths [1]. However, decades of evidence indicate that substan- tial health risks are incurred by the shooters themselves in the form of lead exposure and subsequent poisoning. Indeed, as pointed out as early as 1994 by Ozonoff, based on high blood lead levels (BLLS) of shooters, "... `Correspondence: mark.laidlaw@rmit.edu.au 'Centre for Environmental Sustainability and Remediation (EnSuRe), School of Science, RMIT University, PO Box 71, Bundoora, VIC 3083, Australia Full list of author information is available at the end of the article firing ranges comprise one of the largest unregulated sources of occupational or para -occupational lead expos- ure for adults. The perils of firearms exist at both ends of the barrel." [2]. The past two decades have brought substantial improvements in firing range environmental oversight as well as analytical capabilities to detect lead in humans, but literature evidence indicates that we fall far short of human health safety criteria in firing ranges of all types, and among occupational and recreational shooters. This review fills a gap in the literature by com- piling data from a broad range of recent studies of firing range users, employees, and their families, including in- door and outdoor ranges, in an attempt to document and clarify risks by firing range use, setting, and shooting m The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 BioMet! Central International License (http)/creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http.//creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Laidlaw et al. Environmental Health (2017) 16:34 behaviour. The emphasis of this review is on BLLs of shooters as a marker for adverse health effects among members of the shooting population. Shooting statistics In the United States alone an estimated 16,000-18,000 indoor firing ranges exist which employ tens of thou- sands of employees [3]. An estimated 1 million law en- forcement officers train at indoor firing ranges [3]. In 2011 there were approximately 270 million civilian - owned firearms owners in the US and in 2007 there were approximately 650 million civilian -owned weapons globally [4] and 200 million firearms owned by nation states worldwide [5]. In the United States approximately 20 million citizens practice target shooting as a leisure activity [6]. The National Sport Shooting Foundation (NSSF) [7] stated that in 2011 in the United States there were 13,049,050 handgun shooters, 13,170,417 rifle shooters, 9,713.,033 shotgun shooters, and 3,730,567 muzzleloader shooters who participated in 156,790,412 handgun shooting days, 146,652,398 rifle shooting days, 113,866,661 shotgun shooting days and 29,042,237 muz- zleloader shooting days. The global statistics regarding the number of firing ranges and shooting prevalence are not available, but it is likely there are a very large num- ber of shooters at firing ranges. The United States Geo- logical Survey (USGS) [8] calculated that in 2012 about 60,100 metric tonnes of lead were used in ammunition and bullets in the United States. Given that the domin- ant metal in bullets is lead, there are a large number of people globally who are exposed to lead from shooting at firing ranges. Source of exposure from shooting lead bullets There are several sources of potential lead exposure from shooting guns and firing ranges. Most bullet projectiles are made from lead, but a large amount of lead is also present in the primer, composed of approximately 35% lead styphnate and lead peroxide (and also contains bar- ium and antimony compounds), that ignites in a firearm barrel to provide the propulsion for the projectile [9-13]. A portion of the lead bullet disintegrates into fine frag- ments while passing through the gun due to misalign- ments of the gun barrel [9]. The lead particles, along with dust and fumes originating from the lead primer and the bullet fragments are ejected at high pressures (18,000- 20,000 psi; 124-128 mpa) from the gun barrel, a large pro- portion of which occurs at right angles to the direction of fire in close proximity to the shooter [9]. The shooter can inhale fine Pb particulates (mainly from the primer) which constitutes the proximal exposure pathway. Fine and coarse particulates from both the primer and bullet frag- ments also attach to the shooters hands, clothing, and other surfaces, and can be inadvertently ingested, Page 2 of 15 providing another lead exposure pathway [14, 15]. When changing targets at outdoor firing ranges shooters can be exposed to lead that has accumulated in soil dust. Add- itionally, the shooters can then bring these particulates back to their home and expose their families as with other lead occupational hazards. Firing range personnel are employed by the shooting galleries, and thus also receive proximal lead exposure. They are also charged with cleaning the ranges and re- moving lead particulates on floors, targets, and the ven- tilation systems (for indoor ranges). Furthermore, they work at firing ranges for extended hours during the working week, compounding potential lead exposure. Finally, although not the focus of this review, there are environmental impacts arising from firing ranges. Emis- sions in firing ranges result in the accumulation of ele- vated lead concentrations in surface soils [16-18]. This is concerning because lead particles do not naturally bio- degrade in soil as do some contaminants such as hydro- carbons. The half-life of lead in surface soil has been estimated as approximately 700 years [19]. Therefore, if not remediated following closure, lead contaminated surface soils at firing ranges could result in lead expo- sures for hundreds of years. Dust from lead contami- nated soil can be resuspended into the atmosphere and transported from a firing range whether outdoor or in- door [20, 21]. Lead in soils and dusts at firing ranges are highly bioavailable [22]. Lead in soil could weather/ oxidize and migrate down -gradient to underlying groundwater beyond the firing range boundaries [23]. The low solubility of lead in natural water (i.e., not min- ing related), however, limits off-site aquatic transport. The factors most likely to affect the amount of lead car- ried by the groundwater in solution are p] 1, depth to groundwater, soil chemistry, soil type and annual pre- cipitation [24]. Soil -derived sediment discharged during rain events from lead contaminated firing range soils has the potential to migrate to surrounding properties and into waterways through runoff or storm drains. Wildlife [25-27], biota [28] and humans can be exposed to lead contaminated soils, sediments and airborne particulates near firing ranges. Bellinger et al. (2013) [29] provided a consensus statement about the health risks arising from lead-based ammunition in the environment. Health outcomes associated with blood lead levels (BLLs) In 2012, The United States National Toxicology Program (NTP) published evidence regarding health effects asso- ciated with BLL exposure in adults and children [30]. For adult men and women there is "sufficient evidence" that BLLs <10 µg/dL are associated with essential tremor, hypertension, cardiovascular -related mortality and electrocardiography abnormalities, and decreased kidney glomerular filtration rate. For women there is Laidlaw et at. Environmental Health (2017) 16:34 "sufficient evidence" that BLLs <5 µg/dL are associated with reduced foetal growth. For adult men and women there is "limited evidence" that BLLs <10 µg/dL were as- sociated with psychiatric effects, decreased hearing and cognitive function, incidence of amyotrophic lateral sclerosis, and increased spontaneous abortion in women. For adults there is "limited evidence" that BLLs <5 µg/ dL were associated with incidence of essential tremor. For children with BLLs <5 µg/dL there is "sufficient evi- dence" of decreased academic achievement, intelligence quotient (IQ), specific cognitive measures, increased at- tention related behaviours, delayed puberty and reduced postnatal growth. For children with blood lead levels < 10 µg/dL there is "sufficient evidence" of decreased hear- ing. For children with BLLs < 5 µg/dL there is "limited evidence" of an association of decreased kidney glomeru- lar filtration rate, and delayed puberty. For prenatal expos- ure with BLLs < 5 µg/dL there is "limited evidence" of decreases in measures of cognitive function. For prenatal lead exposure < 10 µg/dL there is "limited evidence" of de- creased IQ, increased incidence of attention -related and problem behaviors and decreased hearing. For adult men and women there is "limited evidence" that BLLs between 15 and 20 µg/dL are associated with adverse sperm pa- rameters and increased time to pregnancy in women. There is "limited evidence" that BLLs 210 µg/dL are asso- ciated with decreased fertility. There is "limited evidence" that spontaneous abortion occurs in female partners of men with BLLs >_ 31 µg/dL. However, modern exposures are orders of magnitude larger than early hominids [31] with pre -industrial blood lead levels in humans estimated at 0.016 µg/dL [32]. Bellinger (2011) [33] noted that ad- verse health effects are continually being associated with decreasing exposures. Methodology The search engines Google Scholar, Pubmed and Science Direct were accessed for studies that provided informa- tion about BLLs associated with firearms using the search terms "blood lead", "lead poisoning", "lead expos- ure", "marksmen", "firearms", "shooting", "guns", "rifle" and "firing ranges". The literature regarding the health effects specifically associated with shooting lead bullets at firing ranges was also reviewed. Studies that reported BLLs associated with shooters at firing ranges were com- piled into Table 1. Results - blood lead levels at firing ranges The search identified 36 articles originating from 15 countries around the world published between 1975 and 2016 that included BLLs of shooters. Over half of the re- ports were from the U.S. The articles describe BLLs of law enforcement personnel, high school shooting Page 3 of 15 coaches, and family members ranging from as young as 1 -year-old to adult men and women. Summary of blood lead levels reported Data from collected studies reveals the widespread oc- currence of BLL by occupational and recreational shooters. The vast majority of these articles reported at least one BLL that exceeded 10 µg/dL. About half of the studies further reported BLLs exceeding 20 µg/dL (18 ar- ticles), exceeding 30 µg/dL (17), and even exceeding > 40 µg/dL (15). Indeed, all 36 of the articles indicated BLLs of shooters exceeded 2 µg/dL. Considering that the geometric mean BLL of the U.S. adult population in 2009-2010 was 1.2 µg/dL [34], the BLLs among shooters provide stark evidence of significant exposure, particu- larly to recreational shooters who do not typically self - screen for BLL. Several key characteristics about BLLs and exposure variables arising from shooting are gleaned from the literature. Baseline and post -shooting blood lead level relationships Several studies focused on before -after comparisons of shooters, particularly shooters in military and police oc- cupations, and found marked increases in BLL resulting from firing range activities. Tripathi et al. (1989) [9] measured BLLs in police cadets before, and 1, 2 and 5 days after starting shooting practice, and 69 days after the start of shooting. At 69 days after the start of shoot- ing, the BLLs of the cadets remained above baseline levels prior to shooting. Rocha et al. (2014) [35] con- ducted a study of BLLs of police cadets before a shoot- ing course and 3 days after the cessation of the shooting course. The mean BLL of cadets increased from 3.3 µg/ dL (95% Cl = 3.0-3.6 µg/dL) before the course to 18.4 µg/dL (95% Cl 16-21 µg/dL) 3 days after comple- tion of the course. In all cases the BLL increased signifi- cantly after the course (p <0.001). Within 3 days, the BLLs of the course instructors increased from 3.6 µg/dL to 22.1 µg/dL in one case and from 7.7 µg/dL to 18.3 µg/dL in another. Fischbein et al. (1979) [36] con- ducted a study of 23 firearms instructors and reported that the BLLs increased measurably after firearms train- ing. Vivante et al. (2008) [37] reported a statistically sig- nificant (p <0.001) increase in BLLs of 29 Israeli soldiers from a baseline of 10.3±2.0 µg/dL to 18.9±3.6 µg/dL six weeks after training. Decline in blood lead levels after shooting events Several studies provide insight into the decline in BLLs following shooting events. Goldberg et al. (1991) [38] observed that average BLLs in 7 firing range instructors decreased from 45 µg/dL to 31 µg/dL 6 months after a training event. George et al. (1993) [39] observed that average BLLs in 52 small bore rifle recreational shooters Laidlaw et al. Environmental Health (2017) 16:34 Table 1 Blood Lead Levels Observed Following Shooting Firearms at Shooting ranges Page 4 of 15 Activity Firing Type Range Category Blood Lead (µg/d L) Mean SD (Median") Range Location n Reference Occupational Indoor Arsenal Firing Range Workers 37.2 11.7 22-59.6 Taiwan 10 Chau et al. (1995) [80] Arsenal Other Workers 13.3 5.6 98 Firing Range and Gun Store Employees 19.9- California, USA 6 CDC (2014) [811 40.7 Firearms instructor & range cleaning and 88 New York, USA 1 Fisher-Fischbein et al. maintenance (1987) [821 Firearm Instructors Before Indoor Training: <20 New York, USA 1 Fischbein et al. (1979) 4.3% [361 Firearm Instructors Before Indoor Training: 20-39 19 82.6% Firearm Instructors Before Indoor Training: 40-59 2 8-71% Firearm Instructors Before Indoor Training: >60 1 4.3% Firearm Instructors After Indoor Training: 4.3% <20 1. Firearm Instructors After Indoor Training: 20-39 12 52.2% Firearm Instructors After Indoor Training: 40-59 8 34.8% Firearm Instructors After Indoor Training: 8.7% >60 2 Firearms Instructors and Officers: 42% <40 New York, USA 19 Fischbein (1992) [83] Firearms Instructors and Officers: 34% 40-60 15 Firearms Instructors and Officers: 24% >60 11 Firearm Instructors 125 15 USA 3 Landrigan et al. (1975) [84] Male Police Officcr5 5 1-18.2 Sweden 75 L6fstedt et al (1999) [85] Female Police Officers 3.7 3 Full Time Employee 77 Colorado, USA 1 Novotny et al. (1987) [861 Full Time Employee 59 1 Full Time Employee 49 1 Part Time Employee 41 1 Shooting range supervisor 5.8 1.6 2.1-17.3 Republic of 35 Park et al. (2016) [87] Korea Professional shooter 11.6 1.9 3.0-34.3 24 Shooting range manager 9.5 2.2 2.0-64.0 61 All job types 8.6 2.1 2.0-64.0 120 Firing Range Instructors 5.5 0.6 4.2-6.7 Sao Paulo, 20 Rocha et al. (2014) [35] Brazil Cadets - Before Training 3.3 0.15 3.0-3.6 21 Cadets - After Training 18.2 1.5 16-21 21 Instructor 1 Before Training 3.6 1 Laidlaw et al. Environmental Health (2017) 16:34 Page 5 of 15 Table 1 Blood Lead Levels Observed Following Shooting Firearms at Shooting ranges (Continued) Instructor 1 After Training 22.1 1 Instructor 2 Before Training 7.7 1 Instructor 2 After Training 18.3 1 Instructors 19 7 Amman, 31 Abudhaise et al, (1996) Jordan [881 Trainees 22.9 4.6 54 Controls 2.1 1.4 unknown Police Small Arms Instructors 43.5 6.2 33.1- England 7 Smith (1976) [891 49.7 US Coastguard Firearm Instructors - Pre BLL 2,4 1.6 0;9-5-6 Washington, 9 Torres (2014) [901 USA US Coastguard Firearm Instructors - Post BLL 2.3 1.2 0.9-0 9 US Coastguard Firearm Instructors - Pre -Post 2.4 1A 0.9-5.1 9 BLL Police Trainees: Before Training - (1/29/87) 6.0 (6.4*) Colorado, USA 17 Valway et at, (1989) [451 Police Trainees: Training - (3/3/87) 511 (51,6*) 17 Police Trainees: Training - (3/31/87) 443 (43.1 *) 17 Police Trainees: Training - (5/3/87) 39.5 (40:0*) 17 Israeli Defence Soldiers Baseline 10.3 2.3 Israel 29 Vivante et al. (2008) [371 Israeli Defence Soldiers Postexposure 18:8 3.6 29 Indoor Range Instructors 8.5 7.6 Italy unknown Di Lorenzo et al, (2006) [911 Indoor/outdoor FBI Instructors 1989 14.6 9-21 Virginia, USA 7 CDC (1996) [651 FBI Instructors 1990 13.7 6-27 7 FBI Instructors 1991 7.6 <4-12 14 FBI Range Techs 1989 16.2 10-24 5 FBI Range Techs 1990 10.4 6-14 5 FBI Range Techs 1991 13.6 8-28 5 US Special Operations Forces - Year 2000 13.90 USA 255 Mancuso et al. (2008) [921 US Special Operations Forces - Year 2005 6.80 Adult Target Shooters - Occupational - 21.6% <25 New York, USA 26 Gelberg and DePersis (2009) [931 Adult Target Shooters - Occupational - 50.8% 25-39 61 Adult Target Shooters - Occupational - 25% 40-59 30 Adult Target Shooters - Occupational - 2.5% 60+ 3 Outdoor Range Instructors 6.7 53 Italy unknown Di Lorenzo et al. (2006) [911 Firing Range Instructors Before Training 41 10 28-66 California, USA 7 Goldberg et aL (1991) [381 Firing Range Instructors After Training 45 14 28-70 7 Firing Range Instructors 6 Months After 31 5 28-38 7 Training Soldiers Before Basic Training <0.29 Israel 22 Greenberg et al. (2016) [941 Soldiers After Basic Training 1.17 1.73 22 Laidlaw et at Environmental Health (2017) 16:34 Page 6 of 15 Table 1 Blood Lead Levels Observed Following Shooting Firearms at Shooting ranges (Continued) Soldiers After Advanced Training 3.92 1.99 7-14 7 22 Body guards 8.10 2.70 3.0-14.4 Mexico 26 Madrid et al. (2016) [41] Instructors 7.60 1.40 6.6-86 2 Shooting Range Caretakers 40.65 15.63 29.6- 2 Outdoor Firing Range Police Cadets: Day 69 9 Non -Occupational 51.7 Indoor Administrative 4.20 1.20 2.7-6.5 9 Security 4.90 1.20 3.0-73 9 Services 6.50 3.60 3.1-14.2 10 Elite Group 6.40 2.60 4.2-11.4 6 All Categories 7.60 6.80 2.7-51.7 64 Howitzer Operators - Baseline 5.5 Shooter: Q2 200-399 rounds/month 4.33- Oklahoma, 20 Smart et al. (1994) [401 11.8* Shooter: Q4 > 680 rounds/month 13.8* 6.73 USA 3.3* Howitzer Operators - After 3rd Exercise 20.1 17.94- 20 22.44 Howitzer Operators - 8 Weeks After Exposure 11.9 9.92- 12 14.02 ShLxuting Instructor 41 Non -Jacketed bullets 24.02 Shooting Instructor #1 Copper Jacketed 21.95 Bullets 7-14 7 Shooting Instructor #2 Non -Jacketed bullets 14.08 Shooting Instructor #2 Copper Jacketed 13.04 Bullets 29 Outdoor Firing Range Police Cadets: Baseline - 6 Day 0 20 Outdoor Firing Range Police Cadets: Day 1 6 Outdoor Firing Range Police Cadets: Day 2 11 Outdoor Firing Range Police Cadets: Day 5 15 Outdoor Firing Range Police Cadets: Day 69 9 Non -Occupational Indoor High School Shooting Coach 44 Firing Range A (School Range) - Students 24.3 Aged 15-17 years Firing Range B (Commercial) - Students Aged 2.1 13-16 years Firing Range C (Volunteer Run) - Students 18.5 Aged 15-19 years Firing Range D (School Range) - Students 8.9 Aged 14-17 years Firing Range E (Volunteer Run) - Students 7.6 Aged 7-17 years Shooter 92* Shooter: Q1 200 rounds/month 8.7* Shooter: Q2 200-399 rounds/month 9* Shooter: Q3 400-680 rounds/month 11.8* Shooter: Q4 > 680 rounds/month 13.8* Airguns 3.3* Virginia, USA 1 1 N 5-8 Virginia, USA 7 1.0 5-8 7 2.1 7-14 7 5.4 9-26 7 2.8 6-14 7 Alaska, USA 1 21.0- 7 31.0 8 5-37 24 3.0-14.0 7 2-13 20 Tripathi et al. (1991) [461 Tripathi et al. (1989) [91 CDC (2005) [56] 2.7-52.1 Germany 129 Demmeler et al. (2009) [441 2.8-31.4 27 2.7-31.5 28 2.9-37.5 29 3.7-52.1 23 1.8-12.7 20 Laidlaw et al. Environmental Health (2017) 16:34 Table 1 Blood Lead Levels Observed Following Shooting Firearms at Shooting ranges (Continued) Airguns and .22 caliber 8:7* .22 Ir bore & large caliber 10.7* Large caliber handgun 10* IPSC (International Practical Shooting 19.2* Federation) Adult Target Shooters - Both Occupational & Non - Occupational - 1.5% Adult Target Shooters - Both Occupational & Non - Occupational - 71.3% Adult Target Shooters - Both Occupational & Non - Occupational - 20.9% Adult Target Shooters - Both Occupational & Non - Occupational - 6.2% Small Bore Rifle Shooter - End of Indoor 54.65 Season Small Bore Rifle Shooter- Preseason 33.13 Following Year Shooting Range #2 10.5 Shooting Range #3' 16.1 Shooting Range #4 19.2 Child (Age 1 year) - "index case" 46 Mother - (Age 25 years) 11 Father - (Age 25 years) 15 Sibling - (Age 4) 14 Sibling - (Age 2) 19 Cousin - (Age 6) 28 Cousin - (Age 8) 31 Aunt - (Age 37) 30 Child (Age 1 year.) "index case": 3 Months 19 After Intervention Mother - (Age 25 years): 3 Months After 8 Intervention Father - (Age 25 years): 3 Months After Not Intervention Measured Sibling - (Age 4): 3 Months After Intervention 11 Sibling - (Age 2): 3 Months After Intervention 12 Cousin- (Age 6): 3 Months After Intervention 13 Cousin - (Age 8): 3 Months After Intervention 13 Aunt - (Age 37): 3 Months After Intervention 13 Indoor Shooting Range Employee Spouse 6 Indoor Shooting Range Employee Spouse 11 Indoor Shooting Range Employee Spouse 6 Recreational Shooters 29* Competitive Marksmen - Adolescents Aged 21.3 14-16 years Shooters before indoor shooting season 10.6* 1.4-17,2 15 2.7-37.5 51 2:8-326 32 3,2-521 11 <25 New York, USA 2 25-39 92 40-59 27 60+ 8 New Zealand 52 37 Page 7 of 15 Gelberg and DePersis (2009) [931 George et al. (1993) [391 7 South Africa 30 Mathee et al. (2017) [151 9.8 17 16.3 14 USA 1 Moore 0 995) [951 1 1 1 1 1 1 1 1 1 i 1 1 1 1 1 Colorado, USA 1 1 1 24-45 Germany 7 18-28 Massachusetts, 4 USA 3.2-17,6 Sweden 22 Novotny et al. (1987) [861 Ochsmann et al_ (2009) [61 Shannon (1999) [571 Svensson et al. (1992) [961 Laidlaw et al. Environmental Health (2017) 16:34 Table 1 Blood Lead Levels Observed Following Shooting Firearms at Shooting ranges (Continued) Page 8 of 15 Shooters after indoor shooting season 13.8* 6.9-28,8 22 Airgun Shooters before indoor shooting 9.1* 4.7-17.9 21 season Airgun Shooters after indoor shooting season 8.4* 2.0-222 21 Archers before shooting season 6.1* 2.7-9.2 13 Archers after shooting season 5.6* 3.1-8:7 13 Shooter: shot 600 rounds 3 times per week 43.5 United 1 White (1996) [97] for past 4 months Kingdom Indoor/Outdoor Shooter 45 6.3 35-47 Connecticut, 6 Cook et al. (2015) [98] USA Irregular Frequency Indoor and Outdoor 6.7 Australia 9 Gulson et al. (2002) [991 Shooter Archers who also shot guns 7.8 10,26 South Africa 15 Mathee et al. (2017) [15] Gun shooters only (excluding archers and 12.13 10.18 62 employees) Gun shooters who also work at the shooting 16.3 7,83 8 range All gun shooters (including archers and 11.9 10.15 85 employees) Less than monthly 8.4 5.5 23 > monthly, but less than weekly 11.8 8.7 35 > weekly, but < 3 times per week 14.3 15,2 21 >3 times per week 12,5 9.7 7 Pistol Sport Shooters 10.76 8.28 Helsinki, 20 Asa-Makitaipale et al. Finland (2009) [421 Outdoor Archery Range 4.5 Shooting Range #1 7 Practised archery only 3.3 declined from 54.7 µg/dL at the end of the indoor sea- son to 33.1 µg/dL in 37 of the shooters by the preseason of the following year. Smart et al. (1994) [40] observed that average BLLs of 20 howitzer operators declined from 20.1 µg/dL to 11.9 µg/dL in 12 operators 8 weeks after ending the firing exercise. Tripathi et al. (1989) [9] observed that BLLs of 7 outdoor firing range police ca- dets had a baseline average of 6 µg/dL prior to commen- cing shooting training and an average BLL of 15 µg/dL at the end of training 5 days later. At follow up 69 days after training, the average BLL was 9 µg/dL. Thus, the results indicate that BLLs following shooting events can remain elevated for a considerable time after cessation of shooting, especially for participants with higher BLLs. Association between blood lead levels and bullets fired, caliber of weapon, copper jacketed or unjacketed bullets and air lead levels Several characteristics such as shooting frequency, cali- ber of the gun, type of bullet, and air lead at firing 27 South Africa 14 Mathee et al. (2017) [151 4.3 12 2.25 31 ranges have been studied. Each of these variables relate to BLLs and can also be associated with environmental issues at firing ranges. BLLs and frequency of shooting activity Most studies reviewed indicate a strong positive correlation between the use frequency of shooters at firing ranges and their BLLs. Madrid et al. (2016) [41] reported that BLLs were higher (p <0.001) in individuals who participated in greater than 12 shooting practice sessions per year (8.3 ± 2.4 µg/dQ compared with controls who shot less than 12 times per year (5.2 ± 2.5 pg/dL). Tripathi et al. (1989) [9] ob- served a positive association between the total number of rounds fired and BLLs (r = 0.84, p <0.02) and personal - breathing -zone air lead levels (r = 0.92; p <0.001). Air lead levels were also correlated with BLLs (r = 0.85; p <0.02). Asa-Makitaipale et al. (2009) [42] reported a correlation be- tween BLLs and bullets fired during the last month (r = 0.71; p 0.001) and the past year (r = 0.55; p 0.012). Betancourt (2012) [43] observed a linear relationship between air lead Laidlaw et al. Environmental Health (2017) 16:34 exposure and total number of rounds fired by caliber of weapon used. Blood lead and gun caliber Relationships between BLL and caliber of firearms have also been described. Demmeler et al. (2009) [44] ob- served that the larger the caliber of the weapon, the higher the shooters BLL. The following median BLLs were reported: airguns — 3.3 µg/dL (range 1.8-12.7 µg/ dQ; 0.22 caliber weapons — 8.7 µg/dL (range 1.4- 17.2 µg/dL); 0.22 caliber and large caliber handguns (9 mm or larger) — 10.7 µg/dL (range 2.7-37.5 µg/dL); and large caliber handguns — 10.0 µg/dL (range 2.8- 32.6 µg/dQ. Demmeler et al. [44] also reported that shooters belonging to the International Practical Shoot- ing Confederation (IPSC) had the highest median BLL of 19.2 µg/dL. Additionally, studies indicated a positive cor- relation between cumulative air lead exposure in firing ranges and BLL of shooters [40, 451. BLLs and copper jacketed vs. unjacketed bullets Tripathi et al. (1991) [46] compared the BLLs in firearm instructors using copper jacketed and non-jacketed bul- lets. One shooting instructor exhibited BLLs of 24.0 µg/ dL and 22.0 µg/dL using non-jacketed bullets and copper -jacketed bullets, respectively. A second in- structor exhibited BLLs of 14.1 µg/dL and 13.0 µg/dL using non-jacketed bullets and copper -jacketed bullets, respectively. BLLs and air lead Elevated BLLs especially arising from indoor firing ranges are the result of the greater absorption of lead from inhalation compared with ingestion and dermal ab- sorption. For example, the amount of absorption of ingested lead by adults under non-fasting conditions ranges from 3 to 10% and in young children from 40 to 50% whereas inhaled lead lodging deep in the respiratory tract seems to be absorbed equally and totally, regardless of chemical form [47]. As shooting involves generation of extremely fine particles and gases, the high rate of ab- sorption logically results in elevated BLLs. Outdoor ranges, presumably well -ventilated by natural flow and large air volumes, do not necessarily prevent lead expos- ure from shooting activities. The following sections dis- cuss the implications of the results. Discussion The results in Table 1 must be evaluated in the context of BLL recommendations, special need populations, air lead measured at firing ranges, and prevention. The use of ventilation to manage exposure at firing ranges and prevent lead exposure of shooters is appraised. Page 9 of 15 Blood lead level recommendations from public and occupational health communities Several United States (US) governmental agencies have developed recommendations regarding BLLs. The Cen- ters for Disease Control and Prevention (CDC) makes health recommendations to protect public health whereas the National Institute for Occupational Safety and Health (NIOSH) and the Occupational Safety and Health Administration (OSHA) focus on worker health. The trend for BLL recommendations has been declining over several decades since regulations were first established. CDC and NIOSH The CDC [34] makes the following statement regarding recommended BLLs in adults: "In 2015, NIOSH designated S pg/dL five micrograms per deciliter) of whole blood, in a venous blood sample, as the reference blood lead level for adults. An elevated BLL is defined as a BLL >_5 ug/dL. This case definition is used by the ABLES program, the Council of State and Territorial Epidemiologists (CSTE), and CDCs National Notifiable Diseases Surveillance System (NNDSS). Previously (i.e. from 2009 until November 2015), the case definition for an elevated BLL was a BLL >_10 feg/dL. The U.S. Department of Health and Human Services recommends that BLLs among all adults be reduced to <10 µg/dL. The U.S. Occupational Safety and Health Administration (OSHA) Lead Standards require workers to be removed from lead exposure when BLLs are equal or greater than 50 µg/dL (construction industry) or 60 pg/dL (general industry) and allow workers to return to work when the BLL is below 40 pg/dL.... OSHA Lead Standards give the examining physician broad flexibility to tailor special protective procedures to the needs of individual employees. Therefore, the most current guidelines for management of lead - exposed adults should be implemented by the medical community at the current CDC/NIOSH reference BLL of 5 yg/dL. Recommendations for medical manage- ment are available from the Association of Occupa- tional and Environmental Clinics, California Department of Public Health, and the Council of State and Territorial Epidemiologist (CSTE) Occupational Health Surveillance Subcommittee." Council of state and territorial epidemiologists (CSTE) The CSTE is an organization of member states and terri- tories representing public health epidemiologists in the United States. The CSTE [48] makes the following rec- ommendations actions for various blood lead levels in adults (Table 2): Laidlaw et al. Environmental Health (2017) 16:34 Table 2 Council of State and Territorial Epidemiologists Management Recommendations for Adult Blood Lead Levels Blood Lead Level Management Recommendations (pg/dL) <5 No action needed Monitor BLL if ongoing exposure 5-9 Discuss health risks Minimize exposure Consider removal for pregnancy and certain medical conditions Monitor BLL 10-19 Decrease exposure Remove from exposure for pregnancy Consider removal for certain medical conditions or BLL > 10 for an extended period of time Monitor BLL 20-29 Remove from exposure for pregnancy Remove from exposure if repeat BLL in 4 weeks remains > 20 Annual lead medical exam recommended 30-49 Remove from exposure Prompt medical evaluation 50-79 Remove from exposure Prompt medical evaluation Consider chelation with significant symptoms >!80 Remove from exposure Urgent medical evaluation Chelation may be indicated Ideally, recommendation triggering immediate cessa- tion of exposure at shooting ranges should not be based on a single blood lead level measurement. The duration of an elevated BLL over multiple BLL measurements should determine the nature of the intervention. Current public health recommendations call first for education and attention to risk factors that can mitigate future exposures. Occupational health and safety administration (OSHA) and the new science -based recommendations For occupational shooters and firing range workers, the U.S. OSHA Lead Standards require general industry workers to be removed from lead exposure when BLLs are equal or greater than 60 µg/dL, and allows them to return to work when their BLL is below 40 µg/dL [34]. Based on the recommended BLLs by the CDC/NIOSH [34], the CSTE [48] and the comprehensive compilation of health effects of low level lead exposure by the NTP [30], the OSHA regulation that allows workers to return to work with BLLs greater than 40 pg/dL seems Page 10 of 15 nonsensical as a health risk avoidance guideline, and should be lowered in line with the Council of State and Territorial Epidemiologists (CSTE) recommendations, as shown in Council of state and territorial epidemiologists (CSTE). Special needs of women and children Lead exposure of women and children have special char- acteristics that must be taken into account. The needs relate to the effect of lead on future generations. For women the needs are related to the effect of lead on the developing fetus and post -natal exposure associated with breast-feeding. For children the special needs for low ex- posure are related to the extraordinary sensitivity of the developing organs of children. These concerns indicate the need for a margin of safety. The special lead risks of women The risk to women exposed to lead at firing ranges is of particular concern because, once absorbed, a proportion of the lead is deposited in the skeleton and more than 90% of lead in adults is stored in their bones. Bone stor- age takes place because due to their similar ionic radius and charge lead is substituted for calcium. Furthermore, when a woman becomes pregnant the fetus requires cal- cium and, depending on the dietary intakes, a proportion of calcium is derived from remodelling of the bones. Skeletal lead stores are released from the remodelling exposing the fetus during critical development windows [49-51]. Even modestly elevated BLLs have been associ- ated with serious neurological disorders such as autism [52]. Lead released from a woman's bones during preg- nancy is associated with foetal developmental problems [53]. Another consideration for female shooters is that when their BLL becomes elevated, they can pass the lead on to their children through breast milk [54, 55]. Given the known lead contamination at firing ranges, intending -to- conceive, pregnant women, and nursing mothers should curtail exposure from shooting activities (employed in the security, military and police, and recre- ational shooters) and observe precautionary prevention. Health risks related to children shooters The CDC (2005) [56] reported that children (aged 7-18) shooting bullets at multiple firing ranges in Alaska ex- hibited highly elevated BLLs (see Table 1). Shannon (1999) [57] reported that children (aged 14-16) who were competitive marksmen exhibited an average BLL of 21.3 µg/dl, (range 18-28 µg/dL). Blood lead levels ob- served in children from shooting activities are within the range known to cause long-term detrimental health ef- fects [30]. Exposure of young females to lead is of par- ticular concern because it is stored in their bones and Laidlaw et al. Environmental Health (2017) 16:34 can then be transferred to their developing fetus many years later when they become pregnant [49-51]. Health-related lead issues and law enforcement personnel Law enforcement includes a number of services to pro- tect and ensure the safety of citizens and the commu- nity. The public requires law enforcement personnel to be "calm, cool and collected" when in service conducting their duties. However, the adverse health effects, espe- cially on the nervous system that are associated with ele- vated BLLs arising from firearm use are inconsistent with these ideals. Air lead levels at firing ranges The OSHA 8-h air lead time weighted average (TWA) action level is 30 µg/m3 and the OSHA permissible ex- posure limit (PEL) is 50 µg/m3 [58]. The California De- partment of Public Health Occupational Lead Poisoning Prevention Program (CDPH-OLPPP) recommended 8 h TWA PEL is 0.5 to 2.1 µg/m3 [59]. Based on this guide- line, the CDPH-OLPPP states "At a PEL of 0.S pg/m3, 95% of workers would have a BLL less than 5µg/dL over a 40 year working lifetime. At a PEL of 2.1 yg/m3, 95% of workers would have a BLL less than 10 14g/dL and 57% would have a BLL less than 5 ug/dL over their working lifetime." Wang et al. (2016) [60] conducted a review of studies of airborne lead concentrations and possible ex- posure at firing ranges (Additional file 1). Wang et al. [60] found that the OSHA 8 h TWA PEL is exceeded in many studies, and even more noteworthy, the California PEL is exceeded in all of the studies. It must be noted that the recommended PEL and action levels are not the only paths to controlling lead exposures. Biomonitoring and primary prevention Kosnett et al. (2007) [61] recommend that: "individuals be removed from occupational lead exposure if a single blood lead concentration exceeds 30 microg/dL or if two successive blood lead concentrations measured over a 4 - week interval are > or = 20 microg/dL. Removal of indi- viduals from lead exposure should be considered to avoid long-term risk to health if exposure control measures over an extended period do not decrease blood lead concen- trations to < 10 microg/dL or if selected medical condi- tions exist that would increase the risk of continued exposure." A more conservative approach are the recom- mendations by CSTE in Council of state and territorial epidemiologists (CSTE). A critical issue is that biomoni- toring is not primary prevention. Biomonitoring only as- sesses the degree of exposure and potential health damage after exposure has taken place. Primary preven- tion requires curtailing lead exposure and maintenance of air quality. Several steps have been proposed above to minimize lead exposure. Recommendations to prevent Page 11 of 15 occupational lead poisoning by shooters are provided by U.S. Government [62]. The recommendations appear as topics in school rifle team programs [63]. One of the challenges in a biomonitoring program is the frequency which shooters should have their BLLs monitored. The Australian organisation Safe Work Australia has recently carefully made recommendations for multiple scenarios of blood lead testing frequency for workers exposed to lead in the work place [64]. Similar BLL testing frequency recommendations could be adopted for shooters exposed to lead in occupational settings such as law enforcement, military, security and shooting range workers. Recreational shooters that shoot frequently could voluntarily use these blood lead testing frequency recommendations as a guide if they wanted to protect their health. Potential health risks from 'take home lead' In contrast to occupational environments where work clothes should not be taken home, lead dust can adhere to shooters clothes and potentially contaminate vehicles and homes. The CDC (1996) [65] measured carpet dust lead concentrations in FBI student dormitory rooms and in 14 non—student dormitory rooms at a firing range and training facility. They observed that student dormi- tory rooms had significantly higher lead levels than non—student dormitory rooms, suggesting that the FBI students were contaminating their living quarters with lead. `Take home lead' has been described mostly for oc- cupational settings [66-68] but given the fine particle nature and lead concentrations of dust associated with shooting, the `take home lead' pathway of exposure from shooting must be recognized and curtailed. Prevention of lead aerosols with ventilation improvements The air lead table from Wang et al. 2016 [60] (Add- itional file 1) and the National Research Council [69] are the only compilations of air Pb levels at shooting ranges that were identified. Wang et al. do not discuss the ven- tilation practices in the various studies that may account for lower air lead levels. A 1975 NIOSH study found that at all 9 ranges studied, the air lead guideline was exceeded at the time (200 µg/m3) [70]. A 2009 NIOSH review describes a case study on air lead exposure of law enforcement trainees and reports that the mean airborne lead concentration of >2000 µg/m3 was reduced by 94- 97% to 60-120 µg/m3 but this was still above the OSHA PEL of 50 µg/m3. Commercial ventilation companies claim they can meet guidelines (i.e. Camfil air filters) but no published studies supporting this achievement at fir- ing ranges were located. There is a "lack of evidence" gap in the literature dem- onstrating that ventilation systems can maintain air lead levels at indoor ranges below the current OSHA (50 µg/ Laidlaw et al. Environmental Health (2017) 16:34 m3) or California (0.5-2.2 µg/m3) guideline. The litera- ture gap raises questions about whether or not the guidelines can actually be achieved, especially the Cali- fornia guideline. Further, as discussed in Special needs of women and children, meeting the guideline does not ne- cessarily provide a margin of safety from lead exposure. Primary prevention requires eliminating lead in primers and bullets Lead from projectile primers is a significant proximal source of lead exposure and uptake. The development of primers is described by Brede et al. [71]. During the 19th century primers were composed of mercury fulminate; however, the mercury fulminate was found to be too toxic to shooters. In the early 20th Century, Dynamit Nobel developed the primer SINOXID which was for- mulated with lead and became a universal primer. By "... the 1960s exposure of shooters and firing range supervi- sors to lead reached intolerably high levels, as evidenced by the elevated blood lead values [71]." Dynamit Nobel developed SINTOX, a Pb -free (as well as Sb and Ba free) primer [71]. However, the results of some tests of the lead-free primers have proven disappointing, with sig- nificant variations in ignition timing, peak blast pressure, higher barrel frictions, and reliability in different climate conditions, compared with their lead-based equivalents [72]. The performance of lead-free primers are being tested by the U.S. Department of Defense (DoD) and North Atlantic Treaty Organisation (NATO) to reduce exposure of personnel to known lead sources [73]. Despite the critical observations, there is lead-free am- munition on the market. SINTOX is NATO approved and outlets for lead-free amntunitiun are available [74, 75]. Some states are taking the issue seriously and re- quire lead-free (or non-toxic "NT") ammunition at firing ranges [76]. Widespread acceptance of the need to re- place lead must take place, and until this happens one of the most significant health risks to shooters will remain lead -rich primers. "Green bullets" have also been proposed as a preventa- tive measure that could minimize lead exposure to par- ticipants and the environment. These bullets consist of copper rather than lead bullets. Bismuth has been pro- posed as a substitute for lead bullets but its environmen- tal health impacts are poorly understood [77]. It is clear that firing lead-free bullets results in dramatic decreases in airborne lead exposures at firing ranges [78]. The use of copper -jacketed lead bullets does not appear to be a solution to a reduction in lead exposure because it re- sults in only minor reductions in BLLs (see Tripathi et al. (1991, Table 1) [46]. The United States Department of Defence (DoD) is aware of the health threat posed by lead exposure from small arms [69] and efforts are Page 12 of 15 underway to test and replace lead in both primer and bullets [73, 79]. Table 1 provides evidence -based information about the BLL sensitivity of shooters to lead dust at firing ranges. The major gap in preventing risk of lead exposure at fir- ing ranges are the fundamental lead -bearing materials used for the explosive power and bullet projectiles. Pri- mary prevention requires eliminating all lead materials in primers and bullets in order to end the dispersal of lead dust at firing ranges. Conclusions Shooting lead bullets at firing ranges results in elevated BLLs at concentrations that are associated with a variety of adverse health outcomes and the topic of health risk is an ongoing topic of study. Of major concern is the number of women and children among recreational shooters, who are not afforded similar health protections as occupational users of firing ranges. Nearly all BLL measurements compiled in the reviewed studies exceed the level of 5 µg/dL recommended by the U.S. CDC/ NIOSH, and thus firing ranges, regardless of type and user classification, constitute a significant and currently largely unmanaged public health concern. Primary pre- vention of this risk requires development of lead-free primers and projectile bullets. Prevention includes better oversight of ventilation systems in indoor ranges and de- velopment of airflow systems at outdoor ranges, protect- ive clothing that is changed after shooting, and cessation of smoking and eating at firing ranges. The mismatch between what is recommended for individuals by the U.S. CDC is in stark contrast to the allowable levels for occupational exposure, and there are no real systematic biomonitoring programs for tiring range users to meas- ure cumulative health effects caused by persistent low and even high-level lead exposure. Recreational shooters and the general public are provided no legal protections from lead exposures at firing ranges. In conclusion, while the past two decades have brought substantial im- provements in analytical capabilities to detect lead in humans the literature evidence indicates that we fall far short of human health safety criteria in firing ranges of all types, and among occupational and recreational shooters. Additional file Additional fife 1. Summary of Studies on Airborne Lead Lxposure and Concentration from Shooting Activities, by Chronological Orders (modified frorn Wang et al, 2016) (DOCX ig kb) Abbreviations ABLES: Adult blood lead and epidemiology surveillance; BLLs: Blood lead levels; CDC: Centers for disease control and prevention;- California department of public health occupational lead poisoning Laidlaw et al. Environmental Health (2017) 16:34 prevention program; CSTE: Council of state and territorial epidemiologists; DOD: Department of defence; IPSC: International practical shooting confederation; IQ: Intelligence quotient; NATO: North atlantic treaty organisation; NIOSH: National institute for occupational safety and health; NNDSS: National notifiable diseases surveillance system; NSSF: National sports shooting foundation; NT: Non-toxic; NTP: National toxicology program; OSHA: Occupational safety and health administration; Pb: Lead; PEL: Permissible exposure level; US: United States; USGS: United States geological survey Acknowledgements We are very thankful to the three reviewers whose valuable comments substantially improved this manuscript. Mark Laidlaw thanks RMIT University for providing his funding through the Vice Chancellors Postdoctoral Fellowship Scheme. We would also like to thank Elizabeth O'Brien of the Lead Group Inc. in Sydney who stimulated the idea for this review. Thanks to Christopher Gonzales for assistance with Primary prevention requires eliminating lead in primers and bullets Funding Mark A.S. Laidlaw received funding from the RMIT University Vice Chancellor's Postdoctoral Fellowship. Funding for the remaining authors was from their salaries at their respective universities, Availability of data and material All data generated or analysed during this study are included in this published article. Authors' contributions ML conducted the initial literature review and wrote the first draft. HM, GF, BG, and AB reviewed and edited the subsequent drafts of the manuscript All authors read and approved the final manuscript. Competing interests The authors declare they have no actual or potential competing financial interests. Consent for publication Not Applicable. Ethics approval and consent to participate Not Applicable Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations; Author details 'Centre for Environmental Sustainability and Remediation (FnSuRe), School of Science, RMIT University, PO Box 71, Bundoora, VIC 3083, Australia. 2Department of Earth Sciences and Center for Urban Health, Indiana University -Purdue University Indianapolis (IUPUI), Indianapolis, IN, USA. 'Tulane University School of Medicine, New Orleans, LA, USA. 4Department of Environmental Sciences, Macquarie University, Sydney, Australia,. Received: 26 October 2016 Accepted: 30 March 2017 Published online: 04 April 2017 References I. Swedler DI, Simmons MM, Dominici F, Hemenway D. Firearm prevalence and homicides of law enforcement officers in the United States. Am J Public Health. 2015; 105:2042-8, 2, Ozonoff D. Lead on the range. Lancet 1994;343:6-7. 3. 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Changes in blood lead of a recreational shooter. Sci Total Environ. 2002;293:143-50. Page 15 of 15 Submit your next manuscript to BioMed Central and we will help you at every step: • We accept pre -submission inquiries • Our selector tool helps you to find the most relevant journal • We provide round the clock customer support • Convenient online submission • Thorough peer review • Inclusion in PubMed and all major indexing services • Maximum visibility for your research Submit your manuscript at 1 www,biomedcentral.com/submit 0 B1olVled Central