The present study represents the most comprehensive assessment of the radionuclide content of STPs published to date. Seventy-eight contemporary STPs from the USA and Sweden, covering the main product categories and manufacturers, were assessed for the presence of 28 radionuclides, encompassing all of the major sources of environmental radioactivity. Three of the species for which we found quantifiable amounts (14C, 3H, and 230Th) have not previously been reported in tobacco.
Several radionuclides are present at low levels in STPs
In contrast to the conclusions of recent literature reviews of radionuclides in STPs [1, 6] focusing on 210Po, 235U and 238U, this study has revealed a plurality of radionuclides in contemporary STPs. All STPs were found to contain α- and β-emitting radionuclides [generically categorized by IARC as Group 1 carcinogens when internally deposited—Table 1], and the specific IARC Group 1 carcinogens 226Ra, and 232Th were identified in a number of STPs. However, none of the radionuclides investigated were detected in all STPs. 14C, 226Ra, 210Po (and by inference, 210Pb) and 40K were found in almost all (66–69) of the STPs examined, 228Th, was identified in over half, and 3H, 238Pu, 239,240Pu, 238U, 234U, 232Th, and 230Th, were found in only a few. Other than 40K, the mass of radionuclides measured in these STPs were very low in comparison with other toxicants identified in STPs [1, 6], often by many orders of magnitude.
Members of both the 238U and 232Th decay series were present in the STPs. The most active species from the 238U series were 210Po (210Pb) > (238U ~ 234U ~ 230Th ~ 226Ra) respectively in order of activity. For the 232Th series, only 232Th and 228Th were detected, with 228Th showing greater activity. Radium-228 (228Ra; τ, 5.74 years; SA = 10.1 TBq/g) is a member of the 232Th series that was not examined in this study; however, previous reports suggest that it might be present in tobacco at levels similar to or slightly higher than those of the other members of the 232Th decay series [34,35,36].
Radionuclides resulting from cosmic ray irradiation of the atmosphere were also found in the STPs. Particularly notable is the presence of the β-emitter 14C, which was found in all but one of the samples examined; 14C has not been reported in tobacco before, and it represents a previously unconsidered source of radioactive exposure from tobacco products. 3H, also not reported previously in tobacco products, was identified in two STPs. In these two samples, although 3H was present at much lower mass concentrations than 14C, its radioactivity levels were similar to 14C. The substantially lower mass concentrations of 3H than 14C probably reflect differences in atmospheric production rates and subsequent uptake by the growing tobacco plant. Among the man-made radionuclides examined, some STPs showed measurable quantities of three plutonium radionuclides.
Many radionuclides are either undetectable or absent from STPs
Although some members of the 238U and 232Th decay series were present, others (234Th, 234Pa, 214Bi, 214Pb, and 228Ac, 212Pb, 212Bi, 208Tl respectively), as well as 235U, 131I and the two caesium radionuclides, showed no activity in any of the STPs examined. Some of these radionuclides have been previously detected in tobacco (228Ac, 214Bi, 134Cs, 137Cs, 214Pb, 212Pb, and 235U). When a species was not detected it may be due either to the absence of the species in the analyzed matrix or to insufficient sensitivity of the analytical method for the sample being examined.
There are some indications to the reasons underlying the absence of measured activity from specific radionuclides in some samples. The presence of members of the 238U and 232Th decay series, particularly the originating radionuclides, in an STP means the presence of other members of the decay series cannot be precluded, albeit at levels below the detection limit of the assay. This is exemplified by the uranium isotopes examined in this study. No STP was found with measurable 235U, five samples showed detectable levels of both 234U and 238U, and two STP samples were found to contain 234U but did not have measurable levels of 238U. Natural sources of uranium contain these radionuclides at a ratio of 99.27% 238U to 0.72% 235U to 0.0054% 234U; however, 234U is the most radioactive uranium isotope, and thus lower concentrations could be detected by the method used in this work. Therefore, 238U and 235U will also be present, even if not detectable, in the samples containing 234U. Moreover, given the very short half-lives of many of the progeny of the 238U decay series (such as 214Pb and 214Bi) it is reasonable to assume that such species may be present, however fleetingly, at some point between production and consumption of an STP.
In contrast, some of the man-made radionuclides with relatively short half-lives (e.g. 137Cs, 134Cs, 131I) were not detected in the STPs, and it is plausible that these species are not present owing to a combination of their decay rates and the age of the tobacco in the STPs post-harvest. The radionuclides 134Cs (τ = 2 years) and 131I (τ = 8 days) would be expected to have decayed to their progeny in the time scale between recent nuclear reactor incidents (e.g. Chernobyl in 1986) and the date of this study (2008–2010). However, 137Cs (τ = 30 years) would have undergone less decay since its emission into the environment following the Chernobyl nuclear accident; therefore, the absence of detectable 137Cs probably reflects low levels, if any, absorbed from the environment into the tobaccos used to make these STPs. The analytical method is sufficiently sensitive to detect the levels reported in many of the historical observations, and therefore 137Cs may not be present in these STPs. The plutonium radionuclides identified in small numbers of STPs during the present work have half-lives from 87 to 24,000 years. Appreciable quantities of plutonium radionuclides were released into the atmosphere during atmospheric nuclear weapons testing in the mid to last half of the 20th century, and their presence has subsequently been detected in several plant species [32]. However, 241Am (τ = 432 years), also a product of man-made nuclear reactions, and a daughter product of 241Pu, was not detected in the STPs, but may be present at levels below the sensitivity of the method.
In the present work, upper bounds for the possible presence of undetected radionuclides were calculated from the reporting limits of the activity counting method. For some radionuclides with very short half-lives, the upper reporting limit corresponds to a few atoms of the radionuclide within the STP sample. Notably, no radionuclides were detected with half-lives shorter than 132 days. Conversely, all naturally present radionuclides (other than 235U, which, if present in these STPs, would have levels below the sensitivity of the analytical method) with half-lives greater than 132 days were detected in some of the STPs examined in this work. This may either point to an effective cut-off point, based on radionuclide half-life, for the analytical capability of the current approach, or perhaps reflect the age of tobacco at the time of measurement.
Activity from β-emitters in STPs by far exceed those of α-emitters
The 2008 SCENIHR report [9] stated that “according to Hoffmann et al. [37], the average total activity of alpha emitters in 5 major brands of US snuff was found to be 0.16–1.22 pCi/g” (6–45 mBq/g). Examination of the Hoffmann et al. study [37] reveals the SCENIHR reports statement to be incorrect, and probably an underestimate, in that Hoffmann et al. reported the presence of 0.16–1.22 pCi/g 210Po, rather than total α-activity, in 5 US snuff brands. The total α-emissions from the STPs in the current study ranged from 4 to 50 mBq/g wwb and β-emissions ranged from 164 to 1980 mBq/g wwb (plus the unmeasured contribution of 210Pb, estimated by comparison to 210Po at 1.8–18 mBq/g). Mean values for total α- and total β-emissions are graphically compared in Fig. 2, which clearly shows that total β-emissions are substantially greater than total α-emissions, with β-emissions accounting for 98% on average of the measured activity. Figure 3 shows that in terms of the radioactive emissions from constituents within STPs, the greatest contribution by far was from the β-emitter 40K; and, when detectable, the activities of the other β-emitters (14C, and 3H) were also greater than that of α-emitters. Unlike the potential risk from more volatile radionuclides such as 210Po in cigarette tobacco, transfer to smoke is not a factor in assessing exposure to radionuclides in STPs. Among the STPs examined here, the radioactivity of 210Po was approximately 1% of that of 40K, and therefore 210Po is a relatively minor contributor to STP radioactivity. Although as depicted in Fig. 4, and discussed later in more detail, the presence of a given radionuclide in an STP cannot be directly extrapolated to human exposure.
Radionuclide content varies with STP product type
Some variations in radionuclide content were observed among the different STP categories. Only the HP products had consistently measurable levels of 238U, 234U and 230Th. HP products also had higher levels of 226Ra than the other categories on a wwb. The higher levels of these radionuclides likely reflect the presence of non-tobacco (such as calcium carbonate [38]) materials within the HP products. Estimation of the inorganic content (via ashing) of the STPs showed higher inorganic contents in the HP products than in CT, MS, plug, SP, loose snus and all pouched snus other than the low moisture brands. However, the inorganic contents of the DS, dry pouched snus and HP products were comparable. Hence these measurements suggest that the nature of the non-tobacco materials in the HP products may be more important than the quantity. Uranium is known to interchange with calcium in bone samples [39], and the presence of calcium salts in the HP products may act as a source of uranium and daughter radionuclides in STPs.
For the most abundant radionuclide present, 40K, the highest levels were found in DS products, and the lowest in an STP whose tobacco content appeared diluted with other materials. No differences were found among product categories for 14C or 228Th when adjusted for the moisture content of the STPs. The STPs in which 238Pu and 239,240Pu were detected had similar levels of these man-made radionuclides.
A review of the literature generally indicates that the radionuclides we identified in STPs are similar to levels historically reported in tobacco, except, as noted above, where non-tobacco materials appear to be included in the STP. However, we identified several radionuclides in STPs that have not previously been reported in tobacco.
Assessing exposure to radionuclides in STPs
There is no existing radiological model for evaluating exposure from STPs
Establishing the radionuclide content of STPs is an essential first step in understanding the incremental contribution of radionuclides associated with STP use to the background exposure from radionuclides in our diet, water and air. A key step is to calculate the radiation dose to tissues of STP users, because it allows estimation of the relative risk profiles of different STP product categories, and in principle it facilitates estimation of the risks associated with radionuclides in STPs. Models exist for calculating the radiation dose (exposure energy divided by mass of exposed tissue) resulting from exposure to radionuclides present in our diet, water and air, as well as from occupational exposure (e.g. [40,41,42]).
However, the type of exposure associated with STP use (shown schematically for use of a generic STP in Fig. 4) is somewhat different to established exposure models. Perhaps the closest established model is that used to calculate the exposure to, and risk from, ingested radionuclides. However, models of ingestion assume rapid mouth transit of the ingested material, and also incorporate the metabolic processes of the body that lead to dispersal of the radionuclide from the gastrointestinal tract to the physiologically preferred accumulation site (e.g. the skeleton for inhaled and ingested uranium radionuclides). STP-use typically involves extended mouth residence (e.g. in the case of Swedish snus an average of 1 h per portion for 12–14 h/day [43]) at habitual locations within the mouth. During this time, the user’s saliva extracts constituents from the STP [16], and the radionuclide-containing saliva may be swallowed or expectorated, but can in principle act as a carrier for radionuclides from STP to mouth tissues for absorption through mucous membranes. During residence in the mouth, radionuclides in the STP may also potentially directly irradiate the tissues adjacent to the STP. Some STPs are dispersed in saliva and not designed to be expectorated; these STPs and their radionuclides will be more readily absorbed or ingested. In those STP categories that are designed for expectoration of the used product, some loose tobacco particles may be swallowed during use. When use of a non-dispersing product is complete, the remaining STP solids (which are heavily loaded with saliva) are removed by the user and discarded.
Direct radioactive exposure of oral tissues by STPs is limited
Localized irradiation of the oral tissue of STP users by α- and β-radiation from STPs during use is possible, and Hoffmann et al. [37] suggested that α-radiation emitted by STPs may contribute to an increased risk of snuff dippers for oral cancer due to concentrated irradiation of a relatively small area of the cheek and gum.
However, α-radiation can cause only localized damage owing to its short path length in air and biological matrices (< 0.1 mm) [12], and it is important to note that the dimensions of STP portions are considerably larger than this path length. Therefore only those radionuclides lying very close to the periphery of the STP portion could possibly lead to direct irradiation of oral tissue. For example, we estimate that approximately 1% of the α particles emitted within a snus pouch (i.e. those emitted near the periphery of the portion) would be capable of travelling far enough to exit the snus matrix. In addition, the average thickness of the salivary film, 0.07–0.1 mm [44] will act as an additional barrier to emitted α-radiation, further reducing the likelihood of tissue exposure from α-particles emitted within an STP.
The ability of β-radiation emitted by STP constituents to exit the STP matrix and contact the oral mucosa is highly dependent on the energy of the β-radiation emitted [45]. Low energy β-radiation emitted from 3H and 210Pb could penetrate only 5–6 μm from the site of emission within the STP, whereas the more energetic β-radiation from 14C and 40K can potentially penetrate 0.3 and ~ 5 mm respectively [45, 46].
In addition to the barrier properties of the mouth’s salivary film noted above, the outer layer of the oral cavity epithelium, being composed of keratin and subject to continuous sloughing, is a further physical barrier to α- and β-particles. The thickness of the epithelium of the buccal mucosa (the relevant site for STP users) has been measured at around 250 μm in normal healthy subjects [47], and the most superficial keratinized squamous cells are nonvital. It is likely that STP users have somewhat thicker epithelium and a thicker keratin layer, which will physically increase the path length that emitted α- and β-particles must traverse to damage the critical cells in the basal layer. The combination of these factors make it unlikely that biologically-significant damage to oral tissue will result from STP-borne α-emitters and the majority of the β-emitters; however exposure to β-radiation emitted from 14C and particularly 40K in STPs may be of concern.
These estimations highlight the need for more sophisticated exposure models to assess radiological dose in STP users. These models should consider the committed effective dose arising from exposure to alpha and beta generating radionuclides; internal exposure to alpha radiation is considered more damaging than beta radiation due to the way in which energy is imparted to tissue by these two types of radiation. Several further aspects of direct irradiation need to be considered. First, the main decay mode of many radionuclides that emit α- or β-radiation can be accompanied by gamma radiation emissions. The emitted gamma radiation can introduce an additional radiation dose to the STP user, as gamma radiation can penetrate further and potentially interact with critical biological tissue; this both widens the area of potential radiation exposure but also introduces a relatively low potential for tissue damage due to the comparatively weak interaction of gamma radiation with tissue. Second, there is also potential for bremsstrahlung radiation resulting from interaction of emitted β-radiation with mercury-based dental amalgams in the mouths of some STP users. Some further, potentially important, exposure mechanisms are also important to consider in the development of a model and are described below.
Radionuclides can be extracted from STPs by users’ saliva
STP users may also be exposed to radionuclides extracted from the STP by saliva during STP use. Extracted radionuclides may come into closer contact with oral tissues than those remaining within the STP [48], and therefore may more readily expose STP users to radiation. Syed et al. [48] considered 210Po extracted in this way to be the main source of irradiation from STPs. However, for most categories of STP (other than dispersable products, for which complete ingestion can be assumed), uncertainties exist over the extent of extraction of individual radionuclides into saliva. There are few data on constituent extraction during STP use, but estimates of the extractability of 210Po from US moist snuff in a model system using human saliva was reported as being very low, at 2–10% [48]. There are no data on the extractability of other α-emitters from STPs. It is also difficult to estimate the solubility of these species in tobacco because the exact chemical forms are unknown: recent work has demonstrated that inorganic metalloids in tobacco can be present in multiple chemical states [49] and with differing solubilities [50]. Environmental studies have shown that radium is only moderately soluble in water, but is most soluble under chloride-rich reducing aqueous systems with a high total content of dissolved solids, a condition that might relate to STPs that have a high salt and water content [51]. Environmental thorium has very low aqueous solubility [46]. Aqueous solubilities of uranium, plutonium and neptunium are low but pH dependent [52]. These data suggest limited bioavailability of these α-emitting radionuclides in tobacco, but further studies are required to draw a definitive conclusion.
Regarding the extraction of β-emitters into saliva, a study on the extractability of lead from US moist snuff and Iqmik using artificial saliva showed that lead (and hence 210Pb) was not readily extracted (< 8%) from these STPs [53]. Similarly, no measurable level of lead extraction was found during use of snus by US snus consumers [54]. However, 14C is incorporated chemically into the tobacco plant in several soluble organic species such as sugars, sugar esters and starches [30], and 3H can be present as tritiated water or organic species [41]. Therefore it is likely that these two species would be bioavailable from STPs, although the extent of availability is unclear at present. There are no data on potassium extraction from tobacco; however, a study of the extraction of a range of snus constituents by users showed that ~ 30% of the sodium content was extracted [16]. Because potassium and sodium ions share very similar aqueous solubilities it is plausible to assume that potassium (and hence 40K) extractability is also ~ 30% from snus.
Overall, these data suggest that most of the radionuclide content of STPs may remain within the STP during use, but some extraction of radionuclides into saliva, particularly 40K, 3H and 14C, will occur. Once released into saliva, the radiation emitted by saliva-soluble radionuclides will have to overcome the physical shielding effects of saliva, air and non-vital epithelium cells within the oral cavity in order to encounter biologically-important tissue. However, this mechanism does represent a plausible route to the irradiation of STP users’ oral cavities, particularly by 40K and 14C.
Systemic exposure from STP radionuclides
Figure 4 illustrates that systemic dispersion of radionuclides may arise in principle from two routes during STP use: uptake through oral tissues, and swallowing tobacco and tobacco-constituents in saliva.
Radionuclides extracted from STP portions may potentially be absorbed into oral cavity tissues (Fig. 4). If tissue clearance mechanisms are relatively slow compared with STP usage duration, this may lead to a localized build-up of radionuclide in the oral tissue during use, particularly as STP users generally position the tobacco portion at a fixed location within the mouth. However, radiation exposure may be limited in this scenario, as noted above the identified STP radionuclides all have half-life times in excess of 132 days. Standard radiological models do not account for this potential source of exposure, and this is an area requiring further attention.
In contrast, the incremental exposure to radionuclides after swallowing during STP use, is within the scope of the standard radiological dose models for ingested radionuclides from the diet. Systemic dispersion of radionuclides after ingestion is well understood. Potassium (including 40K) is almost completely absorbed after ingestion and is quickly distributed to all of the organs and tissues of the body via the bloodstream; it is eliminated from the body with a biological half-life of 30 days. However, the level of potassium in the body is under strict homeostatic control and is not influenced by environmental factors, with an adult male having a body content of 3700 Bq of 40K [46]; hence STP use will not increase the body content of 40K. Increased exposure to radiation from 40K may arise in the GI tract of STP users during transit of swallowed materials; however, comparison to the recommended USA adult daily dietary intake of 4.7 g potassium [55] suggests that GI exposure of STP-sourced 40K will be 1–2 orders of magnitude lower than dietary intake. Hence the risk of systemic exposure to 40K from STPs will be small. In contrast, STP use can add to the body concentrations of 3H, 14C, and the progeny of 238U and 232Th, at levels corresponding to their extractability. Depending upon the effectiveness of fractional absorption from the gut there may also be some GI exposure to radionuclides that undergo extended intestinal transit. The extent of these sources of exposure is unclear, as noted above, but is likely to present a minimal increase in exposure and hence risk in comparison to dietary intake.
The risk of radiation exposure from STPs appears low
The greatest potential radiological risk from radionuclides in STPs therefore appears to be from 40K, and to a lesser degree 14C. Given the localized and extended time of STP use in the mouth, exposure of STP users’ oral tissues to radioactivity may occur either via direct irradiation from within the STP portion or by radionuclides extracted by users’ saliva. With the uncertainties surrounding STP portion size and geometry (and the resulting attenuation of radiation emitted from within STPs), and the differential extent and kinetics of extraction into saliva by users of different STPs, it is challenging to establish an accurate estimate for effective dose to the oral cavity. Clearly, more sophisticated models that account for localized exposure are desirable to quantify radionuclide exposure within the oral cavity, and their development would represent an advance in understanding the potential for oral toxicity of STP use.
Ultimately, epidemiology provides the most informative insights into the risks associated with STP use. Rosenquist et al. [56], Luo et al. [57] and Rodu and Jansson [58] have reviewed the evidence for oral cancer associated with several STP categories. These authors identified no increased risk of oral cancer for snus use by Swedes, and moist snuff and chewing tobacco use by Americans. Assuming that the radionuclide contents of STPs measured in this study are no higher than those present in STPs during the extended time periods corresponding to the epidemiological studies examined in the reviews above, then the levels of radionuclides measured in this study can be regarded as posing no significant hazard to STP users. This conclusion concurs with that expressed in the 2008 SCENIHR report [9] which stated: “the dose of ionising radiation from these sources must be considered as negligible in comparison e.g. with the natural radiation background and other sources of ionising radiations”.
Regulatory implications of STP radionuclides
The FDA issued a list [5, 59] of harmful or potentially harmful constituents (HPHC) in tobacco products and tobacco smoke, as required by the Federal Food, Drug, and Cosmetic Act (the FD&C Act). The list contains three radionuclides, 210Po, 235U and 238U, and their presence on the list arises [60, 61] from chemical data summarised in IARC Monograph 89 [1], which is in turn based on earlier reviews [62, 63].
However, IARC Monograph 89 (and earlier reviews) contain factual errors relating to these uranium isotopes. Specifically, Table 3 of IARC Monograph 89 (page 58) lists 2.4 pCi/g of 235U and 1.91 pCi/g 238U in MS, arising from (page 85) a study by Sharma et al. [4] of the uranium content of five Indian snuff products. However, examination of the Sharma et al. study shows that the authors reported no specific data for 235U or 238U, instead they disclosed specific activity measurements (2.4–6.4 pCi/g) and mass concentrations (7.4–19.1 ppm) for the presence of total uranium [4]. Consequently, the presence of these uranium isotopes on the FDA list is based on flawed data summaries within the IARC monograph.
The findings of this work, which show a more complex picture of STP radiochemistry than previously considered, coupled with errors in IARC Monograph 89, may justify re-examination of the radionuclides currently identified on the FDA HPHC list.