The Beechey Island bodies

The ice-preserved bodies of John Torrington (20 years), John Hartnell (25 years) and William Braine (33 years) in graves on Beechey Island were subjected to detailed forensic examination in a remarkable series of autopsies conducted in arduous conditions (Amy and others Reference Amy, Bhatnagar, Damkjar and Beattie1986; Beattie and Geiger Reference Beattie and Geiger1987: Notman and others Reference Notman, Anderson, Beattie and Amy1987). Their emaciated condition was taken to imply prolonged illness prior to death and would be consistent with the suspected evidence of tuberculosis (Amy and others Reference Amy, Bhatnagar, Damkjar and Beattie1986) that was common amongst nineteenth-century naval crews and the population in general. Most significantly, however, the examinations also revealed a high lead content in bone, soft tissue and hair. In an initial report, Torrington's body provided samples from a single rib, radius and clavicle having a range of lead content of 110–151 ppm or μgPb/g (contents of the individual bones were not published: Amy and others Reference Amy, Bhatnagar, Damkjar and Beattie1986). For unstated reasons, Torrington's clavicle was omitted from a subsequent publication (Kowal and others Reference Kowal, Krahn and Beattie1989: Table 1) which added bones from Hartnell and Braine to form a sample comprising a single radius (presumably from Torrington), femur, skull and vertebra, and two ribs (one, again presumably, from Torrington) and yielded a mean lead content of 128.3 μgPb/g (SD = 45.0; range 69–183). It was not stated which of the other bones were sampled from Hartnell and Braine respectively but, given the overall range when compared to that for Torrington alone, it may reasonably be concluded that the levels varied between the three men.

The analysis of soft tissue is of greater importance because it indicates more immediate lead exposure than the long-term accumulation reflected in bone. Levels of lead in the aorta and spleen were similar to those in present-day lead-exposed groups, but the levels in liver, kidney, stomach and skin were, relatively, very high and would imply recent exposure (Kowal and others Reference Kowal, Beattie, Baadsgaard and Krahn1991: Table 2). Regrettably, individual data for the three men were not published, nor the standard deviation or range, thus leaving it unclear whether the published values were means or single values, and thus whether all three bodies contributed data for each organ. It is therefore unclear whether all the men had accumulated similar levels of lead in their soft tissues or whether, as in the case of bone and hair (see below), they showed large inter-individual differences.

Differences between the three men in lead accumulation are clearly evident in the analysis by Kowal and others (Reference Kowal, Krahn and Beattie1989) of hair that was sampled in 1 cm segments from 10 cm hairs taken from the nape (that is 10 samples from each hair). Whilst it is important to consider the implications of the hair analysis, it has been noted that many factors seriously affect the reliability of hair as a biomarker of lead exposure (Barbosa and others Reference Barbosa, Tanus–Santos, Gerlach and Parsons2005; Kowal and others Reference Kowal, Beattie, Baadsgaard and Krahn1991; Rodrigues and others 2008). As hair grows at approximately 1.1 cm per month (Kowal and others Reference Kowal, Beattie, Baadsgaard and Krahn1991), the 10 cm length equates to some eight to nine months of growth which, in the case of Torrington and Hartnell, conveniently encompasses their time from departure in May 1845 until their deaths in the first week of January 1846. The segment of root at the nape was indicative of lead exposure in the four to eight weeks prior to death. The mean levels (SD: range) and the levels in the root segments were: Torrington 565 μgPb/g (117 μgPb/g: 330–707 μgPb/g) and 330 μgPb/g; Hartnell 326 μgPb/g (110 μgPb/g: 222–510 μgPb/g) and 265 μgPb/g; Braine 225 μgPb/g (90 μgPb/g: 158–317 μgPb/g) and 211 μgPb/g (from Kowal and others Reference Kowal, Krahn and Beattie1989: Table 6). Thus, the means for Hartnell and Braine (both of Erebus) were 42% and 60% lower, respectively, than that of Torrington (of Terror). The difference in means could be explained if the domestic economies of the two ships exposed their companies to different levels of lead contamination, or it might be a consequence of each individual's propensity to accumulate lead, or to some unknown factor. Whilst the range of lead content and the level in the 1 cm sample at the root were published for each man, it is regrettable that the lead contents of the other nine 1 cm sections were not published as they would have provided an excellent time-line of change in hair-lead content over the eight-month period.

Torrington's hair also provides evidence of a high lead content at the time of joining the expedition. The root segment had a content of 330 μgPb/g and, as the lowest value of the range was precisely 330 μgPb/g, it can be assumed the root was the lowest value in the range. Logically, therefore, the most distal segment of his 10 cm hair sample (which at the time of departure was growing at the nape and whose lead content therefore indicated exposure both prior to, and at the time of, departure) must have had a lead content that at least equalled, and most probably exceeded, 330 μgPb/g. As the concentration of trace elements in the root segment lags the blood-lead level by approximately 20 days (Clarkson and Magos Reference Clarkson and Magos2006), the implication is then that Torrington had already accumulated high levels of lead at the time of departure. Moreover, given that ‘only over the last inch or so [that is the 1 cm root segment] did the level [of lead in Torrington's hair] drop (Beattie and Geiger Reference Beattie and Geiger1987: 194), the figures above would imply that the levels in his hair were high over the eight-month period from embarkation.

If so, it is unclear what sustained those high levels in the first two or three months when the supposed lead-contaminated tinned provisions were little used, if at all (Farrer Reference Farrer1993), and where snow was not being melted to produce drinking water having a plumbo-solvent effect on lead supply pipes. Certainly, Torrington's duties as stoker on the Terror may have exposed him to lead in coal dust which might have found its way into his hair via ingestion and exogenous contamination, but Beattie and Geiger (Reference Beattie and Geiger1987) observed that the lack of callouses on his hands indicated that he had been too ill to work for a considerable time prior to death, and further that there is no evidence that the ships' auxiliary engines had been used in 1845. If, as proposed by Farrer (Reference Farrer1993), Torrington received different treatment from the surgeons on the Terror than did Hartnell and Braine from those on the Erebus for conditions that may have included tuberculosis, then an iatrogenic factor may have been relevant. The Royal Navy provided ‘comforts for the sick’ which included wine which was often adulterated with acetate of lead and administered in pewter vessels. Acetate of lead was recognised as a poison but also had medical uses in treatment of diarrhoea associated with tuberculosis and for the common sailors’ affliction of gonorrhoea. In this context it is notable that Hartnell's body also contained high levels of mercury (Amy and others Reference Amy, Bhatnagar, Damkjar and Beattie1986) which was a recognised treatment for the equally common affliction of syphilis. The expedition is also known to have suffered widely and severely from chilblains during their time at Greenland (Bell Reference Bell1881: 126) for which acetate of lead was a recognised treatment as an astringent. The standard Royal Naval ‘Medicine Chests Nos. 1 to 4’ were stocked according to the size of a ship's complement and all included lead- and mercury-based medications; for example liquoris plumbi acet. and hydrargarum submuriatis (His Majesty's Stationery Office 1835: 56–57). A medicine chest recovered from Victory Point appeared to be non-standard issue for it bore no Government mark and may have been the personal possession of an officer, but it also contained a bottle labelled ‘Mur. Hyd.’, which would be perchloride of mercury (Cyriax Reference Cyriax1947). Only the recovery of the surgeons’ sick lists would confirm this speculation about an iatrogenic factor (see final discussion) but it is mentioned here to reinforce the fact that there was the potential for lead to have accumulated from many sources. Re-analysis of the hair might clarify the time-line of accumulation, subject to criticism of the reliability of hair analysis as a marker of exposure (Barbosa and others Reference Barbosa, Tanus–Santos, Gerlach and Parsons2005; Rodrigues and others 2008).

The data from Beechey Island reveal levels of lead in bone, soft tissue and hair that, at the upper range, would be consistent with lead poisoning. Other outcomes of the forensic examinations provide grounds for caution, however. For example, in their examination of the oral cavity, Amy and others (Reference Amy, Bhatnagar, Damkjar and Beattie1986) made no mention of ‘Burton's line’ (a bluish-grey line on the gingiva) which is a common, although not inevitable, sign of lead poisoning (Burton Reference Burton1840; Pearce 2006; Troesken Reference Troesken2006). Similarly, Notman and others (Reference Notman, Anderson, Beattie and Amy1987) noted explicitly that there was no calcification of the basal ganglia of the brain associated with lead poisoning, although the portable X-ray equipment used may have lacked the resolution to detect subtle or early changes associated with acute exposure. As the presence of tuberculosis and pneumonia was also suspected (Amy and others Reference Amy, Bhatnagar, Damkjar and Beattie1986; Notman and others Reference Notman, Anderson, Beattie and Amy1987), it would be difficult to ascribe the deaths to lead alone.

Given the present focus upon individual variation, the further question is whether there is evidence that other men were subject to the effects of lead at Beechey Island. Beattie and Geiger concluded that ‘the effects of lead poisoning [on the three men who died on Beechey Island] were catastrophic’ and that others ‘would have been as severely affected’, but they also allowed that some ‘may not have shown any obvious effects of the poison’ (Beattie and Geiger Reference Beattie and Geiger1987: 241–242). If lead poisoning were catastrophic and widespread it is notable that no others died at Beechey Island (unless their remains have yet to be found). Lloyd–Jones (Reference Lloyd–Jones2004: 325) has observed that it is ‘much more likely [that these men died of tuberculosis] than that they suddenly succumbed to lead poisoning when others did not.’ Moreover, if lead poisoning were widespread at Beechey Island one might assume that the consequent reduction in effective manpower would have prevented the expedition from proceeding. In fact, the men were fit enough to construct a well-founded winter base including a site for magnetic observations, several large cairns, one on a 200-metre-high cliff, and to undertake physically-demanding, man-hauled sledging exploration (Cyriax Reference Cyriax1939; Hansen Reference Hansen2010; Powell Reference Powell2006). They also constructed a small garden (an ‘anti-scorbutic gardening patch’; Kane Reference Kane1856: 163) and shooting range which would reflect, respectively, the awareness of the need for fresh greens to ward off scurvy and other dietary deficiencies, and for training in marksmanship which was vital to the procurement of game to supplement their provisions. Such forward planning and physically-demanding activities would seem inconsistent with widespread lead poisoning. The expedition then proceeded when the ice opened later in 1846. In April 1847, Commander Fitzjames of the Erebus could still state ‘All Well’ (and underline it for emphasis) when signing off the position report deposited at Victory Point. His emphatic statement would not seem consistent with a serious situation affecting the health of a large proportion of the crew some two years into the expedition.

Clearly, however, significant mortality did occur over the following year and it is bone samples from King William Island that offer insight to the state of the crew at the desertion of the ships.

King William Island skeletal remains

Kowal and others (Reference Kowal, Krahn and Beattie1989) employed graphite furnace atomic absorption spectrometry to determine the levels of lead (μgPb/g dry weight) in bones collected from the western and southern coasts of King William Island and which represented an uncertain number of men who had died during the attempt to reach the mainland. Although 23 bones are listed by Kowal and others (Reference Kowal, Krahn and Beattie1989: Table 1), the correct total is in fact 14 due to an error which had gone undetected until an enquiry by the present authors (Beattie, personal communication, 16 August 2013). These bones comprised a single vertebra, rib and metacarpal, two parietal bones and two ulnae, three femurs and four tibiae (originally published erroneously as thirteen tibiae). The mean lead content was 138.1 μgPb/g (SD 35.0: range 87–223) but the contents of individual bones were not given. Only a very cautious comparison can be made between the mean bone-lead content of this unknown number of men who died after deserting the ships and the three who died two to four years earlier on Beechey Island, but the difference is slight at 10 μgPb/g and the standard deviations of the two samples completely overlap. The very slight difference might imply that there had been little further accumulation of lead during the two- to four-year period leading to, and following, the desertion of the ships, but such a conclusion would be very tenuous given the small numbers involved. Similarly, whilst the wide range of lead content of the King William Island bones might imply considerable inter-individual variation in accumulation of lead, it cannot be confirmed because it is quite uncertain whether several bones may have belonged to the same man.

Clearer insight to inter-individual variation in lead burdens is found in a highly detailed study by Keenleyside and others (Reference Keenleyside, Song, Chettle and Webber1996) of a further sample of 52 bones collected from a site at Erebus Bay on King William Island which was relatively near to the point where the ships were deserted. A non-destructive X-ray procedure was used to estimate bone-lead content. Depending upon the bone type, the ranges observed were either wider or narrower than the overall range of 83–223 μgPb/g observed by Kowal and others (Reference Kowal, Krahn and Beattie1989 above); for example, the ranges for the tibia (62–151 μgPb/g) and femur (103–203 μgPb/g) were narrower, while those of the radius (73–373 μgPb/g) and (most extremely) the vertebra (580–1740 μgPb/g) were wider. The overall greater range may simply reflect the larger sample size of Keenleyside and others which would inevitably tend to sample a wider range of the crew's lead levels. (Parenthetically, if the exceptionally high levels seen in the vertebrae are reliable, they might seem difficult to reconcile with the levels that could possibly have been accumulated from the canned provisions, particularly in light of comments by Farrer Reference Farrer1993). The different procedures used by Kowal and others (Reference Kowal, Krahn and Beattie1989) and Keenleyside and others (Reference Keenleyside, Song, Chettle and Webber1996) to determine bone lead may also account for some of the differences between the studies. When, in a later study, Keenleyside and others (Reference Keenleyside, Bertulli and Fricke1997) employed the same procedure as Kowal and others (Reference Kowal, Krahn and Beattie1989) in a re-analysis of a sub-set of the data of Keenleyside and others (Reference Keenleyside, Song, Chettle and Webber1996), the levels of lead in two of the tibiae differed by +34% and −18% respectively from the levels reported in the earlier publication. This fact is not obvious from the two publications themselves but was confirmed by Keenleyside (personal communication, 19 July 2013) following enquiries from the present authors. Thus, the potential for substantial measurement variation must be borne in mind in addition to any ‘real’ inter-individual variation in bone lead. Hie and others (Reference Hie, Hu and Chettle2008) have discussed in detail the variable consistency of data derived from in vivo assessment of bone lead.

As the lead contents of different bones within an individual have been shown to bear particular relationships (Wittmers and others Reference Wittmers, Wallgren, Alich, Aufderheide and Rapp1988), Keenleyside and others (Reference Keenleyside, Song, Chettle and Webber1996) employed established techniques to allocate sets of bones to seven separate skeletal identities. Data adapted from Tables 2 and 3 of Keenleyside and others (Reference Keenleyside, Song, Chettle and Webber1996) are presented in Fig. 1 for the seven skeletons identified by the latter authors. The range of lead values was very wide but, as there was no reason to suppose that extreme values were anomalous, they were not excluded as outliers. Missing data points were not interpolated.

Fig. 1. An estimation of the distribution of lead (μgPb/g) across the Franklin crew as calculated from the bones of seven individual skeletons (individual raw data from Keenleyside and others Reference Keenleyside, Song, Chettle and Webber1996: adapted with permission). The shaded area encompasses +/− 2 standard deviations around the mean bone-lead and therefore represents approximately 81% of the crew.

Whole-crew (population) estimates of lead burdens

An analytic procedure was applied to the data in Fig. 1 to allow estimation of the variation in ‘population’ lead levels across the crew (after Galwey Reference Galwey2006). Analysis employed the ‘nlme package’ in the R Statistical Computing Environment (Pinheiro and Others Reference Pinheiro, Bates, DebRoy and Sarkhar2013) The data in Fig. 1 were modelled first with a factor which reflected the different mean lead concentrations in each bone. More critically, a ‘random factor’ was included to capture the variation in lead levels from individual to individual. Specifically, the underlying lead level associated with each person is assumed to be drawn from a normal distribution with mean = 0 and standard deviation (SD) = δ_s and so this distribution reflects the variation in lead levels among the crew.

It was evident from initial data analysis and visual inspection of Fig. 1 that the range was very wide, that the distribution had a positive skew and that the SDs of the lead values for each bone increased as a function of their respective means. A logarithmic transformation was therefore applied as a very effective way of placing the data on a scale of variation which was constant across bones and served to provide a closer approximation to a Gaussian distribution which is a requirement of the analytic procedure. The abscissa of Fig. 1 has been constructed on a log scale which still allows lead levels to be referenced on the original measurement scale of μgPb/g.

An important caveat applies to this analysis. The sample is small and the identities of the skeletons are unknown so that it is uncertain whether they are a representative sample of the 105 crewmen. Nothing is known of variables that might influence the lead burden such as age (and thus life-time exposure to lead), education and rank, and previous occupational exposure to lead: such variables would normally be covariates in an analysis.

The random effects model estimates the SD of mean lead levels across the crew members on the log scale as 0.48 (95% CI = 0.27-0.85). The shaded area in Fig. 1 allows the meaning of this variation to be expressed on the original measurement scale of μgPb/g by calculating (mean +/− 2SDs) on the log scale and transforming the end points of these intervals back to the original scale. The variation shown in Fig. 1 then allows estimates to be made of the proportion of the crew whose bone lead levels fell above or below any nominated value of interest.

The overall implication of the shaded area of Fig. 1 is that levels of bone lead differed very substantially across the crew. The proportions of men who carried particular lead burdens can be estimated very cautiously. Formally, one SD encompasses 68.2% of values around the mean and thus corresponds to ~72 of the 105 crew, half of whom (~36) would have lead levels above, and half below, the mean. Two SDs account for a further 13.6%, or ~28 men of whom 14 would have values below, and 14 above, the mean. The remaining ~5 men would lie in the tails of the distributions between 2 and 3 SDs above or below the mean. It is then deducible that, overall, some 14 (13%) to 16 (15%) men would have bone-lead levels between −1 and −3 SDs below the mean and would have carried relatively lower burdens of lead. A corresponding number between +1 to +3 SDs would, obviously, have had relatively higher levels.

Implications for Franklin's crew of present-day studies of lead-related neurocognitive and physical morbidity

The crew's tibia lead data are of particular relevance because they allow cautious comparison with present-day studies of the relationship between cognition and tibia lead which have been made by in vivo estimation of tibia lead using X-ray methodology similar to that of Keenleyside and others (Reference Keenleyside, Song, Chettle and Webber1996). The tibia is composed principally of cortical bone which provides a stable storage of lead with a long half-life recently estimated as 48.6 years (Wilker and others Reference Wilker, Korrick, Nie, Sparrow, Vokonas, Coull, Wright, Schwartz and Hu2011) and thus is a reliable indicator of cumulative exposure. The crew's tibia data (from Keenleyside and others Reference Keenleyside, Song, Chettle and Webber1996) are shown in Fig. 2 which also shows tibia lead from five studies of the association between lead and cognitive function in present-day samples (Bleeker and others Reference Bleeker, Lindgren and Ford1997, data from Table 1 for age group 24–43 years; Hänninen and others 1998, data from Table 1 for subjects with BPb max >2.4; Schwartz and others Reference Schwartz, Lee, Lee, Stewart, Lee, Hwang, Ahn, Kim, Bolla, Simin, Parsons and Todd2001, data from Table 3; Schwartz and others Reference Schwartz, Lee, Bandeen–Roche, Stewart, Bolla, Links, Weaver and Todd2005,109; Dorsey and others Reference Dorsey, Lee, Bolla, Weaver, Lee, Todd, Shi and Schwartz2006, data from Table 2). The studies are relevant because their participants may approximate, although imperfectly, to the Franklin crew at the time of deserting the ships: their age distribution only slightly exceeds the crew's range of 21–52 (the range excludes Franklin himself who died before the desertion of the ships); the subjects have current occupational lead exposure and therefore bear comparison with the contaminated nineteenth-century population; the subjects are living in the community and apparently functioning normally.

Fig. 2. Tibia lead (μgPb/g) of four Franklin crew (Keenleyside and others Reference Keenleyside, Song, Chettle and Webber1996) compared to five present-day studies (means and 2 standard deviations: △ = inter-quartile range). Bleeker and others (Reference Bleeker, Lindgren and Ford1997); Dorsey and others (Reference Dorsey, Lee, Bolla, Weaver, Lee, Todd, Shi and Schwartz2006); Schwartz and others (Reference Schwartz, Lee, Bandeen–Roche, Stewart, Bolla, Links, Weaver and Todd2005): reproduced with permission of Wolters Kluwer Health / Lippincott, Williams & Wilkins, and American Academy of Neurology (Bleeker and others Reference Bleeker, Lindgren and Ford1997). Hänninen and others (Reference Hänninen, Aitio, Kovola, Luukonen, Matikainen, Mannelin, Erkkilä and Riihimäki1997): reproduced with permission of BMJ Publishing Group Ltd. Schwartz and others (Reference Schwartz, Lee, Lee, Stewart, Lee, Hwang, Ahn, Kim, Bolla, Simin, Parsons and Todd2001): reproduced with permission of Oxford University Press.

The very small sample of crew tibiae available for analysis is clearly a severely limiting factor and it would be inappropriate to attempt to construct a distribution from four data points in order to allow comparison with present-day studies. The authors sought to increase the sample size by including the four tibiae in the sample of Kowal and others (Reference Kowal, Krahn and Beattie1989) but, regrettably, the data could not be obtained. Their inclusion might, in any case, have introduced further uncertainty if it could not be determined whether the tibiae were from different individuals. Given these considerations, the tentative nature of the following discussion must be emphasised.

The levels of lead in the four individual tibiae from Keenleyside and others (Reference Keenleyside, Song, Chettle and Webber1996) are plotted in Fig. 2. It may reasonably be proposed that the tibiae of the remainder of the crew would be distributed around those four values with a positive skew as evident in Fig. 1, but where the end points of the range cannot be determined. In order to be consistent with the log scale employed in Fig. 1, the data for the present-day studies shown in Fig. 2 have been transformed from their original scales to a log scale. This transformation would seem appropriate because the prediction intervals on their original scales led to lower end points below 0, which is a clear indication that a normal model on several of these original scales is not appropriate. Schwartz and others (Reference Schwartz, Lee, Lee, Stewart, Lee, Hwang, Ahn, Kim, Bolla, Simin, Parsons and Todd2001: 455) have described how the procedure for estimating tibia lead can result in some values of less than zero. As the mean (μ) and SD (δ) on the log scale relate to the mean and variance on the original scale through the following formulae where ‘exp’ denotes the exponential function, the means and variances of the present-day studies were transformed by simple inversions of these formulae

(1)\begin{equation} {\rm Mean:}\,\exp \,(\mu + \delta^{2}/2) \end{equation}

(2)\begin{equation} {\rm Variance:}\,(\exp \,(\delta ^2 ) - 1)\,\exp \,(2\mu + \delta ^2 ) \end{equation}

The resultant means, confidence intervals and inter-quartile ranges are shown in Fig. 2.

It is evident that the crew's data points lie outside the upper quartiles of the present-day distributions, but they are encompassed by the confidence intervals of Schwartz and others (Reference Schwartz, Lee, Lee, Stewart, Lee, Hwang, Ahn, Kim, Bolla, Simin, Parsons and Todd2001, Reference Schwartz, Lee, Bandeen–Roche, Stewart, Bolla, Links, Weaver and Todd2005) and Dorsey and others (Reference Dorsey, Lee, Bolla, Weaver, Lee, Todd, Shi and Schwartz2006), and partially so by those of Bleeker and others (Reference Bleeker, Lindgren and Ford1997) and Hänninen and others (1998). It may be tentatively proposed that the association between high levels of tibia lead and cognitive function in the present-day studies may be broadly reflective of effects in crewmen having those same levels of lead. The study by Bleeker and others shows an overlap with the notional lower distribution of the crew: they found no relationship between tibia lead on cognitive performance in a sub-group of exposed workers who were broadly equivalent in age to the majority of the crew (<43 years of age). The study by Hänninen and others shows a similar overlap with the lower distribution of the crew and found no association between tibia lead and performance. There was, however, an association between blood lead and performance on tests of attention, verbal comprehension and visual and motor co-ordination. As there are no crew data for blood lead, this result will be considered later below. Thus, within the range of overlap of the two studies with that of the lower tibia lead levels of the crew, there is little evidence of associated cognitive impairment.

Fig. 2 shows the studies by Schwartz and others (Reference Schwartz, Lee, Lee, Stewart, Lee, Hwang, Ahn, Kim, Bolla, Simin, Parsons and Todd2001, Reference Schwartz, Lee, Bandeen–Roche, Stewart, Bolla, Links, Weaver and Todd2005) and Dorsey and others (Reference Dorsey, Lee, Bolla, Weaver, Lee, Todd, Shi and Schwartz2006) which involved longitudinal follow-up of a large cohort of lead-exposed workers. Early in the follow-up period, Schwartz and others (Reference Schwartz, Lee, Lee, Stewart, Lee, Hwang, Ahn, Kim, Bolla, Simin, Parsons and Todd2001) found no relationship between tibia lead and cognition, but a reliable association between blood lead and tests of speeded co-ordination and attention (discussed later). In later follow-up, significant associations were found between both tibia and blood lead and decrements in higher-order executive functions involving planning, decision-making, memory and manual dexterity (Schwartz and others Reference Schwartz, Lee, Bandeen–Roche, Stewart, Bolla, Links, Weaver and Todd2005).

In the case of Dorsey and others (Reference Dorsey, Lee, Bolla, Weaver, Lee, Todd, Shi and Schwartz2006), increasing levels of both tibia and blood lead were associated with slower reaction time and impaired executive function. It may be of particular relevance to the crew that the greatest adverse effect of lead was upon the task of ‘pursuit aiming’. Given that in the later stages of the expedition, and certainly after deserting the ships, the crew would have depended upon procuring fresh meat by hunting, any impairment of the ability to aim a weapon accurately would have had serious consequences.

The evidence that poorer cognitive test scores in present-day samples were associated with levels of tibia lead which overlapped with the lower distribution of that of the crew might imply that broadly similar effects would have been present in the crew. If so, then given that the subjects in the present-day cohorts were all employed and functioning normally in the community, it would appear that the degree of impairment due to lead, while statistically significant, is not of a nature or extent to impair everyday function. The matter of test sensitivity is relevant here. The studies cited above used sensitive neuropsychological assessments of the relationship between lead and cognitive function. They confirmed a significant inverse relationship that is consistent with the known effects of lead upon mid-brain structures and the occipital and frontal lobes (Hsieh and others Reference Hsieh, Chen, Li, Chiu and Chuang2009; Sanders and others Reference Sanders, Liu, Buchner and Tchounwou2009; Stewart and others Reference Stewart, Schwartz, Davatzikos, Shen, Liu, Wu, Todd, Shi, Bassett and Youssen2006). However, the sensitivity of such assessments means that whilst the effects are statistically significant, they may be subtle and not readily evident in everyday functioning. In this respect it is evident from the data tables of the studies cited above that the β coefficients describing the significant effects of lead upon cognition are often relatively small.

It is also relevant that whilst present-day studies confirm an overall significant relationship between lead and cognitive function, there is known to be marked individual variation in susceptibility to the effects of the metal. For example, great variability is clearly evident in the scatterplots relating tibia and blood lead to cognitive performance in the data of Schwartz and others (Reference Schwartz, Lee, Lee, Stewart, Lee, Hwang, Ahn, Kim, Bolla, Simin, Parsons and Todd2001: Figs. 1 and 2) and for tibia in the data of Stewart and others (Reference Stewart, Schwartz, Simon, Bolla, Todd and Links1999: Figs. a to k). Similar variability is evident in the results of Weisskopf and others (Reference Weisskopf, Wright, Schwartz, Spiro, Sparrow, Aro and Hu2004: Figs. 1 and 2) in an older group of lead-exposed workers. Earlier research has also shown an obvious overlap in cognitive performance between lead-exposed and non-exposed workers (Baker and others 1984) and that even when performance is ‘significantly’ impaired relative to a non-exposed group it may remain within the normal range of function (Grandjean and others Reference Grandjean, Arnvig and Beckmann1978). On this evidence, the proportion of the crew with levels of tibia lead within the upper range of the present-day samples shown in Fig. 2 may have experienced effects of lead on their cognitive function that would not be incapacitating.

The considerations above would lead to the conclusion that members of the crew whose tibia lead exceeds that of the present-day samples would have suffered proportionally greater impairment. Whether such impairment would have been associated with frank incapacity must be considered in light of the variability already noted in the studies above and the very high individual levels of tibia lead also reported by Schwartz and others and Dorsey and others in their apparently normally-functioning subjects. For example, the range of tibia lead reported by Schwartz and others (Reference Schwartz, Lee, Bandeen–Roche, Stewart, Bolla, Links, Weaver and Todd2005: 109) extended to 338 μgPb/g which would encompass a large proportion of the crew's estimated tibia lead shown by the shaded area in Fig. 1. Equally, however, when considered in population terms, the cognitive function of a proportion of individuals is likely to be affected at such levels and it would be reasonable to conclude that some of the crew would have experienced a decline in function.

Blood lead and neurocognitive and physical morbidity

Tibia lead reflects the individual's long-term exposure to, and accumulation of, the metal. However, the level of lead currently circulating in the blood, and thus having the potential to exert immediate effects upon the brain and other organs, may be a more relevant metric (Shih and others Reference Shih, Hu, Weisskopf and Schwartz2007). It was noted above that several of the present-day studies found associations between blood lead and cognition in the absence of tibia-lead associations. The difficulty with respect to the Franklin expedition is that there are no blood-lead data for the crew, but Keenleyside and others (Reference Keenleyside, Song, Chettle and Webber1996) estimated blood lead from the tibia data shown in the present Fig. 2. Their estimate was based on evidence that a blood-lead concentration of 20 μgPb/dl would increase tibia lead by 1 μg if maintained for 1 year (after Cake Reference Cake1994 unpublished). Whilst Hu and others (Reference Hu, Shih, Rothenberg and Schwartz2007) have largely confirmed the latter relationship, there is evidence of non-linearity in the association between tibia lead and blood lead so that prediction of the latter must be considered cautiously (Healy and others Reference Healy, Chettle, McNeill and Fleming2008; Schwartz and others Reference Schwartz, Hu, Rothenberg and Todd2008). Keenleyside and others (Reference Keenleyside, Song, Chettle and Webber1996) postulated what might be termed a ‘worst-case’ assumption that one half of the lead in the four tibiae (range 60–150 μgPb/g) had been accumulated during the three years of the expedition (thus approximating to one half of the range, i.e. 30–75 μgPb/g). On the basis of this assumption, the blood-lead equivalent was then calculated to be 600–1500 μgPb/dl, which would correspond to blood lead during the expedition of 200-500 μgPb/dl/year which, as Keenleyside and others concluded, would represent significant lead poisoning.

However, the assumption that one half of the crew's lead burden was accumulated over three years would require a source of considerable lead contamination over and above the background level present as part of nineteenth-century life aboard ship. This has prompted a speculative search for a possible source which would be sufficiently potent. One such could have been the ships’ ‘soft’ drinking water which would dissolve lead from storage tanks and pipes (Battersby Reference Battersby2008; Battersby and Carney Reference Battersby and Carney2011; Farrer Reference Farrer1993). However, the assumption that half of the total lead burden was incurred during the three-year expedition has the problematic corollary that the other half must have been accumulated over a preceding median lifetime of 29 years (the median age of the crew at the time of embarking on the expedition). If so, then, following the calculation procedure of Hu and others (Reference Hu, Shih, Rothenberg and Schwartz2007: 458), the accumulation would correspond to an annual blood-lead range of only 21–52 μg/dl, the lower range of which falls well below current recommended exposure limits in the United Kingdom (>50 μg/dl requires remedial action; >60 μg/dl requires suspension of a worker from duties: Health and Safety Executive 2012). The range would seem implausibly low in light of the known lead contamination of nineteenth-century Britain.

Given this difficulty, a parsimonious assumption would be that lead accumulated at largely the same rate prior to, and during, the expedition. It would seem plausible that the well-recognised sources of lead contamination on land and during employment on previous voyages (that is ingestion via food, tableware and drinking vessels, water supplies, atmospheric dust etc.) would be largely replicated during the expedition. When re-calculated on this basis, the estimate of blood-lead range at the time of deserting the ships is 38–94 μgPb/dl (median years of accumulation being 32 years by that time). The latter range certainly exceeds current United Kingdom exposure recommendations and would be consistent, at higher levels, with the degree of blood-lead-related reduction in cognitive function observed in present-day studies (Hänninen and others 1998; Schwartz and others Reference Schwartz, Lee, Bandeen–Roche, Stewart, Bolla, Links, Weaver and Todd2005; Dorsey and others Reference Dorsey, Lee, Bolla, Weaver, Lee, Todd, Shi and Schwartz2006).

A tentative insight to the possible distribution of blood lead in the crew, and its associated physical effects, is provided in Fig. 3. The blood-lead equivalents (median 32-year lifetime) of the four tibiae lead levels available to this analysis (from Keenleyside and others Reference Keenleyside, Song, Chettle and Webber1996, as described above) were calculated after Hu and others (Reference Hu, Shih, Rothenberg and Schwartz2007) and are shown as single points along the X axis in Fig. 3. The figure also shows the gradual increase in type and severity of symptoms as blood lead increases from 10 to 80 μgPb/dl and beyond (adapted from Kosnett and others Reference Kosnett, Wedeen, Rothenberg, Hipkins, Materna, Schwartz, Hu and Woolf2007: Table 1). Given that there are only four data points, and that these are themselves estimates rather than objectively-determined levels of blood lead, it was thought highly inappropriate to construct yet another estimate of the distribution of blood lead across the crew. Rather, following the example of Fig. 2 above, on the basis of visual inspection of Fig. 3 it may reasonably be proposed that the blood levels of the crew would be distributed around those four points but that the minimum and maximum values of the range cannot be determined.

Fig. 3. Symptoms associated with increasing levels of blood lead (μgPb/dl) adapted with permission from Kosnett and others in Environmental Health Perspectives 2007; 115 (3): 463-471. ● = blood-lead levels calculated from the four tibiae of the Franklin crew. The United Kingdom's Health and Safety Executive's (2012) recommended blood-lead thresholds for ‘action’ and ‘suspension’ of a worker are also shown for contemporary comparison.

Fig. 3 shows that symptoms of lead intoxication become more likely as blood lead levels rise above approximately 40 μgPb/dl, but one should note that the latter level is not a threshold at which symptoms must immediately appear. High levels of blood lead are not inevitably associated with the symptoms shown in Fig. 3 and it has been noted that clinical symptoms may rarely be seen below 60 μg/dl (Needleman Reference Needleman2004). It may tentatively be proposed that a proportion of the crew whose blood lead was below 60 μgPb/dl would have experienced few subjective ill-effects or mild to moderate symptoms including those classically associated with chronic lead exposure such as hypertension, mild headache and gastric disturbance. A proportion of these men would have had blood-lead levels at the thresholds of the United Kingdom Health and Safety Executive's (2012) current recommendations for investigative action or suspension of a worker. Equally, those whose blood lead exceeded some 80 μgPb/g would be at increasing risk of more serious morbidity including neuropathies, severe colic and anaemia (Gordon and others Reference Gordon, Taylor and Bennett2002).

The very limited data available make it is impossible to draw conclusions from Fig. 3 as to the proportions of men who might have suffered particular symptoms. Conclusions would, in any case, be uncertain in view of the long-standing clinical observation that a degree of tolerance develops to chronic lead exposure and that there is ‘substantial inter-individual variability in susceptibility to symptomatic adverse effects’ (Kosnett and others Reference Kosnett, Wedeen, Rothenberg, Hipkins, Materna, Schwartz, Hu and Woolf2007: 464). A final difficulty concerns the fact that the estimation of blood lead uses the duration of exposure (that is age) as a denominator in the calculation. Here, the median crew age of 32 years at desertion of the ships has been used because there is no information as to the age of the men whose tibiae are involved. However, it is readily seen that the blood-lead equivalent calculated for any given tibia would be substantially lower if the man were one of the oldest of the crew, and substantially higher if he were one of the youngest. Such unknown factors conspire with the limited data available to render conclusions highly tentative.

Factors moderating the effects of lead

Final consideration can be given to four factors that might have contributed to individual variation in debility by exacerbating or mitigating the effects of lead.

Nutritional deficiencies

The fact that many of the crew appeared to have died within a short distance of deserting the ships has been taken as evidence for marked debility at that time. Similar debility was recorded on other Arctic missions, particularly when more than two winters had been endured. Nutritional deficiencies were often to blame and vitamin C deficiency commonly led to scurvy (for example Armstrong Reference Armstrong1853; Robertson Reference Robertson1849). The state of provisions at the time of deserting the Erebus and Terror is unknown. The expedition was supplied with lemon juice as an antiscorbutic agent but Cyriax (Reference Cyriax1939) proposed that storage conditions and time reduced its effectiveness and caused widespread scurvy, although this has been cast in doubt by Mays and others (Reference Mays, Maat and De Boer2013) on the basis of their evaluation of skeletal evidence. A daily minimum of 10mg of vitamin C will preclude scorbutic symptoms in men engaged in light work (Pemberton Reference Pemberton2006) and may have been sufficient when idle whilst beset, but men sent on sledging expeditions would have required more. Vitamin C is relevant to lead exposure because serum levels of ascorbic acid are inversely related to blood lead, probably due to altered intestinal absorption and renal clearance (Cheng and others Reference Cheng, Willett, Schwartz, Sparrow, Weiss and Hu1998; Dawson and others Reference Dawson, Evans, Harris, Teter and McGanit1999; Simon and Hudes Reference Simon and Hudes1999).

Vitamin D is associated with increased levels of blood lead in winter. The mechanism is complex (see Cheng and others Reference Cheng, Willett, Schwartz, Sparrow, Weiss and Hu1998; Onalaja and Claudio Reference Onalaja and Claudio2000; Sanders and others Reference Sanders, Liu, Buchner and Tchounwou2009) but a factor of relevance to the expedition is that of exposure to sunlight in the body's synthesis of vitamin D. Oliveira and others (Reference Oliveira, Aro and Hu2002) propose that reduced sunlight in winter leads to lower levels of vitamin D which, in turn, result in increased resorption of lead from bone into the blood. The crew's ‘last’ winter of 1847–1848 involved more than two months of darkness so that an increase in blood lead in men with existing high levels may have exacerbated other physical morbidity and contributed to a debilitated state when the ships were deserted in April 1848.

Stress

The effect of lead on cognition is exacerbated by stress, putatively because both activate the hypothalamic-pituitary axis to release cortisol which is associated with impaired cognitive function (Peters and others Reference Peters, Weissfopf, Spiro, Schwartz, Sparrow, Nie, Hu, Wright and Wright2010; Virgiolini and others Reference Virgiolini, Chen, Weston, Bauter and Cory-Slechta2005). Increasing stress during the final months preparing to desert the ships may have contributed to debility in those with a higher lead burden.

Genetic factors

The adverse neurocognitive effects of lead are greater in individuals who carry the ε4 allele of the apolipoprotein E gene which is implicated in elevated deposition of β-amyloid in the brain (Stewart and others Reference Stewart, Schwartz, Simon, Kelsey and Todd2002). We have confirmed modest effects of the allele which are less evident in younger age (Millar and others Reference Millar, Nicoll, Thornhill, Murray and Teasdale2003). Given a median crew age of 32 years at desertion of the ships, and that some 30% of the population carry the ε4 allele, the number potentially affected would be small. Complex genetic influences upon variables affecting the accumulation of lead have also been proposed via effects including carrier proteins for lead in the blood, and vitamin D synthesis, but are beyond discussion here (see Scinicariello and others Reference Scinicariello, Yesupriya, Chang and Fowler2010). Whilst there has been much attention devoted to factors influencing the accumulation of lead, The Editor of this journal has also observed that individual variation in excretion of lead may be highly relevant. Support for this proposal is found in the observation by Barbosa and others (Reference Barbosa, Tanus–Santos, Gerlach and Parsons2005) that individual variation in the burden of body lead may be wrongly attributed to exogenous sources when, in fact, it reflects inter-individual variation in physiological processes involved in urinary and faecal excretion of the metal.

Cognitive reserve

One factor may have been protective. Individuals vary in their degree of ‘cognitive reserve’ (Reed and others Reference Reed, Mungas, Tomaszewski Farias, Harvey, Beckett, Widaman, Hinton and DeCarli2010) which buffers the brain against the harmful effects of physical injury and some neurotoxins, and is positively associated, in part, with longer education, higher occupational status and intellect. Cognitive reserve protects against effects of chronic lead exposure on higher mental functions (Bleecker and others Reference Bleeker, Ford, Celio, Vaughan and Lindgren2007) and may therefore have afforded some men a degree of protection from the cognitive effects of lead and other debilitating conditions. If some of those men were officers then there might have been positive implications for planning and morale, at least in the short term.