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Depleted uranium and radiation-induced lung cancer and leukaemia

41 Ewhurst Avenue, Sanderstead, South Croydon, Surrey CR2 0DH, UK

	Introduction

Top Introduction Uranium and depleted uranium Radiation-induced lung cancer Radiation-induced leukaemia Lung cancer and leukaemia... Iraqi cancer statistics Depleted uranium in the... References

 
Reports of leukaemias and other cancers among servicemen who took part in the 1991 Gulf War or in the more recent operations in the Balkans are of continuing interest, as is the possibility, however slight, that depleted uranium (DU) is one of the causative factors. This commentary includes the results of a UK epidemiological study on the mortality of Gulf War veterans and, although not containing information on DU exposure, gives data on overall levels of mortality and therefore carries more weight than anecdotal reports. Also included are brief summaries on radiation-induced lung cancer in uranium workers as well as radiation-induced leukaemia in Japanese atomic bomb survivors and patients with ankylosing spondylitis treated using X-rays. This commentary concludes with a critique of Iraqi cancer statistics as well as giving information on environmental contamination in Kosovo and the use of DU ammunition.

	Uranium and depleted uranium

Top Introduction Uranium and depleted uranium Radiation-induced lung cancer Radiation-induced leukaemia Lung cancer and leukaemia... Iraqi cancer statistics Depleted uranium in the... References

 
The long-lived naturally occurring element uranium has three radionuclides. It has been used since the 1940s principally in the atomic energy industry, where reactor fuel rods are composed of refined ²³⁵U (half-life 704 x 10⁶ years), and the waste product from this refining is DU, which is predominantly ²³⁸U (half-life 4470 x 10⁶ years). Another radionuclide is ²³⁴U (half-life 245 000 years). The relative abundances of ²³⁸U, ²³⁵U and ²³⁴U are, respectively, 99.2745%, 0.7200% and 0.0055%. Typically, DU contains some 0.2% of the fissionable ²³⁵U. The density of metallic uranium is 19.05 g cm^-3, higher than that of lead (11.3 g cm^-3).

Uses of DU
Owing to the high density of metallic uranium, DU has been used for the last 20 years in the manufacture of armour and armour piercing shells in several countries. It has also been used as counterweights in wide-body aircraft such as the DC-10 and the Boeing 747, and for shielding in teletherapy machines. Prior to this use of DU, in 1953 the British Journal of Radiology [1], describing a modification to a radium bomb to accommodate a ⁶⁰Co source, was the first to publish on the use of uranium for radiotherapy shielding.

Pyrophoricity
Uranium metal is combustible and readily ignites when finely divided in air, a property known as pyrophoricity. Hence, when used militarily, or when present in an air crash or a fierce fire, the uranium may form large quantities of dust containing a mixture of uranium oxides that can be ingested or inhaled. For example, the Boeing 747 that crashed into a block of flats in Amsterdam in 1992 carried 282 kg of DU counterweights but only 130 kg was recovered and the Dutch commission of enquiry concluded that the remaining amount had been released in the form of particles that could have been inhaled by rescue workers and the local population [2].

Chemical toxicity
A detailed toxicological profile for uranium has been published by the Agency for Toxic Substances and Disease Registry [3]; information is also available from the World Health Organisation in their recent report [4]. Both reports show that, without doubt, the major hazard from DU is chemical rather than radiological.

The kidney is the organ primarily affected by ingested uranium [3–5] and dysfunction caused by uranium chemical toxicity has been proven in both animal and human populations. In terms of Gulf War syndrome, which is described as a spectrum of symptoms and medical disorders, not only those related to the kidney, there are likely to be a combination of causative factors and not just the single factor of DU exposure. One study [6] has concluded that uranium intake in the range 0.004–9 µg kg^-1 body weight affects kidney function in a dose-dependent manner.

Measurement of uranium in urine
The standard test to determine the presence of uranium in the body is a urine test. In a study of 29 DU-exposed American Gulf War veterans and 22 non-exposed veterans, spot samples and 24 h samples were collected and analysed for uranium determination, and it was found that there was a high correlation of spot collection measurements when corrected for creatinine concentration with the 24 h creatinine standardized collection [7]. However, the correlation declines with urinary uranium values below 0.05 µg g^-1 creatinine. This suggests that reliance on spot samples for presumed low level uranium exposed populations may not be advisable [7]. This is an important finding for screening programmes and it is generally regarded that the most reliable data from urine analysis are obtained from samples collected over a 24-h period and corrected for creatinine excretion [8].

To demonstrate that exposure to DU has taken place it is necessary to determine the ratio of the three uranium isotopes in urine; if there is DU present there will be an unusually low proportion of ²³⁵U since DU contains only some 0.2% of this isotope whereas natural uranium contains 0.72%. Isotope ratio analysis can be performed using inductively coupled plasma mass spectrometry (ICPMS) [9], and it is suggested that the limit of detection is of the order of 10–35 ng l^-1 [8]. However, the most sophisticated form of uranium isotope analysis, able to quantify smaller uranium isotope concentrations than any other test, is thermal ionization mass spectrometry (TIMS). TIMS is used in geochemical research but has yet to be validated for biological specimens, whereas ICPMS has already been validated [8].

Measurement of uranium in bone
As a result of its ionic characteristics, UO₂²⁺ competes with Ca²⁺ for certain transport mechanisms and is rapidly accumulated in bone [10]. Approximately 66% of the total body burden of uranium is estimated to reside in the skeleton [11–13], with clearance half-lives reported in the range 300–5000 days based on a two compartment pharmacokinetic model [14, 15]. Recent advances in the determination of trace metals in bone using K X-ray fluorescence have suggested a role for this technique in uranium analysis [16].

Radiological toxicity
There does exist, albeit small compared with chemical toxicity, a radiological toxicity, which, because of the relatively low doses experienced by military veterans, is difficult to quantify as individual radiation dose measurements at the levels required have not yet become available. It has recently been suggested that electron paramagnetic resonance dosimetry of tooth enamel can be used for measurements down to 20 mSv [17].

Radiation doses will be dependent on several factors, such as the type and pathway of exposure (i.e. external or internal), the situation (e.g. within tanks hit by DU shells or during DU artillery shell manufacture) and whether the DU has lodged in the lungs as oxides or as uranium metal. The UK Defence Committee 7th Report "Gulf Veterans Illnesses" [18] states "When DU hits a target a fine aerosol of ceramic DU is formed. Many of the particles, figures vary from 46% to 70%, are less than 10 micron. This means that they are readily inhaled. Particles under 2.5 micron are particularly dangerous as they enter deep into the lungs".

	Radiation-induced lung cancer

Top Introduction Uranium and depleted uranium Radiation-induced lung cancer Radiation-induced leukaemia Lung cancer and leukaemia... Iraqi cancer statistics Depleted uranium in the... References

 
Uranium miners and radon exposure
Studies of several groups of uranium miners have been conducted over many years in the USA, Canada and the Czech Republic¹. Data from these studies have been the subject of several detailed reviews, including that by the USA National Research Council Committee on Biological Effects of Ionizing Radiation [19]. In common with earlier reviews, this committee concluded that exposure to radon progeny in uranium mines was a cause of lung cancer. In addition, studies on uranium miners have been running in France and Australia, but for a shorter period than studies in the countries quoted above.

View larger version (198K): [in this window] [in a new window]   Figure 1. Woodcut dated 1518 showing a doctor and nurse attending a sick miner in Joachimsthal's hospital. Mining activity can be seen in the background. In the early 1780s the pharmacist Martin Klaproth, who later became Professor of Chemistry at Berlin's Royal Mining Academy, discovered that the black mineral could be used to give glass a brilliant yellow colour and he was also convinced that it contained a new metal. This coincided with the 1781 discovery by William Herschel of a new planet in the solar system, Uranus, and uranium was thus named in honour of the planet by Klaproth. (Courtesy of Dr Fathi Habashi and Dr Adrian Thomas.)

View larger version (142K): [in this window] [in a new window]   Figure 2. The Schneeberg mines in the ore mountains (Erzgebirge) of Saxony. The photograph was taken circa 1946–47 in the period known as the wild years when the mining techniques were primitive. In German textbooks on the aetiology of lung cancer, as far back as 1879 [21] the term Schneeberg lung cancer is mentioned and the ore Pechblende, dumped in vast quantities on slag heaps as a waste material, obtained its name because of Pech used in the context of "bad luck". (Courtesy of Dr Horst Wesch.)

Uranium-associated industries and uranium exposure
A recent report by a committee of the United States National Academy of Sciences Institute of Medicine [24] on "Gulf War and Health" reviewed studies of several uranium-associated industries: uranium mill workers, uranium enrichment workers, uranium processing and laboratory workers, and nuclear materials fabrication workers. The committee concluded that "there is limited/suggestive evidence of no association between exposure to uranium and lung cancer at cumulative internal dose levels lower than 200 mSv or 25 cGy. However, there is inadequate/insufficient evidence to determine whether an association does or does not exist between exposure to uranium and lung cancer at higher levels of cumulative exposure."

The committee [24] also repeated the BEIR VI [19] opinion regarding studies on uranium miners that "the effect of uranium is difficult to interpret because the miners were simultaneously exposed to radon progeny". Another confounding factor when trying to determine the relative effect of uranium is the lack of direct information on individual workers' exposure to cigarette smoke.

	Radiation-induced leukaemia

Top Introduction Uranium and depleted uranium Radiation-induced lung cancer Radiation-induced leukaemia Lung cancer and leukaemia... Iraqi cancer statistics Depleted uranium in the... References

 
Hiroshima and Nagasaki
It is known from atomic bomb data that leukaemia can be radiation induced. Estimates from the Japanese data [25] showed that the latency period was some 2.5 years, an increased incidence was suspected during the following 2.5 years and this was clearly observed 5 years after the atomic tomb. However, since comprehensive follow-up of the Japanese atomic tomb survivors did not begin until 5 years after the bombings, these data cannot be solely relied upon to infer a latency for leukaemia.

Ankylosing spondylitis
Ankylosing spondylitis is a non-malignant disease that has been treated using X-rays. In 1965, Brown and Doll [26] investigated the mortality from cancer and from other causes in a series of patients from 81 radiotherapy centres treated between 1935 and 1954. They reported an excess of deaths from leukaemia and aplastic anaemia following treatment and that deaths attributed to cancers in heavily irradiated areas increased approximately two-fold at 6–15 years following treatment. A further analysis of this patient population was made in 1982 by Smith and Doll [27], who took into account estimated organ radiation doses for 14 111 spondylitics treated by a single course of X-rays.

The most recent reference to leukaemia in this population was by Weiss et al in 1995 [28]. These authors found after follow-up to 1 January 1992 that leukaemia-related deaths among the irradiated patients was almost three times that expected from national rates. They also found that the ratio of observed to expected deaths for leukaemia (other than chronic lymphocytic leukaemia (CLL)) was greatest in the period 1–5 years after initial treatment. In addition, using a linear-exponential model they estimated that the average predicted relative risk of leukaemia other than CLL in the period 1–25 years after exposure to a uniform dose of 1 Gy was 7.00.

	Lung cancer and leukaemia in Gulf War veterans

Top Introduction Uranium and depleted uranium Radiation-induced lung cancer Radiation-induced leukaemia Lung cancer and leukaemia... Iraqi cancer statistics Depleted uranium in the... References

 
Reported cases of lung cancer and leukaemia in veterans are mainly anecdotal and not the result of well designed epidemiological surveys. No significantly higher than expected incidence of these two neoplasms has yet been proven. The report of the United States National Academy of Sciences Institute of Medicine [24] and their conclusions regarding exposure to uranium, lung cancer and internal dose levels has already been referred to. This report does not even list leukaemia in its index as a topic of importance, emphasizing that no evidence of a link between DU and leukaemia has yet been found.

American friendly fire victims
A surveillance study is in progress for American Gulf War veterans who were victims of "friendly fire" from DU ammunition. The study initially included 30 veterans but this has now risen to 60. Approximately 15 veterans still have DU fragments in their soft tissues and are excreting raised concentrations of uranium in their urine. None has lung cancer or leukaemia [29, 30].

Mortality study of Gulf War veterans
In a report by Macfarlane et al [31] on mortality among some 53 000 UK Gulf War veterans, with follow-up to 31 March 1999, it was found that although the veterans experienced higher mortality rates than a comparison group, this excess mortality rate is very small and doesnot approach statistical significance. An equivalent-size comparison group (the Era cohort) comprised personnel who were not deployed but who were matched for age, sex, rank, service and level of fitness. The excess mortality is mainly related to accidents rather than disease. This pattern is consistent both with American veterans of the Gulf War and veterans from other conflicts.

The study has now been updated to 30 September 2000 [32], but at the time of writing data have only been presented at a conference. The data show little change from the earlier follow-up [31] and the excess deaths attributed to accidental causes, motor vehicle accidents in particular, are still present. This update also shows that there are fewer deaths due to neoplasms among the Gulf cohort than among the Era cohort. In this latest follow-up, Blatchley et al [32] have presented for the first time a breakdown of the different types of cancer (Table 1). However, because the number of deaths due to individual cancers is so small, it is too early to draw any conclusions other than that there is no evidence at present to claim that there are excessive deaths due to cancers among UK Gulf War veterans.

	Iraqi cancer statistics

Top Introduction Uranium and depleted uranium Radiation-induced lung cancer Radiation-induced leukaemia Lung cancer and leukaemia... Iraqi cancer statistics Depleted uranium in the... References

Patient workload statistics in Mosul
The total number of all cancer registrations in Mosul hospitals for the two periods 1989–90 and 1997–98 were 200 and 894, respectively. Numbers for lung cancer in males were, respectively, 20.5% (25/122) and 25.7% (129/501) and for females they were 2.6% (2/78) and 3.6% (14/393). Corresponding figures for leukaemia for males and females combined were 11% (22/200) for 1989–90 and 10.6% (95/894) for 1997–98. These are percentage workload figures and cannot be equated to cancer incidence figures per 100 000 population for Mosul and its surrounding region. The percentages are similar for the two time periods and there could be several reasons for the increase in absolute numbers. Certainly they cannot be correlated with DU exposure as is sometimes reported in the media. Following a visit to Iraq, Sikora [35] has commented in general on these increases: "stomach cancer is increasing probably due to poor diets and the lack of food storage facilities" and "there is an apparent threefold increase in leukaemia in the southern provinces, the sites of the major battlefields of the Gulf War".

Military statistics
The 1998 report [34] also gives the annual absolute numbers of lung cancers for 1991–97 in "military personnel exposed to a DU explosion" as 4, 6, 39, 40, 41, 40 and 40, and for leukaemia as 10, 28, 45, 53, 65, 70 and 40. The cohort studied, including military and non-military, totalled 1425. However, although this is described as a case control study, the control data are not included in the report, the case and control populations are not properly defined and the data quality must be regarded as poor.

Possible influence of chemical carcinogens
The increase in the number of Iraqi cancer registrations may be due in part to exposure to chemical carcinogens. Of relevance to war is the agent benzene, which has been established as an occupational cause of acute myeloid leukaemia [36]. This is relevant on battlefields since the advent of mechanized warfare because the residues include partially burnt hydrocarbons from fuels, explosives, propellants and plastics. For the Gulf War, there is also the Kuwait oil fires to take into consideration. The retreating Iraqi forces set the Kuwait oil fields alight and the smoke generated was carried by the prevailing winds over Iraq. The types and quantities of soot formed were known to have caused lung damage [36] and, in addition, the soot would have contained large quantities of polycyclic aromatic hydrocarbons, known carcinogens. It is not known where Iraqi chemical and biological weapons stockpiles were sited and whether any were blown up, but certainly chemical warfare was used in the Iraq–Iran war of 1981–88, sulphur mustard being one of the agents. The long-term effects of exposure are known to include damage to the immune system, birth defects and elevated incidences of leukaemia and lymphoma.

	Depleted uranium in the Balkans

Top Introduction Uranium and depleted uranium Radiation-induced lung cancer Radiation-induced leukaemia Lung cancer and leukaemia... Iraqi cancer statistics Depleted uranium in the... References

 
In the March–June 1999 Kosovo conflict, oil refineries, fuel storage facilities and fertiliser plants were extensively damaged and the subsequent environmental contamination will have to be considered when the causes of health effects are assessed. Environmental "hot spots" were found in four cities: Pancevo, Kragujevac, Novi Sad and Bor. It was also reported that "it has occasionally been difficult to separate some of the earlier environment and health problems from those caused as a result of the recent conflict" [37]. Significant contamination was found from mercury, dioxin and other toxic pollutants, some of which had built up over a period of years.

DU shells were fired from American A-10 aircraft, but it is not known [37] whether the cruise missiles that were fired contained DU. According to the United Nations Environment Programme and the United Nations Centre for Human Settlements Balkans Task Force [37], "the present state of knowledge regarding DU use in Kosovo and possibly in Serbia is that neither the quantity of DU weapons used, nor the locations of any targets hit by DU weapons, are known". However, some information was later provided ina February 2000 letter to the UN Secretary General from the NATO Secretary General in which it was stated that 31 000 rounds of DU ammunition were used, containing a total of 8401 kg of DU, but also that "at this moment it is impossible to state accurately every location where DU ammunition was used".

	Acknowledgments

 
I would like to thank Dr Pat Doyle, Mr Richard Guthrie, Dr Gennadi Souchkevitch and Dr Horst Wesch for valuable discussions and for providing useful references, and Mr Nick Blatchley for a copy of his conference poster presentation including data on cancer mortality of Gulf veterans [32] from which Table 1 has been reproduced. I am also grateful to Brigadier Louis Lillywhite for the Ministry of Defence document on the Voluntary Screening Programme [8].

	Footnotes

 
¹Some British Journal of Radiology readers will be aware that the modern-day Czech Republic includes the silver mines at Joachimsthal (Figure 1) from which Marie and Pierre Curie obtained the many tons of pitchblende uranium ore that were processed to discover the radioactive elements polonium and radium in 1898. The mines were in use from the mid-12th century, also producing bismuth, cobalt, nickel and tungsten, and after World War II the Soviet authorities re-opened them to mine uranium, with many of the miners being Stalin's political prisoners. The name Joachimsthal, now Jácymov, is associated with a silver coin, the thaler, of which more than two million were minted in 1520–1528. The currency name dollar is directly derived from this ancient name.

²Cumulative radiation exposure given in working level months (WLMs), where a working level (WL) is defined as 1.3 x 10⁵ MeV of potential alpha energy per litre of air. 1 WLM equals exposure to 1 WL for 170 h [22].

Received for publication January 23, 2001. Accepted for publication May 16, 2001.

	References

Top Introduction Uranium and depleted uranium Radiation-induced lung cancer Radiation-induced leukaemia Lung cancer and leukaemia... Iraqi cancer statistics Depleted uranium in the... References

 

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