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Mortality among UK Gulf War veterans
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Mortality among UK Gulf War veterans Gary J Macfarlane, Elaine Thomas, Nicola Cherry
Summary Background Armed forces personnel who served in the Gulf War report more current ill-health than those who were not deployed. There has been concern expressed that they may also experience higher mortality rates. Methods A retrospective cohort study was done including all 53 462 UK Gulf War veterans (Gulf cohort) and a comparison group equivalent in size of personnel who were not deployed but matched for age, sex, rank, service, and level of fitness (Era cohort). Individuals were identified on central registers of the Office for National Statistics and information on death among cohort subjects, including cause of death, obtained. Follow-up extended from April 1, 1991 (the end of the Gulf War) until March 31, 1999. Findings There were 395 deaths among the Gulf cohort and 378 deaths amongst the Era cohort (mortality rate ratio [MRR] 1·05, 95% CI 0·91–1·21). Mortality from “external” causes was higher in the Gulf cohort (Gulf 254, Era 216; MRR 1·18 [0·98–1·42] while mortality from “disease-related” causes was lower (Gulf 122, Era 141; 0·87 [0·67–1·11]). The higher mortality rate from “external” causes in the Gulf cohort was principally due to higher mortality rates from accidents. There was, however, no excess of deaths recorded as suicide in the Gulf cohort. Interpretation This follow-up of veterans of the Gulf war has shown, 8 years after the end of the conflict, that although they have experienced higher mortality rates than a comparison cohort, the excess mortality rate is very small and does not approach statistical significance. The excess is related mainly to accidents rather than disease, a pattern that is consistent both with US veterans of the Gulf war and veterans from other conflicts. Lancet 2000; 356: 17–21
Unit of Chronic Disease Epidemiology (Prof G J Macfarlane PhD), Arthritis Research Campaign Epidemiology Unit (Prof E Thomas MSc); and Centre for Occupational and Environmental Health (Prof N M Cherry MD), School of Epidemiology and Health Sciences, University of Manchester, UK Correspondence to: Prof Gary J Macfarlane, Unit of Chronic Disease Epidemiology, School of Epidemiology and Health Sciences, Medical School, University of Manchester, Oxford Road, Manchester M13 9PT, UK (e-mail: [email protected])
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Introduction There has been concern that armed forces personnel who served in the Gulf War during 1990–91 are currently experiencing an excess of ill-health. Studies among UK forces who served in the Gulf show that they do report more current ill-health than veterans who were not deployed.1 The excess of ill-health spans a wide range of symptoms. Studies are on-going to find out whether deployment is associated with adverse reproductive outcomes and ill health among offspring. During deployment in the Gulf, troops from the UK encountered a variety of environmental and physical exposures including smoke from oil-well fires, pesticides, nerve agent prophylaxis, and multiple inoculations.1 In addition, adverse psychological experiences such as seeing maimed soldiers and dismembered bodies, and the threat of chemical attack have also been reported as common.1 There is concern that not only may veterans be experiencing more illhealth as a result of such exposures but that they may also have higher mortality rates. This study documents the mortality experience of 53 462 UK Gulf War veterans in the 8 years since the end of the war.
Methods A retrospective cohort study was conducted, including all UK armed forces personnel who served in the Gulf at some time between September, 1990, and June, 1991 (the “Gulf” cohort). The geographical definition of the Gulf area varied according to the service and was determined by the Ministry of Defence. It included all army personnel whose theatre of service during this period was Kuwait, Muscat and Oman, Qatar, United Arab Emirates, Bahrain, Saudi Arabia, Iraq, Iran or Operation Granby. Royal Air Force personnel were included if they had served in the Saudi Arabian peninsula, and Royal Navy personnel if they had served on board a ship east of the Suez during the defined period. In addition, a comparison group of the same number of armed forces personnel was identified (the “Era” cohort). These individuals were recorded on military personnel records as being in service on Jan 1, 1991, but they did not serve in the Gulf. Selection was random but stratified to match the Gulf cohort on age (within a 5year age group), sex, service (army, Royal Navy, Royal Air Force) and rank (commissioned officer/other ranks). For the army and Royal Air Force, Gulf and Era cohorts were also matched on their level of fitness for service and their status as regulars or reservists. Individuals in both the Gulf and Era cohorts were identified by the Ministry of Defence. Information provided for each cohort member included age (at Jan 1, 1991), sex, armed forces service, rank and date of joining and leaving the armed forces (where applicable). Details of everyone in both cohorts were sent, by the Ministry of Defence, to the Office for National Statistics (ONS) for identification on the National Health Service
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ARTICLES
Gulf cohort Sex Male Female Age (years) <20 20–24 25–29 30–34 35–39 >39 Rank Officer Other ranks Service branch Army Royal Navy Royal Air Force Era cohort Sex Male Female Age (years) <20 20–24 25–29 30–34 35–39 >39 Rank Officer Other ranks Service branch Army Royal Navy Royal Air Force
Identified*
Not identified*
Total
50 860 (97·4%) 1098 (88·9%)
1367 (2·6%) 137 (11·1%)
52 227 1235
6189 (97·1%) 18 447 (97·2%) 12 511 (97·2%) 7689 (97·5%) 4240 (97·5%) 2882 (96·4%)
187 (2·9%) 541 (2·8%) 363 (2·8%) 197 (2·5%) 107 (2·5%) 109 (3·6%)
6376 18 988 12 874 7886 4347 2991
5819 (97·7%) 46 139 (97·1%)
137 (2·3%) 1367 (2·9%)
5956 47 506
36 456 (97·4%) 5753 (96·5%) 9749 (96·9%)
978 (2·6%) 211 (3·5%) 315 (3·1%)
37 434 5964 10 064
50 099 (95·9%) 1079 (87·4%)
2128 (4·1%) 156 (12·6%)
52 227 1235
6112 (95·9%) 18 072 (95·2%) 12 343 (95·9%) 7613 (96·5%) 4206 (96·8%) 2832 (94·7%)
264 (4·1%) 916 (4·8%) 531 (4·1%) 273 (3·5%) 141 (3·2%) 159 (5·3%)
6376 18 988 12 874 7886 4347 2991
5665 (95·1%) 45 513 (95·8%)
291 (4·9%) 1993 (4·2%)
5956 47 506
35 677 (95·3%) 5742 (96·3%) 9759 (97·0%)
1757 (4·7%) 222 (3·7%) 305 (3·0%)
37 434 5964 10 064
*On NHS central registers.
Table 1: Demographic and military characteristics of study sample
(NHS) Central Register held in Southport. The computerised register (together with corresponding registers held in Scotland and Northern Ireland, and hereafter referred to collectively as “central registers”) contains an entry for everyone who has been registered with a general medical practitioner in the UK since 1991, and all persons born in, or who were immigrants to, the UK from this date. The current status of individuals on the register could be classified, in almost all cases, as one of the following: “registered with a UK health authority”, “under armed forces care”, “emigrated from the UK”, or “dead”. The status “emigrated from the UK” indicated that an individual had permanently left the country. If the individual was registered as having died in the UK, the ONS provided information on the date and causes of death (entered on the death certificate). The registers also record deaths among armed forces personnel overseas, although cause of death is not always available. Individuals in the Gulf and Era cohorts who could be identified on one of the central registers were “flagged”. In cases where individuals were not identified, a search of pre-1991 paper records was undertaken, by the ONS staff, in an attempt to identify individuals, establish their last known status, and add them to the computerised register. Information on the current status of “flagged” individuals in the Gulf and Era cohorts was obtained. If a person was dead, the underlying cause of death was coded by the ONS according to the ninth revision of the International Classification of Diseases (ICD-9).2 Where death occurred in service overseas, the information on cause of death was obtained either from the Defence Analytical Service Agency (DASA) or, where available,
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from military sources in the country of death. It was thereafter coded by the ONS. In reporting results, information on deaths occurring up to and including March 31, 1999—8 years after the end of the Gulf War—were included. The number of deaths overall and according to “disease-related” and “external” causes categories and subcategories have been reported. In addition the person-years at risk (of dying) has been calculated for each member of the cohorts. This was calculated, for individuals “flagged” on a central register, from April 1, 1991 (the nominal date for the end of the Gulf War), until the earliest of the following dates: date of death, date of emigration from the UK, and March 31, 1999 (the end of the follow-up period). Individuals who were registered as having emigrated from the UK, but who were known to be members of the armed forces after the date of emigration, were followed-up until the earliest of the following dates: date of death, date of leaving the armed forces, and March 31, 1999. For those not “flagged” on one of the central registers, information on death in service could still be reported by the DASA, and these individuals were therefore included in follow-up until the earliest of the following dates: date of death, date of leaving the armed forces, and March 31, 1999. Information on the number of deaths and the personyears at risk of death allowed a mortality rate to be calculated for each cohort and subsequently a mortality rate ratio (MRR) with 95% CI.3
Results Study cohort identification There were 53 462 subjects in both the Gulf and Era cohorts. The matching ensured perfect corresponding between the cohorts by sex, age-group, rank, and service branch (table 1). The cohorts were mostly male (97·7%) and of young age (71·5% <30 years). The army was the largest service (70·0%) and over all the services there was a 1:8 officer to other ranks ratio. There were 3787 individuals, representing 3·5% of the combined cohorts, who could not be identified on central registers. The percentage of individuals not identified was higher among the Era cohort (4·3%) than the Gulf cohort (2·8%). This higher non-identification in the Era cohort was principally among the army. In both cohorts nonidentification was higher among females (possibly due to changes of name) and among the oldest individuals (table 1). Only those who were alive on April 1, 1991, were eligible for inclusion in the follow-up study. Further, individuals who had left the armed forces and emigrated from the UK before this date were also excluded. The
Identified Under Armed Forces care UK Health Authority Emigration registered with NHS Dead‡ Not identified Not identified as dead Dead‡
Gulf cohort (n=53 416*)
Era cohort (n=53 450†)
19 219 31 811 506 376
17 211 33 207 397 352
1485 19
2257 26
*In the Gulf cohort 44 individuals died and two had emigration registered with the NHS and left the Armed Forces before April 1, 1991. †In the Era cohort 10 individuals died and two had emigration registered with the NHS and left the Armed Forces before April 1, 1991. ‡Deaths occurring in the period April 1, 1991, to March 31, 1999.
Table 2: Identification of study subjects on NHS central registers
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UK death certificates Military sources outside UK DASA information
Gulf cohort (n=376)
Era cohort (n=357)
268 53 55
265 44 48
Data does not include 19 Gulf and 21 Era cohort deaths where causal information (from various sources) is not yet available.
Table 3: Source of death information
exclusions were 44 deaths and two emigrations in the Gulf cohort and ten deaths and two emigrations in the Era cohort. The excess of deaths occurring before April 1, 1991, in the Gulf cohort was attributable to deaths in active service. Thereafter there remained 53 416 individuals in the Gulf cohort and 53 450 in the Era cohort. Among the remaining Gulf cohort individuals who had been identified on one of the central registers, 37·0% were recorded as still being under the care of armed forces, while 61·3% were under the care of a UK health authority (table 2). A listing of “under armed forces care” implies that individuals were still serving in the armed forces. However, it would also remain the listing for people who had left the armed forces but had not, to date, registered with a general practitioner. These individuals were included in follow-up after leaving the armed forces, since it was assumed that the vast majority were resident in the UK and therefore that any deaths occurring among this group would be registered with the ONS. The percentage of individuals in the Era cohort showed a slightly lower proportion still under armed forces care (33·6%), and a higher proportion under the care of a UK health authority (64·9%, table 2). Individuals lost to follow-up There were 903 individuals registered as having left the UK and therefore lost to follow-up from their date of emigration, or date of leaving armed forces if later (table 2). There are no reliable procedures for notification of deaths among such individuals to the ONS. Similarly there were 3787 subjects who could not be identified on central registers and who were followed-up only during their period in the armed forces. Given that such subjects were not flagged on central registers, any deaths occurring subsequently (even in the United Kingdom) would not be notified to the study investigators. Gulf cohort (n=395)
Era cohort (n=378)
MRR (95% CI)
Sex Male Female
390 5
371 7
1·05 (0·91–1·22) 0·71 (0·18–2·61)
Age (years)* <20 20–24 25–29 30–34 35–39 >39
54 119 89 46 40 47
58 118 69 48 33 52
0·93 (0·63–1·38) 1·01 (0·77–1·31) 1·29 (0·93–1·80) 0·96 (0·63–1·47) 1·22 (0·75–1·99) 0·91 (0·60–1·37)
Rank Officer Other ranks
64 331
56 322
1·14 (0·78–1·66) 1·03 (0·88–1·20)
Service branch Army Royal Navy Royal Air Force
272 44 79
285 33 60
0·95 (0·81–1·13) 1·33 (0·83–2·16) 1·32 (0·93–1·88)
*Age at Jan 1, 1991.
Table 4: Demographic and military characteristics of individuals who died
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Source of information on deaths There were 773 deaths recorded among cohort individuals, and for 733 of these, information on their underlying cause or ICD-9 code, or both, was available (table 3). In 533 cases information was derived from a UK death certificate. The ONS death drafts or death certificates containing causes of death coded to ICD-9 have been provided for these deaths. In 97 cases the information on death has been provided by military sources outside the UK. The ONS death drafts or death certificates containing causes of death coded to ICD-9 have been provided for 42 of these deaths. For the remainder, only the code of cause of death, derived by the ONS, has been provided. In 103 cases the information on death has been provided by the DASA. Only the code of cause of death, derived by the ONS, has been provided for these deaths. Finally, there have been 40 deaths (with date of death) notified to us by the DASA for which information on the cause of death and ICD-9 code is not yet available. Mortality among Gulf and Era cohorts There were 395 deaths among the Gulf cohort (0·74%, 94 deaths per 100 000 person-years) and 378 deaths among the Era cohort (0·71%, 90 deaths per 100 000 person-years, table 4). This represents an overall MRR of 1·05 (95% CI, 0·91–1·21). Mortality rates were highest in the Gulf cohort, in comparison with the Era cohort, for males, officers, and those serving in the Royal Navy or Royal Air Force (table 4). Information is currently available on cause of death (with coding) for 376 (95%) and 357 (94%) of deaths in the Gulf and Era groups, respectively. Mortality from “external” causes was higher in the Gulf cohort while Gulf cohort
Era MRR (95% CI) cohort
All causes
395
378
1·05 (0·91–1·21)
All causes (with ICD code)
376
357
1·05 (0·91–1·22)
Disease-related causes (001–799) Infectious and parasitic disease (001–139) All cancers (140–208) Benign neoplasms (210–239) Endocrine and immune disorders (240–279) Mental disorders (290–319) Nervous system and sense organs (320–389) Diseases of circulatory system (390–459) Diseases of respiratory system (460–519) Diseases of digestive system (520–579) Other disease-related causes (580–799)
122 3 53 1 0 7 5 43 3 3 4
141 2 48 1 4 7 4 58 3 7 7
0·87 (0·67–1·11) 1·50 (0·17–17·98) 1·11 (0·73–1·67) 1·00 (0·01–78·55) 0·00 (0·00–1·52) 1·00 (0·30–3·34) 1·25 (0·27–6·30) 0·74 (0·49–1·12) 1·00 (0·13–7·47) 0·43 (0·07–1·88) 0·57 (0·12–2·25)
All external causes (E800–E999) Railway accident (E800–E807) Motor vehicle accidents (E810–E825) Water transport accidents (E830–E838) Air and space accidents (E840–E845) Other vehicle accidents (E846–E848) Accidental poisoning (E850–E869) Accidental falls (E880–E888) Accidents due to fire/flames (E890–E899) Accidents due to natural/environmental factors (E900–E909) Accidents by submersion/suffocation/ foreign bodies (E910–E915) Other accidents (E916–E928) Late effects of accident/injury (E929) Suicide (E950–E959) Homicide (E960–E969) Injury undetermined whether accidental (E980–E989) Injury resulting from operations of war (E990–E999)
254 3 91 3 23 0 8 6 0 2
216 1 73 1 13 2 12 6 1 2
1·18 (0·98–1·42) 3·00 (0·24–157·61) 1·25 (0·91–1·72) 3·00 (0·24–157·61) 1·77 (0·86–3·81) 0·00 (0·00–5·33) 0·67 (0·24–1·78) 1·00 (0·27–3·74) 0·00 (0·00–39·04) 1·00 (0·07–13·80)
13
4
3·25 (1·00–13·69)
32 0 50 3 17
25 1 51 4 18
1·28 (0·74–2·25) 0·00 (0·00–39·04) 0·98 (0·65–1·48) 0·75 (0·11–4·44) 0·95 (0·46–1·94)
3
2
1·50 (0·17–17·98)
Table 5: Deaths and causes of death in Gulf and Era cohorts
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ARTICLES
mortality from “disease-related” causes was lower (table 5). There were 53 cancer deaths (ICD-9 140–208) in the Gulf cohort compared with 48 in the Era cohort but this excess was not significant and not related to any single type or group of cancer (data not shown). The higher mortality rate from “external” causes was principally due to a higher number of deaths classified as from motor vehicle or air/space accidents or deaths associated with submersion, suffocation, or foreign bodies. There was no excess of deaths in the Gulf cohort for suicide or from injury where it could not be determined if the cause was intentional or accidental.
Discussion This 8-year follow-up of UK Gulf War veterans has shown only a very small excess mortality compared with a cohort of service personnel matched for age, sex, rank, service, and level of fitness. The pattern of causes of death does, however, show some differences between the cohorts. Individuals who served in the Gulf have a slightly lower mortality from “disease-related” causes of death but a higher mortality from “external” causes. The excess of “external” causes of death is due to more accidents among Gulf War veterans. Suicides or deaths from injuries, where it could not be determined if intentional or accidental, have occurred approximately equally between the Gulf and Era cohorts. Nevertheless, caution is necessary in interpreting specific causes of death within the grouping “external” causes given the difficulty, in some circumstances, of distinguishing between an accident leading to death and a suicide. The results of an analysis of mortality among Gulf War veterans from the USA have previously been reported.4 Although there were some differences in the methods used to define study cohorts (Gulf and comparison group) and in the follow-up of individuals to determine vital status, the results were broadly similar to those from our study. There was a small excess mortality among Gulf veterans. The excess was confined to “external” causes rather than “disease-related” causes. The highest excess mortality among the “external” causes was noted for motor vehicle accidents while mortality from suicides was similar in both the Gulf and comparison cohorts. Such patterns of mortality have previously been noted among veterans of other conflicts. Follow-up studies of male and female veterans from the Vietnam conflict found an excess mortality in comparison with non-deployed.5–7 The excess mortality was principally due to an increased number of deaths from accidents in motor vehicles and other means of transport. Why should deaths from “external” causes, particularly motor vehicle accidents, be more common among Gulf War veterans? The reasons for this are not known, and a detailed evaluation of the motor vehicle accidents that occurred among Vietnam veterans did not find any common aspect to the accidents.5 It has been hypothesised, however, that those who have been on active service may subsequently have different relative perceptions of risk and may participate in high-risk activities or behaviours.8 Whether the lower number of disease-related deaths among veterans of the Gulf and other conflicts is a consequence of a “healthy-warrior” effect, whereby military personnel who are ill are less likely to be deployed in active service, has been the
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subject of intense debate.9–11 Although the current study matched the Gulf and Era cohorts on level of fitness for service (with the exception of the small proportion of individuals in the Royal Navy), a lower mortality rate from disease, albeit not statistically significant, was still observed in the Gulf group. This suggests that there may still have been some selection of healthy personnel even within recorded level of fitness for service. There are several aspects relating to the data collected and reported that should be considered. First, 3·5% of the cohorts could not be identified on UK central health registers. This rate of non-identification is usual, but efforts continue to further reduce the number of individuals not yet identified. Second, there will be inaccuracies in the status information contained on the registers for identified people. For example, there were individuals in the current study who were listed on the register as being in the armed forces while military records show that they are no longer serving. Others were shown as having emigrated from the UK when they were known to have subsequently served in the armed forces. Such inaccuracies in records required assumptions to be made about whether individuals were still resident in the UK and therefore, if they died, whether this would be recorded on central registers. These factors should, however, affect both the Gulf and Era cohorts equally and not bias the estimate of the MRR. The assumptions made in the analysis would generally lead to a slight underestimate of the mortality rate in both cohorts. Finally, no comparison has been made between mortality rates among Gulf war veterans and the general population of the UK. Armed forces personnel, as an occupational group, are more healthy than the general population (the “healthy soldier” effect) and a previous study of Gulf War veterans in the USA has shown that their mortality rates are less than half that expected on the basis of population mortality rates.4 Complete mortality data on the cohort as of March 31, 1999, are not yet available. There are some individuals who have died (with a confirmed date of death) for whom information on cause of death was not available. There were others for whom information on date of death was received, with coded cause of death, for whom a copy of a death certificate or death draft was not available. Further, there are an additional 11 unconfirmed deaths (one Gulf, ten Era) recorded by the Ministry of Defence about which no date or cause of death was available. In the absence of confirmatory information, these latter individuals were considered as alive for the current analysis. However, if such deaths are subsequently confirmed they would reduce further the small excess mortality observed among Gulf war veterans. In summary, although Gulf war veterans report higher levels of current morbidity than those who were not deployed, there is only a very small, and not statistically significant, increase in mortality. The excess mortality is related mainly to accidents, rather than disease-related causes, a finding that is consistent with other studies on US Gulf and Vietnam veterans. The current length of follow-up, however, is likely to be too short to detect any possible increase in disease-related deaths from, for example, cancer. The study cohorts will continue to be followed-up and their mortality experiences carefully monitored.
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Contributors Gary Macfarlane and Nicola Cherry designed the study, monitored study conduct, and supervised the analysis of the data. Elaine Thomas coordinated receiving data and conducted the analysis. Gary Macfarlane and Nicola Cherry wrote the paper, which was reviewed by Elaine Thomas.
Acknowledgments We are grateful to Ministry of Defence staff (in particular Nick Blatchley) who identified the study cohorts and to staff from the ONS who traced them on the NHS Central Register. The Medical Research Council provided funding.
References 1
2 3
Unwin C, Blatchley N, Coker W, et al. Health of UK servicemen who served in Persian Gulf War. Lancet 1999; 353: 169–78. WHO. Manual of the international statistical classification of disease, injuries and causes of death, 9th revision. Geneva: WHO, 1977. Rothman KJ. Modern epidemiology. Boston, Massachusetts: Little Brown and Co, 1986.
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Kang HK, Bullman TA. Mortality among US Veterans of the Persian Gulf War. N Engl J Med 1996; 335: 1498–504. 5 The Centers for Disease Control (CDC) Vietnam Experience Study. Postservice mortality among Vietnam veterans. JAMA 1987; 257: 7890–95. 6 Breslin P, Kang HK, Lee Y, et al. Proportionate mortality study of US Army and US Marine Corps veterans of the Vietnam war. J Occup Med 1988; 30: 412–19. 7 Thomas TL, Kang HK, Dalager NA. Mortality among women Vietnam veterans, 1973–87. Am J Epidemiol 1991; 134: 973–80. 8 Boyle CA, Decouflé P, O’Brien TR. Long-term health consequences of military service in Vietnam. Epidemiol Rev 1989; 11: 1–27. 9 Haley RW. Bias from the “healthy-warrior effect” and unequal follow-up in three government studies of health effects of the Gulf War. Am J Epidemiol 1998; 148: 315–23. 10 Kang HK, Bullman T. Counterpoint: negligible “healthy-warrior effect” on Gulf War veterans’ mortality. Am J Epidemiol 1998; 148: 324–25. 11 Gray GC, Knoke JD, Berg SW, Wignall FS, Barrett-Connor E. Counterpoint: responding to suppositions and misunderstandings. Am J Epidemiol 1998; 148: 328–33.
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Mortality among UK Gulf War veterans Gary J Macfarlane, Elaine Thomas, Nicola Cherry
Summary Background Armed forces personnel who served in the Gulf War report more current ill-health than those who were not deployed. There has been concern expressed that they may also experience higher mortality rates. Methods A retrospective cohort study was done including all 53 462 UK Gulf War veterans (Gulf cohort) and a comparison group equivalent in size of personnel who were not deployed but matched for age, sex, rank, service, and level of fitness (Era cohort). Individuals were identified on central registers of the Office for National Statistics and information on death among cohort subjects, including cause of death, obtained. Follow-up extended from April 1, 1991 (the end of the Gulf War) until March 31, 1999. Findings There were 395 deaths among the Gulf cohort and 378 deaths amongst the Era cohort (mortality rate ratio [MRR] 1·05, 95% CI 0·91–1·21). Mortality from “external” causes was higher in the Gulf cohort (Gulf 254, Era 216; MRR 1·18 [0·98–1·42] while mortality from “disease-related” causes was lower (Gulf 122, Era 141; 0·87 [0·67–1·11]). The higher mortality rate from “external” causes in the Gulf cohort was principally due to higher mortality rates from accidents. There was, however, no excess of deaths recorded as suicide in the Gulf cohort. Interpretation This follow-up of veterans of the Gulf war has shown, 8 years after the end of the conflict, that although they have experienced higher mortality rates than a comparison cohort, the excess mortality rate is very small and does not approach statistical significance. The excess is related mainly to accidents rather than disease, a pattern that is consistent both with US veterans of the Gulf war and veterans from other conflicts. Lancet 2000; 356: 17–21
Unit of Chronic Disease Epidemiology (Prof G J Macfarlane PhD), Arthritis Research Campaign Epidemiology Unit (Prof E Thomas MSc); and Centre for Occupational and Environmental Health (Prof N M Cherry MD), School of Epidemiology and Health Sciences, University of Manchester, UK Correspondence to: Prof Gary J Macfarlane, Unit of Chronic Disease Epidemiology, School of Epidemiology and Health Sciences, Medical School, University of Manchester, Oxford Road, Manchester M13 9PT, UK (e-mail: [email protected])
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Introduction There has been concern that armed forces personnel who served in the Gulf War during 1990–91 are currently experiencing an excess of ill-health. Studies among UK forces who served in the Gulf show that they do report more current ill-health than veterans who were not deployed.1 The excess of ill-health spans a wide range of symptoms. Studies are on-going to find out whether deployment is associated with adverse reproductive outcomes and ill health among offspring. During deployment in the Gulf, troops from the UK encountered a variety of environmental and physical exposures including smoke from oil-well fires, pesticides, nerve agent prophylaxis, and multiple inoculations.1 In addition, adverse psychological experiences such as seeing maimed soldiers and dismembered bodies, and the threat of chemical attack have also been reported as common.1 There is concern that not only may veterans be experiencing more illhealth as a result of such exposures but that they may also have higher mortality rates. This study documents the mortality experience of 53 462 UK Gulf War veterans in the 8 years since the end of the war.
Methods A retrospective cohort study was conducted, including all UK armed forces personnel who served in the Gulf at some time between September, 1990, and June, 1991 (the “Gulf” cohort). The geographical definition of the Gulf area varied according to the service and was determined by the Ministry of Defence. It included all army personnel whose theatre of service during this period was Kuwait, Muscat and Oman, Qatar, United Arab Emirates, Bahrain, Saudi Arabia, Iraq, Iran or Operation Granby. Royal Air Force personnel were included if they had served in the Saudi Arabian peninsula, and Royal Navy personnel if they had served on board a ship east of the Suez during the defined period. In addition, a comparison group of the same number of armed forces personnel was identified (the “Era” cohort). These individuals were recorded on military personnel records as being in service on Jan 1, 1991, but they did not serve in the Gulf. Selection was random but stratified to match the Gulf cohort on age (within a 5year age group), sex, service (army, Royal Navy, Royal Air Force) and rank (commissioned officer/other ranks). For the army and Royal Air Force, Gulf and Era cohorts were also matched on their level of fitness for service and their status as regulars or reservists. Individuals in both the Gulf and Era cohorts were identified by the Ministry of Defence. Information provided for each cohort member included age (at Jan 1, 1991), sex, armed forces service, rank and date of joining and leaving the armed forces (where applicable). Details of everyone in both cohorts were sent, by the Ministry of Defence, to the Office for National Statistics (ONS) for identification on the National Health Service
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Gulf cohort Sex Male Female Age (years) <20 20–24 25–29 30–34 35–39 >39 Rank Officer Other ranks Service branch Army Royal Navy Royal Air Force Era cohort Sex Male Female Age (years) <20 20–24 25–29 30–34 35–39 >39 Rank Officer Other ranks Service branch Army Royal Navy Royal Air Force
Identified*
Not identified*
Total
50 860 (97·4%) 1098 (88·9%)
1367 (2·6%) 137 (11·1%)
52 227 1235
6189 (97·1%) 18 447 (97·2%) 12 511 (97·2%) 7689 (97·5%) 4240 (97·5%) 2882 (96·4%)
187 (2·9%) 541 (2·8%) 363 (2·8%) 197 (2·5%) 107 (2·5%) 109 (3·6%)
6376 18 988 12 874 7886 4347 2991
5819 (97·7%) 46 139 (97·1%)
137 (2·3%) 1367 (2·9%)
5956 47 506
36 456 (97·4%) 5753 (96·5%) 9749 (96·9%)
978 (2·6%) 211 (3·5%) 315 (3·1%)
37 434 5964 10 064
50 099 (95·9%) 1079 (87·4%)
2128 (4·1%) 156 (12·6%)
52 227 1235
6112 (95·9%) 18 072 (95·2%) 12 343 (95·9%) 7613 (96·5%) 4206 (96·8%) 2832 (94·7%)
264 (4·1%) 916 (4·8%) 531 (4·1%) 273 (3·5%) 141 (3·2%) 159 (5·3%)
6376 18 988 12 874 7886 4347 2991
5665 (95·1%) 45 513 (95·8%)
291 (4·9%) 1993 (4·2%)
5956 47 506
35 677 (95·3%) 5742 (96·3%) 9759 (97·0%)
1757 (4·7%) 222 (3·7%) 305 (3·0%)
37 434 5964 10 064
*On NHS central registers.
Table 1: Demographic and military characteristics of study sample
(NHS) Central Register held in Southport. The computerised register (together with corresponding registers held in Scotland and Northern Ireland, and hereafter referred to collectively as “central registers”) contains an entry for everyone who has been registered with a general medical practitioner in the UK since 1991, and all persons born in, or who were immigrants to, the UK from this date. The current status of individuals on the register could be classified, in almost all cases, as one of the following: “registered with a UK health authority”, “under armed forces care”, “emigrated from the UK”, or “dead”. The status “emigrated from the UK” indicated that an individual had permanently left the country. If the individual was registered as having died in the UK, the ONS provided information on the date and causes of death (entered on the death certificate). The registers also record deaths among armed forces personnel overseas, although cause of death is not always available. Individuals in the Gulf and Era cohorts who could be identified on one of the central registers were “flagged”. In cases where individuals were not identified, a search of pre-1991 paper records was undertaken, by the ONS staff, in an attempt to identify individuals, establish their last known status, and add them to the computerised register. Information on the current status of “flagged” individuals in the Gulf and Era cohorts was obtained. If a person was dead, the underlying cause of death was coded by the ONS according to the ninth revision of the International Classification of Diseases (ICD-9).2 Where death occurred in service overseas, the information on cause of death was obtained either from the Defence Analytical Service Agency (DASA) or, where available,
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from military sources in the country of death. It was thereafter coded by the ONS. In reporting results, information on deaths occurring up to and including March 31, 1999—8 years after the end of the Gulf War—were included. The number of deaths overall and according to “disease-related” and “external” causes categories and subcategories have been reported. In addition the person-years at risk (of dying) has been calculated for each member of the cohorts. This was calculated, for individuals “flagged” on a central register, from April 1, 1991 (the nominal date for the end of the Gulf War), until the earliest of the following dates: date of death, date of emigration from the UK, and March 31, 1999 (the end of the follow-up period). Individuals who were registered as having emigrated from the UK, but who were known to be members of the armed forces after the date of emigration, were followed-up until the earliest of the following dates: date of death, date of leaving the armed forces, and March 31, 1999. For those not “flagged” on one of the central registers, information on death in service could still be reported by the DASA, and these individuals were therefore included in follow-up until the earliest of the following dates: date of death, date of leaving the armed forces, and March 31, 1999. Information on the number of deaths and the personyears at risk of death allowed a mortality rate to be calculated for each cohort and subsequently a mortality rate ratio (MRR) with 95% CI.3
Results Study cohort identification There were 53 462 subjects in both the Gulf and Era cohorts. The matching ensured perfect corresponding between the cohorts by sex, age-group, rank, and service branch (table 1). The cohorts were mostly male (97·7%) and of young age (71·5% <30 years). The army was the largest service (70·0%) and over all the services there was a 1:8 officer to other ranks ratio. There were 3787 individuals, representing 3·5% of the combined cohorts, who could not be identified on central registers. The percentage of individuals not identified was higher among the Era cohort (4·3%) than the Gulf cohort (2·8%). This higher non-identification in the Era cohort was principally among the army. In both cohorts nonidentification was higher among females (possibly due to changes of name) and among the oldest individuals (table 1). Only those who were alive on April 1, 1991, were eligible for inclusion in the follow-up study. Further, individuals who had left the armed forces and emigrated from the UK before this date were also excluded. The
Identified Under Armed Forces care UK Health Authority Emigration registered with NHS Dead‡ Not identified Not identified as dead Dead‡
Gulf cohort (n=53 416*)
Era cohort (n=53 450†)
19 219 31 811 506 376
17 211 33 207 397 352
1485 19
2257 26
*In the Gulf cohort 44 individuals died and two had emigration registered with the NHS and left the Armed Forces before April 1, 1991. †In the Era cohort 10 individuals died and two had emigration registered with the NHS and left the Armed Forces before April 1, 1991. ‡Deaths occurring in the period April 1, 1991, to March 31, 1999.
Table 2: Identification of study subjects on NHS central registers
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UK death certificates Military sources outside UK DASA information
Gulf cohort (n=376)
Era cohort (n=357)
268 53 55
265 44 48
Data does not include 19 Gulf and 21 Era cohort deaths where causal information (from various sources) is not yet available.
Table 3: Source of death information
exclusions were 44 deaths and two emigrations in the Gulf cohort and ten deaths and two emigrations in the Era cohort. The excess of deaths occurring before April 1, 1991, in the Gulf cohort was attributable to deaths in active service. Thereafter there remained 53 416 individuals in the Gulf cohort and 53 450 in the Era cohort. Among the remaining Gulf cohort individuals who had been identified on one of the central registers, 37·0% were recorded as still being under the care of armed forces, while 61·3% were under the care of a UK health authority (table 2). A listing of “under armed forces care” implies that individuals were still serving in the armed forces. However, it would also remain the listing for people who had left the armed forces but had not, to date, registered with a general practitioner. These individuals were included in follow-up after leaving the armed forces, since it was assumed that the vast majority were resident in the UK and therefore that any deaths occurring among this group would be registered with the ONS. The percentage of individuals in the Era cohort showed a slightly lower proportion still under armed forces care (33·6%), and a higher proportion under the care of a UK health authority (64·9%, table 2). Individuals lost to follow-up There were 903 individuals registered as having left the UK and therefore lost to follow-up from their date of emigration, or date of leaving armed forces if later (table 2). There are no reliable procedures for notification of deaths among such individuals to the ONS. Similarly there were 3787 subjects who could not be identified on central registers and who were followed-up only during their period in the armed forces. Given that such subjects were not flagged on central registers, any deaths occurring subsequently (even in the United Kingdom) would not be notified to the study investigators. Gulf cohort (n=395)
Era cohort (n=378)
MRR (95% CI)
Sex Male Female
390 5
371 7
1·05 (0·91–1·22) 0·71 (0·18–2·61)
Age (years)* <20 20–24 25–29 30–34 35–39 >39
54 119 89 46 40 47
58 118 69 48 33 52
0·93 (0·63–1·38) 1·01 (0·77–1·31) 1·29 (0·93–1·80) 0·96 (0·63–1·47) 1·22 (0·75–1·99) 0·91 (0·60–1·37)
Rank Officer Other ranks
64 331
56 322
1·14 (0·78–1·66) 1·03 (0·88–1·20)
Service branch Army Royal Navy Royal Air Force
272 44 79
285 33 60
0·95 (0·81–1·13) 1·33 (0·83–2·16) 1·32 (0·93–1·88)
*Age at Jan 1, 1991.
Table 4: Demographic and military characteristics of individuals who died
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Source of information on deaths There were 773 deaths recorded among cohort individuals, and for 733 of these, information on their underlying cause or ICD-9 code, or both, was available (table 3). In 533 cases information was derived from a UK death certificate. The ONS death drafts or death certificates containing causes of death coded to ICD-9 have been provided for these deaths. In 97 cases the information on death has been provided by military sources outside the UK. The ONS death drafts or death certificates containing causes of death coded to ICD-9 have been provided for 42 of these deaths. For the remainder, only the code of cause of death, derived by the ONS, has been provided. In 103 cases the information on death has been provided by the DASA. Only the code of cause of death, derived by the ONS, has been provided for these deaths. Finally, there have been 40 deaths (with date of death) notified to us by the DASA for which information on the cause of death and ICD-9 code is not yet available. Mortality among Gulf and Era cohorts There were 395 deaths among the Gulf cohort (0·74%, 94 deaths per 100 000 person-years) and 378 deaths among the Era cohort (0·71%, 90 deaths per 100 000 person-years, table 4). This represents an overall MRR of 1·05 (95% CI, 0·91–1·21). Mortality rates were highest in the Gulf cohort, in comparison with the Era cohort, for males, officers, and those serving in the Royal Navy or Royal Air Force (table 4). Information is currently available on cause of death (with coding) for 376 (95%) and 357 (94%) of deaths in the Gulf and Era groups, respectively. Mortality from “external” causes was higher in the Gulf cohort while Gulf cohort
Era MRR (95% CI) cohort
All causes
395
378
1·05 (0·91–1·21)
All causes (with ICD code)
376
357
1·05 (0·91–1·22)
Disease-related causes (001–799) Infectious and parasitic disease (001–139) All cancers (140–208) Benign neoplasms (210–239) Endocrine and immune disorders (240–279) Mental disorders (290–319) Nervous system and sense organs (320–389) Diseases of circulatory system (390–459) Diseases of respiratory system (460–519) Diseases of digestive system (520–579) Other disease-related causes (580–799)
122 3 53 1 0 7 5 43 3 3 4
141 2 48 1 4 7 4 58 3 7 7
0·87 (0·67–1·11) 1·50 (0·17–17·98) 1·11 (0·73–1·67) 1·00 (0·01–78·55) 0·00 (0·00–1·52) 1·00 (0·30–3·34) 1·25 (0·27–6·30) 0·74 (0·49–1·12) 1·00 (0·13–7·47) 0·43 (0·07–1·88) 0·57 (0·12–2·25)
All external causes (E800–E999) Railway accident (E800–E807) Motor vehicle accidents (E810–E825) Water transport accidents (E830–E838) Air and space accidents (E840–E845) Other vehicle accidents (E846–E848) Accidental poisoning (E850–E869) Accidental falls (E880–E888) Accidents due to fire/flames (E890–E899) Accidents due to natural/environmental factors (E900–E909) Accidents by submersion/suffocation/ foreign bodies (E910–E915) Other accidents (E916–E928) Late effects of accident/injury (E929) Suicide (E950–E959) Homicide (E960–E969) Injury undetermined whether accidental (E980–E989) Injury resulting from operations of war (E990–E999)
254 3 91 3 23 0 8 6 0 2
216 1 73 1 13 2 12 6 1 2
1·18 (0·98–1·42) 3·00 (0·24–157·61) 1·25 (0·91–1·72) 3·00 (0·24–157·61) 1·77 (0·86–3·81) 0·00 (0·00–5·33) 0·67 (0·24–1·78) 1·00 (0·27–3·74) 0·00 (0·00–39·04) 1·00 (0·07–13·80)
13
4
3·25 (1·00–13·69)
32 0 50 3 17
25 1 51 4 18
1·28 (0·74–2·25) 0·00 (0·00–39·04) 0·98 (0·65–1·48) 0·75 (0·11–4·44) 0·95 (0·46–1·94)
3
2
1·50 (0·17–17·98)
Table 5: Deaths and causes of death in Gulf and Era cohorts
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mortality from “disease-related” causes was lower (table 5). There were 53 cancer deaths (ICD-9 140–208) in the Gulf cohort compared with 48 in the Era cohort but this excess was not significant and not related to any single type or group of cancer (data not shown). The higher mortality rate from “external” causes was principally due to a higher number of deaths classified as from motor vehicle or air/space accidents or deaths associated with submersion, suffocation, or foreign bodies. There was no excess of deaths in the Gulf cohort for suicide or from injury where it could not be determined if the cause was intentional or accidental.
Discussion This 8-year follow-up of UK Gulf War veterans has shown only a very small excess mortality compared with a cohort of service personnel matched for age, sex, rank, service, and level of fitness. The pattern of causes of death does, however, show some differences between the cohorts. Individuals who served in the Gulf have a slightly lower mortality from “disease-related” causes of death but a higher mortality from “external” causes. The excess of “external” causes of death is due to more accidents among Gulf War veterans. Suicides or deaths from injuries, where it could not be determined if intentional or accidental, have occurred approximately equally between the Gulf and Era cohorts. Nevertheless, caution is necessary in interpreting specific causes of death within the grouping “external” causes given the difficulty, in some circumstances, of distinguishing between an accident leading to death and a suicide. The results of an analysis of mortality among Gulf War veterans from the USA have previously been reported.4 Although there were some differences in the methods used to define study cohorts (Gulf and comparison group) and in the follow-up of individuals to determine vital status, the results were broadly similar to those from our study. There was a small excess mortality among Gulf veterans. The excess was confined to “external” causes rather than “disease-related” causes. The highest excess mortality among the “external” causes was noted for motor vehicle accidents while mortality from suicides was similar in both the Gulf and comparison cohorts. Such patterns of mortality have previously been noted among veterans of other conflicts. Follow-up studies of male and female veterans from the Vietnam conflict found an excess mortality in comparison with non-deployed.5–7 The excess mortality was principally due to an increased number of deaths from accidents in motor vehicles and other means of transport. Why should deaths from “external” causes, particularly motor vehicle accidents, be more common among Gulf War veterans? The reasons for this are not known, and a detailed evaluation of the motor vehicle accidents that occurred among Vietnam veterans did not find any common aspect to the accidents.5 It has been hypothesised, however, that those who have been on active service may subsequently have different relative perceptions of risk and may participate in high-risk activities or behaviours.8 Whether the lower number of disease-related deaths among veterans of the Gulf and other conflicts is a consequence of a “healthy-warrior” effect, whereby military personnel who are ill are less likely to be deployed in active service, has been the
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subject of intense debate.9–11 Although the current study matched the Gulf and Era cohorts on level of fitness for service (with the exception of the small proportion of individuals in the Royal Navy), a lower mortality rate from disease, albeit not statistically significant, was still observed in the Gulf group. This suggests that there may still have been some selection of healthy personnel even within recorded level of fitness for service. There are several aspects relating to the data collected and reported that should be considered. First, 3·5% of the cohorts could not be identified on UK central health registers. This rate of non-identification is usual, but efforts continue to further reduce the number of individuals not yet identified. Second, there will be inaccuracies in the status information contained on the registers for identified people. For example, there were individuals in the current study who were listed on the register as being in the armed forces while military records show that they are no longer serving. Others were shown as having emigrated from the UK when they were known to have subsequently served in the armed forces. Such inaccuracies in records required assumptions to be made about whether individuals were still resident in the UK and therefore, if they died, whether this would be recorded on central registers. These factors should, however, affect both the Gulf and Era cohorts equally and not bias the estimate of the MRR. The assumptions made in the analysis would generally lead to a slight underestimate of the mortality rate in both cohorts. Finally, no comparison has been made between mortality rates among Gulf war veterans and the general population of the UK. Armed forces personnel, as an occupational group, are more healthy than the general population (the “healthy soldier” effect) and a previous study of Gulf War veterans in the USA has shown that their mortality rates are less than half that expected on the basis of population mortality rates.4 Complete mortality data on the cohort as of March 31, 1999, are not yet available. There are some individuals who have died (with a confirmed date of death) for whom information on cause of death was not available. There were others for whom information on date of death was received, with coded cause of death, for whom a copy of a death certificate or death draft was not available. Further, there are an additional 11 unconfirmed deaths (one Gulf, ten Era) recorded by the Ministry of Defence about which no date or cause of death was available. In the absence of confirmatory information, these latter individuals were considered as alive for the current analysis. However, if such deaths are subsequently confirmed they would reduce further the small excess mortality observed among Gulf war veterans. In summary, although Gulf war veterans report higher levels of current morbidity than those who were not deployed, there is only a very small, and not statistically significant, increase in mortality. The excess mortality is related mainly to accidents, rather than disease-related causes, a finding that is consistent with other studies on US Gulf and Vietnam veterans. The current length of follow-up, however, is likely to be too short to detect any possible increase in disease-related deaths from, for example, cancer. The study cohorts will continue to be followed-up and their mortality experiences carefully monitored.
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Contributors Gary Macfarlane and Nicola Cherry designed the study, monitored study conduct, and supervised the analysis of the data. Elaine Thomas coordinated receiving data and conducted the analysis. Gary Macfarlane and Nicola Cherry wrote the paper, which was reviewed by Elaine Thomas.
Acknowledgments We are grateful to Ministry of Defence staff (in particular Nick Blatchley) who identified the study cohorts and to staff from the ONS who traced them on the NHS Central Register. The Medical Research Council provided funding.
References 1
2 3
Unwin C, Blatchley N, Coker W, et al. Health of UK servicemen who served in Persian Gulf War. Lancet 1999; 353: 169–78. WHO. Manual of the international statistical classification of disease, injuries and causes of death, 9th revision. Geneva: WHO, 1977. Rothman KJ. Modern epidemiology. Boston, Massachusetts: Little Brown and Co, 1986.
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Kang HK, Bullman TA. Mortality among US Veterans of the Persian Gulf War. N Engl J Med 1996; 335: 1498–504. 5 The Centers for Disease Control (CDC) Vietnam Experience Study. Postservice mortality among Vietnam veterans. JAMA 1987; 257: 7890–95. 6 Breslin P, Kang HK, Lee Y, et al. Proportionate mortality study of US Army and US Marine Corps veterans of the Vietnam war. J Occup Med 1988; 30: 412–19. 7 Thomas TL, Kang HK, Dalager NA. Mortality among women Vietnam veterans, 1973–87. Am J Epidemiol 1991; 134: 973–80. 8 Boyle CA, Decouflé P, O’Brien TR. Long-term health consequences of military service in Vietnam. Epidemiol Rev 1989; 11: 1–27. 9 Haley RW. Bias from the “healthy-warrior effect” and unequal follow-up in three government studies of health effects of the Gulf War. Am J Epidemiol 1998; 148: 315–23. 10 Kang HK, Bullman T. Counterpoint: negligible “healthy-warrior effect” on Gulf War veterans’ mortality. Am J Epidemiol 1998; 148: 324–25. 11 Gray GC, Knoke JD, Berg SW, Wignall FS, Barrett-Connor E. Counterpoint: responding to suppositions and misunderstandings. Am J Epidemiol 1998; 148: 328–33.
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