Baker, MG

Boyd, M

Clement, C

Nisa, S

Wilson, N

Epidemiology and Infection

English

Massey Research Online

SHORT REPORTDid exposure to a severe outbreak of pandemic influenza in 1918impact on long-term survival?N. WILSON1*, M. BOYD2, S. NISA3, C. CLEMENT4 AND M. G. BAKER11Department of Public Health, University of Otago, Wellington, New Zealand2Adapt Research, Wellington, New Zealand3 Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand4Te Puke, Bay of Plenty, New ZealandReceived 19 February 2016; Final revision 19 June 2016; Accepted 29 June 2016;first published online 1 August 2016SUMMARYThere is some suggestion that infection with pandemic influenza may increase long-termmortality risks. Therefore we aimed to determine if exposure to a severe outbreak of pandemicinfluenza on a troopship in 1918 impacted on lifespan in the survivors. The troopship with theoutbreak cohort had 1107 personnel and the comparison cohort was from two contemporaneoustroopships (1108 randomly selected personnel). Data were collected from online individualmilitary files. The main finding was that there was no statistically significant difference in thelifespan of the outbreak cohort and the comparison cohort (means of 71·5 and 71·0 years,respectively). Indeed, the outbreak cohort was actually more likely to survive into the periodfrom 1950 onwards (P= 0·036) and to participate in the Second World War (P = 0·043). Therewere no significant differences between the cohorts in terms of occupational class, but thecomparison cohort had a higher proportion of rural occupations (33·3% vs. 27·0%, P< 0·001)and was very slightly older in mid-1918 (27·8 vs. 27·2 years, P = 0·028). In conclusion, this studyfound no support for the hypothesis that exposure to the 1918 influenza pandemic adverselyimpacted on the lifespan in the survivors, at least in this male and military-age population.Key words: Influenza, pandemic, public health emerging infections.There are some suggestions in the literature of pastpandemic influenza infection being associated withincreased long-term mortality rates. A Norwegianstudy found significantly higher all-cause mortalityat middle and old ages of 1918 pandemic influenzasurvivors who were born between 1895 and 1910 com-pared to age cohorts born before or after this period[1]. Others have suggested that survivors of 1918 pan-demic influenza were primed for late coronary heartdisease (CHD) mortality (contributing to the rise inCHD in the 1920–1967 period), while the demise ofthis cohort may then have contributed to the subse-quent decline (1968–1985) in CHD mortality in theUnited States [2].More specifically, there is evidence for neurologicalsequelae of infection with pandemic influenza, someof which may be permanent. One review for the2009 influenza pandemic reported evidence of the oc-currence of Guillain–Barré syndrome (GBS), poly-neuropathy, and seizures in the infected population[3]. An association between the neurological condition‘encephalitis lethargica’ and the influenza pandemicstrain of 1918/1919 has also been debated, but recent* Author for correspondence: Professor N. Wilson, University ofOtago, Wellington, Mein St, Newtown, Wellington, New Zealand.(Email: nick.wilson@otago.ac.nz)Epidemiol. Infect. (2016), 144, 3166–3169. © Cambridge University Press 2016doi:10.1017/S0950268816001606work involving archived human brain specimens mayfavour other pathogens as being more likely causes [4].Given this background, we hypothesized that survi-vors of a severe outbreak of pandemic influenza in1918 would experience poorer long-term survivalcompared to that of a comparison group which werenot so exposed. To test this hypothesis, we aimed tomake use of a natural experiment whereby a particulargroup of military personnel on a troopship wereexposed to a particularly severe outbreak of pandemicinfluenza in 1918, while those on contemporaneousother troopships were at lower risk of severe infection.That is, in this troopship outbreak nearly all those onthe troopship were reported having symptomatic ill-ness with 77 men dying [5]. The latter resulted in avery high mortality rate from pandemic influenzacompared to the rest of the New Zealand military dur-ing the whole 1918–1919 pandemic period [6]. Indeed,it seems likely that the confined nature of the troop-ship increased both the risk of infection and also theseverity of infection with high case-fatality ratesresulting (possibly due to the higher levels of inoculumin the crowded conditions). In contrast, a probablylower (but not precisely known), proportion of thecomparison cohort were also infected with pandemicinfluenza in the late 1918 and 1919 period. But suchinfections in the comparison group would almost cer-tainly have been in less crowded circumstances thanon a troopship (e.g. training camps in England orback in New Zealand).The outbreak cohort in our study was comprised ofall (n= 1107) of the male military personnel on thetroopship Tahiti [His Majesty’s NZ Transport(HMNZT) 107]. Data on 10 women military person-nel (all nurses) were not included in the analysis.The comparison cohort was comprised of anequivalent number of male military personnel whowere randomly selected from the troopships that eitherdirectly preceded or directly followed the Tahiti’s de-parture from New Zealand on 10 July 1918. Thesewere the Athenic (HMNZT 106) which departed on 13June 1918 with 793 military personnel and theUlimaroa (HMNZT 108) which departed on 27 July1918 with 1010 military personnel. Neither of these ves-sels had disease outbreaks, and, as with the personnelon the Tahiti, none of these personnel were involved insubsequent combat. That is, the First WorldWar endedbefore they had either completed supplementary trainingin England or had moved into front-line positions.Data collection processes were similar to a previ-ously published study [7]. This method involvedexamination of digitalized and publicly available per-sonal military files for the First World War militarypersonnel from Archives New Zealand [8]. Any datathat could not be obtained this way was searched forin the official Births, Deaths and Marriages (BDM)database for New Zealand [9] or other sources (e.g.the Cenotaph database held by Auckland Museum[10] and the website ancestry.com.au for genealogicalrecords). As in the previous work, occupational classwas determined by using an established historical clas-sification system designed for New Zealand [11].There were no data in the archives to help to distin-guish between conscripts vs. volunteers, but the for-mer probably dominated during 1918.The main finding was that there was no statisticallysignificant difference in the lifespan of the outbreakcohort and the comparison cohort from the contem-poraneous troopships (means of 71·5 and 71·0 years,respectively; Table 1). Indeed, there were some sugges-tions that the outbreak cohort was slightly healthier interms of being more likely to survive into the periodfrom 1950 onwards (P= 0·036). They were alsomore likely to participate in military service again inthe Second World War (P= 0·043), which meant pas-sing a health screening process on entry to the mili-tary. Furthermore, they also seemed less likely to diein the year of the subsequent 1957 pandemic causedby a H2N2 strain (but this was not statistically signifi-cant). Collectively, these results are consistent with apossible healthy survivor effect for those in the out-break cohort (i.e. less healthy individuals with under-lying disease may have been more likely to die in thetroopship outbreak). Certainly these results do notsupport any strong impact from differing risk of infec-tion and severity of infection from pandemic influenzain 1918 in increasing long-term mortality, at least forthese military populations.Nevertheless, these results need to be considered inthe context of the slight differences between the twocohorts. That is, more lifespan data were missing forthe comparison cohort (4·6% vs. 2·6%, P = 0·006)and this group was very slightly older in mid-1918(27·8 vs. 27·2 years, P = 0·028, Table 1). The compari-son cohort also had a slightly poorer mean occupa-tional class score (6·9/9 vs. 6·7/9) but the latter wasnot statistically significant. Finally, the comparisoncohort were also more likely to have an occupationthat was classified as rural (33·3% vs. 27·0%, P <0·001), although there was no statistically significantdifference in lifespan by rural vs. non-rural occupation(71·8 vs. 71·0 years, respectively).Pandemic influenza and long-term survival 3167Furthermore, the results from this study may havelimited generalizability to the wider population. Thatis because all these personnel were subject to thehealthy soldier effect [12] (a selection effect analogousto the healthy worker effect). Indeed, the rejection ratefor new military recruits was relatively high forthe November 1916 to November 1918 period inNew Zealand at 57·6% (n = 77 900 rejected out ofTable 1. Comparison of the characteristics of the outbreak cohort with the comparison cohort (from twocontemporaneous troopships) and the results for lifespan and mortality differencesCharacteristicOutbreak cohort Comparison cohortP value*N % or (S.D.) N % or (S.D.)Data quality and pandemic impact (N = 1107) (N = 1108)Missing lifespan data (e.g. date of death not identified) 29 2·6% 51 4·6% 0·006Missing data on occupation 2 0·18% 5 0·45% 0·189Died of pandemic influenza in 1918–1919 77 7·0% 8 0·72% <0·00001Results when excluding influenza pandemic deaths andthose with missing lifespan data(N = 1001) (N = 1049)†Age in mid-1918 (years)Mean (S.D.) 27·2 (6·8) 27·8 (7·0) 0·028Median 25·3 27·0 –Interquartile range (IQR) 20·7–32·5 20·8–33·2 –Range 18·9–49·3 16·9–51·1 –Occupational class (nine levels)Highest status, three classes (e.g. doctor) 49 4·9% 52 5·0% 0·045Middle three classes (e.g. postal officer) 399 40·0% 363 34·7%Lowest three classes (e.g. labourer) 551 55·2% 632 60·4%Mean occupational class score (S.D.) 6·7 (2·0) 6·9 (2·1) 0·204Median occupational class score 7 7 –IQR 5–8 5–9 –Rural occupation 270 27·0% 349 33·3% <0·001Possible ethnicityIndividual had any Māori (indigenous) name (first,middle and surnames)2 0·18% 2 0·19% 0·482Military serviceMean years spent in military service (for those notdying during active service) (S.D.)1·6 (0·48) 1·5 (0·50) 0·050Median discharge date from military service (for theFirst World War)9/17/1919 9/17/1919 –In NZ military forces in the Second World War(1939–1945) out of those alive on 1 Jan. 1939‡142 15·3% 132 12·6% 0·043Lifespan and mortality resultsLifespan. mean years (S.D.) 71·5 (13·6) 71·0 (14·1) 0·501Lifespan, median years 73·0 72·8 –IQR 64·3–81·2 63·6–81·4 –Deaths in the period 1918–1929 35 3·5% 45 4·3% 0·179Deaths in the period 1930–1949 138 13·8% 169 16·1% 0·070Deaths in the period 1950 onwards 828 82·7% 835 79·6% 0·036Died in the year of the 1957 influenza pandemic(all causes)§24 3·6% 34 5·1% 0·088As above but for 1957 and 1958§ 46 6·8% 59 8·8% 0·089* All analyses conducted in Epi Info v. 7.1.3.0 (CDC, USA) using χ2 tests, ANOVA and the Mann–Whitney/Wilcoxontwo-sample test (when ANOVA was not appropriate due to variances not being homogeneous).†Comprised of 541 men on the troopship Athenic and 508 men on the troopship Ulimaroa.‡Many were stationed in New Zealand during the Second World War and not in conflict zones (hence only one was killed).§ The denominators for these calculations were those alive on 1 January 1957 (n= 676 for the outbreak cohort and n= 672 forthe comparison cohort).3168 N. Wilson and othersn = 135 282 examined) [13]. In addition, by selectingmilitary personnel that left New Zealand, rather thanperforming military duties back in the home country,therewas probably also a ‘healthy warrior effect’ operat-ing [14].In a separate analysis we considered deaths frompandemic influenza itself. In the outbreak cohortthere were 77 pandemic-related deaths associatedwith the outbreak on the Tahiti in September/October 1918 with no deaths in these months in thecomparison cohort from the two contemporaneoustroopships (Table 1). But then for the period frommid-October 1918 to the end of 1919 there were nopandemic-related deaths in the outbreak cohort vs.eight such deaths in the comparison cohort (P =0·0023, with all these deaths being in November/December 1918 except for one in 1919, Table 1). Aplausible explanation for this difference is that the out-break cohort may have been immunized against fur-ther infection in the subsequent pandemic waves.In conclusion, this study found no evidence that ex-posure to a severe outbreak of pandemic influenza on atroopship in 1918 reduced the lifespan of the survivorscompared to military personnel on two contemporan-eous troopships.However, these results were for relative-ly healthy youngmale populations of military personneland so may not be generalizable to other populations.ACKNOWLEDGEMENTSThe authors thank Professor Dennis Shanks(Australian Army Malaria Institute, Brisbane,Australia) for providing helpful comments on themanuscript.DECLARATION OF INTERESTNone.REFERENCES1. Mamelund SE. Effects of the Spanish influenza pandem-ic of 1918–19 on later life mortality of Norwegiancohorts born about 1900. Oslo: Department ofEconomics, University of Oslo; 2003.2. Azambuja M. Spanish flu and early 20th-century expan-sion of a coronary heart disease-prone subpopulation.Texas Heart Institute Journal 2004; 31: 14–21.3. Cardenas G, et al. Neurological events related toinfluenza A(H1N1) pdm09. Influenza and Other Res-piratory Viruses 2014; 8: 339–346.4. Tappe D, Alquezar-Planas D. Medical and molecularperspectives into a forgotten epidemic: encephalitislethargica, viruses, and high-throughput sequencing.Journal of Clinical Virology 2014; 61: 189–195.5. Summers JA, et al. Mortality risk factors for pandemicinfluenza on New Zealand troop ship, 1918. EmergingInfectious Diseases 2010; 16: 1931–1937.6. Summers JA, et al.: Severe impact of the 1918–19 pan-demic influenza in a national military force. NewZealand Medical Journal 2013; 126: 36–47.7. Wilson N, et al.: Mortality of first world war militarypersonnel: comparison of two military cohorts. BritishMedical Journal 2014; 349: g7168.8. New Zealand Government. Archway. Archives NewZealand (www.archway.archives.govt.nz).9. Births Deaths and Marriages Historical Records. (http://bdmhistoricalrecords.identityservices.govt.nz/Home/).10. Auckland War Memorial Museum. Cenotaph database(http://muse.aucklandmuseum.com/databases/Cenotaph/locations.aspx?).11. Olssen E, Hickey M. Class and Occupation: The NewZealand Reality. Dunedin: Otago University Press,2005.12. McLaughlin R, Nielsen L, Waller M. An evaluation ofthe effect of military service on mortality: quantifyingthe healthy soldier effect. Annals of Epidemiology2008; 18: 928–936.13. Editorial. Territorial military training and physicalefficiency. New Zealand Medical Journal 1920; 19:245–246.14. Wilson J, et al. Is previous psychological health asso-ciated with the likelihood of Iraq War deployment?An investigation of the ‘healthy warrior effect’.American Journal of Epidemiology 2009; 169: 1362–1369.Pandemic influenza and long-term survival 3169MASSEY UNIVERSITYMASSEY RESEARCH ONLINE http://mro.massey.ac.nz/Massey Documents by Type Journal ArticlesDid exposure to a severe outbreak ofpandemic influenza in 1918 impact onlong-term survival?Nisa, S2016-08-01http://hdl.handle.net/10179/1778417/01/2023 - Downloaded from MASSEY RESEARCH ONLINE

Did exposure to a severe outbreak of pandemic influenza in 1918 impact on long-term survival?

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Did exposure to a severe outbreak of pandemic influenza in 1918 impact on long-term survival?

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