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The evolution of pandemic influenza: evidence from India, 1918–19
© Chandra and Kassens-Noor; licensee BioMed Central Ltd. 2014
Received: 20 March 2014
Accepted: 22 July 2014
Published: 19 September 2014
The 1918–19 ‘Spanish’ Influenza was the most devastating pandemic in recent history, with estimates of global mortality ranging from 20 to 50 million. The focal point of the pandemic was India, with an estimated death toll of between 10 and 20 million. We will characterize the pattern of spread, mortality, and evolution of the 1918 influenza across India using spatial or temporal data.
This study estimates weekly deaths in 213 districts from nine provinces in India. We compute statistical measures of the severity, speed, and duration of the virulent autumn wave of the disease as it evolved and diffused throughout India. These estimates create a clear picture of the spread of the pandemic across India.
Analysis of the timing and mortality patterns of the disease reveals a striking pattern of speed deceleration, reduction in peak-week mortality, a prolonging of the epidemic wave, and a decrease in overall virulence of the pandemic over time.
The findings are consistent with a variety of possible causes, including the changing nature of the dominant viral strain and the timing and severity of the monsoon. The results significantly advance our knowledge of this devastating pandemic at its global focal point.
Keywords1918 influenza pandemic Spanish Influenza Influenza Pandemic Mortality India Epidemic velocity Climatic factors Immunity
Recent influenza outbreaks around the world have generated renewed interest in the study of the spread and properties of pandemic diseases with a view to mitigating their impacts [1–6]. The so-called Spanish Influenza of 1918 was the most devastating in history, with a global death toll of between 20 and 50 million [7–10]. Caused by a member of the H1N1 family of influenza viruses, the first wave of the disease emerged in the early months of 1918. In the autumn of 1918, a second and severe wave of the disease swept across the globe, leaving no major inhabited region untouched [7, 8, 11–19]. The focal point of the epidemic in terms of mortality was India, with an estimated death toll range of 10–20 million, and a point estimate of population loss of 13.8 million for the British-controlled provinces [8, 20, 21]. Surprisingly, no modern study exists that comprehensively characterizes the spatial dynamics of the 1918 influenza in India even though Mills  highlighted its importance through his description of its effects on India. The aim of this study is to use a comprehensive dataset to identify important features of the 1918–19 influenza pandemic in India that are of interest for the understanding of influenza epidemics. Striking findings include a reduction in peak-week mortality, a deceleration in velocity, a prolonging of the epidemic wave, and an overall reduction in virulence of the Spanish Influenza as it spread across India.
Analyzing diffusion patterns of pandemics is difficult, as it depends upon various factors including place-specific public health responses, social interactions among people, travel patterns within cities and across countries, the natural and built environments, and characteristics of the pathogens themselves [5, 23, 24]. For the Spanish Influenza, Crosby  concluded that "the factors at work in the pandemic were so numerous … that very few generalities can be drawn." One such generality, also observed in India, was the phenomenon of two distinct epidemic waves, a mild one in the spring or summer of 1918, and a second and much more lethal one in the autumn or winter . Some countries experienced a third wave in 1919 or 1920 . In an early attempt to characterize the spread of the pandemic, Pyle  presented diffusion patterns of the disease alongside those of other influenza epidemics of the 20th century. For England, Mexico and Peru, Chowell et al. [14, 25, 26] identified spread patterns, estimating mortality and transmissibility rates and distinguishing between rural and urban areas. Across Europe, several researchers including Ansart et al.  and Erkoreka  estimated the mortality burden of the 1918 Pandemic. In addition, early in the second wave, long distance infections were the predominant mode of transmission, with local infections becoming more frequent as the epidemic became widespread .
In India, the second wave originated in Bombay in September 1918, simultaneously spreading north and south, and reaching Sri Lanka and the northern Indian provinces in October 1918 [11, 30]. The pandemic is believed to have originated from influenza-infected World War I troops returning home [7, 11, 12, 31, 32]. The disease was passed on to and spread amongst civilian populations in different regions. Transportation systems aided the spread of the disease. In the case of India, the Sanitary Commissioner in his report  noted that "The railway played a prominent part as was inevitable" (p.61; see also Pyle and Patterson ).
The statistical data are obtained from the sanitary reports of the provinces or presidencies of Assam, Bengal, Bihar and Orissa, Bombay, Central Provinces, Madras, Northwest Frontier Province, Punjab, and United Provinces for the five-year period from 1916 to 1920 [33, 34]. The data were copied from these public reports and entered into a database for analysis. This places 1918, the peak year of the pandemic in India, in the temporal center of the dataset. The nine aforementioned provinces formed the major administrative units of India that were directly ruled by the British. The boundary files for district maps were created by modifying modern-day district boundaries using the information in the census atlas of India  to arrive at the colonial district boundaries in 1918.
The Sanitary Commissioner  (p. 64) reported four syndromes associated with the pandemic influenza, "(a) febrile, (b) bronchial, (c) intestinal, [and] (d) meningeal." The provincial sanitary reports contain monthly counts of deaths from "fevers" for 213 districts from 1916–1920. While "fevers" encompass a variety of conditions, the vast majority of the deaths from the pandemic were recorded under this heading, with the 11,134,441 reported fever deaths far exceeding the decennial mean of 4,308,356 . While data were also reported on mortality from respiratory diseases, we chose to use the "fevers" data because pneumonia and bronchopneumonia were often complications that followed an attack of influenza rather than occurring, like fevers, when the disease itself peaked. Therefore, fevers are a more accurate indicator of when the influenza was occurring in a particular locale. Second, and equally importantly, the "fevers" heading shows a much more dramatic spike in mortality during the pandemic than the "respiratory diseases" heading. Data on influenza cases, while desirable, are unavailable, hence the focus of this paper is on the information conveyed by the mortality statistics instead. These data show a steep spike in fever mortality in late 1918, reflecting the autumn wave of the pandemic. Therefore, while we recognize that the "fever" heading may also have contained deaths from other fever-causing diseases, most importantly seasonal malaria, we focus on the "fevers" data category for this analysis after adjusting it for the presence of seasonal fever deaths from all causes . As is demonstrated below, the use of the "fevers" data does not pose a serious problem for the estimation of the timing of peak influenza-attributable mortality in the districts because of the sheer number of deaths from the pandemic. For this reason, we use seasonally adjusted deaths from "fevers" to capture the temporal and spatial characteristics of the pandemic.
To study patterns of propagation of influenza across the districts, we used the data on the wave to compute four sets of two measures each to capture timing, length, severity, and shape of the wave. The timing of the wave was measured using (i) the date on which the wave peaked (T max) and (ii) the midpoint in time of the wave (i.e., halfway between the start- (T start) and end-dates (T end) of the wave, or ).
Summary statistics on dynamics of the autumn wave* of the 1918 influenza pandemic ( n = 213 districts)
CATEGORY OF VARIABLE
Mean and Standard Deviation
SEVERITY OF WAVE
Peak Excess Mortality
Standardized Peak Excess Mortality
LENGTH OF WAVE
Mean Time to Mortality (Days)
Duration of Wave (Weeks)
TIMING OF WAVE
Peak Date of Wave
Nov. 16, 1918
Midpoint of Wave
Dec. 03, 1918
SHAPE OF WAVE
Variance of Wave
The diminishing virulence and velocity of the epidemic wave and its lengthening as it progressed through India raises the important epidemiological question of why. Coupled with the observation that the spread in the northern portion of India was less spatially uniform than the spread earlier and elsewhere (Figures 2, 5, and the clip in the Additional file 1: Video clip), a number of possible explanations come to mind. Key among them is an important theme in the theory of evolution of epidemics --- competition among strains of a rapidly evolving virus can produce an equilibrium in which the predominant strain is less virulent and slower to travel than the strain that predominated at the onset of the epidemic [43–45].
A second key explanation could be weather. Recent studies suggest that absolute humidity constrains both influenza virus survival and transmission efficiency [46, 47]. The crucial summer monsoon rains were described as follows by the Sanitary Commissioner  (p.47):
"(iii) The monsoon rains (June to September) began earlier than usual, but were very weak over nearly the whole country outside of Burma and northeast India. The deficiency in the seasonal rainfall was as much as 81 per cent. in Sind, 75 per cent. in Rajputana West, 70 per cent. in Baluchistan, 63 per cent. in Guzerat, and about 50 per cent. in the United Provinces West, the Punjab, Rajputana East, Central India East, Berar, the Konkan, the Bombay Deccan, Mysore, and Malabar."
The findings of this paper, while not confirmatory, are broadly consistent with both notions, the theory of evolution of viral pathogens in an epidemic and the association with weather patterns. Given the complexity of epidemics, however, a number of additional factors may have been at play. These include knowledge of the pandemic that may have reached the eastern part of the country via conferences held on the topic , allowing simple social distancing measures to be enacted [6, 48] and early detection through influenza awareness of inspectors and doctors , thereby lowering virulence in the later stages of the epidemic. Another possible interpretation is that populations in the north and east of India may have acquired a higher degree of immunity, or cross-protection from the first wave of the influenza and therefore were not as severely affected by the second wave as their southern and western counterparts [49–51]. The deceleration of the epidemic as it radiated outward from Bombay may also have resulted from multiple influenza carriers being introduced at once into a susceptible population in Bombay, thereby spreading the virus faster, while fewer influenza carriers traveled across the country on account of the rapid and severe onset of the disease . The spread from west to east may be explained by the virus being introduced through European troops. In particular, some British Indian troops were stationed in France during World War I, and the first returnees in India most likely disembarked in western India . Finally, rurality may have contributed to the weakening of the pandemic’s spread .
As the centenary of the 1918–1919 pandemic approaches, scholars are returning to its study to design appropriate pandemic control strategies [54–56]. By establishing a baseline picture of how the worst epidemiologic disaster of the modern era unfolded at its global focal point, it is hoped that this study will prompt future research that delves into the complex factors that created and shaped it spatially and temporally [8, 57, 58]. The lengthening and weakening of the pandemic wave as it swept across India also has broad implications for pandemic control strategies. The duration and intensity of pandemic control measures will need to be judiciously calibrated to the variable nature of any future pandemic wave. In scenarios resembling the 1918 pandemic as it unfolded in India, locations close to an entry point will have extremely short windows of time to deal with a virulent pathogen, placing emphasis on the emergency management of a short and severe wave of illness. While locations that are distant from the entry point will have longer windows of time to prepare for and deal with less lethal variants of the disease, their task will be prolonged by the more gradual build-up and subsidence of the epidemic wave.
Ethical approval was not required for the research conducted in this study.
- Glass RJ, Glass LM, Beyeler WE, Min HJ: Targeted social distancing design for pandemic influenza. Emerg Infect Dis. 2006, 12: 1671-1681. 10.3201/eid1211.060255.View ArticlePubMedPubMed CentralGoogle Scholar
- Bonabeau E, Toubiana L, Flahault A: The geographical spread of influenza. Proc Royal Soc London Ser B: Biol Sci. 1998, 265: 2421-2425. 10.1098/rspb.1998.0593.View ArticleGoogle Scholar
- Cliff AD, Haggett P: Spatial aspects of epidemic control. Prog Hum Geogr. 1989, 13: 315-347.View ArticleGoogle Scholar
- Cliff AD, Haggett P: Time, travel and infection. Br Med Bull. 2004, 69: 87-99. 10.1093/bmb/ldh011.View ArticlePubMedGoogle Scholar
- Viboud C, Bjørnstad ON, Smith DL, Simonsen L, Miller MA, Grenfell BT: Synchrony, waves, and spatial hierarchies in the spread of influenza. Science. 2006, 312: 447-451. 10.1126/science.1125237.View ArticlePubMedGoogle Scholar
- Hobday RAP, Cason JWP: The open-air treatment of pandemic influenza. Am J Public Health. 2009, 99: S236-S242. 10.2105/AJPH.2008.134627.View ArticlePubMedPubMed CentralGoogle Scholar
- Crosby AW: America’s Forgotten Pandemic: The influenza of 1918. 2003, New York, NY: Cambridge University PressView ArticleGoogle Scholar
- Johnson NPAS, Mueller J: Updating the accounts: global mortality of the 1918-1920" Spanish" influenza pandemic. Bull Hist Med. 2002, 76: 105-115. 10.1353/bhm.2002.0022.View ArticlePubMedGoogle Scholar
- Taubenberger JK, Morens DM: 1918 Influenza: the mother of all pandemics. Rev Biomed. 2006, 17: 69-79.Google Scholar
- Jordan E: Epidemic Influenza: A survey. 1927, Chicago, IL: American Medical AssociationGoogle Scholar
- Patterson KD, Pyle GF: The geography and mortality of the 1918 influenza pandemic. Bull Hist Med. 1991, 65: 4-21.PubMedGoogle Scholar
- Pyle GF: The Diffusion of Influenza: Patterns and Paradigms. 1986, Totowa, NJ: Rowman & Littlefield Pub IncorporatedGoogle Scholar
- Barry J: The Great Influenza: The Epic Story of the Deadliest Plague in History. 2004, New York: Penguin GroupGoogle Scholar
- Chowell G, Viboud C, Simonsen L, Miller MA, Acuna-Soto R: Mortality patterns associated with the 1918 influenza pandemic in Mexico: evidence for a spring herald wave and lack of preexisting immunity in older populations. J Infect Dis. 2010, 202: 567-575. 10.1086/654897.View ArticlePubMedPubMed CentralGoogle Scholar
- Viboud C, Eisenstein J, Reid AH, Janczewski TA, Morens DM, Taubenberger JK: Age- and sex-specific mortality associated with the 1918–1919 Influenza Pandemic in Kentucky. J Infect Dis. 2013, 207: 721-729. 10.1093/infdis/jis745.View ArticlePubMedGoogle Scholar
- Potter CW: A history of influenza. J Appl Microbiol. 2008, 91: 572-579.View ArticleGoogle Scholar
- Vynnycky E, Trindall A, Mangtani P: Estimates of the reproduction numbers of Spanish influenza using morbidity data. Int J Epidemiol. 2007, 36: 881-889. 10.1093/ije/dym071.View ArticlePubMedGoogle Scholar
- Minton J, Vanderbloemen L, Dorling D: Visualizing Europe’s demographic scars with coplots and contour plots. Int J Epidemiol. 2013, 42: 1164-1176. 10.1093/ije/dyt115.View ArticlePubMedPubMed CentralGoogle Scholar
- Chandra S: Deaths associated with influenza pandemic of 1918–19 Japan. Emerg Infect Dis. 2013, 19 (4): 616-622. 10.3201/eid1904.120103.View ArticlePubMedPubMed CentralGoogle Scholar
- Davis K: The Population of India and Pakistan. 1951, Princeton, NJ: Princeton University PressGoogle Scholar
- Chandra S, Kuljanin G, Wray J: Mortality from the Influenza Pandemic of 1918–1919: the case of India. Demography. 2012, 49: 857-865. 10.1007/s13524-012-0116-x.View ArticlePubMedGoogle Scholar
- Mills ID: The 1918–1919 Influenza Pandemic – the Indian experience. Indian Econ Soc History Rev. 1986, 23 (1): 1-40. 10.1177/001946468602300102. XXIIIView ArticleGoogle Scholar
- McLafferty S: Placing pandemics: geographical dimensions of vulnerability and spread. Eurasian Geogr Econ. 2010, 51: 143-161. 10.2747/1539-718.104.22.168.View ArticleGoogle Scholar
- Balcan D, Colizza V, Gonçalves B, Hu H, Ramasco JJ, Vespignani A: Multiscale mobility networks and the spatial spreading of infectious diseases. Proc Natl Acad Sci. 2009, 106: 21484-21489. 10.1073/pnas.0906910106.View ArticlePubMedPubMed CentralGoogle Scholar
- Chowell G, Luís MAB, Niall J, Wladimir JA, Cécile V: The 1918–1919 influenza pandemic in England and Wales: spatial patterns in transmissibility and mortality impact. Proc R Soc B. 2008, 275: 501-509. 10.1098/rspb.2007.1477.View ArticlePubMedGoogle Scholar
- Chowell G, Viboud C, Simonsen L, Miller M, Hurtado J, Soto G, Vargas R, Guzman M, Ulloa M, Munayco C: The 1918–1920 influenza pandemic in Peru. Vaccine. 2011, 29: B21-B26.View ArticlePubMedPubMed CentralGoogle Scholar
- Ansart S, Pelat C, Boelle F-Y, Carrat F, Flahault A, Valleron A-J: Mortality burden of the 1918–1919 influenza pandemic in Europe. Influenza Other Respir Viruses. 2009, 3: 99-106. 10.1111/j.1750-2659.2009.00080.x.View ArticlePubMedPubMed CentralGoogle Scholar
- Erkoreka A: The Spanish influenza pandemic in occidental Europe (1918–1920) and victim age. Influenza Other Respir Viruses. 2010, 4: 81-89. 10.1111/j.1750-2659.2009.00125.x.View ArticlePubMedGoogle Scholar
- Eggo RM, Cauchemez S, Ferguson NM: Spatial dynamics of the 1918 influenza pandemic in England, Wales and the United States. J R Soc Interface. 2011, 8: 233-243. 10.1098/rsif.2010.0216.View ArticlePubMedGoogle Scholar
- Chandra S, Sarathchandra D: The influenza pandemic of 1918–1919 in Sri Lanka: its demographic cost, timing, and propagation. Influenza Other Respir Viruses. 2014, 8: 267-273. 10.1111/irv.12238.View ArticlePubMedPubMed CentralGoogle Scholar
- Fee E, Brown TM, Lazarus J, Theerman P: The influenza pandemic of 1918. Am J Public Health. 2001, 91: 1953-10.2105/AJPH.91.12.1953.View ArticlePubMedPubMed CentralGoogle Scholar
- Smallman–Raynor M, Johnson N, Cliff AD: The spatial anatomy of an epidemic: influenza in London and the county boroughs of England and Wales, 1918–1919. Trans Inst Br Geogr. 2002, 27: 452-470. 10.1111/1475-5661.00065.View ArticleGoogle Scholar
- Sanitary Commissioner: Annual Report of the Sanitary Commissioner with the Government of India. 1920, Calcutta: Superintendent of Government PrintingGoogle Scholar
- India Sanitary Commissioners: Annual Reports of the Sanitary Commissioners of Assam, Bihar and Orissa, Bengal, Bombay, Central Provinces, Madras, North West Frontier Provinces, Punjab and United Provinces of Agra and Oudh Government Press. 1916–20, Sanitary Commissions: Provincial Government PressesGoogle Scholar
- Singh RP: India Administrative Atlas 1872–2001. A historical perspective of evolution of districts and states in India. 2004, Delhi: Government of IndiaGoogle Scholar
- Gomez V, Maravall A: Guide for Using the Programs TRAMO and SEATS, Beta Version. 1997, Madrid: Banco de EspañaGoogle Scholar
- SAS Institute Inc: Inc. SI. SAS/ETS 9.3 User’s Guide. 2011, Cary, NC: SAS Institute IncGoogle Scholar
- CDC: Epidemic Disease Occurrence. Office SEaPDP. Edited by: Principles of Epidemiology in Public Health Practice. 2012, Washington, D.C: Center for Disease Control and Prevention, 3Google Scholar
- Trevelyan B, Smallman‒Raynor M, Cliff AD: The spatial structure of epidemic emergence: geographical aspects of poliomyelitis in north‒eastern USA, July–October 1916. J R Stat Soc A Stat Soc. 2005, 168: 701-722. 10.1111/j.1467-985X.2005.00372.x.View ArticleGoogle Scholar
- Cliff AD, Haggett P, Ord JK: Spatial Aspects of Influenza Epidemics. 1986, London: PionGoogle Scholar
- Cliff AD, Haggett P: Methods for the measurement of epidemic velocity from time-series data. Int J Epidemiol. 1982, 11: 82-89. 10.1093/ije/11.1.82.View ArticlePubMedGoogle Scholar
- Cliff AD, Haggett P, Smallman-Raynor M: An exploratory method for estimating the changing speed of epidemic waves from historical data. Int J Epidemiol. 2008, 37: 106-112. 10.1093/ije/dym240.View ArticlePubMedGoogle Scholar
- Frank SA: Models of parasite virulence. Q Rev Biol. 1996, 71: 37-78. 10.1086/419267.View ArticlePubMedGoogle Scholar
- Day T, Proulx SR: A general theory for the evolutionary dynamics of virulence. Am Nat. 2004, 163: E40-E63. 10.1086/382548.View ArticlePubMedGoogle Scholar
- Berngruber TW, Froissart R, Choisy M, Gandon S: Evolution of virulence in emerging epidemics. PLoS Pathog. 2013, 9: e1003209-10.1371/journal.ppat.1003209.View ArticlePubMedPubMed CentralGoogle Scholar
- Shaman J, Kohn M: Absolute humidity modulates influenza survival, transmission, and seasonality. Proc Nat Acad Sci USA. 2009, 206 (9): 3243-3248. doi:10.1073/pnas.0806852106View ArticleGoogle Scholar
- Shaman J, Pitzer VE, Viboud C, Grenfell BT, Lipsitch M: Absolute humidity and the seasonal onset of influenza in the Continental United States. PLoS Biol. 2010, 8: e1000316-10.1371/journal.pbio.1000316.View ArticlePubMedPubMed CentralGoogle Scholar
- He D, Dushoff J, Day T, Ma J, Earn DJD: Inferring the causes of the three waves of the 1918 influenza pandemic in England and Wales. Proc R Soc B. 2013, 280: doi:10.1098/rspb.2013.1345Google Scholar
- Rios-Doria D, Chowell G: Qualitative analysis of the level of cross-protection between epidemic waves of the 1918–1919 influenza pandemic. J Theor Biol. 2009, 261: 584-592. 10.1016/j.jtbi.2009.08.020.View ArticlePubMedGoogle Scholar
- Barry JM, Viboud C, Simonsen L: Cross-protection between successive waves of the 1918–1919 influenza pandemic: epidemiological evidence from US Army camps and from Britain. J Infect Dis. 2008, 198: 1427-1434. 10.1086/592454.View ArticlePubMedPubMed CentralGoogle Scholar
- Mathews JD, McBryde ES, McVernon J, Pallaghy PK, McCaw JM: Prior immunity helps to explain wave-like behaviour of pandemic influenza in 1918–9. BMC Infect Dis. 2010, 10: 1-9. 10.1186/1471-2334-10-1.View ArticleGoogle Scholar
- Jeffery K: ‘An English Barrack in the Oriental Seas’? India in the Aftermath of the First World War. Mod Asian Stud. 1981, 15: 369-386. 10.1017/S0026749X00008635.View ArticleGoogle Scholar
- McSweeny K, Colman A, Fancourt N, Parnell M, Stantiall S, Rice G, Baker M, Wilson N: Was rurality protective in the 1918 influenza pandemic in New Zealand?. N Z Med J. 2007, 120: U2579-PubMedGoogle Scholar
- Morens DM, Fauci AS: The 1918 Influenza Pandemic: insights for the 21st Century. J Infect Dis. 2007, 195: 1018-1028. 10.1086/511989.View ArticlePubMedGoogle Scholar
- Andreasen V, Viboud C, Simonsen L: Epidemiologic characterization of the 1918 influenza pandemic summer wave in Copenhagen: implications for pandemic control strategies. J Infect Dis. 2008, 197: 270-278. 10.1086/524065.View ArticlePubMedPubMed CentralGoogle Scholar
- Chandra S, Kassens-Noor E, Kuljanin G, Vertalka J: A Geographic analysis of population density thresholds in the Influenza Pandemic of 1918–19. Int J Health Geogr. 2013, 12: http://www.ij-healthgeographics.com/content/12/1/9,Google Scholar
- Murray CJL, Lopez AD, Chin B, Feehan D, Hill KH: Estimation of potential global pandemic influenza mortality on the basis of vital registry data from the 1918–20 pandemic: a quantitative analysis. Lancet. 2006, 368: 2211-2218. 10.1016/S0140-6736(06)69895-4.View ArticlePubMedGoogle Scholar
- Mills CE, Robins JM, Lipsitch M: Transmissibility of 1918 pandemic influenza. Nature. 2004, 432: 904-906. 10.1038/nature03063.View ArticlePubMedGoogle Scholar
- The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2334/14/510/prepub
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