Influenza Pandemic Symposium
Excess mortality patterns during 1918–1921 influenza pandemic in the state of Arizona, USA

https://doi.org/10.1016/j.annepidem.2017.12.005Get rights and content

Abstract

Purpose

Our understanding of the temporal dynamics and age-specific mortality patterns of the 1918–1921 influenza pandemic remains scarce due to lack of detailed respiratory mortality datasets in the United States and abroad.

Methods

We manually retrieved individual death records from Arizona during 1915–1921 and applied time series models to estimate the age specific mortality burden of the 1918–1921 influenza pandemic. We estimated influenza-related excess mortality rates and mortality rate ratio increase over baseline based on pneumonia and influenza (P&I), respiratory, tuberculosis and all-cause death categories.

Results

Based on our analysis of 35,151 individual mortality records from Arizona, we identified three successive pandemic waves in spring 1918, fall 1918–winter 1919 and winter 1920. The pandemic associated excess mortality rates per 10,000 population in Arizona was estimated at 83 for P&I, 86 for respiratory causes, 84 for all-causes and 9 for tuberculosis. Age-specific P&I and tuberculosis excess death rates were highest among 25- to 44-year-olds and individuals ≥65 years, respectively. The 25- to 44-year-olds and 5- to 14-year-olds had highest P&I and tuberculosis mortality impact respectively when considering the ratio over background mortality.

Conclusions

The 1918–1921 influenza pandemic killed an estimated 0.8% of the Arizona population in three closely spaced consecutive waves. The mortality impact of the fall 1918 wave in Arizona lies in the upper range of previous estimates reported for other US settings and Europe, with a telltale age distribution of deaths concentrated among young adults. We identified a significant rise in tuberculosis-related mortality during the pandemic, lending support to the hypothesis that tuberculosis was a risk factor for severe pandemic infection. Our findings add to our current understanding of the mortality impact of this pandemic in the US and globally.

Introduction

Pandemic preparedness may be enhanced through a detailed understanding of past pandemics. In particular, the 1918–1920 influenza pandemic, commonly referred to as the “Spanish” flu, is the most devastating influenza pandemic on record [1]. It caused anywhere between 50–100 million deaths globally with a mortality rate of 2.5–5 per 1,000 and approximately 675,000 deaths in the United States alone [1]. In contrast to seasonal influenza epidemics that primarily affect the very young and elderly [2]; the 1918–20 pandemic was characterized by an atypical mortality elevation among young adults [3], [4]. It has been estimated that half of the influenza-related deaths associated with this pandemic occurred among young adults aged 20–40 years [2], [3]. In parallel, several studies in Europe [5], [6], and the US [7] reported low or negative excess mortality among senior populations, suggesting a substantial clinical protection in this age group. Another unusual feature of this pandemic is the rapid succession of pandemic waves over a period of 9–12 months [2], [3], [8].

Up to two distinct 1918 pandemic waves have been identified in 1918 in a number of areas of the world including US cities [7], [9], [10]. The first “herald” wave likely started between February [7] and March 1918 [2] followed by a major pandemic wave in September of the same year [2], [7], [9]. Estimates of the mortality impact of this pandemic relying on mortality data from 24 US states with vital registration systems in place during the pandemic range from 0.25% in Wisconsin to 1% in Colorado [11]. These estimates are imprecise however, as they rely on analyzing annual all-cause mortality data, an approach that poorly controls for background deaths unrelated to influenza. More refined quantitative mortality studies based on daily, weekly or monthly respiratory and all-cause mortality data have estimated the excess pneumonia and influenza (P&I) mortality rate at 51.8 and 42.9 per 10,000 populations in New York City [7] and Kentucky [10] during the fall pandemic wave, respectively. Further studies are needed for a more comprehensive account of the pandemic impact in the US; however intensive efforts to retrieve historical individual-level mortality data make such detailed studies prohibitive [12].

A long-standing debate surrounding the 1918 pandemic is the potential role of tuberculosis in driving the unusually high impact of this outbreak, as tuberculosis was predominant among adults in the early 20th century [13]. It has been observed that tuberculosis mortality in the United States increased sharply during the 1918–1919 pandemic period, followed by a significant decline in tuberculosis mortality rates in the subsequent 2 years, compared to rates during the pre-pandemic period [14], [15]. However, it is unknown whether such patterns are consistent at different spatial scales.

A better understanding of the factors that shaped the mortality patterns during the 1918–1920 influenza pandemic in diverse geographic settings can lead to improved pandemic preparedness plans [16]. Here, we set out to comprehensively analyze the age-specific absolute and relative mortality impact of the pandemic and the role of tuberculosis in the state of Arizona using 35,151 mortality records manually retrieved from the Arizona Genealogy Database in the years surrounding the pandemic.

Section snippets

Study setting

The state of Arizona is located in the southwest United States, bordering Mexico. It became a state of the United States only a few years before the 1918 influenza pandemic. Arizona's climate is arid with a landscape ranging from low-elevation deserts in the south to mountains and forests in the north. Arizona's population increased by 64% in 10 years, from 204,354 in 1910 to 334,162 in 1920 [17].

During late 1800s and early to mid-1900, the state of Arizona was a popular destination for

Results

P&I and respiratory deaths accounted for 37% and 42% of the total recorded mortality in 1918, respectively, while these causes of death represented only an average of 10% and 16% of total mortality in pre-pandemic years (1915–1917). This indicates a 2 to 4-fold increase in P&I and respiratory deaths in 1918 compared to non-pandemic years. In the years following 1918, deaths due to P&I and respiratory deaths started to decline compared to 1918.

Unlike P&I and respiratory deaths, tuberculosis

Discussion

In this study, we characterized the mortality impact of three influenza pandemic waves during the 1918–1920 by age and cause of death in the state of Arizona. The pandemic was associated with an excess mortality rate per 100,000 of 82.8 for P&I, 86.1 for respiratory causes, 84.1 for all causes and 8.6 for tuberculosis. Our estimates fall in the upper range of estimates previously reported for several U.S. settings [7], [10], [11]. While P&I, respiratory, and all-cause excess mortality rates

Acknowledgments

We thank Nirmal Vijayavel, April Cobos, Justin Cheung, Indira Harahap, Shane Dwyer, and Andrew Soule for supporting early data collection efforts. SD was a Fulbright fellow during her MPH studies at the School of Public Health at Georgia State University. LD is a 2CI doctoral fellow at Georgia State University. KM acknowledges support from the Japanese Society for the Promotion of Science (JSPS) KAKENHI Grant Number 15K20936 and 26893048 and from Program for Advancing Strategic International

References (35)

  • M.A. Miller et al.

    The signature features of influenza pandemics—implications for policy

    N Engl J Med

    (2009)
  • J. Luk et al.

    Observations on mortality during the 1918 influenza pandemic

    Clin Infect Dis

    (2001)
  • S.D. Collins

    Excess mortality from causes other than influenza and pneumonia during influenza epidemics

    Public Health Rep

    (1932)
  • D.R. Olson et al.

    Epidemiological evidence of an early wave of the 1918 influenza pandemic in New York City

    Proc Natl Acad Sci U S A

    (2005)
  • G. Chowell et al.

    Death March of 1918

    Natural History

    (2017)
  • C. Viboud et al.

    Age-and sex-specific mortality associated with the 1918–1919 influenza pandemic in Kentucky

    J Infect Dis

    (2013)
  • G. Chowell et al.

    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)
  • Cited by (26)

    • Geospatial Variability in Excess Death Rates during the COVID-19 Pandemic in Mexico: Examining Socio Demographic, Climate and Population Health Characteristics

      2021, International Journal of Infectious Diseases
      Citation Excerpt :

      Summary statistics of these variables from 31 states and Mexico City are provided in Table 1. For both the national data and the data for each state, we separately estimated the baseline mortality level by fitting cyclical Serfling regression models to all-cause deaths in the non-COVID-19 period, after excluding data from March 2020 to April 2021 by employing established methodology (Chowell et al., 2014, Chowell et al., 2012, Dahal et al., 2018a, Serfling, 1963, Viboud et al., 2013). Details on the model equation that was used can be found in (Dahal et al., 2021).

    • Historical and clinical aspects of the 1918 H1N1 pandemic in the United States

      2019, Virology
      Citation Excerpt :

      Historic analysis of available death statistics from select US cities also suggest the appearance of an initial “herald” wave surfacing in the spring of 1918. Findings include a distinct influenza and pneumonia mortality age-shift with increasing deaths in young adults occurring in New York City (Olson et al., 2005), St. Joseph, Missouri (Hoffman, 2011), and the state of Arizona (Dahal et al., 2018). Opie (Opie et al., 1919) reported on an explosive spring outbreak of influenza and pneumonia at Camp Funston, with over 1000 men hospitalized from a population of 30,000.

    • A review of the 1918 herald pandemic wave: importance for contemporary pandemic response strategies

      2018, Annals of Epidemiology
      Citation Excerpt :

      This hypothesis has been investigated by uncovering, reviewing, and analyzing century-old morbidity and mortality data using modern analytical methods. Such data originated from nearly forgotten mortality and morbidity reports available from surveillance systems established in the United States and Europe 100 years ago (see e.g. [1–5]) and from labor-intensive compilation of church records, graveyards, and individual death certificates (e.g. [5–10]). To distinguish the impact of the 1918 pandemic virus from that of seasonal influenza or other respiratory pathogens, epidemiologists have relied on the unique “signature” mortality age pattern associated with the lethal autumn 1918 wave, characterized by an atypical and dramatic increase in mortality risk in young adults, consistently observed across many studied locations [1,2,4–7,9,11–14].

    View all citing articles on Scopus
    View full text