Natality decline and miscarriages associated with the 1918 influenza pandemic: the Scandinavian and United States experiences

Abstract

Background: Although pregnancy is a recognized risk factor for severe influenza infection, the effect of influenza on miscarriages and births remains unclear. We examined the relationship between influenza and birth rates during the 1918 pandemic in the United States, Denmark, Sweden, and Norway.

Methods: We compiled monthly birth rates from 1911 through 1930 in 3 Scandinavian countries and the United States, identified periods of unusually low or high birth rates, and quantified births as "missing" or "in excess" of the normal expectation. Using monthly influenza data, we correlated the timing of peak pandemic exposure and depressions in birth rates, and identified pregnancy stages at risk of influenza-related miscarriage.

Results: Birth rates declined in all study populations in spring 1919 by a mean of 2.2 births per 1000 persons, representing a 5%-15% drop below baseline levels (P < .05). The 1919 natality depression reached its trough 6.1-6.8 months after the autumn pandemic peak, suggesting that missing births were attributable to excess first trimester miscarriages in ∼1 in 10 women who were pregnant during the peak of the pandemic. Pandemic-related mortality was insufficient to explain observed patterns.

Conclusions: The observed birth depressions were consistent with pandemic influenza causing first trimester miscarriages in ∼1 in 10 pregnant women. Causality is suggested by temporal synchrony across geographical areas.

Figure 1.

Timing of influenza pandemic and birth rate reduction in Denmark, Norway, Sweden, and the United States. A, Time series of monthly natality rates in Denmark during several decades surrounding the 1918 pandemic. It can be seen that an unusual and unseasonal birth rate depression occurred in early 1919, followed by an equally unusual increase (compensation) from late 1919 through early 1920. The natality patterns are typical for natality data from each of the populations studied. B, Time series of residual natality rates after subtracting out the expected (modeled) baseline, contrasted with the peak influenza (flu) periods, for Denmark (DK), Norway (NO), Sweden (SE), and the United States (US). For each study population, the severe autumn 1918 peak was followed by a temporary period of compensation 6–9 months later. This decline is attributed to first trimester miscarriages among a subset of all pregnant women who had pandemic influenza. The shaded areas represent the 95% confidence intervals P&I deaths indicate respiratory mortality due to pneumonia and influenza.

Figure 2.

Asynchrony in timing of influenza (flu) activity and birth patterns across Denmark. The influenza epidemic struck Copenhagen (Cph) 1–2 months before it hit the rural areas in Denmark. The delayed effect is mirrored by the birth depression, with the birth rate at its lowest in Copenhagen 1–2 months prior to the low point in rural Denmark. The shaded area represents the 95% confidence interval, which happened to be the same for Copenhagen and rural Denmark.

Figure 3.

Lack of trends in monthly stillbirths in Denmark. Stillbirths are shown as excess numbers per 1000 live births, after normalization by long-term mean. Although there is a significant excess of stillbirths in November 1918 and January 1919, it is not a particularly dramatic or long-lasting signal. The red lines indicate the 95% confidence interval (CI).

Figure 4.

Delayed effect of 1918 influenza (flu) on births as a result of miscarriage. The depression in birth rates occurring in spring 1919 and lasting several months is consistent with a number of first-trimester miscarriages in women who fell ill with influenza.