Figure 5 shows indexed monthly post-neonatal mortality rates for the influenza epidemic in comparison with the other years in the data set. The x-axis shows the year running from July 1918 to June 1919, to capture the entire epidemic year. The graph shows that the second wave, peaking in Derbyshire in November 1918, raised post-neonatal mortality well above its normal seasonal winter peak. Figure 6 shows that mortality for the second year of life was strongly affected in the first and third waves as well as the second, the third wave peaking slightly earlier than for all age groups. In contrast neonatal mortality and the stillbirth rate (Figure 7 and Figure 8) show different patterns. Neonatal mortality appears to have peaked in the third wave: mortality rates were highest in February but also high in April and June. This three-pronged pattern might suggest a lagged effect of the three waves (although the lag is not the same in each case), which would be consistent with the hypothesis that influenza in the first or second trimester of pregnancy increased prematurity rates and consequently neonatal mortality.42 The effect on stillbirths appears to have been concentrated in the second wave with its prolonged high rates. As with neonatal mortality, however, the September peak could represent the delayed first wave, but with a shorter lag, and the question then arises of why the second wave appears to have had an immediate effect. Figure 7 and Figure 8 are drawn to the same scale as Figure 5 and Figure 6, revealing that although in some months the risks of neonatal mortality and stillbirth were around twice as high for the same months in other years, the increases in the risks of death before one month of age were not as great as those for post-neonatal and early child mortality.
| Figure 5 Indexed post-neonatal period monthly death rates in Derbyshire, late 1918 and early 1919 (monthly averages for other years 1917–22=100). (Source: Derbyshire health visitor data.) |
| Figure 6 Indexed early childhood period monthly death rates in Derbyshire, late 1918 and early 1919 (monthly averages for other years 1917–22=100). (Source: Derbyshire health visitor data.) |
| Figure 7 Indexed neonatal period monthly death rates in Derbyshire, late 1918 and early 1919 (monthly averages for other years 1917–22=100). (Source: Derbyshire health visitor data.) |
| Figure 8 Indexed period stillbirth rates in Derbyshire, late 1918 and early 1919 (monthly averages for other years 1917–22=100). (Source: Derbyshire health visitor data.) |
Period death rates identify the time periods at which more deaths occurred, but the comparison of different influences on health and survival needs the identification of children at risk of dying during the epidemic. In other words, it is necessary to isolate a cohort of those who were born in a given time and were therefore in a particular age group during the epidemic. Children at highest risk of stillbirth can be identified simply by their dates of birth: those born between September 1918 and January 1919 were at highest risk and period and cohort rates are identical. It is also easy to identify those at risk of neonatal mortality during the epidemic by date of birth, because as the neonatal period is relatively short, most infants spent all of it or none of it during the epidemic. Also, because the period of risk is just one month following the birth, the cohort death rates for neonatal mortality in Figure 9 show a similar pattern to Figure 7 (although different enough to detect a clearer three month lag from the first and second waves of the epidemic to peaks in October and February). Those born between January and April 1919 are identified as those at greatest risk of neonatal mortality during the epidemic.
| Figure 9 Indexed cohort neonatal mortality rates in Derbyshire, late 1918 and early 1919 (monthly averages for other years 1917–22=100). (Source: Derbyshire health visitor data.) |
It is more difficult to identify those at risk of post-neonatal mortality because infants are at risk for a much longer time. For example, children born in early 1918 would have been in peril from this form of death towards the end of their first year, at the beginning of the epidemic. Children born at the end of 1918 would have been at risk only during their early post-neonatal period, and at the end of the epidemic. Children born in the spring and early summer of 1918 would have been exposed to the entire epidemic during their post-neonatal period. Figure 10 shows monthly post-neonatal mortality rates, distinguishing those born in each month of 1918 from those born in the corresponding month of other years, and demonstrates that, unsurprisingly, all infants born in 1918 were at elevated risk from the epidemic, as they all spent at least part of their post-neonatal lives exposed to the influenza virus. Those born during the summer of 1918 (particularly between July and September) had a much higher risk of dying. Such infants were in their early post-neonatal period at the peak of the second, most virulent wave, and were still in this age group during the third wave. Those born in February 1918, spending the first two waves in this age group had the greatest excess risk, and it is unclear why those infants born in March and April 1918, who were exposed to all three waves, did not suffer as much. The problem of identification is more acute for early child mortality and has not been attempted.
| Figure 10 Indexed cohort post-neonatal mortality rates in Derbyshire, late 1918 and early 1919 (monthly averages for other years 1917–22=100). (Source: Derbyshire health visitor data.) |
Once the cohorts at most risk have been identified, it is possible to quantify and compare the result of exposure to the epidemic of a child born at a particular date with other influences such as multiple birth, legitimacy, parental occupation, number of rooms in the house, urban/rural residence and so on. Such a comparison can be made by using multivariate hazard analysis (for post-neonatal and neonatal mortality) and logistic analysis (for the risk of stillbirth) and the following analyses show the risks of babies being stillborn, of dying in the neonatal period, and of dying in the post-neonatal period associated with birth during the influenza epidemic, while controlling for the effect of other influences on the risk of mortality.43 In the tables each odds ratio is derived from a different analysis, either examining risk of different forms of death (i.e. stillbirth, neonatal mortality, or post-neonatal mortality), or assessing the risks associated with being born at a different time period. The odds ratios show the multiplicative increase in the risk of death for infants born during particular time periods and thus at risk during the influenza epidemic. Thus Table 2 shows that infants born at any time in the second or third waves of the epidemic (July 1918 to April 1919) were 1.247 times (or 25 per cent) more likely to be stillborn than infants born at another time in the 1917 to 1922 period. Those born in the second wave (September 1918 to January 1919) were 1.535 times (or over 50 per cent) more likely to be stillborn. Similarly, while those born in the second or third waves were 1.326 times (or 33 per cent) more likely to die in the neonatal period, those born in early 1919 and at risk in the third wave were at highest risk, being 1.776 times (or over 75 per cent) more likely to die before reaching one month of age. Those born during 1918 were 50 per cent more likely to die between the ages of one month and one year, but the risks of post-neonatal mortality were highest for those born between July and September 1918, who were young during the second wave, still at risk during the third wave, and who were nearly twice as likely to have died.
| Table 2 Increases in mortality connected with being born in time periods which put infants at risk during the 1918–19 influenza epidemic in Derbyshire: stillbirths, neonatal mortality and post-neonatal mortality examined separately |
In order to help identify the ways in which infants were at risk, be it from death from influenza itself, from some complication such as pneumonia, or via maternal health, the analyses were performed separately for different cause of death categories.44 Causes of death in infancy were notoriously poorly recorded in the early twentieth century, with inaccurate, inconsistent diagnoses and a large proportion relegated to the unknown category.45 However, broad causal groupings can minimize these problems while still being instructive. The problems of cause of stillbirth reporting are potentially even greater, as such births did not have to be registered and medically certified.46 However, a reasonably high proportion of stillbirths in the data set have a cause attributed, and although some are rather speculative, many others identify recognized conditions or circumstances such as prematurity, complications of labour, congenital malformations or implicate the ill-health of the mother.
The ways in which influenza caused stillbirths will be considered first. Obviously foetuses in the womb were not at risk of catching influenza in the same way that infants already born were. The only way an unborn child could have been affected by the influenza virus was if its mother were afflicted.47 While comparatively few mothers were recorded as having suffered from influenza, unspecified ill-health was frequently mentioned as a cause of stillbirth, in addition to accident or shock prior to delivery and overexertion. It is reasonable to assume that during the epidemic year a large proportion of unspecified maternal ill-health would have been influenza. Figure 11, showing the proportions of all births associated with maternal ill-health for each quarter of the years 1917 to 1922, suggests that a higher proportion of stillbirths and infant deaths were attributed to maternal ill-health during the epidemic year than in the following years (the first quarter of 1917 is unusually high, and other high rates in 1917 and 1918 could be due to a build up in the influenza epidemic as suggested by Johnson48). However the effect was not dramatic and maternal ill-health may just have been a convenient scapegoat for an otherwise inexplicable stillbirth at any time, an effect exacerbated during the epidemic. Table 3, showing the odds ratios for stillbirths associated with periods of particular risk and different causal groups, while controlling for other factors, confirms the overriding importance of the health of the mother. Infants born during the third wave of the epidemic were 1.928 times (i.e. nearly twice) as likely to be stillborn due to maternal ill-health than infants born at other times.
| Figure 11 The proportion of all births in Derbyshire associated with maternal ill-health, by quarter, 1917–22. (Source: Derbyshire health visitor data.) |
| Table 3 Increases in stillbirth rates connected with being born in time periods which put infants at risk during the 1918–19 influenza epidemic in Derbyshire: different causes of stillbirth examined separately |
Given that influenza may have provoked early labour or interruption of pregnancy, it is also not surprising that the risk of stillbirth due to complications of pregnancy (mainly ante-partum haemorrhage, eclampsia and placenta praevia) rose during the epidemic, although the poor fit of this model warns against placing too much reliance on these figures. The risk of stillbirth due to complications of labour, however, did not rise for births during the epidemic, reflecting the more mechanical nature of such problems, which were dominated by contracted pelvis, prolapse of cord, malpresentation, and a prolonged labour. The risk of malformation with maternal rubella during pregnancy is well known, and there are also risks of abnormalities with non-specific viral illnesses,49 and some for influenza itself.50 The increased odds ratio for stillbirths due to congenital malformations, although not significant, is therefore unsurprising. The lack of significance may be attributable to their small numbers or possibly to the fact that mild abnormalities now classed under newborn encephalopathy (seizures, abnormal consciousness, difficult respiration or feeding, abnormal tone or reflexes) may not have been well enough defined to be classed as congenital defects and, if there was an alternative putative reason such as the mother's health, stillbirths might have been attributed to another causal group.
Table 3 confirms that the additional risks of stillbirth during the influenza epidemic were concentrated under causes specific to the mother's health and pregnancy. Given that the route by which influenza affected the health of unborn infants was via the mother's health, and that neonatal mortality is strongly dependent on the condition of the newborn infant, it also seems plausible that the health of neonates would have been affected by maternal health. This opens the possibility that interruption of a woman's pregnancy due to influenza may have resulted not in a stillbirth but in a live premature or abnormal birth, perhaps after exposure earlier in pregnancy.51 There may therefore have been a larger pool than usual of particularly vulnerable infants at risk of neonatal death. Although such infants may not have succumbed to influenza, the epidemic can be held to have contributed to their death by making them vulnerable to other causes. Table 4 explores this possibility by showing the odds ratios associated with birth at the key periods of the epidemic for the risk of neonatal mortality from different causal groups.
| Table 4 Increases in neonatal mortality connected with being born in time periods which put infants at risk during the 1918–19 influenza epidemic in Derbyshire: different causes of death examined separately |
The most striking results in the table are those which indicate the direct and associated deaths from the epidemic. The two and a half fold risk of neonatal death from the residual group (in which influenza deaths were placed) associated with birth in the third wave of the epidemic suggests that very new babies may have succumbed directly to the disease itself. Inspection of the records suggests that in a large number of these cases the mother was also afflicted. There was an almost identical risk of dying from pneumonia, an associated cause. Even though influenza was not implicated in these deaths, it is very likely that the underlying cause was indeed the 'flu and that poor certification and recording were responsible for underestimation of the effect of influenza.
In addition Table 4 shows that infants born in the third wave (January to April 1919) were 76 per cent more likely to have died from prematurity, wasting and congenital malformations than infants born at other times. This could be taken as support for the proposition that the epidemic created a larger proportion of premature births. However, the fact that viruses such as influenza are also likely to have been connected with malformations suggests another route.
Table 5 separates the prematurity, wasting and congenital malformations group into three and presents the odds ratios for birth during the epidemic for the risk of death from each subcategory. This table suggests that those born during the influenza pandemic ran no additional risk of early death from congenital malformation, and although there was an additional risk of dying from prematurity it was not significant. For those born between January and April 1919, however, the risk of dying in the neonatal period due to wasting was nearly three times higher than normal. This might suggest that infants who caught influenza very young died from subsequent weakness, but it is also compatible with infants disadvantaged as a result their mothers having contracted influenza. The poor recording of the causes of infant deaths has already been mentioned, and the younger the infant at death, the worse the problem. Prematurity was not well defined and, in the absence of the accurate estimation of gestational age, is difficult to assess. Although it was often stated in connection with stillbirths, it may not have been routinely noted for live births in the health visitors' ledgers. Infants who were born premature but who did not die immediately are likely to have had their death recorded under some other heading, even though prematurity may have contributed towards their death. The wasting category includes many causes that would be perfectly compatible with premature infants: “marasmus”, “innutrition”, “malnutrition”, “macerated”, “wasting”, “weakly”, “delicate”, “feeble”, “debility”, “inanition”, “exhaustion”. The lack of distinction between the causal groups, and particularly the problem with identifying premature infants, is one of the reasons for grouping into the broader category, and also suggests that it might not be legitimate to rule out a larger pool of premature weakly children as a cause of higher neonatal death during the epidemic.
| Table 5Increases in neonatal mortality connected with being born in time periods which put infants at risk during the 1918–19 influenza epidemic in Derbyshire: sub-categories of the prematurity, wasting and congenital malformations cause of death examined (more ...) |
Prematurity and conditions within the womb are less likely to have affected post-neonatal mortality, as the most vulnerable infants might already have died during the neonatal period. Table 6 shows that indeed the excess risks for those born in 1918, and particularly for those born in February and exposed during the first and second waves, were concentrated in the risk of death from the infectious disease group, which includes influenza. The risk of dying from these causes was two and a half times greater for children born in 1918 than at any other time, and nearly six times greater for those born in February. It is interesting that although there was a 33 per cent higher chance of dying from bronchitis and pneumonia for those born during the epidemic, this was not significant, perhaps because of small numbers, or perhaps because influenza was mentioned more often for older infants in the health visitors' ledgers.52 For infants exposed during the epidemic, the risk of dying from wasting diseases remained much higher in the post-neonatal period, nearly twice as high for those at risk during any part of the epidemic, and nearly five times as high for those born between July and September. There is a possibility that this can be accounted for by some weakly children who survived into the early post-neonatal period, but this is unlikely as, when the second month of life is excluded, the odds ratio increases to 2.191 (4.362** for those born in February and 5.140*** for those born in the summer), suggesting that older infants were more likely to die of wasting. These infants could have been weakened by the epidemic and succumbed to other causes of death later. A further possibility is that infants whose mothers had influenza were put at risk by their mother's ill health: not directly as stillbirths and possibly neonates were, but indirectly through a very sick mother's inability to feed and care for her children. Infants whose mothers have died are always at higher risk, at least partly because of the lack of breast milk, and it is plausible that mothers who were afflicted with influenza were forced to wean their infants earlier than they might otherwise have done, or that their milk supply was not as plentiful or nutritious as it would normally have been. Infants born in the summer of 1918 and still below the normal weaning age of six to nine months at the height of the second wave would have been particularly vulnerable, and therefore at increased risk of mortality from wasting diseases.
| Table 6 Increases in post neonatal mortality connected with being born in time periods which put infants at risk during the 1918–19 influenza epidemic in Derbyshire: different causes of death examined separately |
Figure 12 shows the percentages of infants in observation at each month whose feeding method was known, who were still being breast fed.53 The broken lines show those born between June and August 1917 and demonstrate that when they were six months old, and before the second wave of the influenza epidemic struck, over 70 per cent of children were still receiving some breast milk. The solid lines show those born in the same months a year later, who were still young and therefore most at risk of early weaning during the influenza epidemic. At six months old not much more than 60 per cent of these infants were being breastfed. There are many other influences on the duration of breast-feeding which this graph does not take into account, so although it is not conclusive, it does suggest that ill-health among mothers may have forced them to wean their infants earlier during the epidemic. The fact that nearly half the monetary value of emergency help given to 'flu victims in Manchester between 4 December 1918 and 11 January 1919 was in the form of the dried baby milk, Glaxo, lends added weight to this suggestion.54
| Figure 12 Percentage of infants in observation at each age who were still receiving breast milk: comparing those born in Derbyshire in the summers of 1917 and 1918. (Source: Derbyshire health visitor data.) |