The mother’s risk of premature death after child loss across two centuries

The death of a child is arguably one of the most stressful events that a parent can experience. Grief is the natural emotional response to such loss and has been described across human populations (Lindemann, 1944; Bowlby, 1980; Parkes, 2014; Boyden et al., 2014; Einarsdóttir, 2004). Intense or prolonged grief can induce behaviours and physiological states that are detrimental to health and survival. Thus, child loss has been associated with elevated risks of psychiatric symptoms (Kreicbergs et al., 2004), psychiatric hospitalizations (Li et al., 2005) and sickness absence (Wilcox et al., 2015), cardiovascular disease (Li et al., 2002a; Li et al., 2003a), and some cancers (Fang et al., 2011; Huang et al., 2013; Li et al., 2002b). Studies also suggest that parents, particularly mothers, who lose a child face increased risk of death (Li et al., 2002a; Li et al., 2003a; Levav et al., 1988; Li et al., 2003b; Qin and Mortensen, 2003; Agerbo, 2005; Rostila et al., 2012; Rostila et al., 2015; Espinosa and Evans, 2013; Harper et al., 2011; Chen et al., 2012; Schorr et al., 2016), both from suicide and natural causes. The aforementioned studies were all conducted in affluent developed populations, where infant mortality rates are low and life expectancy is high. In contemporary developing nations, infant mortality rates (number of deaths during first year per 1000 live births) >50 are common, whereas in developed nations they are usually lower than eight (United Nations, 2015). Parent-child attachment in pre-industrial and developing populations has been a matter of debate, with some historians arguing for parental reluctance to invest emotions in children where mortality rates are high, while others argue that parents' attachment and grief after child loss is similar across human populations, past and present (Magnússon, 2010; Woods, 2003). One way to shed light on this issue is to study the impact of child loss on parent mortality in the same population before and after a demographic transition that dramatically altered infant mortality rates.

Here, we examine the association between child loss and parent mortality in Iceland from 1817 until 2015, a period that spans a drastic transition from a poor agricultural society to an affluent industrial society. One marker of this drastic change is that infant mortality rates in Iceland (per 1000 births) dropped from one of the highest known values in history, 238 in 1881–1885 (Jónsson and Magnússon, 1997), to one of the lowest, 2.07 in 2005–2010 (Statistics Iceland, 2019). We used a comprehensive genealogical database to assess whether the relative rate of parent mortality after child loss changed during this transition, and to determine whether this rate was further affected by factors such as parent’s sex and age at loss, the number of children as well as the age of the lost child. In line with some previous studies (Li et al., 2003b), we used parent mortality as a measure of the cumulative health response to the emotional and physiological strain of child loss. While mortality obviously does not capture the entire range of such reactions, it has the advantage of being reliably recorded at different times in a genealogical database.

We followed all Icelandic parents, born 1800 or later, from the birth of their first child (earliest from 1817) until death or to the end of 2015 (see further in Materials and methods). From 1817 to 2015, 64 044 parents lost at least one child (Supplementary file 1 - Table 1). The proportion of parents who experienced child loss decreased from 61.1% among parents born 1800–1880 to 5.2% among parents born 1931–1996. To adjust for potential confounding by socioeconomic status or other familial factors that might affect the risk of mortality, our primary analyses were focused on the 47,711 parents who lost a child and had at least one sibling who did not lose a child (N = 126,342). Compared to their siblings who did not lose a child, parents who lost a child were more likely to be women, have more children, be younger at first childbirth and older at cohort entry, and have a longer follow-up time (p<0.05; Table 1). Similar patterns were observed for mothers and fathers who lost a child, respectively (Supplementary file 1 - Table 2).

Parent mortality rate after child loss across two centuries

We used a conditional Cox proportional hazards model to contrast the mortality rates of parents who lost at least one child to their respective siblings who did not (Figure 1). Throughout the entire study period, we observed an elevated hazard ratio (HR) of overall mortality rate among parents who lost a child (1.04; 95% confidence interval [CI] 1.02–1.06), which was mostly driven by maternal (HR 1.07; 95% CI 1.04–1.10) rather than paternal mortality rates (HR 1.02; 95% CI 0.99–1.05; p-for-difference=0.0096). Figure 1 shows that there are no obvious temporal trends in the hazard ratios, except for an increase in mortality rate after child loss for parents born after 1930 (p-for-difference = 0.002 when compared to parents born 1800–1930). Similar results were obtained from the population-based matched cohort and a subset of this cohort with identifiable siblings, separately, (Figure 1—figure supplement 1), albeit with greater HRs revealing the importance of the sibling-controlled design to adjust for unmeasured familial confounding factors. The HRs changed minimally after exclusion of parent-child pairs with the same date of death (Figure 1—figure supplement 2).

Figure 1 with 2 supplements see all

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Child loss and premature maternal mortality rate

As the average life expectancy of Icelanders increased considerably from 1817 to the present, we performed separate analyses of parent mortality before and after the age of 50 years (Figure 2). Before the age of 50, mothers who lost a child experienced increased mortality (HR 1.36; 95% CI 1.27–1.45) during the whole study period with the HRs consistently elevated across all seven birth cohorts (Figure 2a). For mothers, the relative mortality rate increase ranged from 35% (born 1800–1930) to 64% (born after 1930), yet was not statistically significantly different between these two cohorts (p=0.0641). In contrast, no such excess mortality was observed for fathers who lost a child in any of the birth cohorts (HR for entire observation period 1.04; 95% CI 0.97–1.11). Interestingly, the excess maternal mortality rates before the age of 50 after child loss seem limited to loss of a child younger than 18 years, while the elevation in paternal mortality rates are more notable after loss of an adult child (Table 2). The difference between mothers and fathers in excess mortality rate before the age of 50 is particularly marked after loss of infants, representing 59% of child losses during the study period. These results were robust to the exclusion of mothers who died within a week after giving birth (Figure 2—figure supplement 1), making it unlikely that the higher mortality rate in mothers is explained by delivery or postpartum complications that resulted in the deaths of both newborn and mother (Nour, 2008).

Figure 2 with 6 supplements see all

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The study period spans two centuries of drastic demographic transition in Iceland, from a poor developing nation with a particularly high infant mortality rate, to a modern affluent nation with one of the lowest rates of infant mortality in history. Although we observed a more modest elevation in overall parent mortality rates after child loss before 1930 compared to thereafter, the most striking finding is the consistent increase in premature maternal deaths in response to child loss throughout the 199 years of observation.

This study leverages a unique nationwide data source of genealogies with virtually complete follow-up over a 199 year period spanning an extreme change in indicators of societal development, for example infant and child mortality rate. Although based on an unusually large set of data, our study has several limitations that should be noted. First, we have no information about the causes of death for children or parents. Such data could be used to help verify the causal relationship between deaths of children and parents and to uncover patterns in the causes of death among parents (e.g. suicide or cardiovascular deaths) after child loss. Some impact of reverse causation, for example the ill-health of parents increasing the mortality risk of their children, cannot be ruled out. However, the health and welfare of children was even more dependent on their parents, particularly fathers, in pre-demographic transition (pre-welfare state times) societies. The relatively stable effect estimates of parent mortality rates after child loss across calendar periods and the consistently lower impact of child loss on paternal mortality argues against a strong influence of reverse causality. Second, we did not have direct information about the socioeconomic status of parents. However, as socioeconomic status tends to cluster in families, our sibling-controlled analysis is likely to adjust for much of the confounding due to this source. Third, it is possible that the fragmented registration of births in earlier times (particularly in the case of infant deaths) resulted in misclassification of some parents who had truly lost a child and, thus, somewhat conservative estimates of excess parent mortality rates in earlier times. Last, in the sibling cohort, parents who lost a child differed somewhat from those that did not lose a child with respect to sex, number of children, age at first birth, age at entry to the cohort, length of follow-up time and age at death. We therefore made every effort to adjust for these covariates in our analyses. We adjusted for age at follow-up and sex in all analyses and presented separate results for the different birth cohorts. We further performed subgroup analyses by age of parents at loss (or matching), parent age at first childbirth, follow-up time and number of children alive at loss, and demonstrated that the association between child loss and parent mortality is observed across the range of these covariates. Indeed, parents who lost a child may have to live longer to experience such an event, however, such survivor bias (if any) due to a selection of survivors to the exposed group would rather yield conservative estimates of parent mortality after a child loss. On the other hand, the siblings used for comparison that were not yet parents at the age as when the index parents lost a child may have a survival advantage, which could yield exaggerated estimates of parent mortality after child loss. However, we observed similar results in a sensitivity analysis that was restricted to unexposed siblings who were already parents at the same age as when the index parents lost a child.

The large increase in the rate of premature maternal mortality after child loss in 19^th century Iceland suggests that mothers formed strong emotional bonds with their children – in spite of very harsh conditions and a strong expectation of child loss. This is consistent with accounts of intense grieving among mothers who lost a child in a contemporary developing society (Einarsdóttir, 2004). In contrast, the paternal mortality response to child loss is much weaker throughout the observation period and only statistically significant for older fathers (i.e. parent mortality after 50 years of age) born after 1930.

What could account for this stable sex difference in parent mortality rate after child loss? One possibility is a difference in the attachment of mothers and fathers to their children, which could result in a greater emotional response of mothers and concomitant psychological and physiological consequences. Throughout the 199-year study period, mothers may have had greater opportunity than fathers to form early emotional attachment to their infants through gestation and breastfeeding. Although historical accounts suggest that breastfeeding may have been rarer in 19th to early 20th century Iceland (Garðarsdóttir, 2005) than in the present, it does not seem to have prevented mothers from forming strong emotional bonds with their children as illustrated by the elevated risks of maternal death after child loss. It is possible that females are born with a tendency to form stronger emotional bonds with children than males. Although our results cannot disentangle the impact of nature and nurture in this context, it is interesting to note that the mortality response of fathers to child loss before the age of 50 has not significantly increased despite the greater contribution of fathers to the postnatal care of children in recent decades (Huerta et al., 2014).

Another possible explanation for our findings is a sex difference in the emotional response to traumatic events in general. Women have been reported to have a greater risk of mental disorders after exposure to emotional trauma than men (Tolin and Foa, 2006). The intensity of such responses may result in a multitude of other mental and physical ailments which in turn can affect the risk of mortality through, for example suicide (Wilcox et al., 2009; Panagioti et al., 2012; Gradus et al., 2010) and cardiovascular disease (Song et al., 2019; Edmondson et al., 2013; Gradus et al., 2015). Previous studies in contemporary developed populations have reported evidence for greater risk of psychiatric hospitalizations (Li et al., 2005) and mortality (Li et al., 2003b) after child loss in mothers than in fathers. Interestingly, an opposite sex difference is seen for mortality rate after spousal loss, where mortality rate elevation is more pronounced among widowers than widows (Moon et al., 2011; Shor et al., 2012). However, this difference may in part be due to a greater dependence of older males on social and emotional support provided by spouses. A similar mechanism is indicated in our results, namely the increased mortality of older parents after child loss in more recent times.

Our results show that even in the poor agricultural population of 19th century Iceland, with one of the highest infant mortality rates measured in humans, there was a considerable impact of child loss on premature maternal mortality rates. This contradicts claims that mothers in poor cultures adapt to high infant mortality rates with reduced emotional investment (as reviewed in Woods, 2003). Indeed, one implication of our findings is that child loss is likely to constitute a major threat to the survival of mothers in societies with high infant mortality rates. Taken together these findings highlight the importance of the mother-child bond and the extensive health threats that arise when it is broken.

The data used in this study are compiled in the Genealogy database (Íslendingabók) at deCODE Genetics and are available for review on site, on request. The use of these data is in accordance with Icelandic law and with permission of the Icelandic Bioethics Committee. Therefore, the authors cannot make the dataset publicly available. On the other hand, interested researchers can obtain data access upon approvals by the Icelandic Bioethics Committee (https://www.vsn.is/en) and by contacting the corresponding authors.

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Author details

1. Unnur A Valdimarsdóttir

   1. Center of Public Health Sciences, Faculty of Medicine, University of Iceland, Reykjavik, Iceland
   2. Department of Epidemiology, Harvard TH Chan School of Public Health, Boston, United States
   3. Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Solna, Sweden

   Contribution

   Conceptualization, Supervision, Funding acquisition, Methodology, Writing—original draft, Writing—review and editing

   Contributed equally with

   Donghao Lu

   For correspondence

   unnurav@hi.is

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-5382-946X

2. Donghao Lu

   1. Center of Public Health Sciences, Faculty of Medicine, University of Iceland, Reykjavik, Iceland
   2. Department of Epidemiology, Harvard TH Chan School of Public Health, Boston, United States
   3. Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Solna, Sweden
   4. Channing Division of Network Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, United States

   Contribution

   Formal analysis, Methodology, Writing—original draft, Writing—review and editing

   Contributed equally with

   Unnur A Valdimarsdóttir

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-4186-8661

3. Sigrún H Lund

   deCODE Genetics, Reykjavik, Iceland

   Contribution

   Formal analysis, Writing—review and editing

   Competing interests

   No competing interests declared

4. Katja Fall

   1. Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Solna, Sweden
   2. Clinical Epidemiology and Biostatistics, School of Medical Sciences, Örebro University, Örebro, Sweden

   Contribution

   Writing—review and editing

   Competing interests

   No competing interests declared

5. Fang Fang

   Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Solna, Sweden

   Contribution

   Writing—review and editing

   Competing interests

   No competing interests declared

6. Þórður Kristjánsson

   deCODE Genetics, Reykjavik, Iceland

   Contribution

   Project administration, Writing—review and editing

   Competing interests

   No competing interests declared

7. Daníel Guðbjartsson

   1. deCODE Genetics, Reykjavik, Iceland
   2. School of Engineering and Natural, Sciences, University of Iceland, Reykjavik, Iceland

   Contribution

   Supervision, Methodology, Writing—review and editing

   Competing interests

   No competing interests declared

8. Agnar Helgason

   1. deCODE Genetics, Reykjavik, Iceland
   2. Department of Anthropology, University of Iceland, Reykjavik, Iceland

   Contribution

   Conceptualization, Data curation, Supervision, Writing—original draft, Writing—review and editing

   Contributed equally with

   Kári Stefánsson

   Competing interests

   No competing interests declared

9. Kári Stefánsson

   1. deCODE Genetics, Reykjavik, Iceland
   2. Faculty of Medicine, School of Health Sciences, University of Iceland, Reykjavik, Iceland

   Contribution

   Conceptualization, Data curation, Writing—review and editing

   Contributed equally with

   Agnar Helgason

   For correspondence

   kstefans@decode.is

   Competing interests

   No competing interests declared

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  citations for umbrella DOI https://doi.org/10.7554/eLife.43476