Original Article
Mortality After the Death of a Spouse in Norway Elinor Ytterstad,a and Tormod Brennb Background: Previous studies on mortality of widowed individuals have produced varying estimates of mortality after the death of a spouse. This variation is because of the various data types used and methodologies applied, as well as to the failure to account for sources of bias. Methods: We followed all married individuals in Norway (1,801,456 individuals) for 32 years, and information on marital status and death was collected for use in a new application of survival analysis in this field of research. Results: We compared mortality of widowed individuals with that of married individuals. Widowed men and women had hazard ratios of 1.34 (95% confidence interval 1.31, 1.36) and 1.29 (1.26, 1.31), respectively, for the first year after spousal death. For the same period, values were highest in ages 60–64 years with 1.78 (1.57, 1.98) in men and 1.50 (1.35, 1.65) in women. Values dropped gradually with age and more rapidly in men than women to a low for ages 85–89 years of 1.24 (1.19, 1.29) in men and 1.25 (1.20, 1.31) in women. The risk was much higher 1 to 7 days after spousal death (1.69 [1.49, 1.88] in men and 1.76 [1.56, 1.96] in women), then it dropped during the first year and from then on remained stable to year 10, which was the last year considered. Conclusion: A considerable excess mortality risk was observed in widowed men and women from immediately after the loss of a spouse and for the next 10 years. (Epidemiology 2015;26: 289–294)
W
hen a loved one dies it can have an effect on the health of those left behind, not only after but also in some instances even before the death occurs.1 Mortality after the death of a spouse has attracted special interest, and several studies have documented that survivors of spousal death have a higher mortality than married individuals.2 However, there is substantial heterogeneity in the magnitude of values reported Submitted 4 July 2014; accepted 15 January 2015. From the aDepartment of Mathematics and Statistics, and bDepartment of Community Medicine, UiT The Arctic University of Norway, N-9037 Tromsø, Norway. The authors report no conflict of interest. Supplemental digital content is available through direct URL citations in the HTML and PDF versions of this article (www.epidem.com). Correspondence: Elinor Ytterstad, Department of Mathematics and Statistics, UiT The Arctic University of Norway, N-9037 Tromsø, Norway. E-mail: [email protected]. Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 1044-3983/15/2603-0289 DOI: 10.1097/EDE.0000000000000266
Epidemiology • Volume 26, Number 3, May 2015
in various studies.3 This variation may be because of differences in study size or data type, a lack of updated data on marital status, the inclusion of moderating factors, and the choice of statistical methodology. It is not an easy task to estimate the precise excess mortality after spousal death, and one major element that contributes to the difficulty is the misclassification of marital status. Indeed, when marital status is recorded at baseline only, without updates during the follow-up period, severe biases can occur.4 Moreover, there are several methodological challenges that come into play when conducting studies on mortality after the death of a spouse. For example, excess mortality among widowed individuals has been found to be especially high when the spouse dies from accidental, violent, or alcohol-related causes.5 In such instances, the true effect of spousal death can be hard to distinguish from those of a common accident. Another challenge is that similar people tend to marry each other, and these similarities may carry through to predispositions to illnesses and death. Spouses also share a common environment, which may very well have a similar influence on their health.6,7 To care properly for widowed individuals and launch preventive efforts, we must know the extent and pattern of the excess mortality as well as understand the reasons behind. Although most widowed individuals eventually come to terms with their loss, there is substantial variation between individuals when it comes to how intensely the loss is felt, and the time needed to adjust to it. Studies have pointed out the effect of loss of income and social support, as well as grief and emotional stress.8 Reactions to spousal death are many; one suggested categorization is as follows: affective, cognitive, behavioral, physiologicalsomatic, and immunologic and endocrine changes.9 The aim of this study was to estimate the excess mortality after spousal death by sex, age, and time since spousal death in a large population (1.8 million married individuals) with a 32-year follow-up in Norway. Marital status was updated annually, and the mortality was considered for various times since spousal death, from 1 day to 10 years. To the best of our knowledge, for the first time in this field of research, survival analysis modeling daily excess mortality rates and utilizing a life table for married men and women was applied.
MATERIALS AND METHODS Study Population Data were provided by Statistics Norway, based on the 1970 population census. The data are not available to the public. www.epidem.com | 289
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For the sake of anonymity, the unique Norwegian 11-digit personal identification number was substituted with a study reference number before we received the data. All inhabitants of Norway who were born in 1952 or earlier and were still alive on January 1, 1975 (n = 2,292,865) were included. Individuals who appeared twice or thrice (n = 757 records from 378 different individuals), were born outside Norway (n = 47,357), or were unmarried, separated, or divorced as of January 1, 1975 (n = 443,295) were excluded, thereby reducing the study population to 1,801,456 married individuals. The number of men and women were 912,597 and 888,859, respectively, and mean age in 1975 were 49.3 and 46.8 years. The data record contained annually updated marital status (unmarried, married, widowed, separated, or divorced) and updated spousal reference numbers during 32 years of follow-up (1975–2006), in addition to sex, year of birth, and, for those who died during follow-up, date of death. Figure 1 illustrates the number of individuals who moved out of the married category during follow-up. Individuals who separated or divorced (n = 198,786) were censored as of the corresponding year. Individuals with missing information on marital status for a specific year were also censored (n = 20,414 married individuals and n = 928 among widowed individuals). Finally, widowed individuals who remarried were also censored (n = 8,882). A total of 291 spousal pairs (582 married individuals) died on the same day. These individuals are included in the analysis in the group of those who were married and died during the study period (n = 508,592); not as widowed, as it was not known who died first, ie, which was the widowed spouse.
Statistical Analyses Life tables (presented in eTable 1; http://links.lww.com/EDE/ A885) for married men and women were produced for the follow-up period, based on all individuals categorized as married at the beginning of a given year, according to the method described by Statistics Norway.10 These tables contain mortality rates by sex, age (each year from 54 to 100 years of 1.1.1975 Married (n=1,801,456)
n=219,200
n=508,592 n=494,735
1.1.1975−31.12.2006 Censored
1.1.1975−31.12.2006 Dead
age) and calendar period (5-year intervals from 1975–1979 to 1995–1999 and 2000–2006). As the youngest married individuals were 23 years of age in 1975, it was only possible to derive life-table values for the last year included (2006) for those age 54 years or more. The mortality of widowed men and women was then compared with the mortality rates in the life tables using survival analysis. Survival time for each of the 494,735 individuals who were widowed during follow-up was defined as days from date of spousal death until the death of the widowed individual, censoring because of remarriage or missing information on marital status, or the end of the study period, whichever occurred first. The age at spousal death was calculated as the difference between the year of spousal death and the year of birth. Survival analysis with the additive excess mortality model was used to estimate hazard rates: α i (t ) = µi (t ) + γ (t ) .11 The rate α i (t ) expresses the individual mortality for a widowed individual i, at day t after spousal death as a sum of a standard mortality µi and an additional excess risk γ. The standard mortality is the mortality rate from the life table for a married individual with the same sex, age, and calendar period. The additional excess risk represents an excess risk because of the change in mortality risk when a spouse dies. The excess mortality may vary by time since spousal death, but is otherwise assumed to be constant in the hazard model we applied. Therefore, a possible sex and age variation was accounted for by categorizing the data into 5- or 10-year age groups before estimating excess mortality. Excess mortality was estimated as the difference between the Nelson-Aalen estimator A (t ) and the accumulated average married mortality M (t ) .12 The excess mortality, which was estimated for each single day t, may be either positive or negative; it would be the latter in cases where the mortality among widowed individuals was lower than that in the married individuals. The hazard ratio (HR) for widowed compared with corresponding married individuals was computed as HR = A(t ) / M (t ) . The expected number of deaths was derived from the life tables by applying survival analysis to corresponding married groups. The confidence intervals (CIs) for HR were calculated based on the fact that the Nelson-Aalen estimator is approximately normally distributed. The CIs for the observed number of deaths are based on the Poisson distribution. Estimation of excess mortality is not available as a standard routine in statistical packages, thus we programmed a routine using the statistical computing language R,13 and the survival package in R.14 This R-code is presented in eAppendix 1 (http://links.lww.com/ EDE/A885).
RESULTS n=9,810
n=277,952
1.1.1975−31.12.2006 Widowed
FIGURE 1. Study population. Norway, 1975–2006. 290 | www.epidem.com
Table 1 displays the absolute number of widowed individuals and number of deaths during the first year after spousal death in selected age groups. The oldest widowed person was 107 years of age. A total of 66,444 women were widowed between 70 and 74 years of age. As expected, because of the well-known tendency of women to marry older men, © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Epidemiology • Volume 26, Number 3, May 2015
Mortality After the Death of a Spouse
TABLE 1. Absolute Numbers of Widowed Individuals and Deaths During the First Year After Spousal Death in Norway, 1975–2006 Age at Spousal Death (Years) 23–54 55–59 60–64 65–69 70–74 75–79 80–84 85–89 90–94 95–107 23–107
Widowed Men
Widowed Women
Total No.
No. Obs
No. Exp
HR (95% CI)
Total No.
No. Obs
No. Exp
HR (95% CI)
9,508 8,202 12,450 17,477 23,661 28,272 25,550 15,167 4,834 745 145,866
63 104 295 611 1,225 2,314 2,938 2,525 1,178 232 11,190a
NA 64.0 166.9 392.2 870.9 1,643.8 2,319.9 2,069.4 969.5 NA 8,496.6
NA 1.64 (1.33, 1.96) 1.78 (1.57, 1.98) 1.57 (1.44, 1.69) 1.42 (1.34, 1.50) 1.43 (1.37, 1.48) 1.28 (1.24, 1.33) 1.24 (1.19, 1.29) 1.25 (1.18, 1.32) NA 1.34a (1.31, 1.36)
31,365 26,756 40,978 55,678 66,444 63,039 43,092 17,574 3,633 310 348,869
105 158 407 784 1,591 2,414 2,837 1,983 695 89 10,869a
NA 113.7 272.8 586.5 1,168.2 1,930.6 2,292.3 1,604.1 543.3 NA 8,510.2
NA 1.39 (1.18, 1.61) 1.50 (1.35, 1.65) 1.34 (1.25, 1.43) 1.37 (1.30, 1.43) 1.26 (1.21, 1.31) 1.25 (1.20, 1.29) 1.25 (1.20, 1.31) 1.31 (1.21, 1.41) NA 1.29a (1.26, 1.31)
a 55-94 years. Obs indicates observed number of deaths; Exp, expected; NA, not available.
and the fact that often men die at earlier ages, the number of widows was considerably larger than widowers. The observed number of deaths in Table 1 exceeded the expected number, showing there were more deaths among widowed individuals than would have been expected if their spouse had not died. As an illustration of the absolute numbers involved, the HR for widows was 1.29, which relates to a 95% CI of 10,688.2– 11,049.8 observed deaths in contrast to the 8,510.2 expected deaths (Table 1).
Table 2 presents the number of observed and expected deaths, and HRs according to time after spousal death. HRs were highest in the first few days after spousal death, then dropped and remained stable and highly significant throughout the tenth year (Table 2). In Figure 2, the excess mortality after spousal death is displayed in terms of HRs by sex, 10-year age groups and time since spousal death on a nonlinear time scale. In the 55- to 64-year age group, 13 widowed men and 26 widowed
TABLE 2. Number of Deaths by Time Since Spousal Death in Widowed Individuals Ages 55 to 94 Years in Norway, 1975–2006 Time Since Spousal Death Days 1–7 8–30 31–100 101–365 1–365 Year 2 3 4 5 6 7 8a 9b 10c 1–10c
Widowed Men
Widowed Women
Observed
Expected
HR (95% CI)
Observed
Expected
HR (95% CI)
294 879 2,278 7,739 11,190
174.5 570.0 1,702.9 6,049.2 8,496.6
1.69 (1.49, 1.88) 1.55 (1.44, 1.65) 1.35 (1.29, 1.40) 1.31 (1.28, 1.34) 1.34 (1.31, 1.36)
300 812 2,179 7,578 10,869
170.6 557.9 1,678.6 6,103.1 8,510.2
1.76 (1.56, 1.96) 1.46 (1.36, 1.56) 1.30 (1.25, 1.36) 1.25 (1.23, 1.28) 1.29 (1.26, 1.31)
9,612 8,837 8,090 7,130 6,630 6,008 5,338 4,802 4,151 70,162
8,038.0 7,559.9 7,082.5 6,575.3 6,076.9 5,438.1 4,984.8 4,508.1 4,103.2 60,688.9
1.25 (1.22, 1.27) 1.25 (1.22, 1.27) 1.25 (1.22, 1.27) 1.21 (1.18, 1.24) 1.25 (1.22, 1.28) 1.26 (1.22, 1.29) 1.25 (1.21, 1.28) 1.27 (1.23, 1.30) 1.24 (1.20, 1.28) 1.26 (1.25, 1.27)
10,315 10,344 10,091 9,897 9,856 9,524 9,366 8,982 8,744 96,948
8,609.4 8,660.0 8,711.8 8,632.2 8,510.7 8,133.0 7,936.0 7,664.0 7,366.4 81,031.9
1.22 (1.20, 1.25) 1.23 (1.21, 1.26) 1.21 (1.19, 1.24) 1.21 (1.19, 1.24) 1.24 (1.22, 1.27) 1.23 (1.21, 1.26) 1.25 (1.23, 1.28) 1.26 (1.23, 1.29) 1.29 (1.26, 1.32) 1.25 (1.24, 1.25)
a
Age 55 to 93. Age 55 to 92. c Age 55 to 91. b
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3.0 2.6 2.2 1.8 1.4
Days
Days
Year
Days
Year
Days
Year
55 − 64
65 − 74
75 − 84
85 − 94
Age (years) at spousal death
women died within 1 week of spousal death, yielding HRs of 2.89 (95% CI: 1.32, 4.46) and 3.48 (2.14, 4.82). For the 75- to 84-year age group, the corresponding numbers rose to 133 (HR: 1.66, 95% CI: 1.38, 1.94) and 141 (HR: 1.68 [1.40, 1.95]; data not shown). Similarly, the total number of deaths was much higher among the oldest men and women (Table 1). As seen in Figure 2, some clear trends appear. First, all HRs are larger than unity, displaying an existing and persistent excess mortality conferred by spousal death. Second, the values declined with age. Third, in the 55- to 64-year age group, the excess mortality is more pronounced among men, but this sex difference gradually disappeared with age. And, finally, the excess mortality was high the first few weeks, then declined sharply and stabilized.
DISCUSSION During 10 years after spousal death, the number of excess deaths among widowed men and women was estimated at 9,473 and 15,916, respectively. This estimate corresponds to 25,389 more deaths among the 494,735 widowed individuals (men and women) than among a corresponding group of married individuals. The importance of these high numbers is further illustrated by findings that the effect of spousal death on mortality is on the rise.15,16 Three published meta-analysis reported estimates of the mortality after spousal death for men and women, respectively, 1.11 and 1.11 (joint 95% CI: 1.08, 1.14) (relative risk),17 1.23 (1.18, 1.28) and 1.04 (1.00, 1.08) (relative risk),3 and 1.27 (1.19, 1.35) and 1.15 (1.08, 1.22) (HR).16 The varying values most likely reflect the diversity of the data types used and methodologies applied. We were able to derive values across 292 | www.epidem.com
Year
1−7 8 − 30 31 − 100 101 − 365 2−3 4−5 6−7 8 − 10a
Time after spousal death
1−7 8 − 30 31 − 100 101 − 365 2−3 4−5 6−7 8 − 10
FIGURE 2. Hazard ratios of mortality by sex, age and time since spousal death. Norway, 1975–2006. Men (solid line) and women (dotted line). aAges 85 to 91. Confidence intervals can be found in Tables 1 and 2.
1−7 8 − 30 31 − 100 101 − 365 2−3 4−5 6−7 8 − 10
1.0
1−7 8 − 30 31 − 100 101 − 365 2−3 4−5 6−7 8 − 10
HR, widowed vs married
3.4
ages and time since loss, and compared with the meta-analyses, our values in general were higher, especially for women. One possible reason for this may be related to the fact that misclassification of marital status has been documented as a serious source of bias in estimates of the mortality after spousal death.4 Indeed, studies on large samples or entire populations often lack updates on the status under investigation, whereas we were able to update our information on marital status. In our analyses, widowed individuals who remarried were censored. However, they comprised only 8,882 of 494,735 individuals. This study had a large amount of suitable data available, with a study population of 1.8 million married individuals including hundreds of thousands of men and women who are widowed or dead, or both. Another strength of this study is the use of life tables. One advantage of this is that the variation in mortality by age and calendar year is incorporated in these tables. Another advantage is that the estimation of excess mortality requires only survival times from widowed individuals. It is therefore unnecessary to obtain survival times from a sample of matched married individuals or any other sample of married people. Third, single-day mortalities can easily be estimated in this model. Other studies have shown a higher excess risk among individuals less than 65 years of age than older individuals,3,5,18,19 or other cut-offs for age have been used.2,20 Our study had the capacity to produce estimates in more age groups, and showed a linear, consistent drop with age, much more among men than women. In contrast to the above-mentioned meta-analyses, we found that, overall, women did not have much less excess risk than men. The reason for this contrast may be that © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Epidemiology • Volume 26, Number 3, May 2015
our study also included very old individuals, and a long follow-up period. Indeed, in their late 50s and 60s, women had much less excess risk than men, but this discrepancy gradually disappeared until it was no longer present in men and women in their 80s. Also, women had less excess risk during the first year after spousal death, but again the sex difference was almost absent when considering the first 10 years combined. Others have found that mortality is much higher immediately after the loss of a spouse.6,19–22 Six months after spousal death has often been used as a cut-point to compare mortality, whereas we were able to consider single days. There was a particularly high number of spouse pairs that died on the same day (291 spousal pairs, 582 individuals). In comparison, the number of spousal pairs that died 1 day apart was much lower (100 spousal pairs, 200 individuals), and continued to decline to a daily average for the first week of 174 individuals, for days 8 to 30 of 151.2 individuals, for days 31 to 100 of 130.4 individuals, and for days 101 to 365 of 118 individuals. Interestingly, as this study provided unique values down to single days, we could also follow how the HRs were especially high in the first days after spousal death before gradually dropping. These numbers suggest that common incidents such as car crashes, fires, and drowning are the reason that a majority of spouse pairs die on the same day or a few days apart. In such instances, it can be impossible to know whether deaths are related solely to a common incident or whether some element of the widowhood effect may be present. If we had considered cause-specific information on death, our study would have been more informative. This is a limitation of the study, and variation of risk across causes of death has been found elsewhere.5 We excluded those who died on the same day, and from the next day we estimated excess mortality irrespective of whether or not deaths might be related to the widowhood effect. Due to this fact, and also as the term excess mortality is used in the statistical model employed, we found this term more precise and correct than the commonly used phrase “widowhood effect.”23 At the other end of the time scale for spousal death, increased mortality risk was still present after 10 years. Marriage has been well documented to improve life length,24 and thus there is no surprise that the excess mortality continues throughout the years of analyses. The HRs in our study illustrates well the persistent and long-lasting elevated mortality risk for many men and women throughout life. A limitation with this study is the lack of information on possible confounders. Socioeconomic status has been described to be important to adjust for in countries like the USA with very marked socioeconomic inequalities in health.23 In that study, the widowhood effect prevailed, but was weakened after adjusting for socioeconomic status. In Norway, health inequalities vary less with socioeconomic status and a smaller effect would thereby be expected. © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Mortality After the Death of a Spouse
CONCLUSION This study not only shines new light on mortality risk after the loss of a spouse but it also paints a more detailed picture across ages and time since loss. Not only men but also women are strongly affected and for a very long time. From the first day after the loss, excess mortality is present and it remains substantially elevated after that.
ETHICS APPROVAL The study was approved by the Data Inspectorate and by the Regional Committee for Medical Research Ethics, North Norway. No informed consent was found necessary because of the type of data and that no details were included that might disclose the identity of the subjects. The study has therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. REFERENCES 1. Shah SM, Carey IM, Harris T, et al. Impact of partner bereavement on quality of cardiovascular disease management. Circulation. 2013;128:2745–2753. 2. Blomgren J, Martikainen P, Grundy E, et al. Marital history 1971–91 and mortality 1991–2004 in England & Wales and Finland. J Epidemiol Community Health. 2012;66:30–36. 3. Moon JR, Kondo N, Glymour MM, et al. Widowhood and mortality: a meta-analysis. PLoS One. 2011;e23465. 4. Korenman S, Goldman N, Fu H. Misclassification bias in estimates of bereavement effects. Am J Epidemiol. 1997;145:995–1002. 5. Martikainen P, Valkonen T. Mortality after the death of a spouse: rates and causes of death in a large Finnish cohort. Am J Public Health. 1996;86:1087–1093. 6. Martikainen P, Valkonen T. Mortality after death of spouse in relation to duration of bereavement in Finland. J Epidemiol Community Health. 1996;50:264–268. 7. Espinosa J, Evans WN. Heightened mortality after the death of a spouse: marriage protection or marriage selection? J Health Econ. 2008;27:1326– 1342. 8. Bowling A. Mortality after bereavement: a review of the literature on survival periods and factors affecting survival. Soc Sci Med. 1987;24:117– 124. 9. Stroebe M, Schut H, Stroebe W. Health outcomes of bereavement. Lancet. 2007;370:1960–1973. 10. Foss AH. Definisjoner og beregningsmetoder for dødelighetstabell. Available at www.ssb.no/a/histstat/not/not_9889.pdf. Statistics Norway 1998. 11. Aalen OO, Borgan Ø, Gjessing HK. Survival and Event History Analysis. New York: Springer; 2008:99–102. 12. Andersen PK, Vaeth M. Simple parametric and nonparametric models for excess and relative mortality. Biometrics. 1989;45:523–535. 13. R Development Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria: The R Foundation for Statistical Computing; 2012. Available at http:// www.R-project.org/. 14. Therneau T. A package for survival analysis in S. R package version 2.36– 12. 2012. 15. Berntsen KN. Trends in total and cause-specific mortality by marital status among elderly Norwegian men and women. BMC Public Health. 2011;11:537. 16. Shor E, Roelfs DJ, Curreli M, et al. Widowhood and mortality: a metaanalysis and meta-regression. Demography. 2012;49:575–606. 17. Manzoli L, Villari P, M Pirone G, et al. Marital status and mortality in the elderly: a systematic review and meta-analysis. Soc Sci Med. 2007;64:77– 94. 18. Smith KR, Zick CD. Risk of mortality following widowhood: age and sex differences by mode of death. Soc Biol. 1996;43:59–71.
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19. Johnson NJ, Backlund E, Sorlie PD, et al. Marital status and mortality: the national longitudinal mortality study. Ann Epidemiol. 2000;10:224–238. 20. Manor O, Eisenbach Z. Mortality after spousal loss: are there socio-demographic differences? Soc Sci Med. 2003;56:405–413. 21. Kaprio J, Koskenvuo M, Rita H. Mortality after bereavement: a prospective study of 95,647 widowed persons. Am J Public Health. 1987;77:283–287.
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22. Schaefer C, Quesenberry CP Jr, Wi S. Mortality following conjugal bereavement and the effects of a shared environment. Am J Epidemiol. 1995;141:1142–1152. 23. Moon JR, Glymour MM, Vable AM, et al. Short- and long-term associations between widowhood and mortality in the United States: longitudinal analyses. J Public Health (Oxf). 2014;36:382–389. 24. Rendall MS, Weden MM, Favreault MM, et al. The protective effect of marriage for survival: a review and update. Demography. 2011;48:481–506.
© 2015 Wolters Kluwer Health, Inc. All rights reserved.
Mortality After the Death of a Spouse in Norway Elinor Ytterstad,a and Tormod Brennb Background: Previous studies on mortality of widowed individuals have produced varying estimates of mortality after the death of a spouse. This variation is because of the various data types used and methodologies applied, as well as to the failure to account for sources of bias. Methods: We followed all married individuals in Norway (1,801,456 individuals) for 32 years, and information on marital status and death was collected for use in a new application of survival analysis in this field of research. Results: We compared mortality of widowed individuals with that of married individuals. Widowed men and women had hazard ratios of 1.34 (95% confidence interval 1.31, 1.36) and 1.29 (1.26, 1.31), respectively, for the first year after spousal death. For the same period, values were highest in ages 60–64 years with 1.78 (1.57, 1.98) in men and 1.50 (1.35, 1.65) in women. Values dropped gradually with age and more rapidly in men than women to a low for ages 85–89 years of 1.24 (1.19, 1.29) in men and 1.25 (1.20, 1.31) in women. The risk was much higher 1 to 7 days after spousal death (1.69 [1.49, 1.88] in men and 1.76 [1.56, 1.96] in women), then it dropped during the first year and from then on remained stable to year 10, which was the last year considered. Conclusion: A considerable excess mortality risk was observed in widowed men and women from immediately after the loss of a spouse and for the next 10 years. (Epidemiology 2015;26: 289–294)
W
hen a loved one dies it can have an effect on the health of those left behind, not only after but also in some instances even before the death occurs.1 Mortality after the death of a spouse has attracted special interest, and several studies have documented that survivors of spousal death have a higher mortality than married individuals.2 However, there is substantial heterogeneity in the magnitude of values reported Submitted 4 July 2014; accepted 15 January 2015. From the aDepartment of Mathematics and Statistics, and bDepartment of Community Medicine, UiT The Arctic University of Norway, N-9037 Tromsø, Norway. The authors report no conflict of interest. Supplemental digital content is available through direct URL citations in the HTML and PDF versions of this article (www.epidem.com). Correspondence: Elinor Ytterstad, Department of Mathematics and Statistics, UiT The Arctic University of Norway, N-9037 Tromsø, Norway. E-mail: [email protected]. Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 1044-3983/15/2603-0289 DOI: 10.1097/EDE.0000000000000266
Epidemiology • Volume 26, Number 3, May 2015
in various studies.3 This variation may be because of differences in study size or data type, a lack of updated data on marital status, the inclusion of moderating factors, and the choice of statistical methodology. It is not an easy task to estimate the precise excess mortality after spousal death, and one major element that contributes to the difficulty is the misclassification of marital status. Indeed, when marital status is recorded at baseline only, without updates during the follow-up period, severe biases can occur.4 Moreover, there are several methodological challenges that come into play when conducting studies on mortality after the death of a spouse. For example, excess mortality among widowed individuals has been found to be especially high when the spouse dies from accidental, violent, or alcohol-related causes.5 In such instances, the true effect of spousal death can be hard to distinguish from those of a common accident. Another challenge is that similar people tend to marry each other, and these similarities may carry through to predispositions to illnesses and death. Spouses also share a common environment, which may very well have a similar influence on their health.6,7 To care properly for widowed individuals and launch preventive efforts, we must know the extent and pattern of the excess mortality as well as understand the reasons behind. Although most widowed individuals eventually come to terms with their loss, there is substantial variation between individuals when it comes to how intensely the loss is felt, and the time needed to adjust to it. Studies have pointed out the effect of loss of income and social support, as well as grief and emotional stress.8 Reactions to spousal death are many; one suggested categorization is as follows: affective, cognitive, behavioral, physiologicalsomatic, and immunologic and endocrine changes.9 The aim of this study was to estimate the excess mortality after spousal death by sex, age, and time since spousal death in a large population (1.8 million married individuals) with a 32-year follow-up in Norway. Marital status was updated annually, and the mortality was considered for various times since spousal death, from 1 day to 10 years. To the best of our knowledge, for the first time in this field of research, survival analysis modeling daily excess mortality rates and utilizing a life table for married men and women was applied.
MATERIALS AND METHODS Study Population Data were provided by Statistics Norway, based on the 1970 population census. The data are not available to the public. www.epidem.com | 289
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For the sake of anonymity, the unique Norwegian 11-digit personal identification number was substituted with a study reference number before we received the data. All inhabitants of Norway who were born in 1952 or earlier and were still alive on January 1, 1975 (n = 2,292,865) were included. Individuals who appeared twice or thrice (n = 757 records from 378 different individuals), were born outside Norway (n = 47,357), or were unmarried, separated, or divorced as of January 1, 1975 (n = 443,295) were excluded, thereby reducing the study population to 1,801,456 married individuals. The number of men and women were 912,597 and 888,859, respectively, and mean age in 1975 were 49.3 and 46.8 years. The data record contained annually updated marital status (unmarried, married, widowed, separated, or divorced) and updated spousal reference numbers during 32 years of follow-up (1975–2006), in addition to sex, year of birth, and, for those who died during follow-up, date of death. Figure 1 illustrates the number of individuals who moved out of the married category during follow-up. Individuals who separated or divorced (n = 198,786) were censored as of the corresponding year. Individuals with missing information on marital status for a specific year were also censored (n = 20,414 married individuals and n = 928 among widowed individuals). Finally, widowed individuals who remarried were also censored (n = 8,882). A total of 291 spousal pairs (582 married individuals) died on the same day. These individuals are included in the analysis in the group of those who were married and died during the study period (n = 508,592); not as widowed, as it was not known who died first, ie, which was the widowed spouse.
Statistical Analyses Life tables (presented in eTable 1; http://links.lww.com/EDE/ A885) for married men and women were produced for the follow-up period, based on all individuals categorized as married at the beginning of a given year, according to the method described by Statistics Norway.10 These tables contain mortality rates by sex, age (each year from 54 to 100 years of 1.1.1975 Married (n=1,801,456)
n=219,200
n=508,592 n=494,735
1.1.1975−31.12.2006 Censored
1.1.1975−31.12.2006 Dead
age) and calendar period (5-year intervals from 1975–1979 to 1995–1999 and 2000–2006). As the youngest married individuals were 23 years of age in 1975, it was only possible to derive life-table values for the last year included (2006) for those age 54 years or more. The mortality of widowed men and women was then compared with the mortality rates in the life tables using survival analysis. Survival time for each of the 494,735 individuals who were widowed during follow-up was defined as days from date of spousal death until the death of the widowed individual, censoring because of remarriage or missing information on marital status, or the end of the study period, whichever occurred first. The age at spousal death was calculated as the difference between the year of spousal death and the year of birth. Survival analysis with the additive excess mortality model was used to estimate hazard rates: α i (t ) = µi (t ) + γ (t ) .11 The rate α i (t ) expresses the individual mortality for a widowed individual i, at day t after spousal death as a sum of a standard mortality µi and an additional excess risk γ. The standard mortality is the mortality rate from the life table for a married individual with the same sex, age, and calendar period. The additional excess risk represents an excess risk because of the change in mortality risk when a spouse dies. The excess mortality may vary by time since spousal death, but is otherwise assumed to be constant in the hazard model we applied. Therefore, a possible sex and age variation was accounted for by categorizing the data into 5- or 10-year age groups before estimating excess mortality. Excess mortality was estimated as the difference between the Nelson-Aalen estimator A (t ) and the accumulated average married mortality M (t ) .12 The excess mortality, which was estimated for each single day t, may be either positive or negative; it would be the latter in cases where the mortality among widowed individuals was lower than that in the married individuals. The hazard ratio (HR) for widowed compared with corresponding married individuals was computed as HR = A(t ) / M (t ) . The expected number of deaths was derived from the life tables by applying survival analysis to corresponding married groups. The confidence intervals (CIs) for HR were calculated based on the fact that the Nelson-Aalen estimator is approximately normally distributed. The CIs for the observed number of deaths are based on the Poisson distribution. Estimation of excess mortality is not available as a standard routine in statistical packages, thus we programmed a routine using the statistical computing language R,13 and the survival package in R.14 This R-code is presented in eAppendix 1 (http://links.lww.com/ EDE/A885).
RESULTS n=9,810
n=277,952
1.1.1975−31.12.2006 Widowed
FIGURE 1. Study population. Norway, 1975–2006. 290 | www.epidem.com
Table 1 displays the absolute number of widowed individuals and number of deaths during the first year after spousal death in selected age groups. The oldest widowed person was 107 years of age. A total of 66,444 women were widowed between 70 and 74 years of age. As expected, because of the well-known tendency of women to marry older men, © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Epidemiology • Volume 26, Number 3, May 2015
Mortality After the Death of a Spouse
TABLE 1. Absolute Numbers of Widowed Individuals and Deaths During the First Year After Spousal Death in Norway, 1975–2006 Age at Spousal Death (Years) 23–54 55–59 60–64 65–69 70–74 75–79 80–84 85–89 90–94 95–107 23–107
Widowed Men
Widowed Women
Total No.
No. Obs
No. Exp
HR (95% CI)
Total No.
No. Obs
No. Exp
HR (95% CI)
9,508 8,202 12,450 17,477 23,661 28,272 25,550 15,167 4,834 745 145,866
63 104 295 611 1,225 2,314 2,938 2,525 1,178 232 11,190a
NA 64.0 166.9 392.2 870.9 1,643.8 2,319.9 2,069.4 969.5 NA 8,496.6
NA 1.64 (1.33, 1.96) 1.78 (1.57, 1.98) 1.57 (1.44, 1.69) 1.42 (1.34, 1.50) 1.43 (1.37, 1.48) 1.28 (1.24, 1.33) 1.24 (1.19, 1.29) 1.25 (1.18, 1.32) NA 1.34a (1.31, 1.36)
31,365 26,756 40,978 55,678 66,444 63,039 43,092 17,574 3,633 310 348,869
105 158 407 784 1,591 2,414 2,837 1,983 695 89 10,869a
NA 113.7 272.8 586.5 1,168.2 1,930.6 2,292.3 1,604.1 543.3 NA 8,510.2
NA 1.39 (1.18, 1.61) 1.50 (1.35, 1.65) 1.34 (1.25, 1.43) 1.37 (1.30, 1.43) 1.26 (1.21, 1.31) 1.25 (1.20, 1.29) 1.25 (1.20, 1.31) 1.31 (1.21, 1.41) NA 1.29a (1.26, 1.31)
a 55-94 years. Obs indicates observed number of deaths; Exp, expected; NA, not available.
and the fact that often men die at earlier ages, the number of widows was considerably larger than widowers. The observed number of deaths in Table 1 exceeded the expected number, showing there were more deaths among widowed individuals than would have been expected if their spouse had not died. As an illustration of the absolute numbers involved, the HR for widows was 1.29, which relates to a 95% CI of 10,688.2– 11,049.8 observed deaths in contrast to the 8,510.2 expected deaths (Table 1).
Table 2 presents the number of observed and expected deaths, and HRs according to time after spousal death. HRs were highest in the first few days after spousal death, then dropped and remained stable and highly significant throughout the tenth year (Table 2). In Figure 2, the excess mortality after spousal death is displayed in terms of HRs by sex, 10-year age groups and time since spousal death on a nonlinear time scale. In the 55- to 64-year age group, 13 widowed men and 26 widowed
TABLE 2. Number of Deaths by Time Since Spousal Death in Widowed Individuals Ages 55 to 94 Years in Norway, 1975–2006 Time Since Spousal Death Days 1–7 8–30 31–100 101–365 1–365 Year 2 3 4 5 6 7 8a 9b 10c 1–10c
Widowed Men
Widowed Women
Observed
Expected
HR (95% CI)
Observed
Expected
HR (95% CI)
294 879 2,278 7,739 11,190
174.5 570.0 1,702.9 6,049.2 8,496.6
1.69 (1.49, 1.88) 1.55 (1.44, 1.65) 1.35 (1.29, 1.40) 1.31 (1.28, 1.34) 1.34 (1.31, 1.36)
300 812 2,179 7,578 10,869
170.6 557.9 1,678.6 6,103.1 8,510.2
1.76 (1.56, 1.96) 1.46 (1.36, 1.56) 1.30 (1.25, 1.36) 1.25 (1.23, 1.28) 1.29 (1.26, 1.31)
9,612 8,837 8,090 7,130 6,630 6,008 5,338 4,802 4,151 70,162
8,038.0 7,559.9 7,082.5 6,575.3 6,076.9 5,438.1 4,984.8 4,508.1 4,103.2 60,688.9
1.25 (1.22, 1.27) 1.25 (1.22, 1.27) 1.25 (1.22, 1.27) 1.21 (1.18, 1.24) 1.25 (1.22, 1.28) 1.26 (1.22, 1.29) 1.25 (1.21, 1.28) 1.27 (1.23, 1.30) 1.24 (1.20, 1.28) 1.26 (1.25, 1.27)
10,315 10,344 10,091 9,897 9,856 9,524 9,366 8,982 8,744 96,948
8,609.4 8,660.0 8,711.8 8,632.2 8,510.7 8,133.0 7,936.0 7,664.0 7,366.4 81,031.9
1.22 (1.20, 1.25) 1.23 (1.21, 1.26) 1.21 (1.19, 1.24) 1.21 (1.19, 1.24) 1.24 (1.22, 1.27) 1.23 (1.21, 1.26) 1.25 (1.23, 1.28) 1.26 (1.23, 1.29) 1.29 (1.26, 1.32) 1.25 (1.24, 1.25)
a
Age 55 to 93. Age 55 to 92. c Age 55 to 91. b
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3.0 2.6 2.2 1.8 1.4
Days
Days
Year
Days
Year
Days
Year
55 − 64
65 − 74
75 − 84
85 − 94
Age (years) at spousal death
women died within 1 week of spousal death, yielding HRs of 2.89 (95% CI: 1.32, 4.46) and 3.48 (2.14, 4.82). For the 75- to 84-year age group, the corresponding numbers rose to 133 (HR: 1.66, 95% CI: 1.38, 1.94) and 141 (HR: 1.68 [1.40, 1.95]; data not shown). Similarly, the total number of deaths was much higher among the oldest men and women (Table 1). As seen in Figure 2, some clear trends appear. First, all HRs are larger than unity, displaying an existing and persistent excess mortality conferred by spousal death. Second, the values declined with age. Third, in the 55- to 64-year age group, the excess mortality is more pronounced among men, but this sex difference gradually disappeared with age. And, finally, the excess mortality was high the first few weeks, then declined sharply and stabilized.
DISCUSSION During 10 years after spousal death, the number of excess deaths among widowed men and women was estimated at 9,473 and 15,916, respectively. This estimate corresponds to 25,389 more deaths among the 494,735 widowed individuals (men and women) than among a corresponding group of married individuals. The importance of these high numbers is further illustrated by findings that the effect of spousal death on mortality is on the rise.15,16 Three published meta-analysis reported estimates of the mortality after spousal death for men and women, respectively, 1.11 and 1.11 (joint 95% CI: 1.08, 1.14) (relative risk),17 1.23 (1.18, 1.28) and 1.04 (1.00, 1.08) (relative risk),3 and 1.27 (1.19, 1.35) and 1.15 (1.08, 1.22) (HR).16 The varying values most likely reflect the diversity of the data types used and methodologies applied. We were able to derive values across 292 | www.epidem.com
Year
1−7 8 − 30 31 − 100 101 − 365 2−3 4−5 6−7 8 − 10a
Time after spousal death
1−7 8 − 30 31 − 100 101 − 365 2−3 4−5 6−7 8 − 10
FIGURE 2. Hazard ratios of mortality by sex, age and time since spousal death. Norway, 1975–2006. Men (solid line) and women (dotted line). aAges 85 to 91. Confidence intervals can be found in Tables 1 and 2.
1−7 8 − 30 31 − 100 101 − 365 2−3 4−5 6−7 8 − 10
1.0
1−7 8 − 30 31 − 100 101 − 365 2−3 4−5 6−7 8 − 10
HR, widowed vs married
3.4
ages and time since loss, and compared with the meta-analyses, our values in general were higher, especially for women. One possible reason for this may be related to the fact that misclassification of marital status has been documented as a serious source of bias in estimates of the mortality after spousal death.4 Indeed, studies on large samples or entire populations often lack updates on the status under investigation, whereas we were able to update our information on marital status. In our analyses, widowed individuals who remarried were censored. However, they comprised only 8,882 of 494,735 individuals. This study had a large amount of suitable data available, with a study population of 1.8 million married individuals including hundreds of thousands of men and women who are widowed or dead, or both. Another strength of this study is the use of life tables. One advantage of this is that the variation in mortality by age and calendar year is incorporated in these tables. Another advantage is that the estimation of excess mortality requires only survival times from widowed individuals. It is therefore unnecessary to obtain survival times from a sample of matched married individuals or any other sample of married people. Third, single-day mortalities can easily be estimated in this model. Other studies have shown a higher excess risk among individuals less than 65 years of age than older individuals,3,5,18,19 or other cut-offs for age have been used.2,20 Our study had the capacity to produce estimates in more age groups, and showed a linear, consistent drop with age, much more among men than women. In contrast to the above-mentioned meta-analyses, we found that, overall, women did not have much less excess risk than men. The reason for this contrast may be that © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Epidemiology • Volume 26, Number 3, May 2015
our study also included very old individuals, and a long follow-up period. Indeed, in their late 50s and 60s, women had much less excess risk than men, but this discrepancy gradually disappeared until it was no longer present in men and women in their 80s. Also, women had less excess risk during the first year after spousal death, but again the sex difference was almost absent when considering the first 10 years combined. Others have found that mortality is much higher immediately after the loss of a spouse.6,19–22 Six months after spousal death has often been used as a cut-point to compare mortality, whereas we were able to consider single days. There was a particularly high number of spouse pairs that died on the same day (291 spousal pairs, 582 individuals). In comparison, the number of spousal pairs that died 1 day apart was much lower (100 spousal pairs, 200 individuals), and continued to decline to a daily average for the first week of 174 individuals, for days 8 to 30 of 151.2 individuals, for days 31 to 100 of 130.4 individuals, and for days 101 to 365 of 118 individuals. Interestingly, as this study provided unique values down to single days, we could also follow how the HRs were especially high in the first days after spousal death before gradually dropping. These numbers suggest that common incidents such as car crashes, fires, and drowning are the reason that a majority of spouse pairs die on the same day or a few days apart. In such instances, it can be impossible to know whether deaths are related solely to a common incident or whether some element of the widowhood effect may be present. If we had considered cause-specific information on death, our study would have been more informative. This is a limitation of the study, and variation of risk across causes of death has been found elsewhere.5 We excluded those who died on the same day, and from the next day we estimated excess mortality irrespective of whether or not deaths might be related to the widowhood effect. Due to this fact, and also as the term excess mortality is used in the statistical model employed, we found this term more precise and correct than the commonly used phrase “widowhood effect.”23 At the other end of the time scale for spousal death, increased mortality risk was still present after 10 years. Marriage has been well documented to improve life length,24 and thus there is no surprise that the excess mortality continues throughout the years of analyses. The HRs in our study illustrates well the persistent and long-lasting elevated mortality risk for many men and women throughout life. A limitation with this study is the lack of information on possible confounders. Socioeconomic status has been described to be important to adjust for in countries like the USA with very marked socioeconomic inequalities in health.23 In that study, the widowhood effect prevailed, but was weakened after adjusting for socioeconomic status. In Norway, health inequalities vary less with socioeconomic status and a smaller effect would thereby be expected. © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Mortality After the Death of a Spouse
CONCLUSION This study not only shines new light on mortality risk after the loss of a spouse but it also paints a more detailed picture across ages and time since loss. Not only men but also women are strongly affected and for a very long time. From the first day after the loss, excess mortality is present and it remains substantially elevated after that.
ETHICS APPROVAL The study was approved by the Data Inspectorate and by the Regional Committee for Medical Research Ethics, North Norway. No informed consent was found necessary because of the type of data and that no details were included that might disclose the identity of the subjects. The study has therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. REFERENCES 1. Shah SM, Carey IM, Harris T, et al. Impact of partner bereavement on quality of cardiovascular disease management. Circulation. 2013;128:2745–2753. 2. Blomgren J, Martikainen P, Grundy E, et al. Marital history 1971–91 and mortality 1991–2004 in England & Wales and Finland. J Epidemiol Community Health. 2012;66:30–36. 3. Moon JR, Kondo N, Glymour MM, et al. Widowhood and mortality: a meta-analysis. PLoS One. 2011;e23465. 4. Korenman S, Goldman N, Fu H. Misclassification bias in estimates of bereavement effects. Am J Epidemiol. 1997;145:995–1002. 5. Martikainen P, Valkonen T. Mortality after the death of a spouse: rates and causes of death in a large Finnish cohort. Am J Public Health. 1996;86:1087–1093. 6. Martikainen P, Valkonen T. Mortality after death of spouse in relation to duration of bereavement in Finland. J Epidemiol Community Health. 1996;50:264–268. 7. Espinosa J, Evans WN. Heightened mortality after the death of a spouse: marriage protection or marriage selection? J Health Econ. 2008;27:1326– 1342. 8. Bowling A. Mortality after bereavement: a review of the literature on survival periods and factors affecting survival. Soc Sci Med. 1987;24:117– 124. 9. Stroebe M, Schut H, Stroebe W. Health outcomes of bereavement. Lancet. 2007;370:1960–1973. 10. Foss AH. Definisjoner og beregningsmetoder for dødelighetstabell. Available at www.ssb.no/a/histstat/not/not_9889.pdf. Statistics Norway 1998. 11. Aalen OO, Borgan Ø, Gjessing HK. Survival and Event History Analysis. New York: Springer; 2008:99–102. 12. Andersen PK, Vaeth M. Simple parametric and nonparametric models for excess and relative mortality. Biometrics. 1989;45:523–535. 13. R Development Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria: The R Foundation for Statistical Computing; 2012. Available at http:// www.R-project.org/. 14. Therneau T. A package for survival analysis in S. R package version 2.36– 12. 2012. 15. Berntsen KN. Trends in total and cause-specific mortality by marital status among elderly Norwegian men and women. BMC Public Health. 2011;11:537. 16. Shor E, Roelfs DJ, Curreli M, et al. Widowhood and mortality: a metaanalysis and meta-regression. Demography. 2012;49:575–606. 17. Manzoli L, Villari P, M Pirone G, et al. Marital status and mortality in the elderly: a systematic review and meta-analysis. Soc Sci Med. 2007;64:77– 94. 18. Smith KR, Zick CD. Risk of mortality following widowhood: age and sex differences by mode of death. Soc Biol. 1996;43:59–71.
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19. Johnson NJ, Backlund E, Sorlie PD, et al. Marital status and mortality: the national longitudinal mortality study. Ann Epidemiol. 2000;10:224–238. 20. Manor O, Eisenbach Z. Mortality after spousal loss: are there socio-demographic differences? Soc Sci Med. 2003;56:405–413. 21. Kaprio J, Koskenvuo M, Rita H. Mortality after bereavement: a prospective study of 95,647 widowed persons. Am J Public Health. 1987;77:283–287.
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22. Schaefer C, Quesenberry CP Jr, Wi S. Mortality following conjugal bereavement and the effects of a shared environment. Am J Epidemiol. 1995;141:1142–1152. 23. Moon JR, Glymour MM, Vable AM, et al. Short- and long-term associations between widowhood and mortality in the United States: longitudinal analyses. J Public Health (Oxf). 2014;36:382–389. 24. Rendall MS, Weden MM, Favreault MM, et al. The protective effect of marriage for survival: a review and update. Demography. 2011;48:481–506.
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