Stillbirths: how should its rate be reported, its disability-adjusted-life-years (DALY), and stillbirths adjusted life expectancy

Background A 2016 study standardized the definition of stillbirths. It estimated the rate as a proportion of total births. A 2015 paper addressed the problem of disability-adjusted life-years (DALY) for stillbirths. There has been no adjustment of life expectancy at birth to account for stillbirths. Methods and results We follow mathematical and computational methods, use algebra to derive relationships, and large databases. We express the rate as a proportion of live births and use this rate to adjust life expectancy at birth for stillbirths. We then use the difference between the traditional life expectancy and stillbirths adjusted life expectancy (SALE) to obtain DALY for stillbirths for 194 countries, the Millennium Development Goal regions, and income groups. We show defining stillbirths’ rate as a proportion of live births enhances stillbirths’ importance, especially in poorer countries; negates some of its under-statement vis-a-vis neonatal mortality rate, accentuates its decrease; and permits inference about relative magnitudes of stillbirths and neonatal mortality from the two rates. Using it, we derive stillbirths adjusted life expectancy, and suggest it reflects a more complete and accurate measure of comparative life expectancies of different countries. Its difference from the traditional life expectancy is used to measure DALY for stillbirths that totals 165.3 million years worldwide. Conclusion Stillbirths almost equals neonatal mortality yet have not received almost equal attention. We hope highlighting them and adjusting life expectancy for it will spur health interventions so that grand convergence of health outcomes in different countries can be more rapidly achieved. We also believe SALE is a more complete and accurate measure of comparative life expectancies. Electronic supplementary material The online version of this article (10.1186/s12911-019-0850-8) contains supplementary material, which is available to authorized users.

3 Stillbirths: How should its rate be reported, its disability-adjusted-life-years (DALY), and stillbirths adjusted life expectancy

Background
Health professionals, social scientists, and international organizations have not given as much attention to stillbirths as to neonatal mortality. The first data-set for stillbirths in almost all countries became available in 2006, and was for 2000, while that on neonatal mortality have been available since 1990. 1,2 In 2011 stillbirth's data for 2008 and 2009 became available; and were retrospectively estimated to 1995 for about 40% of the sample. 3 The first international goal on stillbirths (and neonatal mortality) was adopted in 2014. 4 Using revised and updated estimates, Blencowe and colleagues estimate 2.60 million stillbirths occur yearly. 5 The stillborn rate arguably reflects a country's quality of health care system to a greater extent than life expectancy (since the latter is affected more by smoking, diet, exercise, public sanitation and pollution) and can be an independent/supplementary health indicator. Causes of stillbirths are not fully understood. In the US, about one-fourth of stillbirths are unexplained; and stillbirths after 24 weeks of pregnancy are primarily due to pregnancy/birth related causes like placenta/ umbilical cord problems, birth defects, and infection. 6 In low income countries, where about 98% of the stillbirths globally occur and almost half of the deliveries take place at home, difficult, prolonged and obstructed labor, infections without adequate treatment, and lack of trained obstetric care (compounded by 35-45% absenteeism of health and extension workers) are the primary causes. 7,8,9 Earlier studies define stillbirth as fetal death in third trimester with birthweight of 1000g or more. 1,3 When birthweight is unavailable, 28 or more completed weeks of gestation is used (or a length of ≥ 35cm if the reported gestation age is not judged reliable). Blencowe and colleagues find using birthweight as the primary criterion reduces number of stillbirths in rich 4 countries by 15%, since fetal growth restriction causes many stillbirths. 5 They use fetal death at 28 or more completed weeks of gestation as their exclusive definition. In poor countries, famine increases stillbirths and fortifying pregnant women's diet with protein-rich supplements reduces stillbirths by as much as 38%. 10,11,12 If mothers' under-nourishment during pregnancy causes stillbirths, using birthweight lower than 1000g as the primary criterion will undercount stillbirths in poor countries also. Accordingly, we follow fetal death at 28 or more completed gestationweeks as our exclusive definition. Using it also excludes voluntary abortion from stillbirths, and protects women's choice to terminate their pregnancies, since abortion after 28 weeks is rare and is mostly due to severe fetal abnormality or if pregnancy is threatening mother's life. 13,14 In addition, "[I]n terms of ethics the ethical concept of the fetus as a patient should replace the discourse of "unborn child" when that phrase is used normatively." 15 "In term of science it is well recognized that between 20 and 24 weeks, it is likely that the fetus "experiences" touch and pain." 16 "The inability to communicate does not mean that there is no pain or need of treatment." 17 Although viability in Western countries is between 22 -24 gestational weeks, it is higher in low income countries; and 28 weeks is chosen as a pragmatic cut-off limit to classify stillbirths.
The World Health Organization (WHO) notes the widespread perception that stillbirths are unavoidable due to congenital abnormalities. 1 It finds it to be untrue -estimating only 7.4% of stillbirths after 28 weeks are due to such factors. Its wide variation among countries (as shown following) also belies the perception of congenital abnormalities being the primarily cause.
The aim and purpose of this paper is to i) highlight the stillbirth rate that is defined consistent with neonatal mortality rate, ii) use it to adjust life expectancy at births to account for stillbirths, and iii) use the latter to obtain DALY for stillbirths. As will be clear below, the paper 5 is a kind of review proposing new aspects for classification.

2.1.A. Methods: Stillbirth rate defined consistent with neonatal mortality rate
There is no consistency among various authors on how they define the stillbirth rate.
Some report it (like neonatal mortality) as a proportion of live births. 18 Others, while noting its definition varies among countries and even among states of the US, define it as a proportion of total (= still + live) births. 19 Blencowe and colleagues estimate stillbirth rates based on 2207 data points. 5 They do not break-up data into whether it reported stillbirth rate as a proportion of total or of live births.
Since it is natural to define all rates (stillbirths, neonatal, infant, and child mortality) included in a study similarly, it is unlikely all 2207 data points would report stillbirth rate as a proportion of total births. Their definition is apparently based ultimately on Goldenberg and colleagues. 20,21 Goldenberg and colleagues summarize key findings in the previous five reports in Lancet's 2011 Stillbirth Series. 22, 23, 24, 25, 26 They define stillbirth rate as "per 1000 births," not as "per 1000 total births," at eight places, including in their Conclusion and Call to Action. Since the commonly accepted meaning of "births" is "live births," by "per 1000 births," they must mean "per 1000 live births." International statistical classification of diseases terms stillbirths (SB) as a proportion of live births (LB) "fetal death ratio;" and calls stillbirths as a proportion of total births (TB = SB + LB) "fetal death rate." 27 It encourages both to be reported and requires the denominator to be always specified. Specifying the denominator in the definition itself, we term the two as still live birth rate (SLBR = SB/LB) and still total birth rate (STBR = SB/TB), respectively.
Using our nomenclature, Blencowe and colleagues provide data for STBR. 5 Mortality after live birth with 22 to 27 weeks and six days' gestational age are included in the neonatal 6 mortality rates (NMR =NM/LB) while fetal deaths with the same gestational age are excluded from STBR -since it includes stillbirths only after 28 weeks gestational age. That understates stillbirth rate's magnitude vis-à-vis NMR. Dividing stillbirths by a bigger number (total births) and neonatal mortality by a smaller number (live births) compounds its understatement.
We can show the difference between SLBR and STBR is SLBR -STBR = SLBR × STBR/1000 > 0 (1), the two rates either both decrease or both increases, and when they decrease, the rate of decline in SLBR must be greater than that in STBR (see, Additional file 1).
(1) tells us greater the SLBR, greater is its excess over STBR. For richer countries where the stillbirth rates are low, SLBR and STBR will be quite close; but for poorer countries where they are high, the excess of SLBR over STBR will be significant.
To infer about the relative numbers of stillbirths and neonatal mortality from their relative rates requires that both adverse events be divided by the same number. That requirement is met when SLBR = SB/LB is used in the stillbirth rate to NMR ratio but not when STBR= SB/TB is used.
Since (LB/TB) < 1, stillbirth rate to NMR ratio when STBR is used is smaller than when SLBR is used in the ratio instead.
Blencowe and colleagues use STBR:NMR ratio of less than 0.33 to exclude 156 data points on grounds that a ratio so low is implausible; and use this ratio of greater than 0.5 as one criterion to classify data from national routine information systems as high quality. 5 But, 7 STBR:NMR ratio does not equal SB: NM, as Blencowe and colleagues mistakenly imply; SLBR: NMR does. This distinction needs to be recognized. Table 1 compares SLBR to STBR for countries with the ten highest stillbirth rates in 2015.

2.1.B. Results of defining stillbirth rate consistent with neonatal mortality rate
Results for all countries are given in Additional file 2. They show excess of SLBR over STBR is approximately two for Pakistan and Nigeria and between one and two for 12 other countries.
SLBR is higher than 30 for 14 countries (compared to 13 for STBR); its decrease is greater than that in STBR by about one percentage point for some countries. See, Additional file 2.
<Place Table 1 here.> Table 2 provides SLBR and SLBR:NMR ratio for 2000 and 2015 by Millennium Development Goal (MDG) regions and two income groupings: 1) high and upper mid income (richer) and 2) lower mid and low income (poorer). It also provides within region/group standard deviation and dispersion measured as standard deviation/mean (i.e., coefficient of variation), because the means are different. Table 2 shows SLBR declined for each region, signifying success. The failure is the increase in its dispersion everywhere (except one region). The increased dispersion is not accounted for anywhere in the recent stillbirth study. 5 <Place Table 2 here.>  1,2 The protein-supplemental study cited above found it decreased low-weight live births by 32% also (in addition to reducing stillbirths by 38%). 12 If stillbirths are included in DALY, nutrition and medical interventions focused on pregnant mothers may yield benefits in potential DALY reduction that are two to ten times, and potential cost per DALY reduction one-half to one-tenth. 36 Since DALY is an important population health measure, not counting stillbirth's reduction in DALY estimates will also yield anomalous situations where a population with a neonatal mortality reduction, whether or not achieved by moving prenatal care resources to post-natal, is considered healthier even if its incidence of late-gestation stillbirths increases.
Other substantive arguments for including stillbirths in DALY estimates are as follows.
The current practice violates one of the four general principles underlying DALYs, namely "treating like outcomes as like." 34 A 28 gestational-age fetus that is stillborn and one that dies ten minutes after live birth are essentially like outcomes. Yet, the former is not included in DALY estimates while the latter is. We have discussed above how following fetal death at 28 or more completed gestation-weeks as our exclusive definition of stillbirths protects women's rights and choice to terminate their pregnancies. Including stillbirths in DALY estimates will spur interventions to reduce it -interventions that predominantly focus on pregnant mother's health, wellbeing, and prenatal and partum care -and will enhance women's rights and condition. 37 newborn infant, at the time of birth," 36 That is, DALY of stillbirths should be zero, or let us say 0.01, at 28 weeks gestational age increasing to 1.00 at full-term; or increasing 100 times. Since a fetus does not develop 100 times from 28 weeks to full-term, this proposal is counter-intuitive and against medical evidence. At 28 weeks gestational age, survival without major morbidity for infants surviving to discharge is closer to one (it is 0.59) than to zero. 39 In a situation where most of the stillbirths (and pre-term neonatal mortality) take place in poor countries where the gestation age at mortality between 28 to 39 weeks are not certain, attempting precision in DALY estimation (which perforce has to make bold assumptions in valuing vastly disparate morbidity) more than in our proposal above will not be productive. In addition, this proposal suffers from its implicit assumption equating life expectancy of a still birth -that is zero -to that of a live birth.
13 Stillbirths (like neonatal mortality) also cause parental suffering and psychological distress and may affect parents' life spans. Data for these effects is limited, especially in low income countries. 40 If available, it will be challenging to add it to measure like DALY of stillbirths. Nevertheless, this effect needs to be recognized.

2.2.B. Results
: adjusting life expectancy to account for stillbirths and using it to obtain DALY for stillbirths <Place Table 3 here.>

Conclusion
Main Findings: Stillbirths almost equals neonatal mortality yet have not received almost equal attention. Defining stillbirths' rate as a proportion of live births enhances stillbirths' importance, especially in poorer countries; and negates some of its under-statement vis-a-vis neonatal mortality rate. We employ this definition to adjust life expectancy for stillbirths; and propose the latter to get stillbirths' DALY that equal 165.3 million years.
Meaning of the Findings, Research Implications: Stillbirth rate arguably reflects a country's quality of health care system to a greater extent than life expectancy; and stillbirths adjusted life expectancy reflects a more complete and accurate measure of comparative life expectancies. Including it in DALY will lead to better priorities in health care spending.
Highlighting stillbirths and adjusting life expectancy for it will spur research on stillbirths whose causes are not well understood.
Clinical and Health Implications: Some key interventions such as syphilis treatment in pregnancy, fetal heart monitoring, and labor surveillance could be crucial in preventing intrapartum stillbirths. 3 In low income countries, only a minority of deliveries occur in health facilities or with the assistance of a trained personnel. This is due to both inadequate resources and absenteeism of health workers. 9, 10 The implication is need for both more resources and better governance. Further, resuscitation training of health care workers in poorer countries is sorely needed.
Strength and Weaknesses: The paper's strengths are a) highlighting that having different divisors for stillbirths and neonatal mortality rates may give inconsistent results. and b) traditional life expectancy suffers from the limitation that what is stillbirth and what is a live birth is subject to considerable error. Its weakness is that data on stillbirths are not estimated by UN Inter-agency Group for Child Mortality Estimation, childmortality.org. If the latter estimates stillbirths while appraising its neonatal mortality numbers, the estimates of both are likely to improve.
In 2016, the definition of stillbirths was standardized to mean fetal loss after 28 weeks of gestation. 5 It defined stillbirth rate as a proportion of total (still + live) births. We are proposing it be called still total birth rate, and what international statistical classification of diseases terms "fetal death ratio," (stillbirths as a proportion of live births) be called still live birth rate. 27 The latter accentuates its decline and makes the stillbirth rate comparable to NMR. Using it, we 16 derive stillbirths adjusted life expectancy. Its difference from the traditional life expectancy reflects DALY for stillbirths that totals 165.3 million years worldwide.
There has been a call for better prenatal, natal, and neonatal health monitoring and improved data definitions/methods with consistent metrics. 21 There are triple benefits from such attention: benefits i) for stillbirths, ii) for neonatal deaths, and iii) for mothers; life complications and disability may also be reduced. 21 Stillbirths in poorer countries are another dimension of health that needs to be addressed when seeking, hopefully rapid, grand convergence to health outcomes in richer countries. A stillbirth-incorporated definition of the widely used life expectancy measure will attract more attention to stillbirth. Life expectancy at birth ignores morbidity and is a "very imperfect measure of health." 41 Adjusting it for stillbirths will also remove some of its imperfections.  ii iii iv

Additional file 1: Mathematical derivations
The equations for the two stillbirth rates are: Multiplying and dividing the right-hand side of (A1) by LB, we have Subtracting the RHS of (A1), that equals STBR, from SLBR, we get We now derive expressions for the changes in the two stillbirth rates. Let SLBR1, STBR1, SLBR2, and STBR2 represent the two stillbirth rates, and LB1, SB1, LB2, and SB2 the number of live and stillbirths for years 1 and 2, respectively. Let When k > 1, the number of stillbirths in year 2 is greater than that in year 1; when it is < 1, the number in year 2 is smaller.
Thus, the two rates change in the same direction: They either both decrease or they both increase.
The proportionate (i.e., ignoring the 100) rate of change (= growth or reduction) in the two stillbirth rates are and (A10) implies the absolute rate of change in SLBR must be greater than that in STBR. When the two rates are falling, it means the rate of fall in SLBR must be greater than that in STBR. When they are increasing, the rate of increase in SLBR must be greater than that in STBR.
The two life expectancies: Subtracting the RHS of (5) in the text from LE = LELB, we have LELB -LETB = LELB (1 -(1000 /(1000 + SLBR))), or Notes: SLBR and STBR stand for still live and total birth rates, SB for the number stillborn, and NM and NMR for the number and rate of neonatal mortality. The STBR is from Blencowe et al. (2016), SLBR is derived by using the number stillborn from Blencowe et al. (2016) and number of live births as calculated by using the neonatal mortality number and rate from World Development Indicators. Niue (population 1,190 in July 2014 per CIA World Fact Book) for which Blencowe et al. (2016) give the rate but not the number stillborn is excluded from the above