The massive global variation in caesarean-section (C-section) rate is usually attributed to socio-economic, medical and cultural heterogeneity. Here, we show that a third of the global variance in current national C-section rate can be explained by the trends of adult body height from the 1970s to the 1990s. In many countries, living conditions have continually improved during the last century, which has led to an increase in both fetal and adult average body size. As the fetus is one generation ahead of the mother, the fetus is likely to experience better environmental conditions during development than the mother did, causing a disproportionately large fetus and an increased risk of obstructed labour. A structural equation model revealed that socio-economic development and access to healthcare affect C-section rate via multiple causal pathways, but the strongest direct effect on C-section rate was body height change. These results indicate that the historical trajectory of socio-economic development affects—via its influence on pre- and postnatal growth—the intergenerational relationship between maternal and fetal dimensions and thus the difficulty of labour. This sheds new light on historic and prehistoric transitions of childbirth and questions the World Health Organization (WHO) suggestion for a global ‘ideal' C-section rate.

1. Background

Compared with other mammals, childbirth in humans is strikingly difficult owing to the tight fit between the baby's head and shoulders and the mother's pelvis [1–5]. United States (US) statistics suggest that cephalopelvic disproportion—a mismatch of the fetal head and the maternal birth canal—occurs in 2.3% of infants weighing 3–4 kg at birth and in 5.8% of those weighing more [6]. A number of individual risk factors for cephalopelvic disproportion have been identified, including maternal and paternal body height, obesity and the age of the mother [7–14]. In most countries, however, the rate (i.e. incidence) of caesarean section (C-section) greatly exceeds that of actual anatomical disproportion [15–17]. Even if the birth canal can accommodate the fetus, a tight feto-pelvic fit can delay labour and increase the risk of maternal and fetal morbidity, which is often prevented by caesarean intervention. C-section rates have been reported to correlate also with psychological factors such as fear and anxiety, socio-economic factors such as family income and education, as well as with access to healthcare [18–23]. As a result, C-section rate varies considerably across social and demographic groups within most countries. At a global level, C-section rate varies even more starkly, ranging from 1–2% in many sub-Saharan African countries, up to about 50% in Egypt, Turkey or Brazil. Even in Europe, which is culturally and socio-economically relatively homogeneous, incidences range from about 15% in Scandinavia to more than 35% in Portugal, Romania and Italy [16,17]. Especially in developing countries, incidences are rising rapidly [16,24,25]. Despite global differences in obstetric traditions, healthcare system and nutrition, this massive international variation of C-section rate remains puzzling. It is usually attributed to socio-economic, legal and cultural heterogeneity [24,26,27].

Here, we propose an additional perspective. It is well known that the prenatal environment, including maternal nutrition, affects the fetus' growth trajectory [28–32]. In most countries, especially those of the Global North, these environmental conditions have continually improved during the last century. In parallel, both average birth weight [31,33–37] and adult body height [36–39] have increased for many decades (only more recently, birth weight and stature have remained stable or even decreased in certain countries; see below). It is assumed that this secular trend is a result of continually improving living conditions [31,37,38,40,41]. Yet, as the fetus is one generation ahead of the mother, the fetus is likely to have experienced—on average—a more beneficial environment than the mother did. The fetus' body size may thus be—again just on average—disproportionately large: larger than the optimal size for the mother's birth canal. Despite a certain degree of adaptation of fetal growth to the intrauterine environment [32,42,43], the rapid intergenerational improvement of living conditions, and thus also fetal provisioning, may challenge childbirth.

Secular changes in adult body height are not homogeneous at a global level. While body height increased globally until the 1960–1970s, more recent trends in height differ considerably across countries [39], witnessing the heterogeneity of socio-economic development. For example, the increase in average birth weight and stature has levelled off in several industrialized countries; birth weight has even been reported to have declined, but owing primarily to shortened gestation length and higher survival rates of premature babies [35,36,44,45]. In most African countries stature has declined since the 1970s (figure 1a; electronic supplementary material, figure S1). We thus propose that the international variation in current C-section rate is partly attributable to variation in the secular trends of body dimensions: all else being equal, we expect that a fast increase in stature is associated with a high incidence of C-section. Figure 1. Distributions of body height change and caesarean section (C-section) rate. (a) Histogram of the average annual body height change (pooled over males and females) from birth years 1971 to 1996 for all countries in the sample. (b) Histogram of current C-section rate for all countries. (Online version in colour.)

For obstetricians, our hypothesis may appear unintuitive because many previous studies documented that—at an individual level—taller women have lower, not higher, rates of obstructed labour [7,11,14,46]. However, we propose that—at a population level—the intergenerational change of body size, not only current body size, affects obstructed labour: the faster the environmentally induced increase in body size, the more frequent is fetopelvic disproportion. Similarly, it may appear paradoxical that improving living conditions can challenge—rather than ease—childbirth. However, the underlying mechanism, namely the environmental and nutritional influence on maternal and fetal body dimensions, is well documented. For example, owing to their high-caloric diet, obese mothers tend to give birth to large neonates and thus show an increased risk of fetopelvic disproportion [8–10,14]. High-caloric diet also affects the balance between maternal and fetal metabolism and can lead to increased gestation length with higher risks of post-term delivery and obstetric complications [47–49]. Even higher risks are experienced by women who were born in underdeveloped countries and later migrated to the US [50,51]. Exposed to under-nutrition in childhood and early adulthood, these women tend to have a short stature and a narrow pelvic canal. After migration, they consumed a high-caloric diet during pregnancy, leading to large newborns and high risks of obstructed labour owing to fetopelvic disproportion. It is not primarily the mother's short stature that causes disproportion, but the large newborn relative to the maternal body dimensions, caused by the environmental change throughout the mother's lifetime. We propose that the same phenomenon of environmentally induced anatomical disproportion contributes to the international variation in C-section rate and has also contributed to the global rise of C-section throughout the last decades.

To test this hypothesis, we used worldwide data on national C-section rates and the secular changes of adult body height from the birth years 1896 to 1996, retrieved from the non-communicable disease (NCD) Risk Factor Collaboration [39]. Our data on C-section rates comprise estimates from 2005 to 2017 (electronic supplementary material, table S1). As most women who gave birth within this period were born in between the 1970s and the 1990s, we restricted our estimation of body height change to the 25-year birth interval from 1971 to 1996.

Clearly, many more biological, sociocultural and medical factors concur in determining C-section rate. Furthermore, a significant association between body height change and C-section rate, as predicted here, can also result from other factors that influence both obstetric practices and physical growth. Hence, in order to test our hypothesis, it does not suffice to show a correlation between body height change and C-section rate, but we need to demonstrate that this association persists even if we account for a large set of socio-economic, demographic and medical factors that have the potential to affect both body height change and parturition. To this end, we collated data on national obesity and diabetes rates as well as the mean age of the mother at first birth, which are all known to affect labour outcome at an individual level [8,9,52]. As maternal body height is also a risk factor for obstructed labour, we used average female body height in 1996 (as opposed to intergenerational height change) as a further covariate. To account for socio-economic and healthcare factors we used three widely applied indices: the Human Development Index (HDI), a composite index of life expectancy at birth, education and per capita income [53]; the Healthcare Access and Quality (HAQ) Index computed from risk-standardized and cause-specific death rates [54]; and national health expenditure (HE) in per cent of gross domestic product (GDP) [55]. In a first step of the analysis, we statistically removed the effects of all these variables from body height change and C-section rate in order to see if an association persists, and second, we investigated the mutual interaction of these factors by a series of structural equation models (SEM).

2. Methods

(a) Variables

C-section rate was calculated as the total number of caesarean deliveries divided by the total number of live births. Data were obtained by national surveys, routine vital statistics and reports from health authorities, including the ‘European Health for All' database of the World Health Organization (WHO) and international health surveys of Unicef. For each country, we used the most recent rates available (most data were from 2010 to 2017; no data before 2005 were used). If two different equally recent statistics were reported for a country, we used the mean of the two. However, different estimates were relatively similar with the only exception of Cyprus. The various sources and the actual rates are provided in the electronic supplementary material, table S1.

Data on average adult body height, obesity and diabetes rates were retrieved from a database of the NCD Risk Factor Collaboration [39] (www.ncdrisc.org/index.html). The variable obesity is the percentage of adult obese women (body mass index > 30) for each country in the year 2014. Data on the average age (in years) of the mother at first birth were collected from the CIA's ‘The World Factbook', which receives its data from national health surveys and other national or regional demographic surveys (electronic supplementary material, table S1). The HDI is a composite index defined by the United Nations Development Program (http://hdr.undp.org/en/data). It is computed as the mean of normalized indices for life expectancy, education and income per capita. The HAQ index, developed by the Global Burden of Disease Study [54], measures the accessibility and quality of healthcare based on risk-standardized and cause-specific death rates. HE, expressed as percentage of GDP, was retrieved from the WHO website www.who.int/countries/en/.

(b) Statistical analysis

We computed the average annual change of body height (in cm year−1) as the slope of the linear ordinary least squares regression of average body height on the birth year with sex as a covariate. We estimated these average annual changes separately for the birth year intervals 1896–1960 and 1971–1996. In both intervals, the trends in body height were relatively linear; changes in the trends occurred largely in the 1960s (see the electronic supplementary material, figure S1, for examples). The estimates of average body height change for birth years 1971–1996 were used as predictor of C-section rate in the subsequent analyses.

To account for HDI, HAQ, HE, obesity rate, diabetes rate, average maternal body height (1996) and average age of the mother, we regressed both C-section rate and height change on these variables and plotted the resulting regression residuals in figure 3. This is equivalent to a multiple regression of C-section rate on height change with these seven variables as covariates. The correlation and regression slope between the residuals is equivalent to the corresponding partial correlation and partial regression slope, respectively. Type I errors were estimated by Monte Carlo permutation tests [56]. These analyses were performed in Mathematica 10.0 (Wolfram Research).

SEM [57,58] were generated by maximum-likelihood estimation in R using the lavaan package [59]. The results presented in figure 4a were based on all 194 countries (except Egypt). Twenty of those had missing data, which were imputed using full information maximum-likelihood estimation. Constraining the analysis to the countries with all variables present led to very similar coefficients. The SEM in figure 4b was computed using the 104 countries with available data.

The pairwise associations among the studied variables were all approximately linear. Only HAQ and HDI had a slightly curvilinear relationship because HDI is the geometric, not arithmetic, mean of life expectancy, education and per capita income. We thus log-transformed HAQ for our analyses, but this had little effect on the results. Also, log transformation of the other variables yielded qualitatively similar results compared with the raw variables.

3. Results

We estimated the average annual change in body height separately for two birth year intervals: from 1896 to 1960 and from 1971 to 1996. Until 1960, all 200 countries with available data showed a positive trend in body height both for males and females; the average annual height increases ranged from 0.4 mm yr−1 in Samoa to 2.3 mm yr−1 in Japan, with a global mean slope of 1.3 mm yr−1 and a standard deviation among slopes of 0.32 mm yr−1. In the birth year interval 1971–1996, by contrast, slopes ranged from −1.7 mm yr−1 in Mauritania to 1.4 mm yr−1 in Taiwan (figure 1), with a mean slope of −0.13 mm yr−1 and a standard deviation of 0.63 mm yr−1, twice as high as that of the earlier interval. We pooled males and females in these analyses; using either only female or only male data did not considerably change the results.

Plotting national C-section rate versus average body height change from birth years 1971 to 1996 (figure 2; electronic supplementary material, figure S2) revealed a strong linear association (193 countries with available data, r = 0.75, p < 0.001). Only Egypt was a clear outlier with a C-section rate of 51.8% well above that predicted for the body height change of −0.11 cm yr−1. We thus excluded Egypt from the following analyses, but this had only very little effect on the results. As noted above, this observed association does not necessarily imply direct causation; it may, at least in part, result from other factors that affect both height change and labour. Statistically correcting (via multiple regression) for obesity and diabetes rates, mean age of the mother, average female body height, HDI, HAQ Index and national HE reduced the strength of association, but height change still accounted for 32% of the global variation in C-section rate (figure 3; 165 countries, r = 0.57, p < 0.001). Figure 2. Relationship between current C-section rate and average annual body height change (cm yr−1 for birth years 1971–1996) for 181 countries. With a C-section rate well above that expected for its body height change (a decrease of 0.11 cm yr−1), Egypt is a clear outlier of this linear trend (r = 0.76; p < 0.001); it was excluded from further analyses. (Online version in colour.) Figure 3. Relationship between C-section rate and average body height change (from birth years 1971 to 1996) after accounting for the effects of Human Development Index (HDI), Healthcare Access and Quality Index (HAQ), HE, mean age of the mother, obesity and diabetes rates, and female average body height in 1996. For the 165 countries with available data, both body height change and C-section rate were linearly regressed on all these covariates, and the resulting residuals are plotted here (r = 0.57, p < 0.001). Hence, even after accounting for all these covariates, body height change still accounts for about a third of the variance in national C-section rates. (Online version in colour.)

We further disentangled the various effects of the variables on C-section rate using SEM. After specifying the potential causal pathways in a path model (figure 4a), SEM allows for quantitatively estimating the strength of the corresponding direct and indirect effects among the variables. The strength of a direct effect was estimated by the regression slope between the standardized variables after correcting for all causally prior and intervening variables. Indirect effects are those mediated by an intervening variable [57]. We considered HDI, HAQ and HE independent variables that can all potentially influence C-section rate directly and also indirectly via effects on body height change, obesity and diabetes rates, mean age of the mother and average female body height in 1996. Of these variables, body height change and HAQ had the strongest direct effects on C-section rate (standardized regression coefficients of 0.55 and 0.42, respectively). Mean age of the mother and obesity rate, which were both affected by HDI and HAQ, had small effects on C-section rate. HDI, the measure of socio-economic development, affected C-section rate only indirectly via body height change, age of the mother and obesity rate. Together, all these variables explained 69% of the global variance in C-section rate (193 countries; root mean square error of approximation = 0.087, comparative fit index = 0.987, Tucker-Lewis index = 0.962). Female height in 1996, diabetes rate and HE were weakly associated with national C-section rate at the bivariate level, but had no relevant direct effects after accounting for the other variables (p-values 0.61, 0.19, and 0.06, respectively; standardized regression coefficients −0.12, −0.06 and 0.06). Hence, we excluded these variables from the final model presented here (see the electronic supplementary material, figure S3 for the full model). Figure 4. (a) Path model representing the direct effects of Human Development Index (HDI) and Healthcare Access and Quality Index (HAQ) on C-section rate, along with their indirect effects via average body height change (from 1971 to 1996), average age of the mother and obesity rate. The values on the paths represent the magnitude of the effects (standardized regression coefficients), estimated by the corresponding structural equation model. All indicated effects were statistically significant (p < 0.001 for all effects). This model explains 69% of the international variation in C-section rate, with secular height change and HAQ being the strongest direct factors. Diabetes rate, body height in 1996 and health expenditure had no significant effects and did not improve the model (electronic supplementary material, figure S3). (b) For a subset of 104 countries, historical HDI values were available. The change of HDI from 1960 to 1995 affected current C-section rate primarily via height change; the direct effect of HDI change on C-section rate was negligible (0.12, p = 0.11).

Even though the change in living conditions (best reflected by HDI change) is assumed to have driven the change in average body height, we used only current HDI estimates in the above model because historical HDI data are not available for all countries. However, we could investigate these relationships within a subsample of 104 countries, for which we had access to historical HDI data [60]. The difference in HDI between 1960 and 1995 significantly correlated both with annual height change from the birth years 1971 to 1996 (r = 0.54) and with current C-section rate (r = 0.50). However, the association between HDI change and C-section rate diminishes when correcting for height increase, indicating that HDI change affects C-section rate only indirectly via height change (figure 4b); the direct effect on C-section rate was negligible. Computing for the 104 countries with available data the full SEM with HDI change from 1960 to 1995 (instead of current HDI) led to very similar path coefficients as in figure 4a (not shown).

4. Discussion

The startling global variation in C-section rate is commonly attributed to current heterogeneity in medical tradition, economic development and other sociocultural factors. Our results, however, indicate that the global variation in C-section rate is also—and in fact quite considerably—influenced by variation in biological factors: the anatomical (dis)proportion of neonatal and maternal dimensions, which are affected by the historical trajectory of socio-economic development (not merely its current state). Hence, we propose that—in addition to all the sociocultural and demographic factors that influence obstetric practices—the actual difficulty of labour varies globally owing to variation in the size of the fetus relative to that of the mother. Indeed, our results suggest that the faster the intergenerational increase in body size because of improving living conditions, the larger the fetus tends to be in relation to the mother. This mechanism deeply entrenches human reproductive biology and childbirth with the local socio-economic development and environmental transitions [14,61–63].

Clearly, we could not prove this effect experimentally (even though the epidemiological studies on migration and labour [50,51] may be considered a kind of ‘natural experiment'), but we tested the observed statistical association of body height change and C-section rate against a list of possible confounding effects and estimated their separate contributions in an SEM. Expectedly, a strong direct effect on C-section rate (i.e. a strong statistical association after controlling for all the hypothesized causally prior and intervening variables) was HAQ, the quality and accessibility of healthcare, which also correlates strongly with HDI, the measure of socio-economic development. However, the direct effect of body height change (from birth years 1971 to 1996) on C-section rate was even stronger, showing a standardized regression coefficient of 0.55 (the raw coefficient equals 10.6% C-section rate per mm yr−1 height change). In other words, global variation in the trend of body height explained about a third of the international variation in C-section rate, even after accounting for socio-economic development, access to healthcare, and their various indirect effects on C-section rate. Together, all these variables in the SEM explained more than two-thirds of the variation in C-section rate.

Many more biological, cultural and psychological factors than those studied here do influence the success of labour and the mode of delivery; they contribute to the roughly 30% of variation in national C-section rate that our model leaves unexplained. But, importantly, as long as these factors are unrelated to the trend in body height, they cannot ‘explain away' our results. To show that the observed correlation between height change and C-section rate indeed reflects a causal relationship (rather than a spurious association), we had to capture all the major factors linked to both height change and C-section rate.

We used two proxies in this analysis. First, we used only adult stature, whereas the immediate causal effect that we propose is the change of body dimensions from the adult mother to her newborn offspring, caused by altered living conditions. Global data on trends in birth weight are not available, but birth weight and size are significantly correlated with adult body height across both individuals and populations [32,64–67]. We could thus use trends in adult height as a proxy in our statistical analysis on the country level. However, as environmental transitions can influence birth weight even if the weight in older ages remains largely unchanged [45], the actual effect of socio-economic transition on labour may be even larger than that estimated here based on adult body height alone. Second, we used only current HDI values in the full model even though the changes in body dimensions are assumed to be because of changes in living conditions. Only for a subset of 104 countries, could we show that HDI change from 1960 to 1995 was strongly correlated with height change as well as with current HDI. Using HDI change instead of current HDI for the SEM within this subsample led to very similar path coefficients as in figure 4a.

Anthropologists and biologists have long argued that ecological and nutritional transitions, such as a change in subsistence strategy, may have affected childbirth and aggravated the tight fit between the large head of the human fetus and the narrow birth canal [2,43,68,69]. For example, Wells and colleagues proposed that selection for decreased body size during the transition from the Palaeolithic into the Neolithic may have increased obstructed labour owing to a lagged decrease of fetal dimensions [2,70]. Our hypothesis, by contrast, implies that childbirth has been challenged by an increase in body size as a plastic (i.e. non-genetic) response to improving living conditions. We tested this hypothesis on the international variation in current C-section rate, but the same process may also have occurred in the past. Both in Europe and North Africa, the change to an agricultural subsistence strategy in the transition from the Palaeolithic to the Mesolithic and Neolithic was accompanied by a substantial decline in average stature of more than 10 cm, followed by a slow recovery until the nineteenth century, and then a rapid increase in the last century [2,71,72]. This continual, presumably environmentally driven increase of body height within the Holocene may have elevated the risk of obstructed labour, especially in the last century. Note that natural selection for increased stature would not have this effect on childbirth. Limited heritability of stature along with an incomplete genetic correlation between adult stature and birth weight would lead to a lagged evolutionary response of birth weight to the selection for increased adult stature, which would even ease childbirth.

Recently, Mitteroecker and colleagues showed that the regular application of lifesaving caesareans has the potential to evolutionarily increase fetopelvic disproportion [5,73]. They estimated that the altered selective regime during the last half-century has already increased the actual disproportion rates by roughly half a percentage point. The obstetric burden resulting from environmentally induced body size increase, as presented here, is even considerably stronger than this evolutionary effect. For example, our model predicts that a continual height increase of 1 mm per year (as was characteristic for or even exceeded by most countries throughout the nineteenth and twentieth centuries, and as is still typical for many developing countries) would increase the caesarean rate by more than 10 percentage points. Of course, this does not suggest that 10% of the mothers really would experience fetopelvic disproportion, but that the aggravated fit of fetal and maternal dimensions would increase the average length and difficulty of labour and the resulting risk of morbidity, which would in turn increase C-section rate (if access to hospitals is available); only a small part of the increase in C-section rate would be owing to complete disproportion. Even after rapid economic development and the associated body height increase have declined (as, e.g. in post-second world war Europe), C-section rates may not easily reduce again if obstetric practices have been established already.

The WHO has suggested an ‘ideal rate for caesarean sections to be between 10% and 15%' [15]. Our results call for a more differentiated view. The actual difficulty of labour—and thus also the risks of birth-related morbidity and obstructed labour—may differ more considerably across geographical and social groups than anticipated. Benchmarks for ‘ideal' rates of C-section should take into account local environmental factors and the historical trajectory of socio-economic development [14]. We encourage a paradigm shift, away from purely cultural explanations of C-section rates, towards a combined biocultural perspective. In response to sociocultural transition and altered selective regimes, human anatomy and physiology have been changing at variable rates and directions around the globe [74].

Data accessibility

Data available as part of the electronic supplementary material.

Authors' contributions

E.Z. collated and analysed the data and contributed to the manuscript. P.M. designed and supervised the study, analysed the data and wrote the manuscript.

Competing interests

We declare we have no competing interests.

Funding

P.M. was supported by the FWF grant no. P29397 and E.Z. by a European Union student exchange programme (ERASMUS).

Acknowledgements We thank Barbara Fischer (KLI Institute, Austria), Nicole Grunstra and Sonja Windhager (Univ. of Vienna, Austria), as well as Roberto Ambrosini (Univ. of Milan, Italy) for discussion and advice.

Footnotes

Electronic supplementary material is available online at https://dx.doi.org/10.6084/m9.figshare.c.4381766.