Department of Biological and Experimental Psychology, School of Biological and Behavioural Sciences, Queen Mary University of London;
Fiona S. McEwen
Department of Biological and Experimental Psychology, School of Biological and Behavioural Sciences, Queen Mary University of London
Demelza Smeeth
Department of Biological and Experimental Psychology, School of Biological and Behavioural Sciences, Queen Mary University of London
Cassandra M. Popham
Department of Biological and Experimental Psychology, School of Biological and Behavioural Sciences, Queen Mary University of London
Elie Karam
Department of Psychiatry and Clinical Psychology, Balamand University;
St Georges Hospital University Medical Center, Beirut, Lebanon;
Institute for Development, Research, Advocacy and Applied Care (IDRAAC), Beirut, Lebanon
Michael Pluess
Department of Biological and Experimental Psychology, School of Biological and Behavioural Sciences, Queen Mary University of London
Acknowledgement: Michael Pluess is now at the Department of Psychological Sciences, School of Psychology, University of Surrey.
We warmly thank all participating families for their participation. We thank Robert Brennan, Paul Allison, Emil Coman, and the others who helped us formulate our data analytic strategy. We also thank the broader BIOPATH team that made this research possible. The BIOPATH study was funded by the Eunice Shriver National Institute of Child Health and Human Development (R01HD083387). Candace J. Black’s effort is funded by the European Union’s Horizon 2020 research and innovation program under Marie Skłodowska-Curie Grant Agreement No. 896988. The authors declare no competing interests or financial support.
The study was performed in accordance with the ethical standards as laid down in the 1964 Declaration of Helsinki and its later amendments or comparable standards. Ethical approval was granted by the Institutional Review Board of the University of Balamand/Saint George Hospital University Medical Center, Lebanon (ref: IRB/O/024-16/1815). The study was also reviewed by the Lebanese National Consultative Committee on Ethics and approved by the Ministry of Public Health. Researchers interested in accessing data should contact Michael Pluess at
Candace J. Black served as lead for conceptualization, data curation, formal analysis, methodology, visualization, writing–original draft, and writing–review and editing. Fiona S. McEwen served as lead for data curation, contributed equally to validation, and served in a supporting role for investigation, methodology, project administration, and writing–review and editing. Demelza Smeeth served in a supporting role for data curation and writing–review and editing. Cassandra M. Popham served in a supporting role for data curation and writing–review and editing. Elie Karam contributed equally to investigation, project administration, resources, and supervision and served in a supporting role for writing–review and editing. Michael Pluess served as lead for investigation, methodology, project administration, resources, supervision, and validation, contributed equally to conceptualization, and served in a supporting role for writing–review and editing. Candace J. Black, Michael Pluess, and Elie Karam contributed to funding acquisition.
In recent years, increasing evidence has linked the timing and pace of puberty to mental and physical health later in life (
For over 10 years, Syria has faced a brutal civil war characterized by state-sponsored chemical warfare, barbaric atrocities by terrorist groups, and millions of Syrian families fleeing the country in one of the worst humanitarian crises of the modern era. The Syrian conflict led to widespread displacement, resulting in 6.8 million refugees and 6.7 million internally displaced people (
Evolutionary models of human development offer a unique lens for understanding biological embedding of exposure to adversity (
While PAT has offered a strong framework for identifying environmental risk factors that may influence pubertal development, it does not consider several elements which might make it more generalizable in LMICs where >90% of adolescents reside (
Of particular relevance to the current study are outcomes anticipated by elevated morbidity and mortality, as well as elevated energetic stress. For populations facing elevated adult-specific or overall morbidity/mortality, reproductive success is enhanced by accelerating maturation and increasing the rate of reproduction. When morbidity/mortality is juvenile-specific, adaptive calibration of development depends on whether effects of morbidity and mortality are mitigated by resource allocation decisions of parents or offspring. When mitigation is possible, reproductive success is enhanced by delaying maturation and acquiring resources to improve condition and competitiveness. When mitigation is not possible, reproductive success benefits from accelerated maturation to increase time at reproductive maturity. Cross-cutting these conditions is resource scarcity/energetic stress. In populations facing resource scarcity and energetic stress, development is delayed to prioritize basic maintenance over growth due to low energy availability.
Pubertal Development and War Exposure
Over the last two decades, accumulating evidence has supported life history predictions about pubertal development, particularly with regard to the accelerating effects of child abuse (e.g.,
Other studies examining menarche in relation to World War II (WWII) focused on birth cohorts without directly measuring war exposures. These studies also tended to find delays in age at menarche, such as in Poland (
In contrast,
The seemingly conflicting results from previous research could be explained if both war exposures and nutrition deprivation are considered. The extant literature, for the most part, relied on archival data and year of birth to approximate war exposure. When war exposure was measured more directly, it lacked granularity (e.g., asking just three questions in
It is increasingly important from a global health standpoint to account for both psychosocial stress and energetic stress when measuring pubertal development, especially in LMICs where political conflict and resource scarcity are more common. Some life history research conducted in Cebu, Philippines, has investigated relative effects of nutrition versus parental instability and/or sibling death, finding that nutrition but not psychosocial stressors predicted rates of maturation in boys and girls (
We address these limitations using longitudinal data from the Biological Pathways of Risk and Resilience in Syrian Refugee Children (BIOPATH) study, which collected questionnaire data and biological samples from 1,600 Syrian refugee children and their caregivers living in tented settlements in the Beqaa region of Lebanon in 2017 and 2018 (
Hypothesis 1: Refugee children experiencing higher energetic stress in the absence of war exposure will experience (a) delayed pubertal timing (in boys) or (b) decreased risk of menarche (in girls).
Hypothesis 2: Refugee children facing lower energetic stress and higher exposure to war events will experience (a) accelerated pubertal timing (in boys) or (b) increased risk of menarche (in girls).
Hypothesis 3: Refugee children facing higher energetic stress and higher exposure to war events will experience (a) attenuated pubertal timing acceleration (in boys) or (b) attenuated increases in risk of menarche (in girls).
Hypothesis 4: Effects of war exposure will be especially strong for war events most closely associated with morbidity and mortality threats.
A detailed description of recruitment and sample characteristics for the BIOPATH study is provided in
The first year of data collection included 1,600 child–caregiver pairs and 1,009 (63%) of these were followed up 1 year later. Five cases were excluded due to: data missing due to tablet failure; child less than 8 years old and unable to understand questions; family not living in a tented settlement; and/or family participated twice. After data cleaning (online supplemental materials), our sample consisted of 1,576 children (748 male and 828 female). Baseline sample characteristics are described in
The study received Institutional Review Board (IRB) approval from the University of Balamand/Saint George Hospital University Medical Center, Lebanon (ref: IRB/O/024-16/1815), sponsorship from Queen Mary University of London, and governmental approvals from the Lebanese Ministry of Public Health. Informed consent was obtained from parents, and assent was obtained from the child. Families were compensated for participation in the study.
Below we describe the measures used in the current study. The analytical models included measures of war exposure, energetic stress, pubertal development, and a covariate measuring the number of years since leaving Syria. The imputation model included all of these variables, as well as several auxiliary variables used to inform the imputation, including hair hormones, biometric data, family demographics, refugee environment, and environmental sensitivity (described in the online supplemental materials).
War Exposure
The War Exposure Questionnaire is a 25-item questionnaire developed by the Institute for Development, Research, Advocacy and Applied Care (IDRAAC) to measure exposure to war, adapted for use with Syrian refugees (
Energetic Stress
Child height in cm, weight in kg, hip and waist circumference in cm were transformed using the World Health Organization’s (WHO) Child Growth Standards SPSS macro, which produced several metrics including body mass index (BMI)-for-age z-scores. These growth standards were developed as part of the
Pubertal Development
Pubertal development was measured with two of five items on the Pubertal Development Scale (
For male children, responses were recoded into one of four stages of pubertal development using the scoring criteria of the Pubertal Development Scale. Having only two of five items meant that no child could be classified as postpubertal (the fifth pubertal stage) even though such children might be present in the sample (n = 9 boys rated changes being complete across both items). It is also possible that having additional items may have increased variability in pubertal staging, and/or increased the precision of our results. Once data were recoded, ordinal pubertal development scores were regressed on age and the standardized residuals were retained as estimates of relative pubertal timing. Negative values indicate delayed pubertal timing, while positive values indicate accelerated pubertal timing.
Among female children, responses to the menarche questions across both waves were transformed into person-period data, such that each girl had a binary observation for each discrete time interval beginning at birth. Girls who reported having not yet achieved menarche were assigned a zero, while girls who reported having achieved menarche were assigned a one for the specified interval. Girls who had not reached menarche by the end of data collection were censored. We dropped time intervals in which there was no variance, ultimately retaining intervals corresponding to between 8 and 15 years of age.
As a result of these different approaches to handling pubertal data from boys and girls, it must be noted that the language around and interpretation of our findings will depend on sex. Specifically, whereas models involving male pubertal data describe effects on pubertal timing relative to other boys in this sample, models involving female pubertal data describe effects on “risk of” menarche due to our modeling approach (see “Data Analysis” section below). These differences are reflected in our language. Pubertal timing, pubertal delay, and pubertal acceleration only apply to boys. For girls, the outcome is not acceleration or deceleration relative to peers, but rather increased or decreased risk of achieving menarche. When describing both boys and girls, we use the more general term, pubertal development.
Number of Years Since Leaving Syria
A single item measured the amount of time since participants had left Syria. Participants were able to report whether they had left Syria: 0–12 months ago (1), 12–24 months ago (2), 24–36 months ago (3), 36–48 months ago (4), or more than 48 months ago (5). While this is an ordinal variable, we elected to treat it as an interval variable because the lower-bound values are precisely 12 months apart and start at zero.
Data cleaning was conducted primarily in IBM SPSS Version 27 (
We conducted path analysis for boys and structural equation modeling for girls. All variables were observed for boys while for girls, pubertal development was a latent variable. This distinction was based on our approach to modeling for girls, which used survival analysis; this approach is appropriate for time-to-event data and accommodates censored data. We used discrete time intervals because girls most often reported age at menarche in whole-year numbers, resulting in data “ties” which means that several girls share event times (i.e., achieving menarche at age 13, for instance). Discrete time survival mixture analysis treats event history variables as indicators of a latent class variable and is highly versatile (
As a primary objective of this paper is to examine whether patterns of pubertal development vary as a function of energetic stress, we conducted a series of nested model comparisons which tested interactions sequentially. Conventional model comparison statistics, such as the log-likelihood ratio and chi-square difference test are unavailable for imputed data. Mplus uses the Wald chi-square test for nested model comparisons with imputed data (
Researchers interested in accessing the data used in this study should contact Professor Michael Pluess at Queen Mary University of London, United Kingdom.
This study is not preregistered.
War Exposure
Examination of prevalence of specific war events revealed remarkable similarities across boys and girls (
Descriptive statistics for the war constructs are shown in
Resource Scarcity/Energetic Stress
Sociodemographic data indicate that participating Syrian refugee families faced significant economic barriers (Tables S1 and S2 in the online supplemental materials). For instance, 47.3% of families with male children and 47.4% of families with female children reported income between zero and 15 USD (LBP 0–23,000) per week. Around a third of families reported receiving cash assistance (33.4% for boys and 38.7% for girls) and nearly two-thirds reported receiving food assistance (65% for boys and 63.9% for girls). The distributions and descriptive statistics for baseline BMI-for-age are displayed in
Pubertal Development
Because our measures of pubertal development consisted of fewer items than are typically used in the literature, we examined associations between pubertal development and other key variables expected to be associated with it, such as age, biometrics (weight, height, hip and waist circumference), and hormone levels, to increase confidence in our measures. These findings are shown in
These analyses revealed strong associations between puberty items and biometric measures among both boys and girls. Only the association between pubertal stage and DHEA was nonsignificant in boys. Taken all together, we felt confident that our measures captured variation in pubertal development. With that said, we do acknowledge that using so few items of pubertal development is not ideal and may reduce the precision of our findings.
Male Syrian Refugee Children
The models for pubertal timing in Year 1 and Year 2 were tested separately. To test whether boys facing energetic stress experience delayed puberty (Hypothesis 1), we tested whether lower BMI-for-age predicted delayed pubertal timing. We found no association with pubertal timing in Year 1 (β = 0.00, SE = 0.03, p = .95, 95% confidence interval [CI] [−0.06 to 0.06]) nor in Year 2 (β = −0.05, SE = 0.04, p = .25, [−0.13 to 0.03]). Tabulation of these results is available in Table S4 of the online supplemental materials. Taken all together, Hypothesis 1 was not supported in boys.
We then tested whether the effect of war exposure on pubertal timing depends on energetic stress (Hypotheses 2 and 3). Tabulated results of these models are presented in Tables S4–S6 in the online supplemental materials. The final model for boys is displayed in
The results reveal that mortality significantly predicted pubertal timing acceleration in Year 1 (β = 0.04, SE = 0.02, p = .05, 95% CI [0.00–0.08]), as did the Mortality × BMI-for-Age interaction (β = 0.03, SE = 0.01, p = .02, [0.01–0.06]). BMI-for-age, bombing, and kidnapping were not associated with pubertal timing in Year 1. The overall model effect size for pubertal timing in Year 1 was not significant (R
In order to interpret the positive interaction between mortality and BMI-for-age, we plotted the interaction at different values of BMI-for-age ranging between −2 SD and +2 SD (
We also plotted the interaction using the Johnson–Neyman technique to reveal the regions of significance for the interaction (Figure S5 in the online supplemental materials). This analysis confirmed the results of our simple slopes analysis. Mortality exposure only accelerates pubertal timing when BMI-for-age is just about average or above (i.e., zero or above).
Female Syrian Refugee Children
To test whether girls facing higher energetic stress have a lower risk of menarche (Hypothesis 1), we first tested a model with only BMI-for-age as a predictor. This test revealed a significant, positive relationship between BMI-for-age and risk of menarche (β = 0.27, SE = 0.07, p = <.001, 95% CI [0.13–0.41]) which supports our hypothesis (Table S8 in the online supplemental materials). That is, for a 1 SD increase in BMI-for-age (because BMI-for-age is a standardized score), there is a 0.27 increase in log odds of menarche. As well, for a 1 SD decrease in BMI-for-age, there is a 0.27 decrease in log odds of menarche, which aligns with our predictions. To make these findings more easily interpretable, we can easily convert log odds coefficients to the more familiar hazard odds ratio with the following hazard probability equation:
To test whether the effect of war exposure on pubertal timing depends on energetic stress (Hypotheses 2 and 3), we followed the same procedures as with boys. Results of these models are available in Tables S9 and S10 in the online supplemental materials. The final model is displayed in
To further probe the detected interaction, we tested the simple slopes and plotted the interaction. The tests of simple slopes, depicted in Table S11 in the online supplemental materials, showed a significant, negative relationship between bombing and risk of menarche only for girls who left Syria four or more years ago (simple slopes β = −0.24, SE = 0.10, p = .02, 95% CI [−0.44 to −0.07], Hazard OR = 0.79). As shown by the plot of the interaction below (
Our study has revealed intriguing findings about pubertal development in war-affected refugee children living in low-resource settings. We observed several novel findings with regard to unique effects of different kinds of war events and sex differences in response to these exposures. We also showed that energetic stress (BMI-for-age) can play a critical role in determining whether effects of war exposure impact pubertal development. As there is a lot to unpack, we begin by summarizing our results for boys followed by those for girls. Then we will take an eagle-eye view to explain our interpretations of the patterns we observed.
Our tests of the effects of war exposure and energetic stress on pubertal timing in boys revealed several key findings. First, we did not find support for Hypothesis 1 which predicted that energetic stress delays pubertal timing in boys. At the same time, our tests of Hypotheses 2 and 3 indicate that energetic stress does in fact impact pubertal development in Year 1, particularly by moderating the effects of morbidity/mortality exposures on pubertal timing. This interaction showed that the effects of morbidity/mortality threats on pubertal timing in Year 1 are attenuated under conditions of elevated energetic stress. In the absence of energetic stress, we find that exposure to morbidity/mortality threats accelerates pubertal timing, as is commonly reported in the pubertal timing literature. That this finding emerged with specific respect to the morbidity/mortality war construct, but not the bombing or kidnapping constructs, is consistent with our expectations that morbidity/mortality threats are especially salient in terms of their influence on pubertal timing, as predicted by Life History Theory.
However, by Year 2, all of the observed effects were absent. Pubertal timing in Year 2 was not predicted by any war exposure construct, nor by any interaction of war with energetic stress. One possible explanation is that pubertal development “caught up” by Year 2. Recall that pubertal timing is a standardized z-score which reflects boys’ pubertal stage regressed on age. Thus, pubertal timing is relative to the child’s age and relative to the sample. In Year 1, boys exposed to more morbidity/mortality-related war events had, on average, higher pubertal timing z-scores than boys exposed to fewer such events. For pubertal timing in Year 2, we recalculated boys’ pubertal timing for their age in Year 2. The results for Year 2 indicate that the pubertal timing z-scores did not vary as a function of war, energetic stress, or their interactions. That is, by Year 2, boys exposed to morbidity/mortality war events did not particularly stand out relative to their peers.
The different results across years of data collection suggest that effects of war exposure on pubertal timing in boys depend on when the data were collected. This may mean that temporal proximity to war exposure is important for detecting effects on pubertal timing. However, we did conduct sensitivity analyses with an item which measured the number of years since the boys had left Syria and we found no effect, neither directly on pubertal timing, nor as a moderator of the effects of war constructs on pubertal timing. In other words, we tested whether the effects of war depended on how recently the exposure occurred and did not find any indication that this might influence our results. One possibility for these disparate findings is that the single item is a poor measure of temporal proximity, at least with respect to pubertal timing in boys. Either way, future research investigating effects of adverse exposures on pubertal development should consider the possibility that temporal proximity to events may influence findings.
Our findings for Syrian refugee girls revealed a completely different pattern of effects. For one, we observed a clear relationship between energetic stress and girls’ risk of menarche. As we predicted, girls facing higher energetic stress are less likely to experience menarche. However, none of our subsequent tests revealed any interactions between war constructs and BMI-for-age as we expected. In fact, the only other significant effect for girls, besides the direct effect of BMI-for-age, was a significant interaction between bombing exposure and time since the girls had left Syria. Our follow-up tests to probe this significant interaction indicated that the effect of bombing predicted a lower probability of menarche, but only for girls who left Syria four or more years prior to data collection. Not only is the direction of the effect of war exposure in contrast to our expectations, but only 12% of Syrian refugee girls had left Syria more than 4 years prior to data collection (according to baseline data), meaning that 88% of girls are not well characterized by this interaction.
We think one possible explanation for the different findings in boys and girls is that they were influenced by our measures of pubertal development. In particular, we were able to calculate pubertal timing at two time points in boys and these models revealed significant effects on pubertal timing in Year 1, but not Year 2. In contrast, for girls, our best use of the data was to conduct discrete time survival analysis. To do so, we had to transform our data to create person-period variables which identified whether girls had achieved menarche or not by the end of the study. In other words, girls’ pubertal development is characterized by survival (or risk of menarche) by Year 2. It is possible that the results may have been different if we had measured girls’ pubertal stages with greater granularity and over multiple time points. Achieving menarche distinguishes girls in the later Tanner stages (4–5) from those in the earlier Tanner stages (1–3); however, a further distinction is not possible. Furthermore, menarche only occurs once, further limiting its utility in measuring change over time. We do think that the possibility that the observed sex differences are due to measurement highlights a need for future research involving longitudinal measures of pubertal development. When such measures are available over multiple time points (in boys and/or girls), studies tend to focus on pubertal tempo (e.g.,
Another possibility is that the results are due to sex differences in reporting on pubertal development. Our measures of pubertal development are likely to reflect Syrian refugee children’s knowledge and understanding of the pubertal transition; however, their access to reproductive health education is likely influenced by culture, gender, and religion. In general, the Western Asia and North African region is characterized by conservative sociocultural norms that discourage youth-friendly sexual and reproductive health services and information (
Indeed, Syrian refugee adolescent girls in Lebanon report menarche as shocking, scary, and unexpected, with varying prior knowledge and access to family members who could help (
The BIOPATH study from which our data are drawn is highly unique in several respects, thereby lending itself particularly well to the hypotheses tested in this paper. It is one of the very few studies which collected data from Syrian refugee families contemporaneously with the Syrian Civil War. The sample of 1,600 refugee child–caregiver dyads living in temporary settlements in Lebanon is highly unique, as are the quality of the measures which include validated, self-report measures of a number of individual and environmental traits as well as biometric measures, hair hormones, and saliva samples. Refugees tend to be fairly mobile which can pose challenges for longitudinal data collection, but because saliva samples were collected and used in genome-wide association analysis, we were able to confirm that we were indeed collecting data from the same child over the two years of data collection. Additionally, to the best of our knowledge, BIOPATH is the only study which has measured characteristics of puberty concurrently with development in a large sample of war-affected children who were displaced at the time of data collection.
The primary limitation of this study is our measurement of pubertal development, which consisted of just two items each for boys and girls. Our selection of items was determined by our need to use caution in how certain questions were asked due to strong cultural and religious boundaries around sexuality and reproductive health. Although we did find strong associations between these items and other measures of growth and development, our findings are likely to lack precision. For instance, we could not actually measure whether boys were postpubertal due to the number of items available. For girls, we were unable to detect earlier stages of puberty at all as menarche typically occurs around Tanner Stage 4 (
It is critical for future research on pubertal development to sample from more diverse settings. As demonstrated here, the patterns of pubertal development we identified in war-affected refugee children depart from those which are commonly found in populations living in more stable, higher resource settings. For children in the latter settings (upon whom the majority of pubertal development research is based), threat exposures typically predict earlier and faster pubertal development, leading some to propose pubertal screening among medical and mental health providers to identify trauma-exposed youth (e.g.,
Exposure to trauma during childhood and adolescence is often linked to accelerated pubertal development in populations living in higher resource settings. This body of evidence is increasingly used to advocate for pubertal screening to identify trauma-affected youth and intervene in the development of psychopathology. We investigated how war and displacement impacted pubertal development in Syrian refugee children, predicting that energetic stress (nutrition deprivation) attenuates effects of war exposure on pubertal development. In Syrian refugee boys, war events linked to morbidity/mortality threats predicted accelerated pubertal timing. As predicted, this pattern is attenuated in boys facing elevated energetic stress. In Syrian refugee girls, elevated energetic stress decreased risk of menarche. Additionally, exposure to war events characterized by bombing and explosions predicted decreased risk of menarche, but only for girls who had left Syria more than four years prior to data collection. All together, these findings reveal that expected effects of trauma on pubertal development may be obscured under conditions of elevated resource scarcity. Further research is needed which investigates pubertal development in non-Western settings, particularly in LMICs where more than 90% of the world’s children and adolescents live.
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Submitted: September 27, 2022 Revised: March 8, 2023 Accepted: April 12, 2023