Age at menarche in relation to nutritional status and critical life events among rural and urban secondary school girls in post-conflict Northern Uganda

Over the past 150 years, the age of menarche has fallen by a full four years in the industrialized West. Much as the secular trend in human size has been an adaptive response to a nutritionally rich environment, the receding age of adolescence and pubertal development has been an adaptive response to positive environmental cues in terms of energy balance [1]. The current mean age at menarche in the United States of America is at 12.55 and 12.0 years among black and white girls, respectively [2]. In Sub-Sahara Africa, a secular trend in age at menarche has also been observed in several countries, with socioeconomic status, altitude, ethnicity and food security playing an important role. A study in Ethiopia compared girls with food security and those without and found a significant earlier age at menarche among the former [3]. Similar results were reported from the Amazonia, Senegal and India [4‐6].

When children experience severe environmental stresses such as malnutrition or disease, maturation is delayed until conditions improve and normal growth can resume, which may be regarded as a wait-and-see strategy for environmental conditions to improve before the affected individual assumes an energetic costly gestation. Hochberg and Belsky have recently stipulated that familial psychosocial stress (e.g., marital conflict, harsh parenting, father absence) or extra-familial ecological stress (e.g., limited income, unemployment) fosters a fast rather than quality-oriented reproductive strategy; psychosocial stress accelerates pubertal maturation and, relatedly, sexual debut, promiscuity and parental investment [7].

Here we tested the puberty-related theory of socialization, in post-conflict northern Uganda in adolescent girls who had been subjected to extreme hardship of war and poverty. Gulu District had been at the center of a two-decade rebellion between the Lord’s Resistance Army led by Joseph Kony and the army of the government of Uganda. More than 95% of the population was displaced into camps with no access to their farmland. Malnutrition was common and affected mostly children and pregnant mothers. Many children were abducted and used as child soldiers or sex slaves by the rebels [8]. Many lost their relatives and were forced to kill others, hence suffered from extreme psychological stress [9]. Girls in rural areas were more at risk of stressful critical life events than those in urban areas; they were more susceptible to abduction, displacement, poverty and malnutrition.

The working hypotheses assumed that (i) girls stressed during their childhood will have earlier menarche; (ii) current nutritional status will correlate with menarche age; (iii) girls in rural environment will have earlier age at menarche than those in urban homes.

Previous studies, as recently reviewed [2], have shown that the nutritional status and the social context of an adolescent girl, such as the family composition, have important influence on the menarche age. It was also shown that the absence of a biological father, the presence of half-brothers and step-brothers, and living in an urban environment are associated with earlier menarche, while menarche age was not affected by the number of brothers in the household, nor was there an effect of birth order [11]. Whereas our study, which was carried out in the unique situation of an African provincial post-war region, confirms the importance of body composition and confirms the earlier menarche of urban girls, we find no impact of an extreme stressful childhood life events on menarche age.

Why is it that adolescent girls of northern Uganda showed such resilience to extreme hardship during their childhood, abduction by rebels and loss of relatives to the war, which did not affect age at menarche? This may be due to a selection bias to the study of girls who attend secondary schools, indicating a higher social class; more than half of the girls in this region drop out of school before reaching secondary school levels due to extreme poverty that forces them to early marriage and child labor.

Indeed, within this group paternal (but not maternal) education was associated with earlier menarche. To understand the findings, we resort to Del Giudice’s integrated evolutionary model of the development of attachment and reproductive strategies [12]. His argument called for two critical ages during late infancy and middle childhood that have adaptive significance for reproductive strategies, including menarche age. Late infantile psychosocial stress and insecure attachment switch development towards early puberty and early mating-oriented reproductive strategies. During middle childhood insecure males adopt avoidant strategies, i.e., they avoid engaging in early sexual activities, whereas insecure females tend to adopt anxious/ambivalent strategies, i.e., early menarche and initiation of sexual activities and reproduction to ensure survival, shifting to dismissing patterns when environmental risk is more severe and/or social resources are scarce. Paternal education is therefore associated with improved household income and since fathers are the greatest contributors and determinants of household income, the lack of paternal education is associated with unemployment, marital conflict and poverty which in turn are stressful life events affecting menarche age [7].

In our study, we also found that urban girls had earlier menarche, in support of previous reports from other countries. Furthermore, children were displaced from the periphery of towns into the town centers as night commuters with minimal adult supervision and hence early initiation of sexual activities, while girls in rural areas lived in IDP camps where they lived with parents [8, 9].

Of the body composition variables, hip circumference stands out with a negative correlation with the age at menarche and significantly discriminating urban girls from rural girls in terms of menarche age. Hip circumference is a unique parameter in body composition, normally greater in females than in males; although directly correlated with BMI, it seems to support a specific protective metabolic role. The gluteo-femoral body fat has been shown to be inversely associated with blood glucose, blood pressure and lipids, and to be associated with reduced risk of CVD, all-cause and cardiovascular mortality [13]. This population-based survey among south Asian and African Mauritians showed that the well-documented waist circumference becomes strongly correlated with mortality only after adjustment for hip circumference and vice versa. More mechanistically, a beneficial adipokine profile is associated with gluteo-femoral fat; leptin and adiponectin levels were positively associated with gluteo-femoral fat while the levels of inflammatory cytokines were negatively associated [14]. It was previously suggested that larger hip circumference reflects greater muscle mass [15]. Manolopolous et al. suggested that “gluteo-femoral fat may protect our bodies, irrespective of gender, by trapping excess fatty acids and preventing chronic exposure to elevated lipid levels” [15]. Interestingly, among hunter-gatherers from north Tanzania, the Hadza men preferred women with “protruding buttocks” [16]. The results presented here support a previous contention that gluteo-femoral fat may be more relevant to menarche age than total fat [17]. Among American girls, an increase in gluteo-femoral fat was associated with an increased likelihood of being at menarche compared to fat distribution in other parts of the body [18]. Cross-sectional data from the third National Health and Nutrition Examination Survey (NHANES III) for females aged 10–14 showed that unit increases in hip circumference were associated with 24% higher odds of menarche, while increases in waist circumference and triceps skinfold lower the odds by 7 and 9%, respectively. On the other end of reproductive life, change from pre- to postmenopausal status is associated with increased waist circumference but reduced hip circumference [19].

In Uganda, little has been done in the area of menarche age, and the national age at menarche is not known. This is the first report of menarche age, and it confirms the urban–rural difference, as reported elsewhere.

The study has several inert limitations: Stressful life events might have been underreported because of fear, past experiences and stigma, especially abduction into rebel captivity. In addition, the degree of stress of such life events was not measured. Finally, girls in the same age group who have dropped out of school were not captured in this study.

Hereditary, environmental and stochastic factors regulate puberty in a unique environment, but their relative contribution to the age at menarche is not known. We emphasize uniqueness of each child in her given genetic background and current environment as they best serve her reproductive fitness. The resilience of pubertal development among Ugandan girls who have been subjected to stressful life events would be better understand by studies of socio-nutritional factors as they interact with or via endocrine mechanisms in generating signals that affect menarche age.