Introduction

There are 1.8 billion adolescents in the world today, the largest generation in history [1]. Globally, this population is highly vulnerable to negative sexual and reproductive health outcomes such as sexually transmitted infections (STIs) including HIV, unintended pregnancy, and the complications that come with early childbirth [2]. This burden falls disproportionately on adolescent girls [3]. In 2013, two-thirds of all new HIV infections among adolescents between the ages of 15–19 occurred in girls [4]. The disparities are even starker in sub-Saharan Africa, where in some countries, girls aged 15–19 are five times more likely to be infected with HIV than boys their age [4]. Furthermore, the consequences of unintended pregnancy and the risks associated with childbirth fall almost entirely on women and girls [5]. Complications from pregnancy and childbirth including maternal hemorrhage and sepsis, and unsafe abortion are among the leading causes of death among adolescent girls and young women aged 10–24 in low- and middle-income countries [6]. Due to their underdeveloped reproductive systems, pregnant adolescents have increased risk from life-threatening complications including obstructed labor and resultant obstetric fistulae [7–9]. They also have a greater risk of eclampsia and pre-eclampsia [7, 10]. Adolescent girls aged 15–19 years are twice as likely as women in their 20s to die during childbirth; girls under the age of 15 have a five times greater maternal mortality risk [11]. In addition, pregnancy in adolescence is associated with increased risk of HIV infection [12].

Menarche, the onset of menstruation, is an often overlooked indicator in public health [13]. Yet, it is a key developmental marker of a girl’s healthy transition from childhood into young adulthood, and an important clinical indicator of girls’ physical, nutritional, and reproductive health [13]. Menarche marks the beginning of a girl’s reproductive life, and has important implications for adolescent sexual and reproductive health outcomes [13]. A substantial body of evidence from high-income countries suggests that early menarche–generally defined as menarche before age 12–increases adolescent girls’ vulnerability to negative sexual and reproductive health outcomes including early pregnancy and childbearing, STIs, early sexual initiation, and sexual violence [14–22]. For example, data from a birth cohort in New Zealand showed that girls who reached menarche at ages 10–11 years were significantly more likely to report being pregnant by age 18 compared to those with a later age at menarche [17]. Specifically, 11% of girls with early menarche reported being pregnant by age 18, compared to 9% and 1.7% among those with menarche at ages 12–13 and 14–15, respectively. In the same birth cohort, 19.2% of those with early menarche reported having an STI by age 18, compared to 8.8% and 6.9% among those with menarche at ages 12–13 and 14–15, respectively [17]. In a study among young women in the United States, age at menarche was directly and positively correlated to age at first sex, which in turn was directly and positively correlated to age at first pregnancy [14]. However, little is known about whether early menarche is also associated with these outcomes in low- and middle-income countries.

Although it is likely that the links between early menarche and sexual and reproductive health in low- and middle-income countries are similar to those found in high-income countries, this might not necessarily be the case due to differences in sociocultural factors related to menarche and sexual and reproductive health. For example, in many low- and middle-income countries, menarche has traditionally served as a cultural rite of passage and marker of adulthood, positioning a girl as ready for marriage; this is not the case in most high-income countries [13]. Thus, early menarche is more likely to be associated with early marriage in low- and middle-income countries. Furthermore, in many low- and middle-income countries, girls’ mobility and social interactions are often restricted once they reach puberty, limiting their opportunities to engage in pre-marital sexual activity [23]. Such restrictions could minimize the correlation between early menarche and early sexual initiation or risky sexual behavior in low- and middle-income countries. Furthermore, differences in contraception access and use between low-, middle- and high-income countries may contribute to differences in the effect of early menarche on early pregnancy and childbirth across the different settings. Early menarche is likely to have a stronger correlation with adolescent pregnancy and childbirth rates for girls in low-income settings, where access to contraceptives is more limited. In addition, the factors that contribute to early menarche, which could in turn affect related sexual and reproductive health outcomes, may differ. For example, recent declines in the age at menarche in low- and middle-income countries have been attributed to improved socioeconomic, health and nutritional status [24, 25]. On the other hand, in high-income countries, earlier age at menarche has been attributed to markers of lower socioeconomic conditions such as family instability, residential instability, and stressful early life conditions [25–28].

Secular trends from several low- and middle-income countries show decreases in age at menarche over the past few decades [29–34]. This may be increasing girls’ vulnerability [35] given the high burden of negative sexual and reproductive health experienced by adolescent girls and young women in such contexts. There is an urgent need to better understand the effect of early menarche on these outcomes, and the process by which it may increase girls’ vulnerability.

To better understand the association between early menarche and sexual and reproductive health outcomes in low- and middle-income countries and identify gaps in the existing evidence, we conducted a systematic review focused on the following questions: (1) Is early menarche associated with negative sexual and reproductive health outcomes in adolescent girls and young women in low- and middle-income countries? (2) What specific outcomes are associated with early menarche in these countries? (3) Are the associations found in low- and middle-income countries the same as those found in high-income countries? (4) What are some underlying factors, mediators, and moderators that influence these associations?

Methods

We report the findings of our systematic review following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [36]. Prior to beginning our review, we developed a protocol to guide the conduct of our systematic review. The study protocol is registered in PROSPERO (CRD42015023349) [37].

Search strategy

We searched PubMed, PsycINFO, Embase, CINAHL, POPLINE, ProQuest Social Science, Social Sciences Full Text, and Social Sciences Citation Index for peer-reviewed studies that assessed the relationship between menarche and various negative sexual and reproductive health outcomes in adolescence and young adulthood including early sexual debut, experiences of sexual advances from older men, early pregnancy and childbirth, sexual risk taking, unsafe sexual behaviors, unwanted pregnancy, sexual violence, sexually transmitted infections, and HIV. We also searched for studies that assessed the association between age at menarche and early marriage, given that the latter is often a gateway to early sexual behavior, pregnancy and childbearing. We compiled a list of potential search terms identified through preliminary searches, pilot tested them and modified them to improve the thoroughness of our final search. To ensure that all relevant studies were captured, we conducted our final searches using both free text keywords and controlled vocabulary specific to each database. (Only free text keywords were used to search Social Sciences Citation Index because the database does not use controlled vocabulary). We limited our searches to human studies published in English between January 1, 1980 and April 9, 2017. The search strategy used in PubMed is presented in Table 1. In addition to the database searches, we also reviewed the bibliographies of relevant studies for additional citations to evaluate for inclusion in our review.

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Table 1. PubMed specifications of search strategy for systematic review on early menarche and sexual and reproductive health in low- and middle-income countries.

https://doi.org/10.1371/journal.pone.0178884.t001

Eligibility criteria

Studies were selected for inclusion in the systematic review through a multi-step process (Fig 1). First, two researchers independently screened the title and abstract of each identified citation for relevance. Next, they each individually reviewed the full texts of each relevant article to ensure that the articles met all eligibility criteria. In each step, the researchers resolved all disagreements through discussion until a consensus was reached. We included studies if they: were conducted in a low- or middle-income country, assessed the association between early menarche and at least one of the sexual and reproductive health outcomes of interest, were peer-reviewed, and published in English since 1980. We excluded case reports and other studies with small sample sizes (n<50 for quantitative studies and n<15 for qualitative studies), due to the fact that such studies might not be representative of the larger population. We also excluded studies that assessed the determinants of early menarche, but not factors that occurred after menarche. Additionally, we excluded studies that assessed the association between early menarche and biological factors pertaining to sexual and reproductive health (other than STIs), such as genetic factors and various forms of cancer.

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Fig 1. PRISMA flowchart of study selection for systematic review on early menarche and sexual and reproductive health in low- and middle-income countries.

https://doi.org/10.1371/journal.pone.0178884.g001

Results

Search results and study characteristics

Our search of the literature yielded 5010 unique citations (Fig 1). Twenty-four studies met all inclusion criteria and were assessed for quality and risk of bias. Nine of the twenty-four studies were of moderate quality (Table 2) while the remaining fifteen studies had several methodological weaknesses (Table 3). The quality assessment and main methodological weaknesses of all eligible studies are presented in the last column of Tables 2 and 3. Due to the small number of articles of moderate quality, we also include a brief discussion of the weak studies below.

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Table 2. Characteristics of the moderate quality studies included in the systematic review on early menarche and sexual and reproductive health in low- and middle-income countries.

https://doi.org/10.1371/journal.pone.0178884.t002

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Table 3. Characteristics of the weak quality studies included in the systematic review on early menarche and sexual and reproductive health in low- and middle-income countries.

https://doi.org/10.1371/journal.pone.0178884.t003

Discussion

Despite the vast body of research on adolescent sexual and reproductive health in low- and middle-income countries, our systematic review shows that very little is known about the associations between early menarche and sexual and reproductive health outcomes in such settings. The review highlighted that early menarche is associated with early marriage, early sexual initiation, early pregnancy and childbirth, and some STIs in lower-income regions of the world; similar to what has been observed in high-income countries. We found limited research on the association between early menarche and sexual risk behavior. However, it is unclear whether this is due to insufficient research on the topic to date or that the association does not exist. Despite similarities in the relationship between early menarche and sexual and reproductive health in low-, middle- and high-income countries, the underlying factors driving these associations might not be the same due to differences in sociocultural contexts and structural factors across and within such countries. Given the small number of eligible studies and the study designs utilized, we were limited in our ability to determine the underlying factors, mediators and moderators of the associations identified.

Of significance, our review highlighted the association between early menarche and early marriage (the outcome assessed in the majority of eligible studies). This finding could be particularly relevant to ongoing global efforts to curb child marriage. In the study from Nepal, Aryal noted that girls from certain ethnic groups may be married off before menarche for cultural or religious reasons [40]. Similarly, two of the weaker studies from Bangladesh found that 10–18% of girls were married before menarche [48, 54]. Continued declines in age of menarche in these regions may lead to girls being married off at even younger ages. In other regions of the world, menarche signals a readiness for marriage, with girls being married off shortly after they reach menarche [43, 44]. The association between early menarche and early marriage, as well as the related factors, may differ across ethnic groups within the same country [58, 60]. This highlights the need for a greater understanding both within and between countries of the cultural and regional variations in the effect of age at menarche on age at marriage. More research may provide important insights to bolster current efforts to end child marriage and improve the sexual and reproductive health outcomes of adolescent girls and young women.

Although not assessed in the studies included in our review, research suggests that age at first marriage may mediate the association between early menarche and other sexual and reproductive health outcomes. For example, early marriage may increase girls’ vulnerability to the negative health effects of early pregnancy and childbirth, since girls are often expected to bear children soon after marriage [12, 63]. In addition, girls who get married early are often unable to effectively negotiate safer sex, increasing their vulnerability to STIs such as HIV [64]. This is evidenced by research from Kenya and Zambia, which shows considerably higher rates of HIV infection among ever-married girls aged 15–19 years compared to their unmarried but sexually active counterparts [12]. Furthermore, girls who are married in adolescence are more likely than those who marry at a later age to experience sexual violence [1, 63, 65].

Despite decreasing rates of child marriage worldwide, 280 million girls today are still at risk of becoming child brides [64]. In particular, girls living in poor and rural areas of South Asia and sub-Saharan Africa experience high rates of child marriage [63, 64]. In Niger–which has the highest prevalence of child marriage in the world–75% of women aged 20–24 were married before the age of 18 in 2006, reflecting a minimal decline from 77% in 1998 [63]. Thus, our findings suggest that child marriage prevention efforts may benefit from targeting programs and policies to early-maturing girls, focusing on areas where girls reach menarche at younger ages and in regions where menarche signals readiness for marriage. Due to varying cultural beliefs regarding early marriage both across and within countries, such efforts should be tailored to the specific context.

Several of the included studies reported an association between early menarche and early sexual initiation. This association is well documented in the research literature from high-income countries [14, 18–22]. Early sexual initiation has important implications for the overall health of young women, and may also be a key driver of associations observed between early menarche and early pregnancy and STIs. Although none of the studies included in our review expressly examined early sexual initiation as a mediator of the association between early menarche and sexual and reproductive health, some studies suggest that this might be the case. For example, in the study from South Africa, Buga et al. found a much stronger correlation between age at first sex and age at pregnancy (r = 0.68) than between age at menarche and age at pregnancy (r = 0.41) [41]. This suggests that early sexual initiation among those with early menarche might be driving the association between early menarche and early pregnancy.

Adolescents who initiate sexual intercourse at a young age are often vulnerable to coerced, risky and unprotected sex [66–68]. Unprotected sexual activity may in turn lead to unwanted pregnancy and childbearing, abortion, or infection with HIV and other STIs [69]. Girls with early menarche who initiate sexual activity at a young age may not be developmentally prepared for sex (both mentally and physically) or knowledgeable about taking precautions to prevent pregnancy and STIs when having sex [66]. High rates of unmet need for contraception in low- and middle-income countries further limit young girls’ abilities to prevent early pregnancies [5]. In addition, the underdeveloped vaginal epithelial lining in younger girls is more vulnerable to tears during sexual intercourse than that of adult women, thus increasing young girls’ risks of contracting STIs including HIV [70–72].

Structural factors may also underlie the association between early menarche and sexual and reproductive health outcomes. Due to gender inequalities, girls are often unable to insist that their sexual partners take the necessary precautions to prevent pregnancy and STIs during sex [65]. They are frequently unable to decide when to have sex for the first time, with younger girls even less likely to have negotiating power within such gendered dynamics [65]. For example, in some parts of sub-Saharan Africa, 45% of girls report that their first sexual intercourse was forced [65]. Girls who reach menarche at an early age may be especially vulnerable, as they may be perceived as sexually mature due to their more adult-like physical appearances [73]. Despite this increased vulnerability, young girls have little access to necessary sexual and reproductive health services, leading to possible long-term morbidity [1]. These factors may explain the associations found between early menarche and early pregnancy and STIs both in our systematic review and in studies from high-income countries [14, 17, 18]. Although early menarche was not found to be associated with HIV infection, its association with other STIs and the decreased likelihood of HIV serostatus disclosure are still of particular concern in countries with generalized HIV epidemics–such as many countries in sub-Saharan Africa–where the age at menarche has also been declining over the past few decades [30, 31, 74, 75]. All these findings highlight the need for better data on age at menarche, and for the inclusion of menarche indicators in nationally-representative surveys such as the Demographic and Health Surveys (DHS), UNICEF’s Multiple Indicator Cluster Survey (MICS) and Performance Monitoring and Accountability 2020 (PMA2020) [13].

Despite these findings, several questions remain unanswered, indicating a need for further research in this area. First, none of the studies included in our review examined the effect of other pubertal changes on sexual and reproductive health. Early menarche is the most commonly used indicator of early sexual maturation since menarche occurs late in the pubertal development sequence and is one of the more salient aspects of puberty for girls [25, 76]. However, other physical and hormonal changes that accompany puberty, including breast development, occur prior to menarche [25] and may play an important role in explaining the association between early menarche and these outcomes [60]. This may especially be the case in societies such as northern Ethiopia, where girls often hide the onset of menarche from others [77]. Girls with more mature looking physiques–with developed breasts and hips–may be more vulnerable to sexual advances from their male peers and older men [73, 78]. In addition, hormonal changes that accompany puberty may lead early-maturing girls to experience sexual desires and engage in sexual behavior at a young age [60, 78, 79]. The pubertal changes that occur before menarche might explain the findings from the studies from Malawi and Kenya, indicating that some girls engage in sexual intercourse before menarche [43, 51].

Second, due to the cross-sectional nature of the included studies, it is impossible to establish the temporal order of the observed associations–that is, whether early menarche precedes the observed outcomes. For biological reasons, some outcomes such as pregnancy and childbirth must be preceded by menarche. However, that is not the case with STIs and early sexual initiation. In one study from Malawi, Glynn et al. noted that only 2.8% of girls engaged in sexual intercourse before menarche, suggesting that for most girls, menarche occurs before first sex [43]. In contrast, the study from Kenya found a larger proportion of girls who had sex before menarche (16%) [51]. No comparisons were made between girls who engaged in sexual intercourse before menarche and those who did not in either study. Yet, such comparisons may provide important insights to support efforts to mitigate vulnerability to negative sexual and reproductive health outcomes in adolescence and young adulthood.

Supporting information

Acknowledgments

The authors would like to thank Ann Hebert for her assistance in the early stages of developing our search strategy and protocol, and for allowing us to use her quality assessment instrument, and Timothy Frasca for his critical review of the manuscript.