7
Original Research Article Secular Trend in Age at Menarche in Indigenous and Nonindigenous Women in Chile X.M. OSSA, 1 * S. MUNOZ, 2 H. AMIGO, 3 AND S.I. BANGDIWALA 4 1 Department of Obstetrics and Gynecology, Faculty of Medicine, La Frontera University, Temuco, Chile 2 Department of Public Health, Faculty of Medicine, La Frontera University, Temuco, Chile 3 Department of Nutrition, Faculty of Medicine, University of Chile, Santiago, Chile 4 Department of Biostatistics, University of North Carolina, Chapel Hill, North Carolina Objectives: To estimate the secular trend in age at menarche, comparing indigenous and nonindigenous women, and its relationship with socio-demographic, family and nutritional factors. Methods: A study (historical cohorts) of 688 indigenous and nonindigenous women, divided into four birth cohorts (1960–69, 1970–79, 1980–89, and 1990–96) in an area in central southern Chile was carried out. Data and measure- ments were collected by health professionals using a previously validated questionnaire. Age at menarche was self- reported (recall). Adjusted differences among cohorts were estimated using a multivariate regression model. Results: A secular trend (P < 0.001) in age at menarche was found in both ethnic groups, with no significant differen- ces between them (P > 0.05). In an adjusted model, a reduction in age at menarche was estimated at 3.7 months per dec- ade between 1960 and 1990. This trend was moderated by higher socio-economic level, smaller number of siblings, and cohabitation with a single parent during infancy. Conclusions: The trend has occurred in a steady progression over time in indigenous women, whereas in nonindige- nous women, it was slow initially but has accelerated in recent years. Nonindigenous women have maintained a slightly lower age of menarche than their indigenous counterparts. Am. J. Hum. Biol. 22:688–694, 2010. ' 2010 Wiley-Liss, Inc. The trend toward an earlier age at menarche has been the subject of study because it reflects changes in living condi- tions of populations, such as improvement in socioeconomic and sanitary conditions (Gama, 2008; Roman et al., 2009), as well as decreased physical activity and nutritional changes that may play an important role in puberty onset (Cho et al., 2009; Kaplowitz, 2008). Earlier menarche also increases risks derived from prolonged exposure to estrogen such as breast cancer, cardiovascular and metabolic disease, and mental health problems (Golub et al., 2008; Lakshman et al., 2008). Various studies from around the world have concluded that, over the last 150 years, there has been a trend toward a progressive reduction in age at menarche, especially in developed countries (Aksglaede et al., 2009; Cho et al. 2009; Harris et al., 2008; Himes, 2006; Kaplowitz, 2006), but this process has not been absent in developing coun- tries either (Bagga and Kulkarni, 2000; Cameron and Nagdee, 1996; Jones et al., 2009; Malina et al., 2004; Silva and Padez, 2006). Yet, others have concluded that the trend has been leveling off in recent decades (Gohlke and Woelfle, 2009; Papadimitriou et al., 2008). In a recent study pub- lished in Italy, the authors compare their results with those of previous studies and suggest that the downward trend in age of menarche is coming to a halt (Rigon et al., 2010). Most reports have indicated that the secular trend to- ward an earlier menarche is influenced by genetic (Ersoy et al., 2005; Palmert and Hirschhorn, 2003; Soriano Guillen et al., 2008) and environmental factors, among them nutrition, socio-economic level, and general health and lifestyle (Anderson et al., 2003; Jones et al., 2009; Junqueira Do Lago et al., 2003; Koo et al., 2002; Laitinen et al., 2001; Petridou et al., 1996; Wattigney et al., 1999). Improvement of these aspects occurred simultaneously with lower rates of certain factors such as infectious dis- ease, malnutrition and poverty, which, according to Tanner (1992), enables the possibility of expressing the biological potential related with reproductive ability. Currently, it is suggested that genetic factors interact with environmental influences, allowing the expression of similarities or differences between female twins or secular trends between mothers and daughters (Chang and Chen, 2008; Salces et al., 2001; van den Berg et al., 2006). Shared or nonshared nutritional influence (obesity) is probably one of the most studied factors that could interrupt or maintain familial resemblance for age at menarche (Ersoy et al., 2005; Keim et al., 2009); however, birth weight, size at birth and childhood growth trajectories, among others, might also play important roles in gene-environment inter- action (Adair, 2001; Karaolis-Danckert et al., 2009). Nevertheless, genes and pathways that may be involved in the timing of normal puberty and onset of menarche are not yet elucidated. The studies in this area are still not con- clusive, but there are some advances in identification of genetic factors primarily or partly responsible for develop- mental problems (Gajdos et al., 2009; Gorai et al., 2003; Long et al., 2005; Rockett et al., 2004; Stavrou et al., 2002). Some studies that show a certain stabilization of age at menarche in European countries have also been published (Gohlke and Woelfle, 2009; Mascaretti and Di Berardino, 2008; Papadimitriou et al., 2008). These results were asso- ciated with a highly homogeneous urbanization in those places. In some specific regions, an inverse trend has been Contract grant sponsor: National Found of Scientific and Technological Development; Contract grant number: FONDECYT Project N8 81060884; Contract grant sponsor: Higher Education Division of the Ministry of Edu- cation; Contract grant number: MECESUP Program FRO003. *Correspondence to: X.M. Ossa, Departamento de Obstetricia y Gineco- logı ´a, Facultad de Medicina, Universidad de La Frontera, Claro Solar #112, Temuco, Chile. E-mail: [email protected] Received 1 December 2009; Revision received 1 April 2010; Accepted 4 April 2010 DOI 10.1002/ajhb.21068 Published online 24 May 2010 in Wiley Online Library (wileyonlinelibrary. com). AMERICAN JOURNAL OF HUMAN BIOLOGY 22:688–694 (2010) V V C 2010 Wiley-Liss, Inc.

Secular trend in age at menarche in indigenous and nonindigenous women in Chile

  • Upload
    xm-ossa

  • View
    214

  • Download
    1

Embed Size (px)

Citation preview

Page 1: Secular trend in age at menarche in indigenous and nonindigenous women in Chile

Original Research Article

Secular Trend in Age at Menarche in Indigenous and NonindigenousWomen in Chile

X.M. OSSA,1* S. MUNOZ,2 H. AMIGO,3 AND S.I. BANGDIWALA4

1Department of Obstetrics and Gynecology, Faculty of Medicine, La Frontera University, Temuco, Chile2Department of Public Health, Faculty of Medicine, La Frontera University, Temuco, Chile3Department of Nutrition, Faculty of Medicine, University of Chile, Santiago, Chile4Department of Biostatistics, University of North Carolina, Chapel Hill, North Carolina

Objectives: To estimate the secular trend in age at menarche, comparing indigenous and nonindigenous women,and its relationship with socio-demographic, family and nutritional factors.Methods: A study (historical cohorts) of 688 indigenous and nonindigenous women, divided into four birth cohorts

(1960–69, 1970–79, 1980–89, and 1990–96) in an area in central southern Chile was carried out. Data and measure-ments were collected by health professionals using a previously validated questionnaire. Age at menarche was self-reported (recall). Adjusted differences among cohorts were estimated using a multivariate regression model.Results: A secular trend (P < 0.001) in age at menarche was found in both ethnic groups, with no significant differen-

ces between them (P > 0.05). In an adjusted model, a reduction in age at menarche was estimated at 3.7 months per dec-ade between 1960 and 1990. This trend was moderated by higher socio-economic level, smaller number of siblings, andcohabitation with a single parent during infancy.Conclusions: The trend has occurred in a steady progression over time in indigenous women, whereas in nonindige-

nous women, it was slow initially but has accelerated in recent years. Nonindigenous women have maintained a slightlylower age of menarche than their indigenous counterparts. Am. J. Hum. Biol. 22:688–694, 2010. ' 2010 Wiley-Liss, Inc.

The trend toward an earlier age at menarche has been thesubject of study because it reflects changes in living condi-tions of populations, such as improvement in socioeconomicand sanitary conditions (Gama, 2008; Roman et al., 2009), aswell as decreased physical activity and nutritional changesthat may play an important role in puberty onset (Cho et al.,2009; Kaplowitz, 2008). Earlier menarche also increases risksderived from prolonged exposure to estrogen such as breastcancer, cardiovascular and metabolic disease, and mentalhealth problems (Golub et al., 2008; Lakshman et al., 2008).Various studies from around the world have concluded

that, over the last 150 years, there has been a trend towarda progressive reduction in age at menarche, especially indeveloped countries (Aksglaede et al., 2009; Cho et al.2009; Harris et al., 2008; Himes, 2006; Kaplowitz, 2006),but this process has not been absent in developing coun-tries either (Bagga and Kulkarni, 2000; Cameron andNagdee, 1996; Jones et al., 2009; Malina et al., 2004; Silvaand Padez, 2006). Yet, others have concluded that the trendhas been leveling off in recent decades (Gohlke and Woelfle,2009; Papadimitriou et al., 2008). In a recent study pub-lished in Italy, the authors compare their results with thoseof previous studies and suggest that the downward trendin age of menarche is coming to a halt (Rigon et al., 2010).Most reports have indicated that the secular trend to-

ward an earlier menarche is influenced by genetic (Ersoyet al., 2005; Palmert and Hirschhorn, 2003; SorianoGuillen et al., 2008) and environmental factors, amongthem nutrition, socio-economic level, and general healthand lifestyle (Anderson et al., 2003; Jones et al., 2009;Junqueira Do Lago et al., 2003; Koo et al., 2002; Laitinenet al., 2001; Petridou et al., 1996; Wattigney et al., 1999).Improvement of these aspects occurred simultaneouslywith lower rates of certain factors such as infectious dis-ease, malnutrition and poverty, which, according toTanner (1992), enables the possibility of expressing thebiological potential related with reproductive ability.

Currently, it is suggested that genetic factors interactwith environmental influences, allowing the expression ofsimilarities or differences between female twins or seculartrends between mothers and daughters (Chang and Chen,2008; Salces et al., 2001; van den Berg et al., 2006). Sharedor nonshared nutritional influence (obesity) is probably oneof the most studied factors that could interrupt or maintainfamilial resemblance for age at menarche (Ersoy et al.,2005; Keim et al., 2009); however, birth weight, size atbirth and childhood growth trajectories, among others,might also play important roles in gene-environment inter-action (Adair, 2001; Karaolis-Danckert et al., 2009).Nevertheless, genes and pathways that may be involved

in the timing of normal puberty and onset of menarche arenot yet elucidated. The studies in this area are still not con-clusive, but there are some advances in identification ofgenetic factors primarily or partly responsible for develop-mental problems (Gajdos et al., 2009; Gorai et al., 2003;Long et al., 2005; Rockett et al., 2004; Stavrou et al., 2002).Some studies that show a certain stabilization of age at

menarche in European countries have also been published(Gohlke and Woelfle, 2009; Mascaretti and Di Berardino,2008; Papadimitriou et al., 2008). These results were asso-ciated with a highly homogeneous urbanization in thoseplaces. In some specific regions, an inverse trend has been

Contract grant sponsor: National Found of Scientific and TechnologicalDevelopment; Contract grant number: FONDECYT Project N8 81060884;Contract grant sponsor: Higher Education Division of the Ministry of Edu-cation; Contract grant number: MECESUP Program FRO003.

*Correspondence to: X.M. Ossa, Departamento de Obstetricia y Gineco-logıa, Facultad de Medicina, Universidad de La Frontera, Claro Solar#112, Temuco, Chile. E-mail: [email protected]

Received 1 December 2009; Revision received 1 April 2010; Accepted 4April 2010

DOI 10.1002/ajhb.21068

Published online 24 May 2010 in Wiley Online Library (wileyonlinelibrary.com).

AMERICAN JOURNAL OF HUMAN BIOLOGY 22:688–694 (2010)

VVC 2010 Wiley-Liss, Inc.

Page 2: Secular trend in age at menarche in indigenous and nonindigenous women in Chile

reported that is associated with psychosocial stressors(Prebeg and Bralic, 2000; Veronesi and Gueresi, 1994).

In Central and South America, studies on secular trend inage at menarche are scarce. Published studies from Colom-bia and Mexico have shown that age at menarche declinedover the last decades of the last century (Malina et al., 2004;Villamor et al., 2009). Trends toward a reduction in age atmenarche in Haiti and Brazil have also been documented.In rural women originating from the admixture of nativeAmerindians, African slaves, and European colonizers, thistrend has reached the lowest age (12.29 6 1.76 years) pub-lished for the region (Barnes-Josiah and Augustin, 1995;Junqueira Do Lago et al., 2003; Silva and Padez, 2006).

In Chile, studies of age at menarche also document atrend toward an earlier menarche until the 1970s andsubsequent maintenance of a steady level until now(Gaete and Codner, 2006). However, trend studies are rareand representative samples of indigenous women havenot been studied (Quevedo et al., 2005).

Chile’s population has a significant proportion of indige-nous people who are concentrated in specific areas. Theseethnic minorities present inequalities in their health indi-cators when compared to the overall population (Rojas,2007). However, in recent decades, this population hasexperienced an improvement in its standard of living(Bustos et al., 2009), which translates into changes in cer-tain sensitive indicators such as age at menarche. In viewof this, the objective of this manuscript is to estimate thesecular trend in age at menarche, comparing indigenousand nonindigenous women, and its relationship withsocio-demographic, family and nutritional factors.

MATERIALS AND METHODS

Study of secular trend (historical cohorts) in age at men-arche in 688 women divided into four cohorts of 172 womeneach (86 indigenous and 86 non-indigenous) with nonover-lapping birth years (1960–1969, 1970–1979, 1980–1989,and 1990–1996). The criteria used for ethnic differentiationwere having both parents with indigenous (Mapuche) sur-names and self-recognition as indigenous. The criterion fornonindigenous women was having both parents with sur-names of Chilean-Spanish origin. Women were recruitedthrough the public health and education systems of urbanand rural districts in central southern Chile (74% of womenin Chile are ascribed to public health service and 97% ofgirls study in public schools; the wealthiest women, with noethnic differentiation, do not belong to these groups).

The youngest cohort was selected after screening�5,000 girls who had declared the occurrence of menarchethrough a survey conducted in schools selected by conven-ience to evaluate inclusion criteria (ethnicity, occurrenceof menarche between 9 and 17 years of age, absence ofmetabolic disease, infancy in locations at an altitudebelow 1,000 m above sea level and not involved in high-performance sports). The number of Indigenous girls whoqualified was limited; it was not the same with nonindige-nous girls. Thus, for each subject from the first group, onefrom the other group was chosen at random from thesame school. The older cohorts were selected at publichealth centers in the same localities through the centers’registration lists. The procedure was similar to that usedfor the girls. For both girls and women, rates of refusal toparticipate were low (two to three per cohort) and therewere no misses. Nonsignificant differences were found

between refusals and their respective cohorts in terms ofage of menarche and socioeconomic factors (P > 0.05).

Data collection

A previously validated questionnaire collected socio-demo-graphic data (Alacala Consultores Asociados Limitada,2006), age at menarche (in months) and information oncohabiting family members from birth to age 10, as well asnutritional state at time of menarche. This activity was car-ried out by professional midwives. The recall of age at men-arche was reiterative, using key dates (birthdays, vacations,public holidays, and school graduation). In the youngestcohort, one of the parents or a close relative corroborated thedata provided by the girls in all cases. In the other cohorts,17% of cases had age at menarche recorded in the clinical re-cord, and thus, we were able to establish the correlationbetween the two data points (Pearson’s r 5 0.80; P < 0.05).Data for nutritional status classification were obtained usingretrospective self-perception methods (body silhouettes), asthere were no records of weight and height during adoles-cence in the older cohorts (Osuna-Ramırez et al., 2006). Par-ticipants self-reported their body image by selecting amongnine numbered silhouettes (thinner to thicker) that best por-trayed them at menarcheal age. Categories obtained fromthis method were validated with a group of 300 adolescentsfrom among the screened girls. In the youngest cohort, addi-tionally, body mass index (BMI5 weight/height2) was meas-ured and nutritional status category was determined accord-ing to the CDC-NCHS classification up to 3 months post-menarche; these data were compared with the classificationresults of the body silhouettes self-perception using theBangdiwala B-statistic (Munoz and Bangdiwala, 1997). Theself-perception method was used for statistical analysis in allcohorts as standard measure.

Data analysis

A comparative descriptive characteristics analysis wasdone by cohort (X2 homogeneity test, a 5 0.05), of age atmenarche by cohort (nonparametric trend test by Cuzick,a 5 0.05) and by ethnic group (T test for unequal varian-ces, a 5 0.05). Subsequently, the association between ageat menarche and cohorts was estimated by simple regres-sion; and a multivariate regression model was usedto evaluate effect modification (a 5 0.1), interactions(a 5 0.2) and confounding effects of the covariables.

Ethical aspects

The study was approved by two Ethics Committees: thatof the South Araucanıa Health Service and that of La Fron-tera University. Every adolescent in the youngest cohortwas asked for her informed assent first (based on Interna-tional Ethical Guidelines for Biomedical Research Involv-ing Human Subjects, Council for International Organiza-tions of Medical Sciences, Geneva, 2002), and the informedconsent of one of the parents was also obtained. In the oldercohorts, informed consent was obtained.

RESULTS

The final sample consisted of 684 women. Four ques-tionnaires were rejected due to insufficient data, so thetwo oldest cohorts had two fewer members than theothers.

689SECULAR TREND IN AGE AT MENARCHE IN WOMEN

American Journal of Human Biology

Page 3: Secular trend in age at menarche in indigenous and nonindigenous women in Chile

The adolescents in the youngest cohort have a higher pro-portion of overweight and obesity than older cohorts; theproportion of rural residents is higher in the older cohorts,while parental education and income levels are lower in theolder cohorts. Cohabitation with just one parent is more fre-quent in the youngest cohort and the number of siblingsand the incidence of being fourth or lower in birth order ishigher in the older cohorts (Table 1). Each of these variablesshows statistical differences among the cohorts (P < 0.05).The concordance of nutritional state measured by the BMIand the categories derived from the self-perception bodysilhouettes in the first cohort seems to be substantial(B5 0.56) for both measurements (not shown).Table 2 shows that average age at menarche (in months)

in the different cohorts declines over time, with a signifi-

cant secular trend (P < 0.001) in both the indigenous andnonindigenous groups. When the means of each cohort arecompared, with a focus on interethnic comparison (hori-zontal analysis), only the youngest cohorts show signifi-cant differences (P < 0.001), but for the four cohorts over-all, the two ethnic groups are not statistically different(P 5 0.06). On average, age at menarche fell by 4.6months per decade between 1960–69 and 1990–96 (4.8and 4.4 months/decade for non-indigenous and indigenouswomen, respectively) without adjusting for socio-demo-graphic and nutritional variables. For nonindigenouswomen this trend was not linear, as the differencebetween the two older cohorts was not significant(P > 0.05), but thereafter, there is an accelerated decline.On the other hand, in indigenous women the decline inage at menarche was steadier and sustained over time,resulting in a more linear trend.In a crude analysis, a difference of slightly more than

one year in age at menarche between the oldest and theyoungest cohort is observed (13.1 months), and the closerthe birth dates, the smaller the time differences. The dif-ferences between the oldest cohort (1960–69) and each ofthe younger cohorts (1990–95 and 1980–89) are statisti-cally significant. Between the two older cohorts (1960–69and 1970–79), the difference is only significant for indige-nous girls (Table 3). When the impact of the interactionbetween age cohort and ethnic group on age at menarcheis considered, no statistical evidence arises (P 5 0.23) tosupport the claim that this interaction might influencethe secular trend (not shown).When the behavior of menarche in the cohorts (secular

trend) is analyzed, adjusting for factors such as ethnic

TABLE 1. Descriptive characteristics of the study group by cohort

1990–1996(1st)

1980–1989(2nd)

1970–1979(3rd)

1960–1969(4th)

n % n % n % n %

Nutritional statea (P < 0.001)Low weight 0 0 27 15.7 38 22.3 53 31.2Normal 79 45.9 109 63.4 86 50.6 73 42.9Overweight 80 46.5 31 18.0 37 21.8 31 18.2Obese 13 7.6 5 2.9 9 5.3 13 7.7

Place of upbringing (P 5 0.005)Urban 78 45.4 75 43.6 60 35.3 44 25.9Rural 86 50.0 85 49.4 103 60.6 115 67.6Mixed 8 4.6 12 7.0 7 4.1 11 6.5

Parents’ education (P < 0.001)Minimal 17 9.9 35 20.3 87 51.2 117 68.8Incomplete 92 53.5 78 45.4 63 37.0 32 18.8Complete and higher 63 63.6 59 34.3 20 11.8 21 12.4

Income level (P < 0.001)No income 18 10.5 11 6.4 7 4.1 9 5.3Low income 94 54.6 93 54.1 120 70.6 123 72.4Medium income 60 34.9 68 39.5 43 25.3 38 22.3

Cohabitation with (P < 0.001)Both parents 128 74.4 125 72.7 134 78.8 138 81.2Only mother or father 39 22.7 27 15.7 14 8.3 17 10.0Relatives 5 2.9 20 11.6 22 12.9 15 8.8

N8 siblings (P < 0.001)0 to 2 133 77.3 109 63.4 55 32.4 41 24.13 or more 39 22.7 63 36.6 115 67.6 129 75.9

Birth order (P < 0.001)First 75 43.6 76 44.2 46 27.0 42 24.7Second 55 32.0 46 26.7 34 20.0 25 14.7Third 25 14.5 20 11.6 21 12.4 35 20.6Fourth or lower 17 9.9 30 17.5 69 40.6 68 40.0Total 172 100 172 100 170 100 170 100

P-value associated with differences among cohorts.aSelf-perception method.

TABLE 2. Decline in age at menarche (in months) by cohorts and withethnic differentiation

Cohort

IndigenousNon

indigenous Total

P**Mean SD Mean SD Mean SD

1990–1996 150.8 9.7 145.6 10.5 148.2 10.4 <0.0011980–1989 155.3 14.8 154.3 15.9 154.8 15.3 0.61970–1979 158.6 16.8 159.4 15.1 159.0 16.0 0.71960–1969 163.9 14.8 160.0 17.9 162.0 16.5 0.2Total P* 157.2 15.0 154.8 16.1 156.0 15.6 0.06

<0.001 <0.001 <0.001

*P value associated with secular trend (nonparametric trend), vertical analysis.**P value associated with comparison of interethnic means (T test for unequalvariances) in each cohort, horizontal analysis.

TABLE 3. Differences in age at menarche (in months) with respect tooldest cohort

Indigenous Nonindigenous Entire group

Age atmenarche Coef CI (95%) Coef CI (95%) Coef CI (95%)

1990–1996 213.1** 217.4 28.8 214.5** 219.0 29.9 213.8** 216.9 210.71980–1989 28.6** 212.9 24.4 25.7* 210.3 21.2 27.2** 210.3 24.11970–1979 25.4* 29.7 21.1 20.6 25.2 3.9 23.0 26.1 0.1

Reference category: 1960–1969 cohort.**P-value < 0.001.*P-value < 0.05.

TABLE 4. Reduced model for association between age at menarche(in months) and cohort adjusted for control variables

Variables Coef. b S.E. Wald X2 P-valueConfidenceInterval 95%

Constant 153.92 2.2 69.2 0.000 149.55 158.23Birth cohorts1990–1996 211.16 1.8 26.37 <0.001 214.60 27.721980–1989 25.23 1.7 23.15 0.002 28.49 22.01970–1979 22.96 1.6 21.87 0.062 26.07 0.151960–1969 Ref. – – – – –

Cohabitation during infancyWith both parents 2.71 1.7 1.63 0.10 20.55 6.00With relatives 4.84 2.5 1.96 0.05 20.01 9.7Only mother/father Ref. – – – – –

Number of siblingsThree or more 3.80 1.3 2.85 0.005 1.18 6.42

Level of incomeNo income 5.12 2.5 2.08 0.04 0.29 9.95Low income 3.50 1.3 2.74 0.006 0.98 5.93Medium income Ref. – – – – –

690 X.M. OSSA ET AL.

American Journal of Human Biology

Page 4: Secular trend in age at menarche in indigenous and nonindigenous women in Chile

group, nutritional status, parental levels of income andeducation levels, place of upbringing (rural or urban),cohabitation during infancy, number of siblings and birthorder, as well as their interactions, a simplified model canbe extracted as shown in Table 4.

Finally, the variables representing the nutritional anddemographic-cultural status of the women do not have aconfounding effect or major influence on the model andthus were discounted. In the model shown in Table 4, thedifference between the youngest and the oldest cohort(11.16 months) is smaller than in crude analysis, estab-lishing an adjusted decline of age at menarche of 3.7months/decade modulated by cohabitation during infancy,number of siblings and parental income level.

DISCUSSION

The results of this study demonstrate that there isindeed a secular trend in the age at menarche over thelast 30 years. This trend has occurred as a steady progres-sion over time in indigenous women, whereas in nonindig-enous women it was slow initially but has accelerated inrecent years. The latter group has maintained a slightlylower age of menarche than its indigenous counterpart.However, this dissimilarity does not constitute evidence ofa trend with significant interethnic differentiation. Fac-tors such as higher income level, smaller number of sib-lings, and cohabitation with a single parent duringinfancy produce effects which moderate the trend.

The trend toward an earlier age at menarche in thisstudy may be related to improvement of socio-economicconditions for the Chilean population in recent decades,similarly to other studies; this would have repercussionsin terms of female maturation stages (Junqueira Do Lagoet al., 2003; Parent et al., 2003; Wronka and Pawlinska-Chmara, 2005). This improvement, observed in increasedlevels of education and family income as well as improvedhealth indicators (UNDP and MIDEPLAN, 2004), hasbenefitted the indigenous population particularly throughthe creation and implementation of development strat-egies stemming from the country’s Indigenous Law.

The decrease in menarcheal age has been more signifi-cant among indigenous females which is consistent withdecreasing levels of poverty for the indigenous populationoverall. Despite this, the age at menarche for young indig-enous females continues to be older than for females withno indigenous family background, which is also consistentwith the less favorable socioeconomic situation of the in-digenous population (of which the Mapuche are the larg-est subgroup) in relation to the overall population (MIDE-PLAN, 2007; UNDP, 2003) On the other hand, a markedfecundity reduction has been occurring in the countrysince 1960 due to government policies aimed at reducingrates of infant-maternal morbidity and mortality (Donosoet al., 2009). This fact is coincident with a lower number ofsiblings in younger cohorts in this study, a situation thatis consistent with the decreasing levels of poverty, influ-encing age at menarche indirectly.

The mechanism through which socio-economic levelinfluences age at menarche cannot be clearly established.One alternative may be nutritional status during child-hood or in adolescence itself (Kirchengast and Bauer,2007; Marco-Hernandez et al., 2008).This might alsoexplain why age at menarche is lower in more obesogenicenvironments. The absence of underweight girls, with an

evident transition to overweight and obesity in theyounger cohort, probably favors the earlier occurrence ofmenarche in this work. There are several studies confirm-ing this inverse relationship as the principal associationwith earlier menarche (Adair and Gordon-Larsen, 2001;Anderson et al., 2003; Hernandez et al., 2007; Kaplowitz,2008; Rosenfield et al., 2009) Some researchers proposethat serum leptin levels may play an outstanding role inmenses onset. This hormone, which acts as a mediatorbetween adipose tissue and the gonadal-hypothalamicaxis, has a positive correlation with body fat percentage,but an inverse relationship with age at menarche, sug-gesting a threshold effect (Bandini et al., 2008; Li et al.,2005).Nevertheless, apparently not only is fat mass impor-

tant, but body fat distribution also plays a significant rolein menses onset especially in women with low levels oftotal body fat (Lassek and Gaulin, 2007). On the otherhand, some studies suggest that quality of diet duringchildhood and the premenarcheal period might also influ-ence the timing of puberty, sometimes independently ofbody composition (Berkey et al., 2000; Cheng et al., 2010;Koo et al., 2002) These potential effects must increasinglybe taken into account because a nutritional transition hasalso been occurring in Chile; this has been marked since1980 and has had a particular effect on the indigenouspopulation (Albala et al., 2002; Bustos et al., 2009). Thus,it might be appropriate to think that some of the afore-mentioned mechanisms may be at work.Some phenomena which occur in early life periods such

as low birth weight, asymmetrical constitution, rapidrates of early childhood growth and weight gain atdifferent ages, among others, are possibly related toan earlier reproductive capability in human females dueto metabolic and endocrine ‘‘programming’’ (Gluckmanand Hanson, 2006a,b; Hernandez and Mericq, 2008;Karaolis-Danckert et al., 2009). Some of these aspectswould have been modeling the decreasing age at men-arche in the older cohorts, especially among indigenouswomen, because of less advantageous socioeconomic con-ditions and higher under-nutrition rates, but follow-updata were not available to contribute to the discussion.In Chile, Gaete and Codner (2006) postulate that age at

menarche has remained stable over recent decades; how-ever, this assertion is based on comparing outcomes of trans-versal studies done at different times in the central regionof the country. Our study was carried out in one of the poor-est regions of Chile, which, although it has experienced aprogressive improvement in living conditions, is offers whatis far from an optimal living standard, raising doubt aboutthe relationship with stabilization of age at menarche.The impact of cohabitation with a single parent during

infancy on the model is consistent with what has beensuggested in other studies and by the psychosocial theory,namely that girls who live in unstable family environ-ments, particularly with the father absent, experiencemenarche earlier than those who grow up in a stable fam-ily environment due to higher levels of psycho-socialstress (Belsky, 2010; Bogaert, 2008; Chisholm, 2005; Ellisand Essex, 2007; Matchock and Susman, 2006). Neverthe-less, other approaches have emerged to explain the poten-tial relationship between earlier menarcheal onset andpaternal absenteeism. A genetic model proposed by Com-ings et al. (2002) explains the early onset of puberty indaughters as a genetic trait inherited from fathers who

691SECULAR TREND IN AGE AT MENARCHE IN WOMEN

American Journal of Human Biology

Page 5: Secular trend in age at menarche in indigenous and nonindigenous women in Chile

have certain behaviors that contribute to marital conflictand family abandonment. Kim and Smith (1998) suggestthat girls’ age at menarche and reproductive developmentmay be linked to inherited maternal personality traitsinvolved in the intergenerational transmission of repro-ductive life history events that eventually contribute tofamily instability. This situation (absentee father) isincreasingly common in Chilean society and requires fur-ther study with better control of those aspects that may becausing certain biases.The differences between the cohorts found in our study

are similar, on average, to what has occurred in some Eu-ropean and North American countries. In Chile, the oldestinformation (from 1888) on age at menarche in the pastindicates a mean (SD) of 13.1 (1.1) for this event in south-ern Chile (Diaz, 1888). Although the outcomes of thisstudy are not comparable, this datum suggests that thedecline in age at menarche was not so marked and thatthe greatest change has occurred in recent decades, unlikeEuropean countries in which much higher ages at men-arche were observed at the end of the 19th century.De Muinich Keizer and Mull (2001) state that the onset ofpuberty in Europe during the Middle Ages was around14 years and shifted to 17–18 years by the 19th century,and then fell progressively during the last century to set-tle at around 13 years in recent decades. Nevertheless,recent studies estimated that the declining trend hascontinued (Aksglaede et al., 2009; Danubio and Sanna,2008; O’Connell et al., 2009), while others postulatethat pubertal onset and age at menarche had reachedtheir limit (Gohlke and Woelfle, 2009; Juul et al.,2006; Mascaretti and Di Berardino, 2008; Papadimitriouet al., 2008).In general, secular trends in America have continued in

recent years. Unfortunately, there are few other studies ofsecular trend in indigenous populations with which to com-pare the results found in this work. In Mexico, no seculartrend has been observed in age at menarche among olderand younger women in an indigenous population over a pe-riod of 80 years, but one of the causes postulated by theauthor is the modest instability of living conditions of thispopulation during the same period (Malina et al., 1983).A weakness of this study is the fact that age at men-

arche was a datum obtained retrospectively so that it islikely to be affected by recall bias. Even so, in the young-est cohort age of menarche was corroborated by themother or a close relative with a correlation of 100%,while the correlation in a sample of the older cohorts was80%. Another weakness is the determination of nutri-tional status at age at menarche through body silhouettes;however, there were no population measurements at thisage, so this method was the only way to obtain the data.Although, real measurements of BMI (weight/height2)and body silhouette perceptions show only substantialconcordance in the younger cohort, the nutritional statustrend of the cohorts in this research is consistent withother studies of children carried out in the country and inthe same area where this study was conducted (Bustoset al., 2009; Kain et al., 2005).Among the strengths of the study is that a validated

questionnaire was used, and this questionnaire wasapplied by qualified reproductive health professionalswith the collaboration of mothers and teachers in the firstcohort; for the other cohorts, the questionnaire wasapplied at a time and place necessary conducive to good

recall. Likewise, it is important to highlight that all of thewomen were rigorously selected, following selection pat-terns for indigenous and nonindigenous women in similargeographical locations so as to maintain homogeneity inthe sample and avoid selection bias.In conclusion, a secular trend in age at menarche with

no ethnic differentiation, correlated with socioeconomicimprovement, lower number of siblings and cohabitationwith just one parent during childhood has been demon-strated in this study. Although a genetic component seemsto be important to determination of age at menarche in aspecific population, the interaction with different types ofenvironmental factors, in the long run, could result in acontinuation of this decline process in this region of Chile.As long as optimum standards of living are achieved andmaintained, especially among indigenous females, morestudies are needed, which consider other environmentalfactors such as differences in body composition, dietaryintake, endocrine disruptors, migratory movement,psychosocial stressors and familial inheritance, amongothers.

LITERATURE CITED

Adair LS. 2001. Size at birth predicts age at menarche. Pediatrics 107:E59.Adair LS, Gordon-Larsen P. 2001. Maturational timing and overweight

prevalence in US adolescent girls. Am J Public Health 91:642–644.Aksglaede L, Sorensen K, Petersen JH, Skakkebaek NE, Juul A. 2009.

Recent decline in age at breast development: the Copenhagen PubertyStudy. Pediatrics 123:932–939.

Albala C, Vio F, Kain J, Uauy R. 2002. Nutrition transition in Chile: deter-minants and consequences. Public Health Nutr 5:123–128.

Alcala Consultores Asociados Limitada. 2006. Evaluacion y validacion delsistema nacional de asignacion con equidad (SINAE) disenada por laJunta Nacional de Auxilio Escolar y Becas [On line] [Cited 2010 Feb 24];[190 screens] Available from URL: http://www.junaeb.cl/prontus_junaeb/site/artic/20100121/pags/20100121112705.html.

Anderson SE, Dallal GE, Must A. 2003. Relative weight and race influenceaverage age at menarche: results from two nationally representativesurveys of US girls studied 25 years apart. Pediatrics 111:844–850.

Bagga A, Kulkarni S. 2000. Age at menarche and secular trend in Mahara-shtrian (Indian) girls. Acta Biol Szeged 44:53–57.

Bandini LG, Must A, Naumova EN, Anderson S, Caprio S, Spadano-Gasbarro JI, Dietz WH. 2008. Change in leptin, body compositionand other hormones around menarche-a visual representation. ActaPaediatr 97:1454–1459.

Barnes-Josiah D, Augustin A. 1995. Secular trend in the age at menarchein Haiti. Am J Hum Biol 7:357–362.

Belsky J. 2010. Childhood experience and the development of reproductivestrategies. Psicothema 22:28–34.

Berkey CS, Gardner JD, Frazier AL, Colditz GA. 2000. Relation of child-hood diet and body size to menarche and adolescent growth in girls. AmJ Epidemiol 152:446–452.

Bogaert AF. 2008. Menarche and father absence in a national probabilitysample. J Biosoc Sci 40:623–636.

Bustos P, Munoz S, Vargas C, Amigo H. 2009. Evolution of the nutritionalsituation of indigenous and non-indigenous Chilean schoolchildren. AnnHum Biol 36:298–307.

Cameron N, Nagdee I. 1996. Menarcheal age in two generations of SouthAfrican Indians. Ann Hum Biol 23:113–119.

Chang SR, Chen KH. 2008. Age at menarche of three-generation familiesin Taiwan. Ann Hum Biol 35:394–405.

Cheng G, Gerlach S, Libuda L, Kranz S, Gunther AL, Karaolis-DanckertN, Kroke A, Buyken AE. 2010. Diet quality in childhood is prospectivelyassociated with the timing of puberty but not with body composition atpuberty onset. J Nutr 140:95–102.

Chisholm JS QJ, Petersen RW, Coall DA. 2005. Early stress predicts age atmenarche and first birth, adult attachment and expected lifespan. HumNat 16:233–265.

Cho GJ, Park HT, Shin JH, Hur JY, Kim YT, Kim SH, Lee KW, Kim T.2009. Age at menarche in a Korean population: secular trends and influ-encing factors Eur J Pediatr 169:89–94.

Comings DE, Muhleman D, Johnson JP, MacMurray JP. 2002. Parent-daughter transmission of the androgen receptor gene as an explanation ofthe effect of father absence on age of menarche. Child Dev 73:1046–1051.

692 X.M. OSSA ET AL.

American Journal of Human Biology

Page 6: Secular trend in age at menarche in indigenous and nonindigenous women in Chile

Danubio ME, Sanna E. 2008. Secular changes in human biological varia-bles in Western Countries: an updated review and synthesis. J Anthro-pol Sci 86:91–112.

de Muinich Keizer SM, Mul D. 2001. Trends in pubertal development inEurope. Hum Reprod Update 7:287–291.

Diaz E. 1888. Breves observaciones sobre la aparicion de la pubertad en lamujer chilena i de las predisposiciones patologicas del sexo. Anales de laUniversidad 15:289–298

Donoso E, Carvajal J, Dominguez MA. 2009. Fecundity reduction andaging in fertile women population in the period 1990-2004 in Chile. RevMed Chil 137:766–773.

Ellis BJ, EssexMJ. 2007. Family environments, adrenarche, and sexual matu-ration: a longitudinal test of a life history model. Child Dev 78:1799–1817.

Ersoy B, Balkan C, Gunay T, Egemen A. 2005. The factors affecting therelation between the menarcheal age of mother and daughter. ChildCare Health Dev 31:303–308.

Gaete X, Codner E. 2006. Adelanto de la pubertad en Chile y el mundo.Rev Chil Pediatr 77:456–465.

Gajdos ZK, Hirschhorn JN, Palmert MR. 2009. What controls the timing ofpuberty? An update on progress from genetic investigation. Curr OpinEndocrinol Diabetes Obes 16:16–24.

Gama A. 2008. Age at menarche in Portuguese rural women from Oleiros.Ann Hum Biol 35:639–655.

Gluckman PD, Hanson MA. 2006a. Changing times: the evolution of pu-berty. Mol Cell Endocrinol 254–255:26–31.

Gluckman PD, Hanson MA. 2006b. Evolution, development and timing ofpuberty. Trends Endocrinol Metab 17:7–12.

Gohlke B, Woelfle J. 2009. Growth and puberty in German children: isthere still a positive secular trend? Dtsch Arztebl Int 106:377–382.

Golub MS, Collman GW, Foster PM, Kimmel CA, Rajpert-De Meyts E,Reiter EO, Sharpe RM, Skakkebaek NE, Toppari J. 2008. Public healthimplications of altered puberty timing. Pediatrics 121Suppl 3:S218–S230.

Gorai I, Tanaka K, Inada M, Morinaga H, Uchiyama Y, Kikuchi R, ChakiO, Hirahara F. 2003. Estrogen-metabolizing gene polymorphisms, butnot estrogen receptor-alpha gene polymorphisms, are associated withthe onset of menarche in healthy postmenopausal Japanese women. JClin Endocrinol Metab 88:799–803.

Harris MA, Prior JC, Koehoorn M. 2008. Age at menarche in the Canadianpopulation: secular trends and relationship to adulthood BMI. J AdolescHealth 43:548–554.

Hernandez MI, Mericq V. 2008. Pubertal development in girls born smallfor gestational age. J Pediatr Endocrinol Metab 21:201–208.

Hernandez MI, Unanue N, Gaete X, Cassorla F, Codner E. 2007. Age ofmenarche and its relationship with body mass index and socioeconomicstatus. Rev Med Chil 135:1429–1436.

Himes JH. 2006. Examining the evidence for recent secular changes in thetiming of puberty in US children in light of increases in the prevalenceof obesity. Mol Cell Endocrinol 254–255:13–21.

Jones LL, Griffiths PL, Norris SA, Pettifor JM, Cameron N. 2009. Age atmenarche and the evidence for a positive secular trend in urban SouthAfrica. Am J Hum Biol 21:130–132.

Junqueira Do Lago M, Faerstein E, De Souza Lopes C, Werneck GL. 2003.Family socio-economic background modified secular trends in age atmenarche: evidence from the Pro-Saude Study (Rio de Janeiro, Brazil).Ann Hum Biol 30:347–352.

Juul A, Teilmann G, Scheike T, Hertel NT, Holm K, Laursen EM, MainKM, Skakkebaek NE. 2006. Pubertal development in Danish children:comparison of recent European and US data. Int J Androl 29:247–255.

Kain J, Uauy R, Lera L, Taibo M, Espejo F, Albala C. 2005. Evolution ofthe nutritional status of six years old Chilean children (1987-2003). RevMed Chil 133:1013–1020.

Kaplowitz P. 2006. Pubertal development in girls: secular trends. CurrOpin Obstet Gynecol 18:487–491.

Kaplowitz PB. 2008. Link between body fat and the timing of puberty.Pediatrics 121Suppl 3:S208–S217.

Karaolis-Danckert N, Buyken AE, Sonntag A, Kroke A. 2009. Birth andearly life influences on the timing of puberty onset: results from theDONALD (DOrtmund Nutritional and Anthropometric LongitudinallyDesigned) Study. Am J Clin Nutr 90:1559–1565.

Keim SA, Branum AM, Klebanoff MA, Zemel BS. 2009. Maternal bodymass index and daughters’ age at menarche. Epidemiology 20:677–681.

Kim K, Smith PK. 1998. Childhood stress, behavioural symptoms andmother-daughter pubertal development. J Adolesc 21:231–240.

Kirchengast S, Bauer M. 2007. Menarcheal onset is associated with bodycomposition parameters but not with socioeconomic status. Coll Antro-pol 31:419–425.

Koo M, Rohan T, Jain M, McLaughlin J, Corey P. 2002. A cohort study ofdietary fibre intake and menarche. Public Health Nutr 5:353–360.

Laitinen J, Power C, Jarvelin MR. 2001. Family social class, maternalbody mass index, childhood body mass index, and age at menarche aspredictors of adult obesity. Am J Clin Nutr 74:287–294.

Lakshman R, Forouhi N, Luben R, Bingham S, Khaw K, Wareham N, OngKK. 2008. Association between age at menarche and risk of diabetes inadults: results from the EPIC-Norfolk cohort study. Diabetologia 51:781–786.

Lassek WD, Gaulin SJ. 2007. Brief communication: menarche is related tofat distribution. Am J Phys Anthropol 133:1147–1151.

Li HJ, Ji CY, Wang W, Hu YH. 2005. A twin study for serum leptin, solubleleptin receptor, and free insulin-like growth factor-I in pubertal females.J Clin Endocrinol Metab 90:3659–3664.

Long JR, Xu H, Zhao LJ, Liu PY, Shen H, Liu YJ, Xiong DH, Xiao P, LiuYZ, Dvornyk V, Li JL, Recker RR, Deng HW. 2005. The oestrogen recep-tor alpha gene is linked and/or associated with age of menarche in differ-ent ethnic groups. J Med Genet 42:796–800.

Malina RM, Pena Reyes ME, Tan SK, Little BB. 2004. Secular change inage at menarche in rural Oaxaca, southern Mexico: 1968–2000. AnnHum Biol 31:634–646.

Malina RM, Selby HA, Buschang PH, Aronson WL, Wilkinson RG. 1983.Adult stature and age at menarche in Zapotec-speaking communities inthe Valley of Oaxaca, Mexico, in a secular perspective. Am J PhysAnthropol 60:437–449.

Marco-Hernandez M, Benitez R, Medranda I, Pizarro C, Mendez MJ. 2008.Normal physiological variations of pubertal development: starting age ofpuberty, menarcheal age and size. Ann Pediatr (Barc) 69:147–153.

Mascaretti G, Di Berardino C. 2008. Study of pubertal development inAbruzzo (Italy) and analysis of factors implicated in puberty variability.Clin Exp Obstet Gynecol 35:117–120.

Matchock RL, Susman EJ. 2006. Family composition and menarcheal age:anti-inbreeding strategies. Am J Hum Biol 18:481–491.

MIDEPLAN, Government of Chile. 2007. La situacion de pobreza en Chile,2006 [On line] [Cited 2010 feb 24]; 1:[52 screens]. Available from URL:http://www.mideplan.cl/casen/cpublica_2006.html

Munoz S, Bangdiwala S. 1997. Interpretation of Kappa and B statisticsmeasures of agreement. J Appl Stat 24:105–111.

O’Connell A, Gavin A, Kelly C, Molcho M, Nic Gabhainn S. 2009. Themean age at menarche of Irish girls in 2006. Ir Med J 102:76–79.

Osuna-Ramırez I, Hernandez-Prado B, Campuzano JC, Salmeron J. 2006.Indice de imagen corporal y percepcion de la imagen corporal en unapoblacion adulta mexicana: la precision del autorreporte. Salud PublicaMex 48:94–103.

Palmert MR, Hirschhorn JN. 2003. Genetic approaches to stature, puber-tal timing, and other complex traits. Mol Genet Metab 80:1–10.

Papadimitriou A, Fytanidis G, Douros K, Bakoula C, Nicolaidou P,Fretzayas A. 2008. Age at menarche in contemporary Greek girls: evi-dence for levelling-off of the secular trend. Acta Paediatr 97:812–815.

Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J, BourguignonJP. 2003. The timing of normal puberty and the age limits of sexual pre-cocity: variations around the world, secular trends, and changes aftermigration. Endocr Rev 24:668–693.

Petridou E, Syrigou E, Toupadaki N, Zavitsanos X, Willett W, TrichopoulosD. 1996. Determinants of age at menarche as early life predictors ofbreast cancer risk. Int J Cancer 68:193–198.

Prebeg Z, Bralic I. 2000. Changes in menarcheal age in girls exposed towar conditions. Am J Hum Biol 12:503–508.

Quevedo I, Flores M, Castillo M. 2005. Caracterısticas reproductivas de lasmujeres consultantes en servicios de urgencia general de la VIII Region.Rev Med Chil 133:929–934.

Rigon F, Bianchin L, Bernasconi S, Bona G, Bozzola M, Buzi F, CicognaniA, De Sanctis C, De Sanctis V, Radetti G, Tato L, Tonini G, PerissinottoE. 2010. Update on age at menarche in Italy: toward the levelling off ofthe secular trend. J Adol Health 46:238–244.

Rockett JC, Lynch CD, Buck GM. 2004. Biomarkers for assessing repro-ductive development and health. I. Pubertal development. EnvironHealth Perspect 112:105–112.

Rojas F. 2007. Poverty determinants of acute respiratory infections amongMapuche indigenous peoples in Chile’s Ninth Region of Araucania, using GISand spatial statistics to identify health disparities. Int J Health Geogr 6:26–38.

Roman EP, Ribeiro RR, Guerra-Junior G, Barros-Filho Ade A. 2009.Antropometry, sexual maturation and menarcheal age according to soci-oeconomic status of schoolgirls from Cascavel (PR). Rev Assoc Med Bras55:317–321.

Rosenfield RL, Lipton RB, DrumML. 2009. Thelarche, pubarche, and men-arche attainment in children with normal and elevated body mass index.Pediatrics 123:84–88.

Salces I, Rebato EM, Susanne C, San Martin L, Rosique J. 2001. Familialresemblance for the age at menarche in Basque population. Ann HumBiol 28:143–156.

Silva HP, Padez C. 2006. Secular trends in age at menarche among Caboclopopulations from Para, Amazonia, Brazil: 1930-1980. Am J Hum Biol18:83–92.

Soriano Guillen L, Blanco Rodriguez M, Cortes Martin M, MartinezMartin C. 2008. Secular trend of menarcheal age in Spanish adolescents.Med Clin (Barc) 131:355–356.

693SECULAR TREND IN AGE AT MENARCHE IN WOMEN

American Journal of Human Biology

Page 7: Secular trend in age at menarche in indigenous and nonindigenous women in Chile

Stavrou I, Zois C, Ioannidis JP, Tsatsoulis A. 2002. Association of polymor-phisms of the oestrogen receptor alpha gene with the age of menarche.Hum Reprod 17:1101–1105.

Tanner JM. 1992. Growth as a measure of the nutritional and hygienic sta-tus of a population. Horm Res 38 Suppl 1:106–115.

UNDP. 2003. El ındice de desarrollo humano en la poblacion mapuche enla region de la Araucanıa [On line] [Cited 2010 Feb 24];8:[54 screens]Available from URL: http://www.desarrollohumano.cl/otraspub/pub08/pub08.pdf

UNDP and MIDEPLAN, Government of Chile. 2004. Las trayectorias deldesarrollo humano en las comunas de Chile (1994-2003) [On line][Cited 2010 Feb 24]; [150 screens]. Available from URL:http://www.desarrollohumano.cl

van den Berg SM, Setiawan A, Bartels M, Polderman TJ, van der Vaart AW,Boomsma DI. 2006. Individual differences in puberty onset in girls: Bayesianestimation of heritabilities and genetic correlations. Behav Genet 36:261–270.

Veronesi FM, Gueresi P. 1994. Trend in menarcheal age and socioeconomicinfluence in Bologna (northern Italy). Ann Hum Biol 21:187–196.

Villamor E, Chavarro JE, Caro LE. 2009. Growing up under generalized vi-olence: an ecological study of homicide rates and secular trends in age atmenarche in Colombia, 1940s-1980s. Econ Hum Biol 7:238–245.

Wattigney WA, Srinivasan SR, Chen W, Greenlund KJ, Berenson GS.1999. Secular trend of earlier onset of menarche with increasing obesityin black and white girls: the Bogalusa Heart Study. Ethn Dis 9:181–189.

Wronka I, Pawlinska-Chmara R. 2005. Menarcheal age and socio-economicfactors in Poland. Ann Hum Biol 32:630–638.

694 X.M. OSSA ET AL.

American Journal of Human Biology