- Email: [email protected]
Biological maturity at birth, the course of the subsequent ontogenetic stages and age at menarche
HOMO - Journal of Comparative Human Biology 63 (2012) 292–300
Contents lists available at SciVerse ScienceDirect
HOMO - Journal of Comparative Human Biology journal homepage: www.elsevier.de/jchb
Biological maturity at birth, the course of the subsequent ontogenetic stages and age at menarche ´ A. Szwed ∗, M. Kosinska Department of Human Biological Development, Institute of Anthropology, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznan, Poland
a r t i c l e
i n f o
Article history: Received 22 March 2011 Accepted 30 January 2012
a b s t r a c t The main aim of the study was to assess the influence of biological maturity at birth on growth processes in the subsequent years and during puberty in girls. The material of this study comes from the outpatient clinic cards and cross-sectional research on girls from the province of Wielkopolska in Poland. It includes data of 527 girls. The influence of perinatal maturity on body weight in the later stages of ontogeny was determined with the use of the Kruskal–Wallis test and the Mann–Whitney U test. In order to determine the relationship between perinatal maturity and age at menarche, the survival analysis module was used. The results show a diverse influence of perinatal maturity on the values of body weight achieved in later years of life. The indicated predictive factors included both birth weight and gestational age. In the examined girls menarche occurred between the 10th year and the 17th year of life (X¯ = 12.87, s = 1.26; Me = 13 years). The comparison showed a significant variation in age at menarche depending on the length of pregnancy (log-rank 22 = 27.068, p < 0.0001) and birth weight (log-rank 22 = 23.241, p < 0.0001). There was no variation in maturation of the examined girls conditioned by the occurrence of intra-uterine growth retardation (log-rank 22 = 2.046, p > 0.05). Remote prognoses as to the postnatal development of preterm-born children and/or children with low birth weight indicate adverse influence of these variables on age at menarche. Perinatal biological maturity of a newborn conditions the course of postnatal development. © 2012 Elsevier GmbH. All rights reserved.
∗ Corresponding author. Tel.: +48 61 829 57 13; fax: +48 61 829 57 30. E-mail address: [email protected] (A. Szwed). 0018-442X/$ – see front matter © 2012 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.jchb.2012.01.003
A. Szwed, M. Kosi´ nska / HOMO - Journal of Comparative Human Biology 63 (2012) 292–300
293
Introduction A description of biological reality and complex ecological systems is one of the most important challenges of modern science. An interesting example of an ecological system is the model of mutual interactions in the ´ and Kosicki, 2007). The basic paradigm of examgenotype–environment–individual system (Kosinska ination of developmental phenomena is the statement that an individual during development in its ontogeny goes through the subsequent stages that are genetically determined. The quality of these stages (level of individual development) depends on interaction between the individual’s genotype and environmental conditions. It should be emphasized that the quality of the subsequent developmental stages is a combined effect of the genetic material and the modifying influence of environmental fac´ and Szwed, 2008; tors in a particular moment of ontogeny and preceding stages of growth (Kosinska ´ Kosinska, 2006). Crossing the selection thresholds: birth, puberty, and reproduction are considered key moments of human development. Reaching the subsequent ontogenetic stages is possible only after crossing the preceding selection threshold, therefore crossing each threshold is an indispensable element of further development. The birth selection threshold is the moment of transition from the prenatal to postnatal stage, understood as the birth of a morphologically and physiologically mature newborn that is capable of independent performance of basic life functions. Entering the puberty stage and achieving the possibility of crossing another post-puberty selection threshold is subject to the normal course of the growth processes and lack of factors impeding the development both in the preceding stages and in the very puberty stage. Crossing this threshold is understood as obtaining the ability to produce gametes, and thus reaching biological maturity that conditions ability to reproduce. A consequence of reaching the threshold is the opportunity to reach the next life stages. However, it should be emphasized that crossing the subsequent ontogenetic stages, and thus the subsequent selection thresholds, does not guarantee completion of the following developmental stages (Kaczmarek and Łastowski, 2004). While assuming continuity of ontogenetic development, one should search for relationships between the course of ontogeny and the developmental stage reached in a particular moment of life. Biological maturity at birth, which results from advancement in prenatal maturation, has a considerable influence on the ability to live under extra-uterine conditions. The optimal course of postnatal development is a characteristic of children born at term, healthy, and properly nourished. Preterm births and delays in intra-uterine development significantly decrease the ability to fully use the developmental potential in later ontogenetic stages. There is a high probability of ´ ´ and Stoinska, 2009). delayed postnatal development – both physical and psychomotor (Kosinska Preterm children and children with low birth weight may exhibit delayed or accelerated development dynamics that enable the compensation of development when factors adversely affecting the process are no longer in place. Remote prognoses as to the development of preterm children and children with low birth weight are uncertain and depend on many factors. There are many reports on the influence of low birth weight and preterm deliveries on the further course of ontogenetic processes during infancy and early childhood (among others Albertsson-Wiklan and ´ Karlberg, 1997; Hediger et al., 1998; Kosinska et al., 2004). Although studies on the influence of the biological maturity at birth on the course of the later ontogenetic processes are numerous, they do not provide unambiguous results (Paz et al., 1993; Romundstad et al., 2003; Vohr et al., 1979). Taking into account the above premises, it should be considered whether remote stages of ontogeny are related to each other, and whether perinatal outcome – an indicator of foetal development – may condition the course of further processes and thereby have an effect on the remote stages of postnatal development. The main aim of the present study was to assess the influence of biological maturity at birth on the growth processes in subsequent years and during puberty in girls.
294
A. Szwed, M. Kosi´ nska / HOMO - Journal of Comparative Human Biology 63 (2012) 292–300
Materials and methods The material comes from the outpatient clinic cards of “Vitamed” general outpatient clinic in the city of Poznan´ and cross-sectional research on girls from the province of Wielkopolska in Poland. The material includes 527 girls born in the years 1985–1995. Thus, at the time of the examination, the girls ranged in age from 10 to 21 years. Perinatal maturity outcome of the examined girls was determined on grounds of gestational age, birth weight, and mutual relationships between these variables that would allow drawing of conclusions about the disturbances during the foetal life. The evaluation of development in the subsequent years of life was based on values of body weight at the ages of 1, 3, 6, 10, and 14 years. Therefore the last measurement of body weight was taken at the age of 14 years. The age at menarche was calculated by retrospective method. Age at menarche was determined in 273 girls who had started their menstrual periods. To the study of the menarchal age, from the entire group of 527 girls, only those at the age of 17 years or older were selected. This was dictated by the fact that in the analyzed group of girls the latest age of menarche was 17. Therefore, to avoid any bias, younger girls were excluded even if they already had a first menstruation. Gestational age of the examined children was determined using Naegele’s rule. According to the recommendations of the World Health Organization (WHO), children born before the 37th week of pregnancy were classified as preterm-born, while children born after the 37th week of pregnancy were classified as born at term (WHO Technical Report Series No. 217, 1961). Body weight measurements were carried out by a qualified medical staff with the use of a medical balance with the accuracy of 10 g. The measurements included birth weight directly after delivery and weights in subsequent years during visits in physicians’ offices. Using the values of birth weight, the following groups of children were distinguished: children born with low (up to 2500 g), appropriate (2500–4000 g) and high birth weight (above 4000 g). In order to determine the relationships between gestational age and birth weight, and thereby to indicate groups of children with intrauterine growth restriction, the values of body weight noted at birth were compared to the norms developed for the Polish provinces of Wielkopolska and Lubuskie (Gadzinowski et al., 2003). On these grounds, newborn groups with too low (<10 percentile; SGA – small-for-gestational age), appropriate (10–90 percentile; AGA – appropriate-for-gestational age) and too high birth weight (>90 percentile; LGA – large-for-gestational age) in relation to gestational age were distinguished (Battaglia and Lubchenko, 1967). The influence of perinatal maturity on body weight in later stages of ontogeny was determined with the use of the Kruskal–Wallis test and the Mann–Whitney U test. In order to determine the relationship between perinatal maturity and age at menarche, the survival analysis module (the product-limit method – the Kaplan–Meier method and c2 test for three and log-rank test for two categories of the independent variable) was used. This analysis was carried out only for 273 girls with the determined age at menarche (hence, there is the lack of censored data). The calculations were performed using statistical package Statistica 9.1 (StatSoft, Inc. 2010). Results The examined girls were born between the 26th and the 42nd week of gestational age (X = 38.76, s = 2.4 weeks; Me = 39 weeks). Birth weight ranged from 1300 to 4800 g (X = 3.249, s = 528 g; Me = 3300 g). In accordance with expectations, the greatest number of births was noted among newborns born at term (76%) and with birth weight ranging from 2500 to 4000 g (77%); births with low birth weight accounted for 10%. As a result of determination of relationships between gestational age and birth weight of the examined children, newborn groups with too low (<10 percentile; SGA – small-for-gestational age), appropriate (10–90 percentile; AGA – appropriate-for-gestational age) and too high birth weight (>90 percentile; LGA – large-for-gestational age) in relation to gestational age were distinguished. The groups accounted for 8%, 83%, and 9% of the examined children, respectively. A relatively small number of preterm-born girls and girls with very low birth weight reflects the typical distribution of birth prevalence and results from the fact that the collected material included girls born in the mid-1980s. A significant decrease in the lower limit of gestational age and birth weight as
A. Szwed, M. Kosi´ nska / HOMO - Journal of Comparative Human Biology 63 (2012) 292–300
295
Table 1 Values of body weight of the examined girls in their subsequent years of life. Age (years)
N
X
SD
0 1 3 6 10 14
527 486 313 361 282 280
3.2 9.9 14.7 21.6 34.3 51.2
0.5 1.7 2.9 4.1 9.2 9.3
Table 2 Influence of perinatal maturity outcome on the values of body weight achieved in the later years of life. U-Mann–Whitney test for variables with two categories, and Kruskal–Wallis test for variables with more categories were used. Perinatal maturity outcome
Age (years)
Kruskal–Wallis/Mann–Whitney U test
p
Body weight
1 3 6 10 14
11.29 9.32 6.75 6.29 3.25
<0.01 <0.05 <0.05 <0.05 >0.05
Percentile position
1 3 6 10 14
9.18 1.89 0.77 0.68 4.25
<0.01 >0.05 >0.05 >0.05 >0.05
Gestational age
1 3 6 10 14
0.89 3.32 1.12 2.86 2.91
>0.05 <0.01 >0.05 <0.01 <0.01
Bold numbers indicate statistical significance.
indicators of newborn survival is an effect of the progress in medicine of the 1990s (Kornacka, 2006; Meadow et al., 2004; Joseph et al., 2007). The values of body weight of the examined girls in their subsequent years of life are presented in Table 1. The obtained results show a diverse influence of perinatal maturity on the values of body weight achieved in later years of life. The indicated predictive factors included both birth weight and gestational age (Table 2, Fig. 1). Until the 10th year of age girls with birth weight lower than 2500 g weighed
Fig. 1. Influence of birth weight on the values of body weight achieved in the later years of life (1–14).
296
A. Szwed, M. Kosi´ nska / HOMO - Journal of Comparative Human Biology 63 (2012) 292–300
percentage of menarche occurence
0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 10
11
12
13
14
15
16
17
age at menarche Fig. 2. Probabilities of the menarche occurrence.
less than those with birth weight above 4000 g, and a tendency was observed that the lowest values of body weight were noted in girls with the lowest birth weight and the highest body weight in girls with the highest birth weight. At the ages of 3, 10, and 14 years, preterm-born girls had lower body weight than their peers born at term. Diverse values of body weight of the examined girls, resulting from their percentile positions, were observed only in the first year of life. In the examined girls menarche occurred between the 10th and the 17th year of life (X = 12.87, s = 1.26; Me = 13 years). The survival analysis demonstrated that in 50% of the examined girls menarche occurred before the 13th year of age (Fig. 2), and in 60% of the examined girls menarche was observed at the age of 12 and 13 years. Assessment of the survival analysis function in the groups of girls distinguished on the basis of gestational age at birth enabled evaluation of the influence of length of pregnancy on age at menarche. The performed comparison showed a significant diversity in age at menarche depending on the length of pregnancy (log-rank c2 = 27.068, df 2, p < 0.0001). The latest crossing of the puberty threshold was observed in girls born before the 33rd week of gestational age (Fig. 3). In this group, age at menarche <=32 weeks
33-36 weeks
>=37 weeks
percentage of menarche occurence
0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 10
11
12
13
14
15
16
17
age at menarche Fig. 3. Probabilities of the menarche occurrence in groups of girls distinguished by the category of gestational age.
A. Szwed, M. Kosi´ nska / HOMO - Journal of Comparative Human Biology 63 (2012) 292–300 < 2500g
2500-4000g
297
>4000
percentage of menarche occurence
0. 0 0. 1 0. 2 0. 3 0. 4 0. 5 0. 6 0. 7 0. 8 0. 9 1. 0 10
11
12
13
14
15
16
17
age at menarche Fig. 4. Probabilities of the menarche occurrence in groups of girls distinguished by the category of birth weight.
was postponed by 2 years in comparison with girls born at term and amounted to 14 years. At this age a sudden decrease in the curve for the examined group was observed. Consistently, a decrease in the curve was observed in girls born between the 33rd and the 36th week of pregnancy in their 13th year of age. The obtained results demonstrated that age at menarche was statistically significantly diverse also with regard to birth weight (log-rank c2 = 23.241, df 2, p < 0.0001). Girls with birth weight below 2500 g were the last to cross the puberty threshold. Also in this group menarche at the age of 17 years was noted (Fig. 4). In the course of further research, an attempt was made to determine the influence of developmental disturbances during the prenatal period on age at menarche, expressed by relating birth weight to gestational age. The analysis showed no variation of maturation of the examined girls conditioned by the occurrence of intrauterine growth retardation (log-rank c2 = 2.046, df 2, p > 0.05). The plotted curves (Fig. 5) intersect many times. The median value for children with too low birth weight (SGA) and appropriate birth weight (AGA) fell on the 13th age of life. It is worthy of noticing that the value was observed for the girls from the group with too high birth weight (LGA) at the age of 12 years. The SGA
AGA
LGA
percentage of menarche occurence
0 0. 1 0. 2 0. 3 0. 4 0. 5 0. 6 0. 7 0. 8 0. 9 1 10
11
12
13
14
15
16
17
age at menarche Fig. 5. Probabilities of the menarche occurrence in groups of girls distinguished by the percentile position.
298
A. Szwed, M. Kosi´ nska / HOMO - Journal of Comparative Human Biology 63 (2012) 292–300
earliest age at menarche – at the age of 10, was observed in the group of girls with appropriate birth weight, while in the girls with intra-uterine growth restriction, the earliest menarche was noted as late as at the age of 12 years. Discussion The theoretical basis of research on ontogenetic development is the occurrence of interactions between the genetic material of an individual and the modifying effect of environmental factors. Ontogenetic processes take place in the time determined by an individual’s life span – from the moment of fertilization until death. Thus the analysis of effect of individual developmental factors on the course of ontogeny thereby assesses their influence on particular populations at stated times. While assuming the continuity of ontogenetic development, also a combined effect of the genetic material of an individual and the modifying influence of environmental factors during the preceding stages should ´ ´ 2006; Kosinska and Szwed, 2008). be considered (Kosinska, Perinatal outcome, which results from advancement in prenatal maturation, has a considerable influence on the ability to live under extra-uterine conditions. Preterm delivery and giving birth to a newborn with low birth weight are related to numerous medical problems both during infancy and in the subsequent life stages (Hamuda et al., 2006; Romundstad et al., 2003). Studies to date show contradictory results as to the phenomena of development compensation and the course of particular ontogenetic stages (among others Hediger et al., 1998; Ounsted et al., 1984; Wollmann, 2004). The obtained results have revealed a composite influence of perinatal maturity on the values of body weight achieved in the later years of life, and these results were subject to the type of variable determining perinatal outcome. The reasons for the variation undoubtedly lie in the diverse etiology of births of newborns with low birth weight and in the complexity of conditions during the ontogenetic development. In the case of the examined group, a distinct negative influence of births with birth weight below 2500 g on further development was observed, and in this case low birth weight seemed to have resulted from preterm deliveries, which confirmed lack of influence of percentile position. Other observation was a noticeable tendency for having higher body weight in the subsequent years of life together with an increase in birth weight, length of pregnancy and percentile position. The influence of perinatal outcome on the processes of children’s growth, including, among others, the phenomenon of development compensation, has been emphasized also in studies by other authors ´ 2006; Paz et al., 1993; Strauss, 1997). A study by Kozieł and (among them Casey et al., 1990; Kosinska, Jankowska (2002a) has showed that foetal growth restriction has a long-term adverse effect on the physical development in the later stages of postnatal development. Girls born with low birth weight did not catch up with their peers during the maturation period. Our results seem to confirm results in previous reports that birth weight is a predictor of further development and its influence is noticeable not only in the first years of life but also during the rest of child’s growth until the sexual maturation. Hence it is essential to conduct further research on the influence of intra-uterine development on the remote periods of postnatal ontogeny. The presented study attempted to determine the influence of perinatal outcome on girls’ puberty. The average age at menarche in our studies, similarly as in studies by some other authors (Kozieł and Jankowska, 2002b; Tam et al., 2006; Romundstad et al., 2003; Whincup et al., 2001), was determined to occur between the 12th and the 13th year of age. Menarche was commonly considered as subject to body weight and BMI values (Biro et al., 2006; Blum et al., 1997; Sloboda et al., 2007). Greater body sizes (greater body weight, height, and BMI) during childhood were related to menarche occurring at an earlier age (Blell et al., 2008; Frisch and Revelle, 1971; St George et al., 1994). Frisch and Revelle (1971) were the first to propose a hypothesis that menarche is related to achieving an essential critical body weight. Relation of the above statements to the results obtained in the analysis of the influence of birth weight on the values of girls’ body weight in the subsequent years of life was expected to prove a relationship between the variable and age at menarche. The obtained results showed a significant relationship between birth weight and age at menarche. Also accelerated maturation in the group of girls with birth weight ranging from 2500 to 4000 g was clearly noticeable. In girls with birth weight below 2500 g and preterm-born (before the 37th week of pregnancy), menarche occurred later in comparison with the girls born at term and with birth weight over 2500 g. Assessment of the survival
A. Szwed, M. Kosi´ nska / HOMO - Journal of Comparative Human Biology 63 (2012) 292–300
299
analysis function in the groups of girls distinguished on the basis of percentile position of birth weight indicated lack of influence of intra-uterine growth restriction on age at menarche. However, similarly as in the case of birth weight, some tendencies were noticeable: earlier maturation was observed in the group of girls born at term and in the group of girls with birth weight too low for gestational age, which were confirmed also by other authors. Fledelius (1982) have suggested that in preterm-born girls and in girls with low birth weight (<2000 g), menarche occurs about 3–6 months later than in girls born at term. Similarly, Berankova (1997) have demonstrated that menarche was delayed by 3–6 months in girls with birth weight lower than 2500 g. Also Terry et al. (2009) related low birth weight (<2500 g) to a higher probability of menarche at about 7.2 months later than in children with birth weight amounting to or greater than 2500 g. It should be emphasized that there is a group of researchers that question low birth weight as a predictor of later menarche and postulate that development compensation is related to menarche at an earlier age. Persson et al. (1999) have stated that girls born with too low birth weight in relation to gestational age mature earlier. Similar results were obtained by Bhargava et al. (1995), who found that girls with birth weight lower than 2500 g had menarche 12 months earlier than girls with appropriate weight at birth. On the other hand, Cooper et al. (1996) and Kozieł and Jankowska (2002b) demonstrated that girls with greater birth weight and girls with birth weight appropriate for gestational age had menarche later when compared to girls with low birth weight. Taking into account the reports (Strauss, 1997; Cooper et al., 1996) which suggest that programming of neuro-endocrine axes occurs during prenatal development and may be modified by intra-uterine growth restriction and then by increasing body weight in childhood, birth weight may have influence on remote developmental stages, such as the course of maturation and age at menarche. As it is stated by Cooper et al. (1996, p. 816), “The effect of birth weight on age at menarche might be mediated through modulation of this pattern of gonadotropin secretion. Hormonal or nutritional influences on growth during critical periods of intra-uterine life (which are reflected in a lower birth weight) may alter the later secretory pattern of GnRH either through a direct effect on the hypothalamus or by changing end-organ responsiveness to GnRH and gonadotropins.” It should also be remembered that postnatal development is affected by genetic and environmental factors, which may also have influence on the diversity of postnatal development and age at menarche.
Conclusions Remote prognoses as to the postnatal development of preterm-born children and/or with low birth weight indicate adverse influence of these variables on age at menarche. Perinatal outcome, which reflects intrauterine development and biological maturity of a newborn, conditions the course of postnatal development. The occurrence and course of subsequent stages of ontogenetic development results from genetic determination and influence of environmental factors which operate in a given particular moment, and is a combined effect of the genetic material of an individual and the modifying influence of environmental factors during the preceding stages.
References Albertsson-Wiklan, K., Karlberg, J., 1997. Postnatal growth of children born small for gestational age. Acta Paediatr. Suppl. 423, 193–195. Battaglia, F.C., Lubchenko, L.O., 1967. A practical classification of newborn infants by weight and gestational age. J. Pediatr. 71, 159–163. Berankova, H., 1997. Maturation and fertility in women with low birth weights. Cas. Lek. Cesk. 136, 413–415. Bhargava, S.K., Ramji, S., Srivastava, U., Sachdev, H.P., Kapani, V., Datta, V., Satyanarayana, L., 1995. Growth and sexual maturation of low birth weight children: a 14 year follow up. Indian Pediatr. 32, 963–970. Biro, F.M., Khoury, P., Morrison, J.A., Anderson, R., Biro, F., von Eyben, F.E., Skakkebaek, N.E., 2006. Influence of obesity on timing of puberty. Int. J. Androl. 29, 272–277. Blell, M., Pollard, T.M., Pearce, M.S., 2008. Predictors of age at menarche in the Newcastle thousand families study. J. Biosoc. Sci. 40, 563–575. ˝ J., Shakkebaek, N.E., Heiman, M.L., Birkett, M., Attanasio, A.M., Blum, W.F., Englaro, P., Hantish, S., Juul, A., Hertel, N.T., Muller, Kiess, W., Rascher, W., 1997. Plasma leptin levels in healthy children and adolescents: dependence on body mass index, body fat mass, gender, pubertal stage, and testosterone. J. Clin. Endocrinol. Metab. 82, 2904–2910.
300
A. Szwed, M. Kosi´ nska / HOMO - Journal of Comparative Human Biology 63 (2012) 292–300
Casey, P.K., Kraemer, H.C., Bernbaum, J., Tyson, J.E., Sells, J.C., Yogman, M.W., Bauer, C.K., 1990. Growth patterns of low birth weight preterm infants: a longitudinal analysis of a large, varied sample. J. Pediatr. 117, 298–307. Cooper, C., Kuh, D., Egger, P., Wadsworth, M., Baker, D., 1996. Childhood growth and age at menarche. Br. J. Obst. Gynaecol. 103, 814–817. Fledelius, H.C., 1982. Inhibited growth and development as permanent features of low birth weight. A longitudinal study of eye size, height, head circumference, interpupillary distance and exophthalmometry, as measured age of 10 and 18 years. Acta Paediatr. Scand. 71, 645–650. Frisch, R.E., Revelle, R., 1971. Height and weight at menarche and a hypothesis of menarche. Arch. Dis. Child. 46, 695–701. ´ ´ M., Mazela, J., Stoinska, B., 2003. Urodzeniowa masa ciała a wiek Gadzinowski, J., Kaliszewska-Drozdowska, M.D., Kosinska, płodowy noworodków regionu Wielkopolski i Ziemi Lubuskiej. Gin. Pol. 74, 186–192. ´ K., 2006. Noworodek z bardzo mała˛ urodzeniowa˛ masa˛ ciała – aktualny problem Hamuda, M., Kowalczykiewicz-Kuta, Wozniak, ˛ z województwa opolskiego. Nowa Pediatr. 1, 22–24. perinatologii. Doniesienia wstepne Hediger, M.L., Overpeck, M.D., Maurer, K.R., Kuczmarski, R.J., McGlynn, A., Davis, W.W., 1998. Growth of infants and young infants born small or large for gestational age. Arch. Pediatr. Adolesc. Med. 152, 1225–1231. Joseph, K.S., Liston, R.M., Dodds, L., Dahlgren, L., Allen, A.C., 2007. Socioeconomic status and perinatal outcomes in a setting with universal access to essential health care services. Can. Med. Assoc. J. 6, 585–590. ´ Studia Filoz. Humanist. 7, 157–193. Kaczmarek, M., Łastowski, K., 2004. Ewolucja a Epigeneza. Poznanskie ´ M., Kosicki, J.Z., 2007. Human breeding ecology – the classification and regression trees (CART) answer to the question Kosinska, how the maternal environment participates in newborn outcome. In: Application of Mathematics to Biology and Medicine. Jagiellonian University, Kraków, pp. 66-71. ´ ´ M., Stoinska, B., Gadzinowski, J., 2004. Are the gestational age and the birth body weight modificators of the develKosinska, opmental dynamic? Arch. Perinat. Med. 10, 49–52. ´ M., 2006. Two methods for estimating age of newborns in catch-up growth studies. Early Hum. Dev. 82, 575–582. Kosinska, ´ ´ M., Stoinska, B., 2009. Ocena rozwoju fizycznego i psychoruchowego dzieci urodzonych przedwcze´snie oraz dzieci Kosinska, ˛ ˛ Wydawnictwo Antropologia˛ a Medycyna. urodzonych z mała˛ masa˛ ciała. In: Kaczmarek, M., Szwed, A. (Eds.), Miedzy ´ pp. 155–169. Naukowe UAM, Poznan, ´ M., Szwed, A., 2008. The effect of developmental status on birth on the age of menarche in the female residents of the Kosinska, province of Wielkopolska. Pol. J. Environ. Stud. 17, 220–223. Kornacka, M.K., 2006. Noworodki płodowe. Klin. Pediatr. 14, 5095–5096. Kozieł, S., Jankowska, E.A., 2002a. Birthweight and stature, body mass index and fat distribution of 14-year-old Polish adolescents. J. Paediatr. Child Health 38, 55–58. Kozieł, S., Jankowska, E.A., 2002b. Effect of low versus normal birthweight on menarche in 14-year-old Polish girls. J. Paediatr. Child Health 38, 268–271. Meadow, W., Lee, G., Lin, K., Lantos, J., 2004. Changes in mortality for extremely low birth weight infants in the 1990s: implication for treatment decisions and resources use. Pediatrics 113, 1223–1229. Ounsted, M., Moar, V., Scott, A., 1984. Infants of deviant birth weight at the age of seven years: health, handicap, size and developmental status. Early Hum. Dev. 9, 323–340. Paz, I., Seidman, D.S., Danon, Y.L., Laor, A., Stevenson, D.K., Gale, R., 1993. Are children born small for gestational age at increased risk of short stature? Am. J. Dis. Child. 147, 337–339. Persson, I., Ahlsson, F., Ewald, U., Tuvemo, T., Qingyuan, M., von Rosen, D., Proos, L., 1999. Influence of perinatal factors on the onset of puberty in boys and girls: implications for interpretation of link with risk of long term diseases. Am. J. Epidemiol. 150, 747–755. Romundstad, P.R., Vatten, L.J., Nilsen, T.I.L., Holmen, T.L., Hsieh, C.-C., Trichpoulos, D., Stuver, S.O., 2003. Birth size in relation to age at menarche and adolescent body size: implications for breast cancer risk. Int. J. Cancer 105, 400–403. Sloboda, D.M., Hart, R., Doherty, D.A., Pennell, C.E., Hickey, M., 2007. Age at menarche: influences of prenatal and postnatal growth. J. Clin. Endocrinol. Metab. 92, 46–50. StatSoft, Inc., 2010. STATISTICA (Data Analysis Software System), Version 9.1., http://www.statsoft.com. St George, I.M., Williams, S., Silva, P.A., 1994. Body size and the menarche: the Dunedin Study. J. Adolesc. Health 15, 573–576. Strauss, R.S., 1997. Effects of the intrauterine environment on childhood growth. Br. Med. Bull. 53, 81–95. Tam, C.S., de Zegher, F., Garnett, S.P., Baur, L.A., Cowell, C.T., 2006. Opposing influences of prenatal and postnatal growth on the timing of menarche. J. Clin. Endocrinol. Metab. 91, 4369–4373. Terry, M.B., Ferris, J.S., Tehranifar, P., Wei, Y., Flom, J.D., 2009. Birth weight, postnatal growth, and age at menarche. Am. J. Epidemiol. 170, 72–79. Vohr, B.R., Oh, W., Rosenfield, A.G., Cowett, R.H., Berstein, J., 1979. The preterm small-for-gestational age infant: a two year follow-up study. Am. J. Obstet. Gynecol. 133, 425–431. Whincup, P.H., Gilg, J.A., Odoki, K., Taylor, S.J.C., Cook, D.G., 2001. Age at menarche in contemporary British teenagers: survey of girls born between 1982 and 1986. Br. Med. J. 322, 1095–1096. World Health Organization Expert Committee on Maternal and Child Health: Public Health Aspects of Low Birth Weight. Third Report of the Expert Committee on Maternal and Child Health, 1961. WHO Technical Report Series No. 217. Geneva. Wollmann, H.A., 2004. Small for gestational age (SGA): growth and long-term effects, German. Monatsschr. Kinderheilkd. 152, 528–535.
Contents lists available at SciVerse ScienceDirect
HOMO - Journal of Comparative Human Biology journal homepage: www.elsevier.de/jchb
Biological maturity at birth, the course of the subsequent ontogenetic stages and age at menarche ´ A. Szwed ∗, M. Kosinska Department of Human Biological Development, Institute of Anthropology, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznan, Poland
a r t i c l e
i n f o
Article history: Received 22 March 2011 Accepted 30 January 2012
a b s t r a c t The main aim of the study was to assess the influence of biological maturity at birth on growth processes in the subsequent years and during puberty in girls. The material of this study comes from the outpatient clinic cards and cross-sectional research on girls from the province of Wielkopolska in Poland. It includes data of 527 girls. The influence of perinatal maturity on body weight in the later stages of ontogeny was determined with the use of the Kruskal–Wallis test and the Mann–Whitney U test. In order to determine the relationship between perinatal maturity and age at menarche, the survival analysis module was used. The results show a diverse influence of perinatal maturity on the values of body weight achieved in later years of life. The indicated predictive factors included both birth weight and gestational age. In the examined girls menarche occurred between the 10th year and the 17th year of life (X¯ = 12.87, s = 1.26; Me = 13 years). The comparison showed a significant variation in age at menarche depending on the length of pregnancy (log-rank 22 = 27.068, p < 0.0001) and birth weight (log-rank 22 = 23.241, p < 0.0001). There was no variation in maturation of the examined girls conditioned by the occurrence of intra-uterine growth retardation (log-rank 22 = 2.046, p > 0.05). Remote prognoses as to the postnatal development of preterm-born children and/or children with low birth weight indicate adverse influence of these variables on age at menarche. Perinatal biological maturity of a newborn conditions the course of postnatal development. © 2012 Elsevier GmbH. All rights reserved.
∗ Corresponding author. Tel.: +48 61 829 57 13; fax: +48 61 829 57 30. E-mail address: [email protected] (A. Szwed). 0018-442X/$ – see front matter © 2012 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.jchb.2012.01.003
A. Szwed, M. Kosi´ nska / HOMO - Journal of Comparative Human Biology 63 (2012) 292–300
293
Introduction A description of biological reality and complex ecological systems is one of the most important challenges of modern science. An interesting example of an ecological system is the model of mutual interactions in the ´ and Kosicki, 2007). The basic paradigm of examgenotype–environment–individual system (Kosinska ination of developmental phenomena is the statement that an individual during development in its ontogeny goes through the subsequent stages that are genetically determined. The quality of these stages (level of individual development) depends on interaction between the individual’s genotype and environmental conditions. It should be emphasized that the quality of the subsequent developmental stages is a combined effect of the genetic material and the modifying influence of environmental fac´ and Szwed, 2008; tors in a particular moment of ontogeny and preceding stages of growth (Kosinska ´ Kosinska, 2006). Crossing the selection thresholds: birth, puberty, and reproduction are considered key moments of human development. Reaching the subsequent ontogenetic stages is possible only after crossing the preceding selection threshold, therefore crossing each threshold is an indispensable element of further development. The birth selection threshold is the moment of transition from the prenatal to postnatal stage, understood as the birth of a morphologically and physiologically mature newborn that is capable of independent performance of basic life functions. Entering the puberty stage and achieving the possibility of crossing another post-puberty selection threshold is subject to the normal course of the growth processes and lack of factors impeding the development both in the preceding stages and in the very puberty stage. Crossing this threshold is understood as obtaining the ability to produce gametes, and thus reaching biological maturity that conditions ability to reproduce. A consequence of reaching the threshold is the opportunity to reach the next life stages. However, it should be emphasized that crossing the subsequent ontogenetic stages, and thus the subsequent selection thresholds, does not guarantee completion of the following developmental stages (Kaczmarek and Łastowski, 2004). While assuming continuity of ontogenetic development, one should search for relationships between the course of ontogeny and the developmental stage reached in a particular moment of life. Biological maturity at birth, which results from advancement in prenatal maturation, has a considerable influence on the ability to live under extra-uterine conditions. The optimal course of postnatal development is a characteristic of children born at term, healthy, and properly nourished. Preterm births and delays in intra-uterine development significantly decrease the ability to fully use the developmental potential in later ontogenetic stages. There is a high probability of ´ ´ and Stoinska, 2009). delayed postnatal development – both physical and psychomotor (Kosinska Preterm children and children with low birth weight may exhibit delayed or accelerated development dynamics that enable the compensation of development when factors adversely affecting the process are no longer in place. Remote prognoses as to the development of preterm children and children with low birth weight are uncertain and depend on many factors. There are many reports on the influence of low birth weight and preterm deliveries on the further course of ontogenetic processes during infancy and early childhood (among others Albertsson-Wiklan and ´ Karlberg, 1997; Hediger et al., 1998; Kosinska et al., 2004). Although studies on the influence of the biological maturity at birth on the course of the later ontogenetic processes are numerous, they do not provide unambiguous results (Paz et al., 1993; Romundstad et al., 2003; Vohr et al., 1979). Taking into account the above premises, it should be considered whether remote stages of ontogeny are related to each other, and whether perinatal outcome – an indicator of foetal development – may condition the course of further processes and thereby have an effect on the remote stages of postnatal development. The main aim of the present study was to assess the influence of biological maturity at birth on the growth processes in subsequent years and during puberty in girls.
294
A. Szwed, M. Kosi´ nska / HOMO - Journal of Comparative Human Biology 63 (2012) 292–300
Materials and methods The material comes from the outpatient clinic cards of “Vitamed” general outpatient clinic in the city of Poznan´ and cross-sectional research on girls from the province of Wielkopolska in Poland. The material includes 527 girls born in the years 1985–1995. Thus, at the time of the examination, the girls ranged in age from 10 to 21 years. Perinatal maturity outcome of the examined girls was determined on grounds of gestational age, birth weight, and mutual relationships between these variables that would allow drawing of conclusions about the disturbances during the foetal life. The evaluation of development in the subsequent years of life was based on values of body weight at the ages of 1, 3, 6, 10, and 14 years. Therefore the last measurement of body weight was taken at the age of 14 years. The age at menarche was calculated by retrospective method. Age at menarche was determined in 273 girls who had started their menstrual periods. To the study of the menarchal age, from the entire group of 527 girls, only those at the age of 17 years or older were selected. This was dictated by the fact that in the analyzed group of girls the latest age of menarche was 17. Therefore, to avoid any bias, younger girls were excluded even if they already had a first menstruation. Gestational age of the examined children was determined using Naegele’s rule. According to the recommendations of the World Health Organization (WHO), children born before the 37th week of pregnancy were classified as preterm-born, while children born after the 37th week of pregnancy were classified as born at term (WHO Technical Report Series No. 217, 1961). Body weight measurements were carried out by a qualified medical staff with the use of a medical balance with the accuracy of 10 g. The measurements included birth weight directly after delivery and weights in subsequent years during visits in physicians’ offices. Using the values of birth weight, the following groups of children were distinguished: children born with low (up to 2500 g), appropriate (2500–4000 g) and high birth weight (above 4000 g). In order to determine the relationships between gestational age and birth weight, and thereby to indicate groups of children with intrauterine growth restriction, the values of body weight noted at birth were compared to the norms developed for the Polish provinces of Wielkopolska and Lubuskie (Gadzinowski et al., 2003). On these grounds, newborn groups with too low (<10 percentile; SGA – small-for-gestational age), appropriate (10–90 percentile; AGA – appropriate-for-gestational age) and too high birth weight (>90 percentile; LGA – large-for-gestational age) in relation to gestational age were distinguished (Battaglia and Lubchenko, 1967). The influence of perinatal maturity on body weight in later stages of ontogeny was determined with the use of the Kruskal–Wallis test and the Mann–Whitney U test. In order to determine the relationship between perinatal maturity and age at menarche, the survival analysis module (the product-limit method – the Kaplan–Meier method and c2 test for three and log-rank test for two categories of the independent variable) was used. This analysis was carried out only for 273 girls with the determined age at menarche (hence, there is the lack of censored data). The calculations were performed using statistical package Statistica 9.1 (StatSoft, Inc. 2010). Results The examined girls were born between the 26th and the 42nd week of gestational age (X = 38.76, s = 2.4 weeks; Me = 39 weeks). Birth weight ranged from 1300 to 4800 g (X = 3.249, s = 528 g; Me = 3300 g). In accordance with expectations, the greatest number of births was noted among newborns born at term (76%) and with birth weight ranging from 2500 to 4000 g (77%); births with low birth weight accounted for 10%. As a result of determination of relationships between gestational age and birth weight of the examined children, newborn groups with too low (<10 percentile; SGA – small-for-gestational age), appropriate (10–90 percentile; AGA – appropriate-for-gestational age) and too high birth weight (>90 percentile; LGA – large-for-gestational age) in relation to gestational age were distinguished. The groups accounted for 8%, 83%, and 9% of the examined children, respectively. A relatively small number of preterm-born girls and girls with very low birth weight reflects the typical distribution of birth prevalence and results from the fact that the collected material included girls born in the mid-1980s. A significant decrease in the lower limit of gestational age and birth weight as
A. Szwed, M. Kosi´ nska / HOMO - Journal of Comparative Human Biology 63 (2012) 292–300
295
Table 1 Values of body weight of the examined girls in their subsequent years of life. Age (years)
N
X
SD
0 1 3 6 10 14
527 486 313 361 282 280
3.2 9.9 14.7 21.6 34.3 51.2
0.5 1.7 2.9 4.1 9.2 9.3
Table 2 Influence of perinatal maturity outcome on the values of body weight achieved in the later years of life. U-Mann–Whitney test for variables with two categories, and Kruskal–Wallis test for variables with more categories were used. Perinatal maturity outcome
Age (years)
Kruskal–Wallis/Mann–Whitney U test
p
Body weight
1 3 6 10 14
11.29 9.32 6.75 6.29 3.25
<0.01 <0.05 <0.05 <0.05 >0.05
Percentile position
1 3 6 10 14
9.18 1.89 0.77 0.68 4.25
<0.01 >0.05 >0.05 >0.05 >0.05
Gestational age
1 3 6 10 14
0.89 3.32 1.12 2.86 2.91
>0.05 <0.01 >0.05 <0.01 <0.01
Bold numbers indicate statistical significance.
indicators of newborn survival is an effect of the progress in medicine of the 1990s (Kornacka, 2006; Meadow et al., 2004; Joseph et al., 2007). The values of body weight of the examined girls in their subsequent years of life are presented in Table 1. The obtained results show a diverse influence of perinatal maturity on the values of body weight achieved in later years of life. The indicated predictive factors included both birth weight and gestational age (Table 2, Fig. 1). Until the 10th year of age girls with birth weight lower than 2500 g weighed
Fig. 1. Influence of birth weight on the values of body weight achieved in the later years of life (1–14).
296
A. Szwed, M. Kosi´ nska / HOMO - Journal of Comparative Human Biology 63 (2012) 292–300
percentage of menarche occurence
0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 10
11
12
13
14
15
16
17
age at menarche Fig. 2. Probabilities of the menarche occurrence.
less than those with birth weight above 4000 g, and a tendency was observed that the lowest values of body weight were noted in girls with the lowest birth weight and the highest body weight in girls with the highest birth weight. At the ages of 3, 10, and 14 years, preterm-born girls had lower body weight than their peers born at term. Diverse values of body weight of the examined girls, resulting from their percentile positions, were observed only in the first year of life. In the examined girls menarche occurred between the 10th and the 17th year of life (X = 12.87, s = 1.26; Me = 13 years). The survival analysis demonstrated that in 50% of the examined girls menarche occurred before the 13th year of age (Fig. 2), and in 60% of the examined girls menarche was observed at the age of 12 and 13 years. Assessment of the survival analysis function in the groups of girls distinguished on the basis of gestational age at birth enabled evaluation of the influence of length of pregnancy on age at menarche. The performed comparison showed a significant diversity in age at menarche depending on the length of pregnancy (log-rank c2 = 27.068, df 2, p < 0.0001). The latest crossing of the puberty threshold was observed in girls born before the 33rd week of gestational age (Fig. 3). In this group, age at menarche <=32 weeks
33-36 weeks
>=37 weeks
percentage of menarche occurence
0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 10
11
12
13
14
15
16
17
age at menarche Fig. 3. Probabilities of the menarche occurrence in groups of girls distinguished by the category of gestational age.
A. Szwed, M. Kosi´ nska / HOMO - Journal of Comparative Human Biology 63 (2012) 292–300 < 2500g
2500-4000g
297
>4000
percentage of menarche occurence
0. 0 0. 1 0. 2 0. 3 0. 4 0. 5 0. 6 0. 7 0. 8 0. 9 1. 0 10
11
12
13
14
15
16
17
age at menarche Fig. 4. Probabilities of the menarche occurrence in groups of girls distinguished by the category of birth weight.
was postponed by 2 years in comparison with girls born at term and amounted to 14 years. At this age a sudden decrease in the curve for the examined group was observed. Consistently, a decrease in the curve was observed in girls born between the 33rd and the 36th week of pregnancy in their 13th year of age. The obtained results demonstrated that age at menarche was statistically significantly diverse also with regard to birth weight (log-rank c2 = 23.241, df 2, p < 0.0001). Girls with birth weight below 2500 g were the last to cross the puberty threshold. Also in this group menarche at the age of 17 years was noted (Fig. 4). In the course of further research, an attempt was made to determine the influence of developmental disturbances during the prenatal period on age at menarche, expressed by relating birth weight to gestational age. The analysis showed no variation of maturation of the examined girls conditioned by the occurrence of intrauterine growth retardation (log-rank c2 = 2.046, df 2, p > 0.05). The plotted curves (Fig. 5) intersect many times. The median value for children with too low birth weight (SGA) and appropriate birth weight (AGA) fell on the 13th age of life. It is worthy of noticing that the value was observed for the girls from the group with too high birth weight (LGA) at the age of 12 years. The SGA
AGA
LGA
percentage of menarche occurence
0 0. 1 0. 2 0. 3 0. 4 0. 5 0. 6 0. 7 0. 8 0. 9 1 10
11
12
13
14
15
16
17
age at menarche Fig. 5. Probabilities of the menarche occurrence in groups of girls distinguished by the percentile position.
298
A. Szwed, M. Kosi´ nska / HOMO - Journal of Comparative Human Biology 63 (2012) 292–300
earliest age at menarche – at the age of 10, was observed in the group of girls with appropriate birth weight, while in the girls with intra-uterine growth restriction, the earliest menarche was noted as late as at the age of 12 years. Discussion The theoretical basis of research on ontogenetic development is the occurrence of interactions between the genetic material of an individual and the modifying effect of environmental factors. Ontogenetic processes take place in the time determined by an individual’s life span – from the moment of fertilization until death. Thus the analysis of effect of individual developmental factors on the course of ontogeny thereby assesses their influence on particular populations at stated times. While assuming the continuity of ontogenetic development, also a combined effect of the genetic material of an individual and the modifying influence of environmental factors during the preceding stages should ´ ´ 2006; Kosinska and Szwed, 2008). be considered (Kosinska, Perinatal outcome, which results from advancement in prenatal maturation, has a considerable influence on the ability to live under extra-uterine conditions. Preterm delivery and giving birth to a newborn with low birth weight are related to numerous medical problems both during infancy and in the subsequent life stages (Hamuda et al., 2006; Romundstad et al., 2003). Studies to date show contradictory results as to the phenomena of development compensation and the course of particular ontogenetic stages (among others Hediger et al., 1998; Ounsted et al., 1984; Wollmann, 2004). The obtained results have revealed a composite influence of perinatal maturity on the values of body weight achieved in the later years of life, and these results were subject to the type of variable determining perinatal outcome. The reasons for the variation undoubtedly lie in the diverse etiology of births of newborns with low birth weight and in the complexity of conditions during the ontogenetic development. In the case of the examined group, a distinct negative influence of births with birth weight below 2500 g on further development was observed, and in this case low birth weight seemed to have resulted from preterm deliveries, which confirmed lack of influence of percentile position. Other observation was a noticeable tendency for having higher body weight in the subsequent years of life together with an increase in birth weight, length of pregnancy and percentile position. The influence of perinatal outcome on the processes of children’s growth, including, among others, the phenomenon of development compensation, has been emphasized also in studies by other authors ´ 2006; Paz et al., 1993; Strauss, 1997). A study by Kozieł and (among them Casey et al., 1990; Kosinska, Jankowska (2002a) has showed that foetal growth restriction has a long-term adverse effect on the physical development in the later stages of postnatal development. Girls born with low birth weight did not catch up with their peers during the maturation period. Our results seem to confirm results in previous reports that birth weight is a predictor of further development and its influence is noticeable not only in the first years of life but also during the rest of child’s growth until the sexual maturation. Hence it is essential to conduct further research on the influence of intra-uterine development on the remote periods of postnatal ontogeny. The presented study attempted to determine the influence of perinatal outcome on girls’ puberty. The average age at menarche in our studies, similarly as in studies by some other authors (Kozieł and Jankowska, 2002b; Tam et al., 2006; Romundstad et al., 2003; Whincup et al., 2001), was determined to occur between the 12th and the 13th year of age. Menarche was commonly considered as subject to body weight and BMI values (Biro et al., 2006; Blum et al., 1997; Sloboda et al., 2007). Greater body sizes (greater body weight, height, and BMI) during childhood were related to menarche occurring at an earlier age (Blell et al., 2008; Frisch and Revelle, 1971; St George et al., 1994). Frisch and Revelle (1971) were the first to propose a hypothesis that menarche is related to achieving an essential critical body weight. Relation of the above statements to the results obtained in the analysis of the influence of birth weight on the values of girls’ body weight in the subsequent years of life was expected to prove a relationship between the variable and age at menarche. The obtained results showed a significant relationship between birth weight and age at menarche. Also accelerated maturation in the group of girls with birth weight ranging from 2500 to 4000 g was clearly noticeable. In girls with birth weight below 2500 g and preterm-born (before the 37th week of pregnancy), menarche occurred later in comparison with the girls born at term and with birth weight over 2500 g. Assessment of the survival
A. Szwed, M. Kosi´ nska / HOMO - Journal of Comparative Human Biology 63 (2012) 292–300
299
analysis function in the groups of girls distinguished on the basis of percentile position of birth weight indicated lack of influence of intra-uterine growth restriction on age at menarche. However, similarly as in the case of birth weight, some tendencies were noticeable: earlier maturation was observed in the group of girls born at term and in the group of girls with birth weight too low for gestational age, which were confirmed also by other authors. Fledelius (1982) have suggested that in preterm-born girls and in girls with low birth weight (<2000 g), menarche occurs about 3–6 months later than in girls born at term. Similarly, Berankova (1997) have demonstrated that menarche was delayed by 3–6 months in girls with birth weight lower than 2500 g. Also Terry et al. (2009) related low birth weight (<2500 g) to a higher probability of menarche at about 7.2 months later than in children with birth weight amounting to or greater than 2500 g. It should be emphasized that there is a group of researchers that question low birth weight as a predictor of later menarche and postulate that development compensation is related to menarche at an earlier age. Persson et al. (1999) have stated that girls born with too low birth weight in relation to gestational age mature earlier. Similar results were obtained by Bhargava et al. (1995), who found that girls with birth weight lower than 2500 g had menarche 12 months earlier than girls with appropriate weight at birth. On the other hand, Cooper et al. (1996) and Kozieł and Jankowska (2002b) demonstrated that girls with greater birth weight and girls with birth weight appropriate for gestational age had menarche later when compared to girls with low birth weight. Taking into account the reports (Strauss, 1997; Cooper et al., 1996) which suggest that programming of neuro-endocrine axes occurs during prenatal development and may be modified by intra-uterine growth restriction and then by increasing body weight in childhood, birth weight may have influence on remote developmental stages, such as the course of maturation and age at menarche. As it is stated by Cooper et al. (1996, p. 816), “The effect of birth weight on age at menarche might be mediated through modulation of this pattern of gonadotropin secretion. Hormonal or nutritional influences on growth during critical periods of intra-uterine life (which are reflected in a lower birth weight) may alter the later secretory pattern of GnRH either through a direct effect on the hypothalamus or by changing end-organ responsiveness to GnRH and gonadotropins.” It should also be remembered that postnatal development is affected by genetic and environmental factors, which may also have influence on the diversity of postnatal development and age at menarche.
Conclusions Remote prognoses as to the postnatal development of preterm-born children and/or with low birth weight indicate adverse influence of these variables on age at menarche. Perinatal outcome, which reflects intrauterine development and biological maturity of a newborn, conditions the course of postnatal development. The occurrence and course of subsequent stages of ontogenetic development results from genetic determination and influence of environmental factors which operate in a given particular moment, and is a combined effect of the genetic material of an individual and the modifying influence of environmental factors during the preceding stages.
References Albertsson-Wiklan, K., Karlberg, J., 1997. Postnatal growth of children born small for gestational age. Acta Paediatr. Suppl. 423, 193–195. Battaglia, F.C., Lubchenko, L.O., 1967. A practical classification of newborn infants by weight and gestational age. J. Pediatr. 71, 159–163. Berankova, H., 1997. Maturation and fertility in women with low birth weights. Cas. Lek. Cesk. 136, 413–415. Bhargava, S.K., Ramji, S., Srivastava, U., Sachdev, H.P., Kapani, V., Datta, V., Satyanarayana, L., 1995. Growth and sexual maturation of low birth weight children: a 14 year follow up. Indian Pediatr. 32, 963–970. Biro, F.M., Khoury, P., Morrison, J.A., Anderson, R., Biro, F., von Eyben, F.E., Skakkebaek, N.E., 2006. Influence of obesity on timing of puberty. Int. J. Androl. 29, 272–277. Blell, M., Pollard, T.M., Pearce, M.S., 2008. Predictors of age at menarche in the Newcastle thousand families study. J. Biosoc. Sci. 40, 563–575. ˝ J., Shakkebaek, N.E., Heiman, M.L., Birkett, M., Attanasio, A.M., Blum, W.F., Englaro, P., Hantish, S., Juul, A., Hertel, N.T., Muller, Kiess, W., Rascher, W., 1997. Plasma leptin levels in healthy children and adolescents: dependence on body mass index, body fat mass, gender, pubertal stage, and testosterone. J. Clin. Endocrinol. Metab. 82, 2904–2910.
300
A. Szwed, M. Kosi´ nska / HOMO - Journal of Comparative Human Biology 63 (2012) 292–300
Casey, P.K., Kraemer, H.C., Bernbaum, J., Tyson, J.E., Sells, J.C., Yogman, M.W., Bauer, C.K., 1990. Growth patterns of low birth weight preterm infants: a longitudinal analysis of a large, varied sample. J. Pediatr. 117, 298–307. Cooper, C., Kuh, D., Egger, P., Wadsworth, M., Baker, D., 1996. Childhood growth and age at menarche. Br. J. Obst. Gynaecol. 103, 814–817. Fledelius, H.C., 1982. Inhibited growth and development as permanent features of low birth weight. A longitudinal study of eye size, height, head circumference, interpupillary distance and exophthalmometry, as measured age of 10 and 18 years. Acta Paediatr. Scand. 71, 645–650. Frisch, R.E., Revelle, R., 1971. Height and weight at menarche and a hypothesis of menarche. Arch. Dis. Child. 46, 695–701. ´ ´ M., Mazela, J., Stoinska, B., 2003. Urodzeniowa masa ciała a wiek Gadzinowski, J., Kaliszewska-Drozdowska, M.D., Kosinska, płodowy noworodków regionu Wielkopolski i Ziemi Lubuskiej. Gin. Pol. 74, 186–192. ´ K., 2006. Noworodek z bardzo mała˛ urodzeniowa˛ masa˛ ciała – aktualny problem Hamuda, M., Kowalczykiewicz-Kuta, Wozniak, ˛ z województwa opolskiego. Nowa Pediatr. 1, 22–24. perinatologii. Doniesienia wstepne Hediger, M.L., Overpeck, M.D., Maurer, K.R., Kuczmarski, R.J., McGlynn, A., Davis, W.W., 1998. Growth of infants and young infants born small or large for gestational age. Arch. Pediatr. Adolesc. Med. 152, 1225–1231. Joseph, K.S., Liston, R.M., Dodds, L., Dahlgren, L., Allen, A.C., 2007. Socioeconomic status and perinatal outcomes in a setting with universal access to essential health care services. Can. Med. Assoc. J. 6, 585–590. ´ Studia Filoz. Humanist. 7, 157–193. Kaczmarek, M., Łastowski, K., 2004. Ewolucja a Epigeneza. Poznanskie ´ M., Kosicki, J.Z., 2007. Human breeding ecology – the classification and regression trees (CART) answer to the question Kosinska, how the maternal environment participates in newborn outcome. In: Application of Mathematics to Biology and Medicine. Jagiellonian University, Kraków, pp. 66-71. ´ ´ M., Stoinska, B., Gadzinowski, J., 2004. Are the gestational age and the birth body weight modificators of the develKosinska, opmental dynamic? Arch. Perinat. Med. 10, 49–52. ´ M., 2006. Two methods for estimating age of newborns in catch-up growth studies. Early Hum. Dev. 82, 575–582. Kosinska, ´ ´ M., Stoinska, B., 2009. Ocena rozwoju fizycznego i psychoruchowego dzieci urodzonych przedwcze´snie oraz dzieci Kosinska, ˛ ˛ Wydawnictwo Antropologia˛ a Medycyna. urodzonych z mała˛ masa˛ ciała. In: Kaczmarek, M., Szwed, A. (Eds.), Miedzy ´ pp. 155–169. Naukowe UAM, Poznan, ´ M., Szwed, A., 2008. The effect of developmental status on birth on the age of menarche in the female residents of the Kosinska, province of Wielkopolska. Pol. J. Environ. Stud. 17, 220–223. Kornacka, M.K., 2006. Noworodki płodowe. Klin. Pediatr. 14, 5095–5096. Kozieł, S., Jankowska, E.A., 2002a. Birthweight and stature, body mass index and fat distribution of 14-year-old Polish adolescents. J. Paediatr. Child Health 38, 55–58. Kozieł, S., Jankowska, E.A., 2002b. Effect of low versus normal birthweight on menarche in 14-year-old Polish girls. J. Paediatr. Child Health 38, 268–271. Meadow, W., Lee, G., Lin, K., Lantos, J., 2004. Changes in mortality for extremely low birth weight infants in the 1990s: implication for treatment decisions and resources use. Pediatrics 113, 1223–1229. Ounsted, M., Moar, V., Scott, A., 1984. Infants of deviant birth weight at the age of seven years: health, handicap, size and developmental status. Early Hum. Dev. 9, 323–340. Paz, I., Seidman, D.S., Danon, Y.L., Laor, A., Stevenson, D.K., Gale, R., 1993. Are children born small for gestational age at increased risk of short stature? Am. J. Dis. Child. 147, 337–339. Persson, I., Ahlsson, F., Ewald, U., Tuvemo, T., Qingyuan, M., von Rosen, D., Proos, L., 1999. Influence of perinatal factors on the onset of puberty in boys and girls: implications for interpretation of link with risk of long term diseases. Am. J. Epidemiol. 150, 747–755. Romundstad, P.R., Vatten, L.J., Nilsen, T.I.L., Holmen, T.L., Hsieh, C.-C., Trichpoulos, D., Stuver, S.O., 2003. Birth size in relation to age at menarche and adolescent body size: implications for breast cancer risk. Int. J. Cancer 105, 400–403. Sloboda, D.M., Hart, R., Doherty, D.A., Pennell, C.E., Hickey, M., 2007. Age at menarche: influences of prenatal and postnatal growth. J. Clin. Endocrinol. Metab. 92, 46–50. StatSoft, Inc., 2010. STATISTICA (Data Analysis Software System), Version 9.1., http://www.statsoft.com. St George, I.M., Williams, S., Silva, P.A., 1994. Body size and the menarche: the Dunedin Study. J. Adolesc. Health 15, 573–576. Strauss, R.S., 1997. Effects of the intrauterine environment on childhood growth. Br. Med. Bull. 53, 81–95. Tam, C.S., de Zegher, F., Garnett, S.P., Baur, L.A., Cowell, C.T., 2006. Opposing influences of prenatal and postnatal growth on the timing of menarche. J. Clin. Endocrinol. Metab. 91, 4369–4373. Terry, M.B., Ferris, J.S., Tehranifar, P., Wei, Y., Flom, J.D., 2009. Birth weight, postnatal growth, and age at menarche. Am. J. Epidemiol. 170, 72–79. Vohr, B.R., Oh, W., Rosenfield, A.G., Cowett, R.H., Berstein, J., 1979. The preterm small-for-gestational age infant: a two year follow-up study. Am. J. Obstet. Gynecol. 133, 425–431. Whincup, P.H., Gilg, J.A., Odoki, K., Taylor, S.J.C., Cook, D.G., 2001. Age at menarche in contemporary British teenagers: survey of girls born between 1982 and 1986. Br. Med. J. 322, 1095–1096. World Health Organization Expert Committee on Maternal and Child Health: Public Health Aspects of Low Birth Weight. Third Report of the Expert Committee on Maternal and Child Health, 1961. WHO Technical Report Series No. 217. Geneva. Wollmann, H.A., 2004. Small for gestational age (SGA): growth and long-term effects, German. Monatsschr. Kinderheilkd. 152, 528–535.