Pattern of pubertal changes in Calabar, South South Nigeria

Introduction Puberty is an essential physiologic process that is characterized by the appearance of secondary sexual features. Secular changes in puberty occur from one generation to another and need to be documented. The assessment of pubertal stages in a child is only useful if recent and reliable reference data from the same population is available for comparison. The study aimed to profile clinical normative sexual maturity characteristics for children in Calabar, South-South Nigeria. Methods A cross-section of primary and secondary school pupils aged 6-18 years in the city of Calabar, Nigeria were randomly selected for the study. Sexual maturating rating was assessed using the pubertal staging for breast development and pubic hair as described by Marshall and Tanner (Tanner staging). Testicular volume in boys was measured using the Prader orchidometer. Menarche and “voice break” were established by recall of the event by the girls and boys respectively. Results A total of 2,830 children were seen, 1542 (54.5%) boys and 1288 (45.5%) girls. The mean age of onset of pubic hair was 11 years in both boys and girls. Pubertal testicular volume of 4 mls was seen in boys at a mean age of 11 years. Breast development in girls occurred at mean age of 11 years and menarche at 13 years. Conclusion in this study, the onset of puberty is occurring at an earlier age than previously reported in Nigeria with a secular trend of a decreasing age at onset of puberty. These sexual characteristics are rather occurring at similar ages reported from western countries.


Introduction
Puberty is an important physiologic process that occurs during human growth and development. It marks the transition from childhood to adulthood and the appearance of secondary sexual features is the most visible manifestations of puberty [1]. In boys, testicular enlargement and development of breast buds in girls are the most important early physical signs of puberty and both are as a result of an increased secretion of androgens (testosterone) and estrogen respectively [2]. These increases in gonadal steroids (testosterone and estrogen) secretion is mediated by an increased gonadotropin-releasing hormone secretion from the Hypothalamus which in turn causes an increased secretion of pituitary gonadotropins (Luteinizing and Follicle Stimulating hormones) [2].
The activation of this hypothalamic-pituitary-gonadal axis (gonadarche) as well as maturation of the adrenal axis (adrenarche) leads to normal puberty. Adrenarche is associated with an increase of adrenal androgen production that leads to first appearance of pubic hair. The increases in adrenal androgens secretions often occur prior to increases in pituitary gonadotropins and gonadal steroids (gonadarche) secretion [3]. The progressive physical changes seen are in the breast, genitals and pubic hair. The tanner staging system has divided these continuous physical changes into one of five stages [1,3]. In boys, there is also a sudden change in voice with ongoing puberty described as "voice break" [4]. In addition to anthropometric changes/secondary sexual characteristics, in boys changes also occur in the organs of phonation. These include an increase in neck length/width and breathing capacity which leads to a relative descent of the larynx and subsequent enlargement of the vocal tract and resonatory system [5]. In natural speech, this voice "break" depends on how the vocal cords vibrate. Spermatogenesis and Menstruation also begins in mid to late puberty [2]. Puberty eventually stops growth in height, at different ages in children through fusion of the epiphysis by the action of estrogens in both boys and girls [6].
Sexual maturation in humans is unique in that there is a 4-5 years physiologic variation in the age at onset of puberty observed among normal individuals living in relatively similar life conditions [7]. Thus, puberty is observed within the age brackets of 8-13 years in girls and 9-14 years in boys [3]. These variability involves genetic factors, ethnicity, nutritional conditions, environmental factors and secular trends in growth and sexual development [7][8][9]. Secular changes (variation in age at onset of puberty for different generations in a given population) in age of menarche in countries of the Western world have been documented over the last two centuries [8]. A secular trend over these periods has shown a steep decline in age of onset of menarche in the Western world [8,9].
Secular changes may reflect the varying health and affluence of populations over time and may also be highlighting inequalities of health and wealth within populations [9]. Therefore it is suggested that national reference data should be collected at 10 to 20 years intervals. Furthermore, normative prevalence data on the pubertal characteristics of young girls at various ages are essential for patient education and the provision of appropriate anticipatory guidance [10]. Sexual maturity rating (SMR) especially for those whom growth and development problems are a concern, are only meaningful when suitable reference data in normal healthy peers are available in that population for comparison [9]. There is paucity of literature in South-South Nigeria especially Cross River State, concerning the age at onset of puberty. Normative reference data is often quoted from developed Western countries which may be different from African and Nigerian values. Also, Nigeria is a vast country with different ethnic groups; and growth and puberty has been shown to vary amongst different racial groups [8]. Assessment of secular changes from one generation to the next is impossible without normative reference data to be compared with previous data or in the future [10]. The earlier studies [11,12]

Study design:
The study was a cross-sectional descriptive study Study population: Children aged between 6-18 years without chronic diseases, growth abnormalities and long term medications like steroids were included for the study. The age of the children studied was calculated based on their last birthday Children of these age groups with chronic diseases, growth abnormalities and on long term medications were excluded from the study. Children who did not give assent to participate in the study as well as those whose parents refused to give consent were also excluded.
Sampling technique: Multistage sampling technique was used to recruit subjects for this study. Five Secondary Schools and two Primary schools, in Calabar metropolis were randomly selected and used for the study. A cross section of primary and secondary school pupils aged 6-18 years in the city of Calabar, Nigeria were randomly selected for the study. These public schools draw children from a variety of social and economic backgrounds in the state. The sample size where the population is above 10,000 was estimated from the following formula [13].
A total of 2401 subjects were recruited for the study. Percentages were also calculated.

Results
General characteristics of the study population: A total of 2830 children aged 6 to 18 years participated in the study, 54.5% were males and 45.5% were females. Age and sex distribution of the study population is shown in Table 1.

Pubertal development (secondary sexual characteristics) in boys:
The distribution of pubic hair in boys according to age is shown in

Pubertal development (secondary sexual characteristics) in girls
Pubic hair: In girls, the development of pubic hair stage 2 was seen as early as 6 years of age as shown on Table 5. However, the mean age of development of pubic hair was 11 years (SD 0.4).
Breast development: years. Two each of these girls had stage 2 and 3 breast development as at time of examining and the rest of the girls, stages 4 and 5. However, the mean age of onset of menstruation was 13 years.

Discussion
In boys, the development of pubic hair in this study occurred at a mean age of 11 years. A small proportion of boys developed pubic hair at 7 years with the proportions increasing incrementally with age. Adult pattern pubic hair was seen from 12 years of age. This finding is in contrast to one previous report in Nigeria by Ezeome et al [11] where pubic hair development was reported to occur from 9- Onset of puberty in boys is said to start when testicular volume reaches 4 mls by the Prader orchidometer [3,14]. This is an easy parameter to assess in boys in the outpatient clinic and during research. A small proportion of boys at 8 years had testicular volume of 4 mls and these proportions increased with age. This age of pubertal onset of testicular volume >4 mls in boys in this study is occurring one year lower than the accepted norm of 9 years [3].
However, the mean age of testicular volume of 4 mls attainment was 11 years and compares with report from Netherland of 11.5 years [15]. There is no other work to our knowledge on testicular volume in boys using Prader orchidometer in this part of South-South Nigeria to compare. However, it would appear that the attainment of puberty in boys in Nigeria is similar to that seen in Europe and the Western world where puberty is said to start from 9-14 years [3]. This may be due to an improved economy since 1999 translating to improved living standard and good health compared to previous decades in Nigeria [16,17]. This also reflects a positive secular change towards early puberty in boys in Nigeria compared to previous report by Ellis [12] about 6 decades ago where pubic hair was noticed from 10 years and genital development from 12 years.
This earlier study used a small sample size of 333 boys and is prone to errors as genital development may be difficult to assess in black skin children and testicular volume was not used in the study. The mean age of voice change ("voice break") to adult type in this study was at 15 years and may correspond to testicular volume of at least 15 mls. This result is similar to that of earlier report of 14 years in the United Kingdom [5]. There are no previous studies of voice "break" in Nigeria to my knowledge. Even though it is a recall event in this study, the result is still reliable as the event is not far from the subject's ages and they can recall it. In girls, the development of secondary sexual characteristics in this study is similarly occurring at younger ages than suggested in previous reports from Nigeria [12,18], Senegal and Ethiopia [19,20]. On the average, girls in this study begin pubertal development between the ages of 8 to 13 years as is in keeping with internationally accepted norm [3]. Breast development was seen in a small proportion of girls at 8 years and increase in proportions with age. The mean age of breast development was 11 years. This is in contrast to earlier reports of mean ages of 12.7 years in Nigeria [18] and 12.6 years in Senegal [19]. In this study, girls appear to be developing breast 6 months-1.5 years sooner than in previous reports [12,19] and rather similar to their European counterpart of 10.7 years in Netherlands [15] and 9.96 years in white American girls [10]. This may still be due to improved living conditions and good health experienced in Nigeria over the past decades [16,17]. The development of pubic hair in girls in this study was similar to that seen in boys and was noticed as early as 6 years with a mean age of 11 years. A similar trend has also been reported in African American girls as young as 6 years developing pubic hair but with a mean age of 8.78 years [10]. The mean age of pubic hair growth of 11 years is similar to that of 10.51 years for white American girls [10].
Page number not for citation purposes 5 In this study, menarche was reported to occur in two girls at the age of 8 years. The corresponding breast development at the time of this study was stage 5 for these 8 year olds (which may have been lower at the time of onset of the menses). Sixteen girls also reported onset of menses at the age of 9 years. Four of these girls had stage 4 breast development and 12 of them had stages 5. This age of onset of menarche is similar to that reported in African American girls at 9 years in an American study [10]. It may also be that these girls just had precocious puberty with breast development occurring earlier than 8 years of age but now culminating in puberty at this age of 8 and 9 years. Also, age at menarche is said to be more sensitive to nutritional and chronic infection status [10,21,22]. It is possible, better nutrition and health experienced by children in most urban Nigeria towns recently may account for this early onset of menstruation and puberty [16].
Ellis [12] observed six decades ago, a mean age of menarche in two series of studies in Nigerian girls to be 14.22 and 14.44 years. Even though the sample size was small (300 girls in the 1 st series and 250 girls in 2 nd series), the result may still reflect the pubertal changes occurring then in Nigeria. The mean age of menarche in this study was 13 years. As age at menarche were asked as ages in whole years, the data about age at menarche may not be very precise.
However, it will appear from this study that there is a positive secular change towards a decreasing age at menarche/puberty by about 1.5 years. This is similar to the reports from Europe over the decades [8,23]. This result of age at menarche of 13 years is also similar to a more recent study in the 1990s from Nigeria with reported mean age at menarche of 13.6 and 13.9 years [19,24] and a more current report of 13.02 years [25] in 2010. It would appear that there is an apparent stabilization of age at menarche at 13 years in Nigeria. It is interesting to note that this age at onset of menarche is similar to that reported from America (12.5 years) [10], Netherland (13.5 years) [15], Uganda (13.3 years) [22] and Bangladesh (13 years) [21]. On the other hand, the result is lower than that reported from some other African countries, Ethiopia (14.8 years) [20] and Senegal (15.9 years) [19]. These two African studies used adolescents in rural communities where living conditions were said to be poor and nutrition not optimal.

Conclusion
There is a downward age trend in start of pubertal development in both boys and girls in Nigeria. It is recommended that regional studies be carried out to corroborate these findings.
What is known about this topic  This study shows that puberty begins at eight years and so policy makers in government should incorporate education on puberty and sexuality in the school curriculum from this age.

Competing interests
The authors declare no competing interest.

Acknowledgments
We want to acknowledge Prof. Maxwell Anah for his patience in proof-reading this manuscript. We thank the Ministry of Education, Cross River State, the Principals and teachers of all the schools used in the Study. We also thank the students for their cooperation and enthusiasm in their quest to know if they are growing normally to adulthood. Table 1: Study population according to age and sex Table 2: Distribution of pubic hair in boys according to age Table 3: Distribution of testicular size according to age Table 4: Reported voice change in boys according to age Table 5: Distribution of pubic hair in girls according to age