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Abstract

Background. Puberty, a stage of development involving sexual maturation, is not well understood in Sudan regarding the onset and pattern of puberty in elementary school boys and girls. Objectives. To investigate the average ages and patterns of pubertal development of male and female school children. Methods. A one-year study involved 1584 students from 50 elementary schools. Result. The study involved 1584 students, with 58.6% male and 41.4% female. The minimum age for pubertal signs was 9 years. Boys showed increased height, body build, interest in adult behavior, acne, gynecomastia, pubic hair growth, axillary hair growth, facial hair growth, while girls showed increased height, breast buds, interest in adult behavior, and menarche. Conclusion. The study revealed that puberty typically begins at 9 years old in both males and females, with pubic hair development occurring before height increase in boys, breast budding and pubic hair appearing later in girls, particularly in Sudan.

Keywords

puberty children adolescence adolescents Sudan

Highlights

• Puberty is the developmental stage that corresponds with a child’s sexual development. Little is known regarding the onset and course of puberty in Sudanese primary school students.

• The purpose of this study was to compare the pubertal growth trends and average ages of school-age males and females.

• In primary schools in the Omdurman locale of Sudan, a descriptive, cross-sectional, community-based study was carried out in 2018 to 2019. Out of all the primary schools—169 in total—50 was chosen at random. There were 43 000 pupils total in the population. To represent the population, a sample size of 2000 pupils was determined.

• According to the study, puberty occurred normally in both sexes, with some symptoms appearing in boys earlier. On the other hand, boys’ pubic hair development came before their height gain. Breast blossoming precedes pubic hair growth in girls during adolescence. The final stage of puberty was menarche, and girls from Sudan menarche later than girls from other African countries. Boys and girls did not differ in terms of height gain, body habits, interest in adult activity, or acne.

Introduction

Puberty is a stage of development marked by rapid changes in physiology and psychology. Along with the physical changes, sexual maturation also occurs during puberty; a process that is a part of becoming an adult. By the end of puberty, children can form offspring. Hence, it is characterized as a stage of sexual development.¹ During puberty, the child’s body undergoes multiple changes in height, shape, and functioning. Notably among that is the development of secondary sex characteristics; the “filling in” of the child’s body; from girl to woman and from boy to man. Puberty is derived from the Latin puberatum meaning the age of maturity, whereas adolescence is the period of mental transition from childhood to adulthood. The word puberty describes the physical changes of sexual maturation, while adolescence describes psychosocial and cultural maturation.² However, the terms puberty and adolescence are commonly used interchangeably.

At the beginning of puberty, the hypothalamus begins to release the gonadotropin-releasing hormone, which causes the pituitary to release gonadotropins, which in turn stimulate the gonadal functions, such as the release of testosterone or estradiol and the maturation of spermatogenesis or the ovarian follicle. Numerous neuroendocrine factors, including adrenergic or dopamine neurotransmitters, endogenous opioids, and melatonin produced by the pineal gland, are likely responsible for the onset of puberty. A postnatal luteinizing hormone surge in the newborn is responsible for infants’ onset of gonadal maturity (gonadarche). Alike, another luteinizing hormone surge is responsible for adrenarche, or adrenal maturation, which occurs between the ages of 7 and 8 years stimulating the onset of puberty.³

To study and understand puberty properly, we must have—in addition to a definition of this developmental stage—a staging system, as puberty is not a sudden and singular event but rather a series of developmental changes. The staging system utilized most popularly to stage puberty was published by Marshall and Tanner, where the sequence of changes of puberty is described by sexual maturity ratings (SMR), also known as “Tanner stages.” These consist of numbered and systematized descriptions of the development of secondary sexual characteristics, consisting of breast changes in females, pubic hair changes in both males and females, and genital changes. The sexual maturity ratings (SMR) of pubic hair, breast, and genitalia consist of five categories, with stage one representing pre-puberty and stage five representing adult development.^4,5

For children, puberty is a period of rapid changes that can be accompanied by psychological turmoil as children do not all go into puberty at the same time and rate, and that variation is normal. The age of onset of puberty is influenced by multiple factors, including racial, ethnic, genetic, geographical, nutritional, and socioeconomic factors.⁶ Thus, definition of an appropriate pubertal age range is crucial to guide diagnostic evaluations and regulate possible therapeutic interventions for children with delayed or premature pubertal development. Over the past 100 years earlier onset of puberty among children was observed consistently. This issue has created a concern among medical researchers, and the exploration of probable causes of early puberty is still under process. This rapid shift in the pubertal ages observed around the globe owes to many contributing elements. The most important factors include dietary quality and amount of consumption that might be responsible for genetic and hormonal changes.⁷ Currently, the age range of normal puberty is defined by the appearance of the first signs of puberty, that is a testicular volume of ≥4 ml in boys and the appearance of breast budding in girls.⁸ Delayed onset of puberty is defined by the absence of testicular enlargement by 14 years in boys, and the absence of thelarche by 13 years or menarche by 15 years in girls.⁸ The age limit considered for delayed completion of puberty is 16 years in girls and 17 years in boys.⁹

As puberty is an important milestone with multiple factors that can affect its time and pattern, and as it is a stage of development with great importance for pediatricians, it becomes important to explore the timing of pubertal signs among children globally across different societies, ethnicities, and geographic locations. As far as this study is concerned, using Western estimated standards of reference on Sudanese children can be misleading due to known differences in genetics and the environmental, social, and nutritional variations that influence the onset of puberty.¹⁰ Although there have been several studies that investigated the onset of menarche among Sudanese girls, to our knowledge, no studies have been conducted to investigate the patterns of puberty in both sexes. Little to no studies were conducted to investigate puberty in boys specifically. This study aims to investigate and mark the age of appearance of pubertal signs of Sudanese children in the elementary school period, which will be the first of its kind primary research investigating this topic, serve as a reference to judge medical variations from this pattern by pediatricians, and guide parents and educators in counseling children to understand the physical and psychological changes accompanied by this stage of development.

Methodology

Study Design

This is a descriptive, cross-sectional, community-based study that was conducted in 2018 to 2019 in elementary schools in Omdurman locality in Khartoum, Sudan.

Study Population

The study’s target population was elementary school students starting from 3rd grade students (7 years of age) up until 8th grade. Thus, our inclusion criteria included students 7 years of age or above, with parents who reported awareness and following of their child’s pubertal development and excluded children from 1st and 2nd grades, questionnaires received from parents who reported that they don’t follow their child’s pubertal development.

Sampling Technique and Sample Size Calculation

Considering the population size of 430 000 students in Omdurman locality elementary schools (according to the Ministry of Education of Sudan records) and a margin of error of 0.05, the study sample was calculated using Yamane formula: n = N/(1 + N(e)²). Considering a design effect of 2 and an anticipated 55% non-response rate, the minimum sample size required to adequately represent the study population is 1580 students.

Data Collection Method and Tool

To ensure proper representation using this sample size, a cluster sampling method was adopted. In the first stage of cluster sampling, 50 out of 169 elementary schools in Omdurman locality were selected using simple random sampling by a random number generator from a list containing all 169 elementary schools of Omdurman locality. For the selection of students from each school stratified random sampling was used to select students from third to eighth grade. The number of the selected students from each school represents the percentage of students in this school to the total number of elementary school students in Omdurman locality. As for the data collection tool, the data was collected through a structured questionnaire filled in by the parents of each student. The questionnaire was designed by the authors of this study and revised by a senior consultant endocrinologist. Subsequently, a pilot study was conducted to test the questionnaire, and feedback from the participants was used to edit the questionnaire. The questionnaire included demographic data (age, grade, sex), choric illness inquiry, and questions about pubertal sign appearance (yes or no questions) with an option for the parents if they don’t know the pubertal signs of their child. All variables in this study were collected in the form of binary data. Each selected student received the questionnaire for his/her parents sealed and attached with written consent. The integrity of data in this study depends on the parents of children as references for information.

Statistical Analysis

Data was entered into Microsoft Excel, cleaned, and analyzed using the SPSS version 27. Frequency tables were used to demonstrate the age of development of secondary sexual characteristics and the timing and pattern of development of pubertal signs in males and females. Inferential statistics represented in Leven’s test were used to assess for the equality of variances in some variables among males and females (comparison of height, change in body shape, adult interest, acne appearance, axillary hair growth, and pubic hair growth). The tables were created using Microsoft Word 2017.

Results

A total number of 1584 students were involved in this study. Of them, 929 were male students (58.6%) and 655 were female students (41.4%). 81 male students (7.71%), and 200 (21.0%) female students who received the questionnaire had parents who refused to participate in this study. A total of 40 (3.80%) male students and 95 (10%) female students who also received the questionnaire had parents who did not know anything about the pubertal development of their sons/daughters.

Male Students’ Pubertal Signs

The minimum age for the appearance of pubertal signs in male students was 9 years old and the maximum was 14 years (mean age 11.66 ± 1.55 years). The age distribution of our male study participants at the time of the study was 11.3% were 9 years old, 14.2% were 10 years old, 19.3% were 11 years old, the majority (21.4%) were 12 years old, 19.7% were 13 years old, and 14.1% were 14 years old.

309 (33.3%) of male participants showed an increase in their height starting at the age of 7 years as the youngest age for this sign and 14 years as the oldest age (mean age 11.92 ± 1.46 years). Then the age at which the male students showed a change in their body build was assessed, 287 (30.9%) were found to have this sign; the minimum age at which this sign appeared was 8 years and the maximum age was 14 years (mean age 12.11 ± 1.39 years). Male study participants were assessed for the development of acne as a sign of puberty, it was found that only 66 students (7%) had acne with 10 years as the earliest age for the appearance of acne and 14 years as the maximum age (mean age 12.71 ± 0.98 years). Only 41 (4.4%) of the male students showed facial hair growth. The youngest age at which this sign appeared was 12 years and 14 was the maximum (mean age 13.19 ± 0.71 years). As for the development of axillary hair for male students reported by the parents, 79 (8.5%) of the students had developed this sign, and it was found to be between the ages of 10 and 14 years (mean age 12.98 ± 0.94). 134 (14.4%) male students between the ages 10 to 14 years had pubic hair growth (mean age 12.91 ± 0.95). The male study participants were also assessed for the change of voice; 142 (15.3%) of them had this sign (mean age 12.86 ± 1.0 years). 65 (7%) developed gynecomastia at a mean age of 12.83 ± 0.94 years. The parents were asked whether they observed that their sons started to show interest or simulate adult behavior, and the answer to this question showed that 319 (34.3%) of the male students showed interest in adult behavior (mean age 12.29 ± 1.34 years). Details of male students’ development of pubertal signs are discussed in Tables 1 and 2.

Table 1.

Distribution of Male Study Participant’s Age of Development of Secondary Sexual Characteristics According to Age.

Frequency and percent of characteristic
Age	Increase in height	Change in body built	Acne	Facial hair growth	Axillary hair growth	Pubic hair growth	Voice change	Gynecomastia	Interest in adult behavior
7.00	1 (0.3%)	—	—	—	—	—	—	—
8.00	2 (0.6%)	2 (0.7%)	—	—	—	—	—	—	2 (0.6%)
9.00	15 (4.9%)	10 (3.5%)	—	—	—	—	1 (0.7%)	—	9 (2.8%)
10.00	41 (13.3%)	29 (10.1%)	2 (3%)	—	2 (2.5%)	3 (2.2%)	3 (2.1%)	1 (1.5%)	26 (8.2%)
11.00	50 (16.2%)	47 (16.4%)	4 (6.1%)	—	2 (2.5%)	8 (6%)	7 (4.9%)	6 (9.2%)	39 (12.2%)
12.00	80 (25.9%)	75 (26.1%)	20 (30.3%)	7 (17.1%)	17 (21.5%)	25 (18.7%)	30 (21.1%)	11 (16.9%)	88 (27.6%)
13.00	73 (23.6%)	73 (25.4%)	25 (37.9%)	19 (46.3%)	32 (40.5%)	59 (44%)	62 (43.7%)	32 (49.2%)	89 (27.9%)
14.00	47 (15.2%)	51 (17.8%)	15 (22.7%)	15 (36.6%)	26 (32.9%)	39 (29.1%)	39 (27.5%)	15 (23.1%)	66 (20.7%)
Total	309	287	66	41	79	134	142	65	319

Table 2.

Timing and Pattern of Development of Male Students’ Pubertal Signs.

Sign	Minimum age	Maximum age	Mean age	±SD
Increased height	7	14	11.92	1.46
Change in body build	8	14	12.11	1.39
Acne	10	14	12.71	.98
Facial hair growth	12	14	13.19	.71
Axillary hair growth	10	14	12.98	.94
Pubic hair growth	10	14	12.91	.95
Change in voice	8	14	12.86	1.0
Gynecomastia	10	14	12.83	.94
Interest in adult behavior	8	14	12.29	1.34

Female Students’ Pubertal Signs

Overall, the minimum age for the development of female pubertal signs was 9 years and the maximum was 15 years (mean age 11.50 ± 1.43 years). 6% of the female participants were 9 years old, 21.8% were 10 years old, the majority (25.2%) were 11 years old, 20% were 12 years old, 18.7% were 13 years old, 6% were 14 years old, and 2.3% were 15 years old.

The female students were assessed in the same way for signs of puberty. The first question was about the appearance of breast buds, 320 (48.9%) had developed breast budding by the time of the questionnaire, with a mean age of 11.16 ± 1.27 years. 333 (50.8%) of female study participants showed an increase in their height (11.13 ± 1.37 years). 299 (45.6%) female students developed female body habitus (mean age 11.39 ± 1.37). Acne was found in 110 (16.8%) of the female students (mean age 12.17 ± 1.24 years). The parents reported development of axillary hair in 155 (23.7%) of their daughters, with a mean age of 12.16 ± 1.17 years. Pubic hair was found in 196 students (29.9%) with a mean age of 12.05 ± 1.25 years. The parents observed a change in the character of their daughters showing more interest in female adult behavior in 279 (42.6%) among our female students, at a mean age of 11.70 ± 1.34 years. As for the age of menarche among our female study participants, (21.8%) had their first menstrual cycle between the ages of 9 and 15 years old (mean age of 12.23 ± 1.14 years). See Tables 3 and 4.

Table 3.

Distribution of Female Study Participant’s Age of Development of Secondary Sexual Characteristics According to Age.

Frequency and percent of characteristics
Age	Breast bud	Increased height	Change to female body habitus	Acne	Axillary hair growth	Pubic hair growth	Interest in female adult behavior	Age at menarche
7.00	—	1 (0.3%)	—	—	—	—	—
8.00	—	4 (1.2%)	2 (0.7%)	—	—	—	1 (0.4%)
9.00	29 (9.1%)	31 (9.3%)	22 (7.4%)	1 (0.9%)	—	4 (2%)	9 (3.2%)	1 (0.7%)
10.00	76 (23.8%)	78 (23.4%)	61 (20.4%)	10 (9.1%)	14 (9%)	19 (9.7%)	41 (14.7%)	7 (4.9%)
11.00	86 (26.9%)	90 (27.0%)	70 (23.4%)	21 (19.1%)	32 (20.6%)	39 (19.9%)	81 (29%)	28 (19.6%)
12.00	82 (25.6%)	75 (22.5%)	77 (25.8%)	32 (29.1%)	43 (27.7%)	62 (31.6%)	69 (24.7%)	51 (35.7%)
13.00	36 (11.3%)	41 (12.3%)	51 (17.1%)	31 (28.2%)	47 (30.3%)	46 (23.5%)	50 (17.9%)	37 (25.9%)
14.00	10 (3.1%)	9 (2.7%)	13 (4.3%)	13 (11.8%)	18 (11.6%)	25 (12.8%)	23 (8.2%)	16 (11.2%)
15.00	1 (0.3%)	4 (1.2%)	3 (1%)	2 (1.8%)	1 (0.6%)	1 (0.5%)	5 (1.8%)	3 (2.1%)
Total	320	333	299	110	155	196	279	143

Table 4.

Timing and Pattern of Female Students’ Pubertal Signs.

Sign	Minimum age	Maximum age	Mean age	±SD
Breast bud	9	15	11.16	1.27
Increased height	7	15	11.13	1.37
Change to female body habitus	8	15	11.39	1.37
Acne	9	15	12.17	1.24
Axillary hair growth	10	15	12.16	1.17
Pubic hair growth	9	15	12.05	1.25
Interest in adult behavior	8	15	11.70	1.34
Menarche	9	15	12.23	1.14

Levene’s test for homogeneity of variance was used to compare the mean age of the appearance of some pubertal signs between male and female study participants. It was found that the mean age at which the study participants showed an increase in their height, change in their body habitus, and the age of the development of adult interest is not different between male and female students (F = 1.351, P-value = .246; F = 0.240, P-value= .624; F = 0.053, P-value = .819). The test of homogeneity when used to compare the mean age of the appearance of acne revealed that the mean ages are approx-imately equal between male and female students (F = 3.57, P-value = .06). However, there was a statistically significant difference in the mean age of the appearance of axillary and pubic hair between male and female study participants (P-value = .000 for both) (see Tables S1-S12 in the Supplementary Material).

Discussion

In this study, a total number of 1584 students were involved. Of these, 929 were males (58.6%), and 655 were females (41.4%). Discussing Puberty of male student participants first, signs of puberty that were investigated were increase in height, change in body built, acne, facial hair growth, axillary hair growth, pubic hair growth, change in voice, gynecomastia, and interest in adult behavior. The minimum noted age of a male pubertal sign development in this study was 9 years. Whereas the eldest age was 14 years with a mean age of (11.66 ± 1.55) years. According to Sizonenko denoting the normal sexual maturation of children, the mean age for the onset of puberty in boys is 10.9 years, concerning the sign considered the first sign of pubertal development for boys which was testicular growth beyond 4 cm² or 4 ml². Although the mean age of our study seems to be earlier than that reported by Sizonenko,³ an agreement on the first sign that marks the beginning of puberty is necessary to make a fair comparison.

In total, 309 (33.3%) of male participants showed an increase in their height, with 7 years as the youngest age for the appearance of this sign and 14 years as the eldest age (mean age 11.92 ± 1.46 years). Studies mention that adolescent boys reach peak height velocity no younger than 14 years of age.¹¹ Then the age at which the male students showed a change in their body build was assessed, 287 (30.9%) were found to have this sign; the minimum age at which this sign appeared was 8 years and the maximum age was 14 years (mean age 12.11 ± 1.39 years). Additionally, parents reported they started noticing voice breaks in their boys at the age of 8 until 14 years, with a mean age of 12.86 ± 1.0 years. In a Danish study, 95% of boys experienced voice break at the age of 13.1 years¹² and in a Turkish study, laryngeal development normally occurred at a mean age of 13.37 years. According to our study boys experienced this change younger. The parents were also asked whether they observed that their sons started to show interest or simulate adult behavior, and the answer to this question showed that 319 (34.3%) of the male students showed interest in adult behavior (mean age 12.29 ± 1.34 years). The male study participants were assessed for the development of acne as a sign of puberty; it was found that only 66 (7%) had acne with 10 years as the earliest year for the development of acne and 14 years as the maximum time (mean age 12.71 ± 0.98 years). Although studies have shown no significant change in the mean age of black girls seeking treatment for acne (specifically acne vulgaris), there has been a noted decrease trend in the average age of children seeking acne treatment. This may indicate a decreasing trend in the age of puberty in boys specifically and in children on average.¹³ Gynecomastia is a frequent sign in pubertal boys. In our study, 65 (7%) developed gynecomastia at a mean age of 12.83 ± 0.94 years. However, in our study, this sign lacks confirmation, as pseudogynecomastia (which is the deposition of adipose tissue in the breast area) can be easily mistaken for true gynecomastia, which occurs due to the true proliferation of glandular elements.¹⁴ A study conducted by Neyzi et al¹⁵ on pubertal development of Turkish boys encountered gynecomastia in 7%; a percentage identical to that of our study.

Pubarche is the term denoted for the starting of the development of pubic hair in boys and girls. Pubarch is generally accompanied by the development of axillary hair as well, which is considered to be abnormal if it occurs before the age of 9 in boys.¹⁶ The presence of axillary hair, pubic hair, and facial hair was investigated in this study. Pubic hair in boys generally appears in 18 to 24 months from the start of testicular development and is considered the initial marker of puberty in adolescent males.¹¹ A total of 134 (14.4%) of male students in our study between the ages of 10 to 14 years had pubic hair growth (mean age 12.91 ± 0.95 years), and 79 (8.5%) of the students had developed axillary hair as well. Axillary hair was found starting at 10 years of age with a mean age of 12.98 ± 0.94 years. Study evidence indicates that pubic and axillary hair development occur almost simultaneously. Only 41 (4.4%) of the male students showed facial hair growth, the youngest age at which this sign appeared was 12 years and 14 was the maximum, with a mean age of 13.19 ± 0.71 years. Facial hair appears later in pubic and axillary hair development as our study suggests. In a study that investigated the mean ages of appearance of pubic, axillary, and facial hair in boys, it was found that the mean age for pubic hair development was 11.80 years, 13.15 years for axillary hair, and 14.45 years for facial hair. The study also mentioned the earlier appearance of pubertal signs in boys from high socioeconomic status families against lower socioeconomic status families.¹⁵ The findings of this study differ from ours in that it found a large disparity in times of pubic hair and axillary hair development, and facial hair development occurred much later than in the subjects of this study. In Nigeria, pubic hair appeared in boys at 11 years old, concurrent with testicular development to 4 mls.¹⁷ This finding is earlier than the subjects of our study.

In conclusion, the pattern of appearance of male pubertal signs was in order, increase in height, change in body build, interest in adult behavior, acne, gynecomastia, change in voice, pubic hair growth, axillary hair growth, and lastly facial hair growth. A cohort by Marshall and Tanner⁵ that investigated the variations of patterns of puberty in boys confirmed that genitalia development is the beginning of all puberty; and although the time of pubic hair appearance could not be confirmed, it preceded the mean age at which boys reached peak height velocity.⁵

For female timing and pattern of pubertal signs development, the study was interested in signs such as the appearance of the breast bud, increase in height, development of female body habitus, Acne, development of axillary hair, development of pubic hair, interest in female adult behavior, and menarche. The minimum age for development of a pubertal sign for female participants was 9 years and the maximum was 15 years (mean age 11.50 ± 1.43 years). In a study conducted by Largo and Prader¹⁸ investigating puberty in Swiss girls, the youngest reported age for the development of puberty signs was between 8 and 9 years, and the latest between 14 and 15 years. The earliest limit of full pubertal development was between 12 and 13 years and the latest was between 17 and 18 years. Another study by Sizonenko³ reports that the mean age for the beginning of pubertal development for girls is 11.2 years, which is quite late in comparison to our study and that of Largo et al report.

The first inquiry about female patterns of puberty was about breast budding, 320 (48.9%) of females developed breast budding. The mean age for this sign was 11.16 ± 1.27 years. Wheeler¹¹ mention that breast development is the first pubertal sign to occur in 85% of girls. The normal range for initial breast development is between 8 and 13 years of age. In urban China, breast development (Thelarche) was noted to start at 8 years old for 19.6% of girls.¹⁹ Menarche generally occurs within 2 years of the start of breast development.¹¹ In Egypt, breast budding for girls started at 10.71 years.¹⁸ Another important and striking feature of puberty is skeletal growth. 333 (50.8%) of our female study participants showed an increase in their height, at a mean age of 11.13 ± 1.37 years. This is within range and supportive of findings by other studies that report that girls reach peak height velocity by 12 years of age.¹¹ Body habitus is another sign of interest in this study, which is the physical consideration of the body of our subjects in terms of physique and body build. Sex hormone spurt drives these changes, and results in an increase in fat mass in girls specifically in the late stages of puberty.¹¹ About 45.6% of female students developed the female body habitus, with a mean age of 11.39 ± 1.37 years. Acne as a sign of puberty was evident in 110 (16.8%) female students (mean age 12.17 ± 1.24 years).

As for pubarche and axillary hair development, the parents reported the development of axillary hair in 155 (23.7%) of their daughters, with a mean age of 12.16 ± 1.17 years. Pubic hair was reported in 196 (29.9%) of girls with a mean age of 12.05 ± 1.25 years for this sign. Studies report that pubarche and axillary hair development are considered abnormal if they start before the age of 8 in girls.¹⁶ A study that investigated the pubic hair development of girls in urban China reported that it occurred in 11.16% of girls with Tanner stage 2 development and in 12.4% of girls with Tanner stage 3 development.¹⁹ In nearby Egypt, pubic hair appeared for girls at 10.46 years and axillary hair at 11.65 years.²⁰ The parents observed a change in the character of their daughters showing more interest in female adult behavior in 279 (42.6%) of our female students; the mean age was 11.70 ± 1.34 years.

As for menarche, female students in this study had their first menstrual cycle at a mean age of 12.23 ± 1.14 years. In a study conducted by Attallah et al²¹ that studied the average ages of menarche for girls in Khartoum, Sudan, classified according to socioeconomic status, the average age of menarche was 13.35 ± 0.14 years for girls from high-income families; 13.85 ± 0.15 years for girls from middle-class families and 14.06 ± 0.18 years for girls from low-income families. This study found that girls in Omdurman, Khartoum now undergo a younger onset of menarche, which confirms a secular trend. This trend of younger puberty has been noticed and reported internationally in the past two decades. Hypotheses that attempt to explain this trend consider the role of nutrition, obesity, and exposure to endocrine-disrupting factors (EDFs).²² In Egypt, the mean menarcheal age is 12.24 years,²⁰ while in Nigeria menarche occurs at the age of 13.0 years.¹⁷ The same mean age was found in Denmark, with daughters having menarche 3.6 months earlier than their mothers.¹² While in Switzerland menarche occurred at 13.4 ± 1.0 years.¹⁸ Another study from Turkey mentions the exact mean age for menarche, 13.4 years.³ In the US, the mean age for menarche is 12.8 years,¹¹ while in urban China it is 12.27 years.¹⁹

As for the pattern of appearance of pubertal signs among the female students in order it was an increase in height, breast bud, interest in adult behavior, change to female body habitus, pubic hair growth, axillary hair growth, acne, and lastly, menarche. In a study by Marshall and Tanner⁴ mean age for breast budding preceded the mean age for peak height velocity, contrary to our findings. In Susman et al²³ as in our study the breast budding in girls also significantly started before pubic hair development (66.2%), although the two signs finished development at the same time, as the study reports. On the contrary, in another study conducted in Switzerland, the order of pubertal development in Swiss girls started with pubic hair development in 53% of girls, while it started with breast budding for 18%. In 29% of girls, both started at the same time. The latter study also found a moderate correlation between the times of initiation of breast budding, pubic hair development, and menarche.¹⁸

Levene’s test was used to compare pubertal development homogeneity between males and females. The test revealed that there is no difference between male and female students in the mean age at which occurs an increase in height, change in body habitus, and the age of the development of adult interest. Further, when the test was used to assess the mean age of acne onset, it was shown that male and female students’ mean ages for the development of acne were comparable. However, there was a statistically significant difference in the mean age of pubic and axillary hair appearance. Studies reported that on average boys reach peak height velocity 2 years later than girls, although their genitalia start development only 6 months later than girls. Pubic hair also appears comparatively 1.5 years later in boys than in girls.⁵ Proportionately adjusting for the onset of puberty in both sexes, our findings seem to be supportive of these two signs.

Conclusion

In this study, a total number of 1584 students were involved of which (58.6%) were males, and (41.4%) were females. The age of the youngest noted pubertal development for males was 9 years and the latest was 14 years. A third of the boys experienced a change in height between 7 - 14 years (mean age 11.92 ± 1.46). Change in body build occurred at a mean age of (12.11 ± 1.39). Only 7% of boys developed acne during puberty, and the age range for the appearance of facial hair was between 12 - 4 years (mean age 13.19 ± 0.71). The minimum age at which axillary hair growth was reported was10 years (mean age 12.98 ± 0.94), with similar starting age for pubic hair growth and a mean age of (12.91 ± 0.95) years. 15% of students experienced a change in voice at a mean age of (12.86 ± 1.0). Only 7% of students developed gynecomastia with mean age (12.83 ± 0.94). 34.3% of the male students showed interest in adult behavior (mean age 12.29 ± 1.34). The order of the pubertal signs according to age was increase in height, change in body build, interest in adult behavior, acne, gynecomastia, pubic hair growth, axillary hair growth, and lastly facial hair growth. For female participants, 48.9% had breast bud at a mean age of (11.16 ± 1.27). (50.8%) of females experienced an increase in their height at (11.13 ± 1.37). Female body habitus was developed at mean age (11.39 ± 1.37). Acne was evident in only (16.8%) of females. (23.7%) developed axillary hair at the mean age (12.16 ± 1.17) and (29.9%) developed pubic hair at the mean age (12.05 ± 1.25). Change in character was observed in (42.6%) of females. The mean age for menarche in girls was (12.23 ± 1.14). As for the timing and pattern of appearance of pubertal signs in the female students in order: increase in height, breast bud, interest in adult behavior, change to female body habitus, pubic hair growth, axillary hair growth, acne, and lastly, menarche.

Limitations

The maximum age range for the appearance of each of the puberty signs in this study might have been largely influenced by the upper limit of age imposed on this study by the nature of its population; as it was conducted among elementary school students only, who mostly do not exceed 14 years of age in average. Hence, this study assesses the age of the first appearance of the signs of puberty and not the maximum age at which it can develop. Additionally, the integrity of data in this study depends on the parents of children as references for information, on their personal assessment of some signs such as interest in adult behavior as it is a behavioral sign rather than a physical one, and on memory recall as with acne.

Recommendations

As most studies on this topic were conducted in schools, and mostly without proper randomization, a cohort that targets a sample size of girls and boys between 8 and 16-18 years should be conducted for the most accurate determination of pubertal patterns and timing. Further studies should be sure to investigate the development of secondary sexual characteristics in and outside of the Tanner classification, considering plotting the different stages of development according to the Tanner classification and the rest of the sexual characteristics against time. All this is to create a clearer cohort of children’s sexual development that encompasses all signs of puberty.

Supplemental Material

sj-docx-1-gph-10.1177_2333794X241310526 – Supplemental material for Onset and Pattern of Puberty in Apparently Healthy Sudanese Children: A Cross-Sectional Multi-Center Community-Based Study

Supplemental material, sj-docx-1-gph-10.1177_2333794X241310526 for Onset and Pattern of Puberty in Apparently Healthy Sudanese Children: A Cross-Sectional Multi-Center Community-Based Study by Lina Hemmeda, Omer A. Mohammed, Ammar Elgadi, Malaz Tarig Abdalla Mohamed, Nifal S. Ariss, Omaima Abdel Majeed Mohamed Salih and Khabab Abbasher Hussien Mohamed Ahmed in Global Pediatric Health

Footnotes

Author Contributions

L.H.,O.A.M.,A.E.,M.T.A.M.,N.S.A.,O.A.M.M.S. and K.A.H.M.A. made a significant contribution to the work reported,whether that is in the conception,study design,execution,acquisition of data,analysis,and interpretation,or all these areas;took part in drafting,revising,or critically reviewing the article;gave final approval. K.A.H.M.A. supervised,revised and edited the study.

All authors made a significant contribution to the work reported,whether that is in the conception,study design,execution,acquisition of data,analysis and interpretation,or in all these areas;took part in drafting,revising or critically reviewing the article;gave final approval of the version to be published;have agreed on the journal to which the article has been submitted;and agree to be accountable for all aspects of the work.

Authors’ Consent for Publication

All authors gave their consent to publish this manuscript.

Availability of data and materials

The data that supports the findings of this study is available with the corresponding author upon reasonable request.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research,authorship,and/or publication of this article.

Funding

The author(s) received no financial support for the research,authorship,and/or publication of this article.

Ethical approval and consent to participate

We obtained approval from the ethics committee of the Ministry of Health in Khartoum,Sudan.

Prior to the commencement of this study,ethical approval to conduct this study was obtained from the ethical committee of Sudan’s Medical Specializations Board. We confirm that all methods were carried out according to relevant research ethics guidelines and regulations. Data was collected after informed consent from all participants and the participants were assured of the confidentiality of all obtained information. The data from this research was managed only by the research team.

Participants’ Consents

Each participant’s caregiver gave written consent to participate.

ORCID iD

Khabab Abbasher Hussien Mohamed Ahmed

Supplemental Material

Supplemental material for this article is available online.

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