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Received: 26 November 2019 Revised: 10 January 2020 Accepted: 19 January 2020 DOI: 10.1111/obr.13005 PEDIATRICS/PHYSIOLOGY Adipokines: A gear shift in puberty Desirée Nieuwenhuis | Natàlia Pujol-Gualdo Amanda J. Kiliaan Department of Anatomy, Radboud university medical center, Donders Institute for Brain, Cognition and Behaviour, Preclinical Imaging Center PRIME, Nijmegen, The Netherlands Correspondence Amanda J. Kiliaan, PhD, Associate Professor, Department of Anatomy, Donders Institute for Brain, Cognition, and Behaviour, Preclinical Imaging Center PRIME, Radboud university medical center, 6500 HB Nijmegen, Geert Grooteplein 21N 6525 EZ Nijmegen, The Netherlands. Email: amanda.kiliaan@radboudumc.nl Funding information Europees Fonds voor Regionale Ontwikkeling (EFRO), Grant/Award Number: BriteN 2016 1 | INTRODUCTION The prevalence of obesity in adolescents and children is increasing in | Ilse A.C. Arnoldussen | Summary In this review, we discuss the role of adipokines in the onset of puberty in children with obesity during adrenarche and gonadarche and provide a clear and detailed overview of the biological processes of two major players, leptin and adiponectin. Adipokines, especially leptin and adiponectin, seem to induce an early onset of puberty in girls and boys with obesity by affecting the hypothalamic-pituitary- gonadal (HPG) axis. Moreover, adipokines and their receptors are expressed in the gonads, suggesting a role in sexual maturation and reproduction. All in all, adipokines may be a clue in understanding mechanisms underlying the onset of puberty in child- hood obesity and puberty onset variability. KEYWORDS adipokines, obesity, puberty 1,2 the age of 5 years were overweight or were with obesity in 2016, and 3 Obesity is defined by an excessive accumulation of white adipose tissue (WAT), and it is often indicated by a body mass index (BMI) 4 above 30. Two main types of adipose tissue were described: WAT and brown adipose tissue (BAT), which differ in morphology and func- 5-7 Ilse A.C. Arnoldussen and Amanda J. Kiliaan contributed equally to this work. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Obesity Reviews published by John Wiley & Sons Ltd on behalf of World Obesity Federation Obesity Reviews. 2020;21:e13005. wileyonlinelibrary.com/journal/obr 1 of 10 https://doi.org/10.1111/obr.13005 alarming rates. Specifically, worldwide, 41 million children below this number is expected to increase to 70 million in 2025. obesity is associated with various severe health complications, includ- ing increased risk of diabetes mellitus type 2, hypertension, heart dis- eases, and disturbances in sex hormone levels. 5,6 and mitochondria and plays a role in thermogenesis. Adipocytes in tion. BAT consists of adipocytes containing multiple lipid droplets WAT contain only a few mitochondria and a single lipid droplet. Adipose tissue has several functions including the storage of energy, thermogenesis, and the production and secretion of adipokines Generally, two physiological processes, adrenarche and gonadarche, 11,24 Childhood 5,7,8 a key role in puberty onset. Puberty is known as a period through which the body changes physically, being a physiological process resulting in the maturation of children, i.e. they develop sexual characteristics and obtain reproduc- 9,11 Adipokines are involved in a number of physiological processes including blood pressure, metabo- lism, glucose, and vascular homeostasis and may play amongst others 8-10 (hormones, cytokines, and peptides). tive functions. between obesity and puberty,2,12-23 the biological mechanisms under- lying obesity and puberty onset remain unclear. Hereafter, we review in detail the role of adipokines in the onset of puberty in childhood obesity. Although many studies have shown associations 2 | INITIATION OF PUBERTY PHYSIOLOGICAL PROCESSES IN THE interact to regulate the onset of puberty. During adrenarche, the adrenal cortex secretes steroid hormones (including 2 of 10 NIEUWENHUIS ET AL. androstenedione, dehydroepiandrosterone, dehydroepiandrosterone sulfate (DHEAS), androstenedione, and cortisol), insulin-like growth factor, and growth hormone, which contribute to the pubertal insights on new genetic loci (e.g. melanocortin-4 receptor, mitochon- drial carrier 2, and mitogen-activated protein kinase 13) and on sev- eral pathways that regulate the timing of puberty; however, it partly 34 9,24,25 Both adrenarche and gonadarche are involved in the development growth spurt, body odor, skin oiliness, and skeletal maturation. explains puberty timing variation. Thereby, defining the role of 25 adipokines is of importance in elucidating the variability in puberty as the expression of adipokines is sex-specific and is altered with body composition, adiposity, and during growth spurts. Moreover, adipokines and their receptors are expressed in gonads and several brain regions suggesting involvement in the onset of puberty and sex- ual maturation. Lastly, adipokines interfere in processes regulating timing and duration of puberty, for instance in the HPA and HPG axes which are both key players during adrenarche and gonadarche. Involvement of adipokines in the onset of puberty and specifically in individuals with obesity will be further reviewed in the next 2,24 3 | Puberty onset in girls is assessed using different markers, such as thelarche (breast development), menarche (the start of of pubic hair. pituitary-gonadal (HPG) axis is activated,2,26 and several hormones have been identified to participate in the activation of the HPG axis During gonadarche (Figure 1), the hypothalamic- 2,27 Kisspeptin, neurokinin B, and dynorphin are released by specialized including kisspeptin, neurokinin B, dynorphin, leptin, and ghrelin. 28 key regulator of the pulsatile secretion of gonadotropin releasing neurons, the KNDy neurons in the hypothalamus. Kisspeptin is a 29,30 B stimulates, and dynorphin inhibits the release of kisspeptin, which hormone (GnRH) from the hypothalamus. In addition, neurokinin implies that both coordinate a pulsatile release of kisspeptin. 31 Sub- sections. sequently, the activated HPG axis induces the pituitary gland to secrete luteinising hormone (LH) and follicle stimulating hormone (FSH). As a result, gametogenesis occurs, and the gonads will release sex hormones. Consequently, secondary sex characteristics develop including breast development in girls and an increased testicular vol- 2,26,32 is possibly due to differences in levels of body fat, hypothalamic-pitui- THE ONSET OF PUBERTY IN GIRLS ume in boys. The age at puberty onset varies greatly among individuals, which 19 35 menstruation), and pubic hair development. 33 genome-wide association studies have provided important new tary-adrenal (HPA) axis activity, and genetic background. Recent The average age of However, this age differs between cultures and ethnicities, and since 1980, age at menarche is girls at start of menarche is 12.4 years. 36 significantly decreasing. 36-39 F I G U R E 1 Hormonal regulation in the initiation of puberty in boys and girls. The secretion of kisspeptin, neurokinin B, and dynorphin from KNDy neurons initiate the release of gonadotropin releasing hormone (GnRH) from the hypothalamus. This activates the pituitary gland to produce and secrete luteinising hormone (LH) and follicle stimulating hormone (FSH), which in turn stimulate the gonads to produce estrogen and testosterone in girls and boys, respectively 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License NIEUWENHUIS ET AL. 3 of 10 T A B L E 1 Summary of included studies Authors Year Country Study Design Primary Outcome Sex Sample Size (n) Age (y) Data Collection Lian et al21 2019 China Cross-sectional Puberty starts earlier in Chinese Han girls with obesity compared with Chinese Han girls with normal weight. Girls 2996 9-19 2012 and 2013 Biro et al12 Lazzeri et al20 2018 USA 2018 Italy Longitudinal Cross-sectional Body mass index had a greater effect on age at menarche than did race and ethnicity. Girls 946 6-16 2004-2014 Li et al23 2018 China Longitudinal For both, boys and girls, a higher BMI (ie, overweight and obese) is associated with earlier onset of puberty Girls Girls Boys Girls 542 Deng et al22 Flom et al15 2017 China Cross-sectional Increased BMI is associated with early timing spermarche and menarche. Boys Girls Girls 1278258 9-15 2005-2012 He et al24 Holmgren et al17 2017 China 2017 Sweden Cross-sectional Longitudinal Onset of puberty is not related to obesity in boys. Boys Boys Girls Girls 782 7-17 972 929 5839 Kelly et al19 2017 UK 2016 Brazil 2016 USA Longitudinal prospective cohort Higher BMI in girls is associated with the onset of menstruation at an earlier age. 11 10-18 11-17 Barcellos Gemelli et al25 Cross-sectional Longitudinal Excess weight is associated with early age of menarche. Girls 727 2014 2003-2009 Glass et al16 Lee et al26 In girls, but not in boys, greater adiposity is associated with the earlier onset of puberty. Boys Girls 135 Cabrera et al27 Leonibus et al14 2014 USA 2013 Italy Cross-sectional Longitudinal Thelarche occurred earlier than recently reported, while age of menarche remained unchanged. Girls 610 3-17.9 2007 2005-2012 Currie et al13 2012 Europe, USA, Canada Cross-sectional Overweight/obesity during childhood predicts the early onset of puberty in girls. Girls 20410 11, 13, 15 2005-2006 2017 USA Prospective birth cohort Overweight/obese status at the age of 7 ye was associated with increased risk of early menarche 788 From birth to menarche occurred Pregnancies 1959-1966 2016 USA Cross-sectional Boys with overweight enter puberty earlier compared with boys with normal weight or obesity, while puberty starts later in boys with obesity compared with boys with normal weight and overweight. Boys 3872 6-16 2005-2010 Overweight during childhood shows a relation with the early onset of puberty in girls. 6535 4259 695 11 15 5.8-12.2 2009/2010 2013/2014 2014-2017 Higher BMI during childhood is associated with early puberty. 2008 and 2009 2000-2002 Obesity during childhood is related to the earlier onset of puberty. Boys Girls 84 123 71 (Continues) 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 4 of 10 NIEUWENHUIS ET AL. 3.1 | Fat storage For the initiation of puberty, the timing of stimulation and/or inhibi- tion of different hormones is important, and additionally, a certain amount and distribution of body fat is needed in order to start menar- che, which emphasizes the importance of body fat. From an evolution- ary point of view, body fat increases in mammalian females during puberty onset, and it highlights the need to guarantee a healthy preg- 40 women with anorexia nervosa. particularly body fat localized predominantly on the gluteofemoral fat depots, is profoundly associated with start of menarche, more than nancy, offspring, and maternal survival. fat, sex-hormones, and neuroendocrine alterations can evolve in men- strual dysfunction, for instance, in women with severe obesity or in 41-43 44-46 to gluteofemoral fat depots suggesting that leptin may convey infor- amount of total body fat. mation on body fat distribution to the hypothalamus during puberty. An improper level of body Importantly, body fat distribution, Blood leptin levels are strongly related 45 3.2 | HPG axis The HPG axis is activated by the release of kisspeptin resulting in the release of GnRH from the hypothalamus, and LH and FSH from the pituitary gland. In girls, FSH is involved in the development of the folli- cles in the ovaries, and it promotes the secretion of estrogen. LH stim- ulates the production of androgen hormones and induces ovulation 48 9,47 the release of kisspeptin and neurokinin B, and kisspeptin thereby (Figure 1). The secretion of estrogen has an inhibitory effect on inhibits the GnRH release from the hypothalamus. pattern of GnRH is important for the regulation of the menstrual cycle. This roughly 28-day-cycle comprises several phases, including the follicular phase and luteal phase. During the follicular phase, increasing levels of FSH stimulate the maturation of follicles and the production of estrogen from the ovaries. This in turn inhibits the release of FSH from the pituitary gland. A high level of estrogen will induce the production of LH by the pituitary gland, resulting in ovula- tion. The matured follicle secretes progesterone thereby inhibiting the release of GnRH. When the corpus luteum is demolished, there is less 48 3.3 | Adipokines According to results from studies reported in Table 1, girls with obe- sity enter puberty earlier compared with girls with normal higher leptin concentrations inhibit the intake of food and increases inhibition of GnRH. As a consequence, the cycle will start again. whole process, starting from the activated HPG axis, results in the development of the secondary sex characteristics in girls including 9,47 thelarche and menarche. 13,14,16-23,49-51 weight. these girls might be found in the secretion of adipokines. For instance, leptin is positively associated with the amount of body fat. Generally, energy expenditure. 9,52-54 An explanation for the early onset of puberty in The expression This TABLE 1 (Continued) Authors Year Country Study Design Primary Outcome Sample Sex Size (n) Age (y) Data Collection Herman-Giddens et al28 2012 USA Cross-sectional Observed mean ages of beginning genital and pubic hair growth and early testicular volumes were earlier than in past studies, depending on the characteristic and race/ethnicity. Boys 4131 6-16 2005-2010 Sorensen et al29 Aksglaede et al30 2010 2009 Denmark Denmark Cross-sectional/longitudinal Longitudinal Puberty onset at earlier ages was associated with an increased BMI in boys. Boys 1528 5.8-19.9 1991-1993/2006-2008 1930-1969 Juul et al31 Ribeiro et al32 2007 2006 Denmark Portugal Retrospective cohort Cross-sectional Higher BMI is associated with early voice break. 11-15 10-15 1990-1999 Kaplowitz et al18 Abbreviation: BMI, body mass USA Cross-sectional The early onset of puberty in Caucasian girls is likely related to an increased BMI. 5-12 1992-1993 2001 index. The higher BMI in boys and girls at 7 y of age, the earlier they enter puberty. Boys 21 612 Girls 135 223 Boys 463 Boys 382 Girls 437 Girls 10 750 Early sexual maturation in boys and girls is associated with overweight. 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License NIEUWENHUIS ET AL. 5 of 10 Leptin may possibly play a role in adrenarche as its plasma level increases with higher levels of body fat and as it can modulate both girls. 33 ing adrenarche. In coherence, in children with obesity, the androgen These findings suggested that lower reproductive status was associated with higher total adiponectin concentrations and that a higher reproductive status was related to higher HMW adiponectin the HPA and HPG axes. These axes are functionally integrated dur- DHEAS was positively associated with leptin levels. Nevertheless, concentrations in girls. In addition, individuals with obesity often another study showed that enhanced adrenal androgen secretion in girls with premature adrenarche was not explained by leptin or BMI 55 ated with androgen levels in girls ; however, it was not related to levels. and IL-6. TNF-α alters, and IL-6 inhibits the expression of 56 8 In addition, the adipokine adiponectin was negatively associ- 57 differences of adiponectin seem to develop during the progression of 56 adiponectin (Figure 2). Thereby, a low level of total adiponectin and/or high levels of inflammatory cytokines in individuals with obe- sity can promote the onset of puberty. Many more adipokines are secreted by WAT including omentin, 52,65-67 9,36,62,68 adrenarche in girls with Prader-Willi syndrome. Interestingly, sex puberty. adrenarche; however, both are not required factors. Thus, leptin and adiponectin might be able to influence In gonadarche, leptin can stimulate the secretion of kisspeptin, and subsequently activation of the HPG axis, which eventually increases the expression of estrogen and androstenedione in the ova- 58 2,60 65-67 The expression of these ries (Figure 2). Ob gene in WAT, resulting in the synthesis and secretion of leptin. Thus, high levels of leptin promote onset of puberty in girls via secre- tion of kisspeptin, and estrogen stimulates leptin secretion addition- ally. Moreover, adiponectin can affect the HPG axis due to the expression of adiponectin receptors in the hypothalamus, pituitary In return, estrogen stimulates the expression of the 59 gland, and gonads. onset as it inhibits the secretion of kisspeptin and GnRH in the hypo- thalamus and the release of GH and LH in the pituitary gland, and 2,60-62 52,60 63 girls with central precocious puberty (CPP). Moreover, total adiponectin had negative correlations with progression of puberty in girls (defined by Tanner stages), whereas HMW adiponectin had FIGURE 2 Adipokinesaffectingthe initiation of puberty in girls. Leptin stimulates the release of kisspeptin in KNDy neurons, which activates the hypothalamus to produce gonadotropin releasing hormone (GnRH). In response to the release of GnRH, the pituitary gland secretes follicle stimulating hormone (FSH) and luteinising hormone (LH), which stimulates the ovaries to release estrogen resulting in the formation of secondary sex characteristics in girls. Estrogen stimulates the production of leptin. Adiponectin inhibits GnRH release resulting in reduced levels of GnRH and thereby a delayed onset of puberty. TNF- α and IL-6 inhibit the production of adiponectin and therefore stimulate the onset of puberty In detail, adiponectin is a regulator of puberty thereby inhibiting the onset of puberty (Figure 2). with obesity often have low levels of adiponectin. et al. showed that total adiponectin was significantly lower, whereas high molecular weight (HMW) adiponectin was significantly higher in ment. 55 63 develop a chronic low-grade inflammatory state, which can be indi- cated by a high level of circulating inflammatory cytokines like TNF-α 64 Individuals Sitticharoon positive associations with LH levels and the progression of puberty in 63 visfatin, resistin, and chemerin. and visfatin are expressed in the ovaries. adipokines in the ovaries suggests a role within the reproductive sys- tem; however, the exact biological processes have to be examined. Thus, specifically leptin, adiponectin, and inflammatory cytokines pro- duced by WAT could be permissive key players during an early onset of puberty in girls with obesity. As an exception, HMW adiponectin seems to have a stimulatory effect on peripheral repro- ductive function as HMW is not able to cross the blood brain 63 barrier. 4 | Markers that are used to assess puberty onset in boys are THE ONSET OF PUBERTY IN BOYS spermarche, voice break, testicular volume, and pubic hair develop- 35 spermarche develop in the early stages of puberty onset, voice In women, omentin, chemerin, While pubic hair development, larger testicular volume, and 69 testicular volume increases, which occurs at an average age of break usually appears in later stages of puberty. Generally, first 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 6 of 10 NIEUWENHUIS ET AL. 11.9 years, followed by the development of pubic hair at 12.2 years of average, and lastly, boys experience spermarche around an aver- 55 related with leptin levels. Thereby, leptin plausibly has a minor impact in adrenarche in boys. Since leptin receptors are found in the hypothalamus, pituitary gland, and testes, they might be involved in the onset of puberty by affecting the HPG axis during gonadarche. Leptin stimulates the release of kisspeptin and GnRH, and as a consequence, it accelerates the onset of puberty (Table 1, Figure 3). In contrast, adiponectin inhibits the secretion of GnRH, GH, LH, and FSH therewith delaying the onset of puberty. However, adiponectin levels are generally lower in men compared with women and even lower in men with obe- age age of 13.4 years. 70 4.1 | Fat storage Many aspects of the reproductive physiology are energetically demanding,71 and therefore, an adequate energy level is necessary. In boys, a dynamic change in body composition occurs around the age of 10 to 13 years, in which they gain approximately 40% of sity. culating inflammatory cytokines. levels can stimulate the HPG axis and therewith an early onset of puberty in boys. Nevertheless, leptin can inhibit the production of tes- 72 mostly consisting of lean mass, which causes exhaustion of most of fat. Subsequently, a growth spurt follows in which they gain tissue 72 in boys, an adequate amount of body fat is important in the onset of their body fat. These alterations in amount of body fat indicate that 4.2 | Puberty in boys is initiated by the release of kisspeptin. As mentioned before, this activates the HPG axis, resulting in the release of GnRH from the hypothalamus, and consequently the release of LH and FSH 9,74 puberty. tosterone from the testes, to estrogen (Figure 3). of the development of secondary sex characteristics in boys. Additionally, leptin can affect fertility in men as it can modulate the nutritional support of spermatogenesis, and moreover, dysfunction of spermatogenesis is associated with an increased leptin level and 73 58 2,60-62 HPG axis from the pituitary gland (Figure 1). and LH stimulates the secretion of testosterone from the testes, which inhibits the release of kisspeptin from the KNDy neurons and 9,48 in men, the release of kisspeptin is more consistent, causing a con- 29,48 subsequently GnRH from the hypothalamus. receptors expressed on KNDy neurons. In humans, KNDy neurons Contrarily to women, LH-induced testosterone levels lead to the stant release of LH. development of secondary sex characteristics in boys. differences between sexes in kisspeptin release are related to a sex- specific and sex steroid-dependent kisspeptin system as estrogen and progesterone modulate kisspeptin activity through the sex-steroid 48 in the infundibular nucleus are involved in negative and positive sex- 48 tal exposure to sex steroids and result in sex-specific differences in steroid feedbacks. kisspeptin release. These sexual dimorphisms are induced by perina- 75,76 4.3 | Adipokines The association between obesity and puberty onset in boys is rather controversial compared with findings in girls. Most studies reported an early onset of puberty in boys associated with increased ate adipose tissue from actual breast tissue. stages are more difficult to assess than female stages as boys lack a more determined marker such as menarche. Thirdly, puberty onset can be indicated by the activation of the HPG axis, and the presence of these secondary sex characteristics is the result of hormonal 2 14,17,22,23,50,51,77,78 BMI, 20,49 all while others reported no associations at Current markers used 79 16,80 or a delayed onset of puberty (Table 1). The presence of excessive adipose tissue can be involved in puberty onset in boys as the secretion of adipokines can modulate both adrenarche and gonadarche. Leptin can affect adrenarche by modulating both the HPG and HPA axes,33 and moreover, androgen levels were positively 55 nal androgen secretion in boys with premature adrenarche was not associated with plasma leptin levels. Nevertheless, enhanced adre- 9 In more detail, 61,62 adiponectin, and individuals with obesity often have high levels of cir- Moreover, inflammatory cytokines, TNF-α, and IL-6, inhibit expression of the leptin receptor in the testis. FSH induces spermatogenesis, too. function and role still have to be examined. 64 High leptin and low adiponectin and fat tissue can convert testosterone Both processes might result in the delay 29,61,79 81,82 In men, other adipokines like chemerin are found in the gonads 65 Thus, particularly high leptin and low adiponectin levels stimulate the HPG axis and thereby accelerate the onset of puberty in boys. Additionally, leptin can dysregulate the development of secondary sex characteristics and spermatogenesis by affecting testosterone levels and nutritional sup- port of spermatogenesis. 5 | LIMITATIONS AND FUTURE RESEARCH DIRECTIONS Even though multiple epidemiological studies have shown the link between puberty onset and obesity, there are some important limita- tions. Firstly, determining both the onset and stage of puberty is rather difficult. For instance, assessing the stage of breast develop- ment in girls with obesity is complicated as clinicians should differenti- 2 changes in response to the activated HPG axis. to determine the onset of puberty refer to secondary sex characteris- tics, such as testicular volume in boys and breast development in girls. A more accurate measurement of puberty onset would be to combine secondary sex characteristics with plasma or serum hormone level measurements such as LH, FSH, adipokines, e.g. leptin. Thereby, differences in puberty measurements could explain variations in the age of puberty onset between boys and girls within different Thereby, resistin is expressed in the testes of rats, but its exact 83 Secondly, male pubertal 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License NIEUWENHUIS ET AL. 7 of 10 FIGURE 3 Adipokines affecting the initiation of puberty in boys. Leptin activates kisspeptin secretion in KNDy neurons, this activates the production of gonadotropin releasing hormone (GnRH) from the hypothalamus. GnRH stimulates the pituitary gland to secrete follicle stimulating hormone (FSH) and luteinising hormone (LH), activating the production of testosterone from the testes allowing the development of secondary sex characteristics. Leptin also inhibits the production of testosterone, which may cause a delayed onset of puberty. Adiponectin inhibits GnRH release. Low levels of adiponectin, as a result of TNF-α and IL-6 expression, lead to a reduced inhibition of GnRH. In response to GnRH release, the pituitary gland will secrete FSH and LH, and the testes will produce testosterone resulting in the development of secondary sex characteristics in boys countries, and In addition, the inclusion of a of puberty. ferent time points is complicated, as subjects examined several decades ago presented pronounced differences concerning lifestyle patterns such as nutrition and exercise habits. Lastly, obesity or over- weight is often determined by BMI, a classification based on weight and height measurements. Additionally, it is important that all studies studies or across continents, ethnicities proper age range (8-16 years) is important when assessing the onset (Figure 4). 12-15,17,20-23,49,77-79,84,85 30,47 Furthermore, comparison between studies from dif- 86 Specifically in children, BMI is often dependent on age and growth use the same anthropometric standards and sex-specific cut-offs. 13,14,16-23,49-51,77-80 fat and would represent a more accurate measurement in its regard. Based on this review, several suggestions can be made for further research. Firstly, the roles of adipokines like resistin, chemerin, visfatin, and omentin in puberty onset, fertility, and sexual maturation should be examined in detail. Secondly, future research examining the onset of puberty should combine indicators of puberty onset (e.g. breast development or testicular volume) with plasma or serum hor- mone measurements such as LH, FSH, sex-steroids, adipokines (e.g. spurts. ment in case of growth spurts. distribution of body fat should be taken into account in determining puberty and obesity in children. For instance, the body adiposity index (BAI), which was introduced in 2011 by Bergman et al.,87 uses hip cir- cumference and height in order to estimate the percentage of body 87 Thereby, BMI is a less accurate measure- F I G U R E 4 87,88 Therefore, both percentage and Average age of puberty onset in Europe, China, and the United States according to several studies from Table 1. Age of puberty onset ranges from 8.47 to 13.33 years in girls and from 8.63 leptin), and body fat distribution (e.g. BAI,87 waist-hip ratio's and/or dual-energy X-ray absorptiometry (DXA)2). Additionally, defining con- sistent and general measurements of puberty in both boys and girls, combined with a proper age range (8-16 years), would facilitate the comparisons between different studies and their results. 12-15, 17, 20-23, 25-29, 31 to 13.7 years in boys. included if average age of markers used to assess puberty was not reported. Pink: girls. Blue: boys Studies (Table 1) were not 39, 56 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 8 of 10 NIEUWENHUIS ET AL. 6 | CONCLUSION In conclusion, epidemiological data regarding obesity and puberty onset in girls show similar outcomes as adiposity results in the early onset of puberty in girls. 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BMC Womens Health. 2018;18(1):168-174. thereby an early onset of obesity. leptin can inhibit the production of testosterone in boys and subse- quently inhibit the development of secondary sex characteristics affecting spermatogenesis. for other adipokines, like resistin and omentin, are present in the testes and ovaries suggesting a role in puberty or reproduction; 58, 71 however, their plausible function is still unknown. that adipokines may be key regulators in an early onset of puberty in both girls and boys with obesity, specifically by affecting the HPG axis during gonadarche. Future research should focus on assessing puberty onset by measuring consistent puberty markers and determine the percentage of body fat and its distribution and adipokines and hormone serum levels particularly involved in the HPG axis. CONFLICTS OF INTEREST The authors declare no conflict of interest. FUNDING INFORMATION This research was funded by Europees Fonds voor Regionale Ontwikkeling (EFRO), project BriteN 2016. ORCID Ilse A.C. Arnoldussen Amanda J. Kiliaan https://orcid.org/0000-0002-7395-5284 https://orcid.org/0000-0002-2158-6210 13, 14, 16-26, 29-32 Furthermore, several receptors Nevertheless, We conclude Search strategy We searched PubMed for articles published before Novem- ber 15th, 2019 using relevant keywords, including ‘onset of puberty and adiposity/obesity’, ‘onset of puberty’, ‘children with obesity’, ‘adipose tissue’, ‘childhood obesity’, ‘adiposity’, ‘obesity’, ‘adipokine(s)’, ‘HPG axis’, ‘adipokines ovary/ova- ries’, or ‘adipokines testes’, either alone or in combination. Selection criteria used were English language, longitudinal or cross-sectional studies assessing the onset of puberty, including menarche, thelarche, spermarche, or voice break, combined with high BMI or obesity/adiposity, and articles assessing or reviewing adipokines and its effects on the reproductive system. 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License NIEUWENHUIS ET AL. 9 of 10 21. Lian Q, Mao Y, Luo S, et al. Puberty timing associated with obesity and central obesity in Chinese Han girls. BMC Pediatr. 2019; 19(1):1-7. 22. Deng Y, Liang J, Zong Y, et al. Timing of spermarche and menarche among urban students in Guangzhou, China: trends from 2005 to 2012 and association with Obesity. 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Obesity Reviews. 2020;21:e13005. https://doi.org/ 10.1111/obr.13005 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are goverCreate me a multiple choice test questions with 4 options on the following topic:Consumer Education for Different Audience 1. Children and Youth: - Focus: Building foundational knowledge about basic consumer concepts, making safe choices, understanding money and value, and recognizing scams and unsafe situations. 2. Teens and Young Adults: - Focus: Building financial literacy, responsible debt management, understanding contracts and agreements, responsible technology use, online safety, and consumer rights. 3. Working Adults and Families: - Focus: Managing budgets, making informed purchasing decisions, understanding credit and debt, finding consumer protection resources, and navigating complex financial products (mortgages, insurance, investments). 4. Seniors: - Focus: Protecting themselves from scams and fraud, understanding common consumer issues like telemarketing, identity theft, and online scams, managing medications and healthcare costs, and accessing community resources. 5. Special Populations: - Focus: Adapting consumer education programs to the specific needs of people with disabilities, immigrants, refugees, and other marginalized communities. 6. Business and Industry:- Focus: Understanding ethical marketing practices, complying with consumer protection laws, and providing clear and accurate information to consumers. 7. Policymakers and Regulators: - Focus: Understanding consumer needs, developing effective consumer protection laws, enforcing regulations, and ensuring a fair and competitive marketplace. Adapting consumer education programs for children, teens, and seniors requires tailoring content and delivery methods to their unique needs and learning styles. Children (Ages 5-12): - Understanding the concept of money: Teaching children about saving, spending, and the value of money. - Developing basic budgeting skills: Helping children learn to make choices about how to spend their allowance or pocket money. EFFECTIVE STRATEGIES •Focus on basic concepts: Introduce core concepts like saving, spending, and budgeting in a fun and engaging way. Use simple language and relatable examples. •Real-life scenarios: Use age-appropriate scenarios to illustrate financial concepts, like buying toys or snacks. •Parental involvement: Encourage parent participation and provide resources to help them reinforce lessons at home. Teens (Ages 13-18): - Building budgeting and financial planning skills: Teaching teens how to manage their money, set financial goals, and plan for the future. - Navigating the digital marketplace: Equipping teens with the knowledge and skills to make safe and informed online purchases, understand digital marketing, and protect themselves from scams. EFFECTIVE STRATEGIES • Practical skills: Focus on skills relevant to teens, like managing money for social activities, saving for college, and understanding credit cards. • Digital literacy: Address the growing influence of online shopping, social media advertising, and financial scams. • Real-world applications: Connect financial concepts to real-life decisions teens make, like choosing a part-time job or making purchases online. Seniors (Ages 65+) - Managing retirement savings and healthcare costs: Providing information and resources on retirement planning, Medicare and Medicaid, and other healthcare options. - Navigating the digital world: Offering technology training and resources to help seniors access online services and information safely and securely. EFFECTIVE STRATEGIES • Addressing specific concerns: Focus on topics relevant to senior citizens, like retirement planning, managing healthcare expenses, and avoiding scams. • Clear and concise communication: Use simple language and visual aids to ensure easy understanding. • Social interaction: Create opportunities for seniors to share experiences and learn from each other. Teaching Financial Literacy in school and Communities In Schools: Curriculum Integration: Financial literacy concepts can be seamlessly integrated into existing subjects, making learning more relevant and engaging. - Math: Budgeting exercises, calculating interest rates, analyzing financial data, and understanding compound interest are all natural applications of math skills. - Social Studies: Exploring the history of money, financial institutions, economic systems, and the impact of financial decisions on society provide valuable context. - Economics: Discussions about supply and demand, inflation, investment, and the role of consumers in the economy enhance financial literacy. Dedicated Courses: Offering elective courses or workshops specifically focused on personal finance provides deeper dives into crucial topics. - Personal Finance: Cover budgeting, saving, investing, credit, debt management, and insurance. - Entrepreneurship: Introduce concepts like business planning, marketing, financial forecasting, and managing cash flow. In Communities: Community Centers and Libraries: Workshops, seminars, and classes tailored to adults and families provide accessible learning opportunities. - Financial Planning: Cover budgeting, retirement planning, debt management, and estate planning. - Homeownership: Provide guidance on buying, selling, and maintaining a home. - Consumer Protection: Educate individuals about their rights and how to avoid scams. Partnerships with Financial Institutions: Collaborations with banks, credit unions, and financial advisors offer valuable resources, workshops, and financial literacy programs. Consumer Education for Low-Income and Vulnerable Populations Low-income refers to individuals or households with limited financial resources, typically below a certain threshold. Low-income individuals may face challenges like: 1. Limited education and job opportunities 2. Poor living conditions and housing 3. Food insecurity and malnutrition Causes of low income: 1. Unemployment or underemployment 2. Low-paying jobs or minimum wage 3. Limited education or skills 4. Single parenthood or large family size Vulnerable population'' is a term that is used to describe a group of people who possess some sort of disadvantage. elderly people, people with low incomes, homeless people, people in prison, migrant workers, pregnant women, Family Consumer Education: Managing Household Finances and Resources Financial literacy is the ability to understand and manage personal finances effectively. 1. Debt Debt is money you spend that isn’t yours. If you borrow money from the bank, use a credit card, or take out a short-term loan, or a payday loan, you are accumulating debt. Good debt is considered money borrowed for things that are absolutely necessary for making a life e.g. a house and for advancing your money-making potential e.g. an education. Bad debt is considered borrowing money or using a credit card to pay for things you don’t need, such as expensive clothes, hi-tech electronics, eating out at restaurants, going on holidays, etc. 2. Saving Saving is an essential part of financial wellness, a secure present, and a happy future. 3. Budgeting Budgeting is the life skill of planning and managing your money. By understanding exactly where your money goes every month, you are empowered to create an actionable plan by which you can spend less, by curtailing those unnecessary expenses and saving more for the things you need and want. 4. Investing Investing is all about creating and growing the wealth you need to enjoy a financially secure and happy future. It’s about putting your money into something that will make you a profit over time, such as property, retirement funds, and unit trusts Integrating Consumer Education into the Home Economics Curriculum. Integrating consumer education into the home economics curriculum can provide students with essential skills for making informed choices about their personal finances, food, clothing, and overall well-being. Here are some strategies and ideas for effectively incorporating consumer education: Financial Literacy Budgeting: Teach students how to create and manage a personal budget, including setting financial goals, tracking expenses, and understanding savings. Saving and Investment: Cover the basics of saving, including different saving accounts, and introduce concepts related to investing. Food and Nutrition Food Label Literacy: Engage students in learning how to read and interpret food labels, including nutrition facts and ingredient lists. Grocery Shopping Skills: Teach students how to compare product costs, understand unit pricing, and make healthy, budget-friendly choices while shopping. Clothing and Textile Education Consumer Choices in Clothing:Discuss factors influencing clothing purchases, such as quality, price, and sustainability. Fashion and Trends: Analyze the impact of marketing and advertising on consumer behavior regarding clothing. Sustainable Purchasing Eco-Friendly Choices: Raise awareness about environmentally friendly products and the importance of sustainability in consumer choices. Project-Based Learning - Assign real-life projects where students must apply their knowledge, such as creating a meal plan within a budget, planning a shopping list based on nutrient needs, or evaluating the cost-effectiveness of different products. Technology Integration - Use technology to teach students about online shopping, price comparison websites, and apps that aid budgeting and financial planning. Collaborative Learning Opportunities - Organize team projects where students work together to solve consumer-related problems, emphasizing teamwork and communication skills. Assessment and Reflection - Incorporate assessments that allow students to reflect on what they have learned about consumer education and how they can apply these skills in their daily lives. Certainly, let's expand on each section in detail so you can learn more from the provided text: # Summary This text aims to explain various aspects related to technology, particularly focusing on a concept known as "Tech Disruption." It explores how technology affects different sectors, outlines the conditions for tech disruption, discusses the industrial revolutions, introduces the laws of disruption, and mentions factors influencing technology choices. ## Concept of Technology **Technology** encompasses a range of elements within organizations. It includes **expertise, equipment, and procedures** used to convert inputs, such as resources or raw materials, into outputs, which can be products or services. This involves various aspects, such as **product design, production techniques, quality assurance measures, human resource development, and management systems**. In essence, technology represents the tools and knowledge used to create and deliver goods or services effectively. ## What is Tech Disruption **Tech Disruption** refers to a phenomenon where smaller companies with limited resources successfully challenge well-established incumbent businesses. This disruption is primarily driven by **technology**, which acts as the catalyst, enabler, or even the sole reason behind the change. The significance of this concept lies in the fact that entrepreneurs must make careful and thoughtful decisions when it comes to adopting and investing in technology. **Why it's Important?** These decisions are crucial because they involve significant investments and will have a substantial impact on a company's ability to create, innovate, and operate its services in a sustainable and cost-effective manner. ## Four Main Impact **Tech Disruption** has four main impacts on businesses and industries: 1. **Shifting Customer Expectations**: As technology evolves, customer expectations change. Companies must adapt to meet these evolving demands to remain competitive. 2. **Enhanced Products Through Data**: Data-driven insights improve the productivity and efficiency of assets, leading to better products and services. 3. **New Partnerships and Collaboration**: Tech disruption encourages companies to form new partnerships and collaborations, recognizing the importance of working together to stay relevant. 4. **Transformation of Operating Models**: Traditional operating models are being transformed into digital models, where technology plays a central role in how businesses operate and deliver value. ## The 11 Macro Sources of Distribution The **11 Macro Sources of Distribution** represent various factors that influence the distribution of resources and opportunities in society. These factors include: 1. **Wealth Distribution**: How wealth is distributed among individuals and entities. 2. **Education**: The availability and quality of education opportunities. 3. **Infrastructure**: The state of infrastructure, such as transportation and communication networks. 4. **Government**: Government policies and regulations that impact resource distribution. 5. **Geopolitics**: Geopolitical factors, such as international relations and conflicts. 6. **Economy**: Economic conditions and trends, including markets and financial systems. 7. **Public Health**: The state of healthcare and public health systems. 8. **Demographics**: Characteristics of the population, such as age and gender. 9. **Environment**: Environmental factors and sustainability concerns. 10. **Media and Telecommunications**: The role of media and communication technologies. 11. **Technology**: Technological advancements and their impact on society. ## When Does Tech Disruption Happen? **Tech Disruption** occurs when specific conditions are met: ### Technology Is Mature Enough - **Technology Accessibility**: Technology must be accessible to a wide range of people and organizations. - **Critical Mass**: It should have reached a critical mass where it can create significant impact. - **Affordability**: Technology must be affordable for businesses to adopt. ### Sector Is Ready For Change - **Tech Infrastructure**: The sector should have the necessary technological infrastructure in place. - **Policy Framework**: A conducive policy framework is essential to support and regulate the use of technology. - **Lack of Disruption**: If the sector is stagnant or facing issues, it becomes ripe for tech disruption. ### Sector + Technology + Timing + Product - **Mature Technology with an Unready Sector**: If technology is mature but the sector is not ready, it can lead to building the wrong product based on incorrect assumptions. - **Unmatured Technology with a Ready Sector**: Conversely, if technology is not matured but the sector is ready, it may take longer to develop the product. ## Ready for Industri 5.0? This section briefly outlines the five industrial revolutions: 1. **Industri 1.0 (1784)**: Marked by mass production assembly lines using electrical power. 2. **Industri 2.0 (1870)**: Introduced mechanization, steam, and water power. 3. **Industri 3.0 (1969)**: Characterized by automated production, computers, IT systems, and robotics. 4. **Industri 4.0 (Present)**: Involves smart factories, autonomous systems, IoT (Internet of Things), and machine learning. 5. **Industri 5.0 (Future)**: Envisions mass customization and cyber-physical cognitive systems. ## Three Laws of Disruption These laws explain the nature of disruption: 1. **Disruption Comes to All**: Disruption is a universal phenomenon; it affects all industries and businesses sooner or later. 2. **Product-Market Fit**: Disruption occurs due to changes in Product-Market Fit, which means aligning a product with its target market effectively. 3. **Methods to Change Product-Market Fit**: To address disruption, a company can change the product, the target market, or influence people's preferences regarding the product. ## The 40% Rule This rule provides a framework for evaluating the fit between a product and its market: - **Value Proposition**: The product should solve customers' problems effectively. - **Channels**: The product should be able to reach customers cost-effectively. - **Monetization**: Customers should be willing to pay for the product. ## PMF Framework: 5 Steps to Product/Market Fit The **PMF (Product/Market Fit) Framework** consists of five steps: 1. **Business Modeling**: Developing a business model that aligns with the market. 2. **Market Validation**: Confirming that there is demand for the product in the market. 3. **Customer Interviews**: Gaining insights from potential customers. 4. **Product Development and Customer Acquisition**: Creating the product and acquiring customers. 5. **Product Analytics**: Using data to determine if the product has achieved Product/Market Fit. ## Factors Determining the Choice of Technology Several factors influence the choice of technology: 1. **Government Policy**: Government regulations and policies can encourage or restrict the adoption of specific technologies. 2. **Available Resources**: The resources, both financial and human, impact the adoption of technology. 3. **Technological Capability**: The organization's technological capabilities influence the choice of technology. 4. **Existing Technological Level**: The current technological state of the industry or organization plays a role. 5. **Institutional Arrangement**: Organizational structures and arrangements affect technology choices. ## Conclusion In conclusion, the text emphasizes the critical role of technology in driving change and disruption in various industries. It highlights the need for informed decision-making when it comes to technology investments, as well as the conditions necessary for tech disruption to occur. Understanding the historical context of industrial revolutions, the laws of disruption, and the factors influencing technology choices is essential in today's fast-paced and tech-driven business environment. Embracing technology disruption is crucial for transforming business models and adapting to evolving market dynamics.President Xi Jinping, who is also general secretary of the Communist Party of China Central Committee and chairman of the Central Military Commission, visits Luoyang Bearing Group Co on Monday afternoon during his inspection of Luoyang, Henan province. During the visit, Xi called for continuous efforts to make the manufacturing industry even stronger to advance Chinese modernization. YAN YAN/XINHUA President Xi Jinping has stressed the importance of keeping businesses, employment, the market and expectations stable in the face of a complex international environment, saying that China will respond to various uncertainties with the certainty of its high-quality development. Xi, who is also general secretary of the Communist Party of China Central Committee and chairman of the Central Military Commission, made the remarks on Tuesday as he wrapped up a two-day fact-finding trip to Central China's Henan province. Speaking to provincial Party and government officials at a work briefing on Tuesday in Zhengzhou, the provincial capital, Xi said that high-quality development is essential to Chinese modernization. Faced with the complex external environment, it is necessary to firm up confidence, unwaveringly manage China's own affairs well, and steadfastly expand high-level opening-up, he said. He also urged Henan, one of the country's economic powerhouses, to further consolidate the foundation of its real economy, and promote the development of new quality productive forces suited to local conditions and led by technological innovation, in order to enhance the capacity of its modern industrial system to support high-quality development. When visiting Luoyang Bearing Group Co in the city of Luoyang on Monday, Xi said: "China has always adhered to the path of developing the real economy. From the past reliance on imported matches, soap and iron, to now becoming the world's largest manufacturing country with the most complete industrial categories, we have taken the right path." As a traditional manufacturing enterprise specializing in bearings, Luoyang Bearing Group's products are widely used in fields such as aerospace, construction machinery, wind power generation, rail transit, port machinery and ships. After learning about the company's efforts to accelerate the development of advanced manufacturing, Xi said that China must continue to strengthen the manufacturing sector, adhere to the principles of building self-reliance and strength, and master core technologies in key fields. "The hope is placed on you," he told the on-site workers. He also called for efforts to strengthen collaboration between industries, universities and research institutes, and cultivate a large number of high-quality talent. Despite internal challenges and increasing external shocks, China's manufacturing industry has withstood pressure and maintained stable growth. In April, the manufacturing sector saw its value-added output climb 6.6 percent year-on-year, with that of equipment manufacturing and high-tech manufacturing up 9.8 percent and 10 percent, respectively, according to data released by the National Bureau of Statistics on Monday. Advanced manufacturing is the high ground in global industrial competition and the main battlefield for technological innovation. Xi has repeatedly emphasized the need to upgrade the country's modernized industrial system, supported by advanced manufacturing. In a resolution adopted at the third plenary session of the 20th CPC Central Committee in July last year, it was clearly stated that China will move faster to advance new industrialization, promote the growth and expansion of advanced manufacturing clusters, and make the manufacturing sector higher-end, smarter and more eco-friendly. On Monday, Xi also visited the White Horse Temple, the first Buddhist temple in China, and the Longmen Grottoes, a UNESCO World Heritage site. Contact the writers at mojingxi@chinadaily.com.cnTechTech 2 - Lesson 13Tech Tools - Technology ReviewTech 4 - Lesson 12