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Narration Through Comparison and Contrast
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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 DesirĂ©e Nieuwenhuis | NatĂ lia 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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Ann Epidemiol. 2017;27(3):187-93.e2. 16. Glass NA, Torner JC, Letuchy EM, et al. The relationship between greater prepubertal adiposity, subsequent age of maturation, and bone strength during adolescence. Journal of bone and mineral research: the official journal of the American Society for Bone and Min- eral Research. 2016;31(7):1455-1465. 17. Holmgren A, Niklasson A, Nierop AF, et al. Pubertal height gain is inversely related to peak BMI in childhood. Pediatr Res. 2017;81(3): 448-454. 18. Kaplowitz PB, Slora EJ, Wasserman RC, Pedlow SE, Herman- Giddens ME. Earlier onset of puberty in girls: relation to increased body mass index and race. Pediatrics. 2001;108(2):347-353. 19. Kelly Y, Zilanawala A, Sacker A, Hiatt R, Viner R. Early puberty in 11-year-old girls: Millennium Cohort Study findings. Arch Dis Child. 2017;102(3):232-237. 20. Lazzeri G, Tosti C, Pammolli A, et al. Overweight and lower age at menarche: evidence from the Italian HBSC cross-sectional survey. 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 âonset of puberty and adiposity/obesityâ, âonset of pubertyâ, âchildren with obesityâ, âadipose tissueâ, âchildhood obesityâ, âadiposityâ, âobesityâ, âadipokine(s)â, âHPG axisâ, âadipokines ovary/ova- riesâ, or âadipokines testesâ, 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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Circulating plasma leptin and IGF-1 levels in girls with premature adrenarche: potential implications of a preliminary study. Horm Metab Res. 2001;33(3):138-143. 34. Cousminer DL, WidĂ©n E, Palmert MR. The genetics of pubertal timing in the general population: recent advances and evidence for sex-spec- ificity. Curr Opin Endocrinol Diabetes Obes. 2016;23(1):57-65. 35. Marshall WA, Tanner JM. Variations in pattern of pubertal changes in girls. Arch Dis Child. 1969;44(235):291-303. 36. Lacroix AE, Whitten R. Physiology. Treasure Island (FL): Menarche. StatPearls. StatPearls Publishing; 2018. 37. McDowell MA, Brody DJ, Hughes JP. Has Age at Menarche Chan- ged? Results from the National Health and Nutrition Examination Sur- vey (NHANES) 1999â2004. J Adolesc Health. 2007;40(3):227-231. 38. de Muinich Keizer SM, Mul D. Trends in pubertal development in Europe. Hum Reprod Update. 2001;7(3):287-291. 39. Talma H, Schönbeck Y, van Dommelen P, Bakker B, van Buuren S, Hirasing RA. Trends in menarcheal age between 1955 and 2009 in the Netherlands. PLoS ONE. 2013;8:e60056-e60056. 40. Kaplan HS, Lancaster JB. An evolutionary and ecological analysis of human fertility, mating patterns, and parental investment. Off- spring: Human fertility behavior in biodemographic perspective. 2003;1: 170-223. 41. Mitan LA. Menstrual dysfunction in anorexia nervosa. J Pediatr Adolesc Gynecol. 2004;17(2):81-85. 42. Xu H, Li P-H, Barrow TM, et al. Obesity as an effect modifier of the association between menstrual abnormalities and hypertension in young adult women: Results from Project ELEFANT. PLoS ONE. 2018; 13(11):e0207929-e0207929. 43. Tauqeer Z, Gomez G, Stanford FC. Obesity in women: insights for the clinician. J Womens Health (Larchmt). 2018;27(4):444-457. 44. de Ridder CM, Thijssen JH, Bruning PF, Van den Brande JL, Zonderland ML, Erich WB. Body fat mass, body fat distribution, and pubertal development: a longitudinal study of physical and hormonal sexual maturation of girls. J Clin Endocrinol Metab. 1992;75(2): 442-446. 45. Lassek W, Gaulin S. Brief communication: menarche is related to fat distribution. Am J Phys Anthropol. 2007;133(4):1147-1151. 46. Loomba-Albrecht LA, Styne DM. Effect of puberty on body composi- tion. Curr Opin Endocrinol Diabetes Obes. 2009;16:10-15. 47. Simonneaux V, Bahougne T. A multi-oscillatory circadian system times female reproduction. Front Endocrinol. 2015;6:1-15. 48. Marques P, Skorupskaite K, George JT, Anderson RA. Physiology of GNRH and gonadotropin secretion. In: Feingold KR, Anawalt B, Boyce A, et al., eds. Endotext. Endotext.org: South Dartmouth (MA); 2000. 49. Barcellos Gemelli IF, Farias EDS, Souza OF. Age at menarche and its association with excess weight and body fat percentage in girls in the Southwestern Region of the Brazilian Amazon. J Pediatr Adolesc Gynecol. 2016;29(5):482-488. 50. Aksglaede L, Juul A, Olsen LW, Sorensen TI. Age at puberty and the emerging obesity epidemic. PLoS ONE. 2009;4:1-6, e8450. 51. Ribeiro J, Santos P, Duarte J, Mota J. Association between over- weight and early sexual maturation in Portuguese boys and girls. Ann Hum Biol. 2006;33(1):55-63. 52. Budak E, Fernandez Sanchez M, Bellver J, Cervero A, Simon C, Pellicer A. Interactions of the hormones leptin, ghrelin, adiponectin, resistin, and PYY3-36 with the reproductive system. Fertil Steril. 2006;85(6):1563-1581. 53. Castellano JM, Tena-Sempere M. Metabolic control of female puberty: potential therapeutic targets. Expert Opin Ther Targets. 2016; 20(10):1181-1193. 54. Venancio JC, Margatho LO, Rorato R, et al. Short-term high-fat diet increases leptin activation of CART neurons and advances puberty in female mice. Endocrinology. 2017;158(11):3929-3942. 55. l'Allemand D, Schmidt S, Rousson V, Brabant G, Gasser T, Gruters A. Associations between body mass, leptin, IGF-I and circulating adrenal androgens in children with obesity and premature adrenarche. Eur J Endocrinol. 2002;146(4):537-543. 56. Böttner A, Jr K, MĂŒller G, et al. Gender Differences of adiponectin levels develop during the progression of puberty and are related to serum androgen levels. J Clin Endocrinol Metabol. 2004;89(8):4053- 4061. 57. Unanue N, Bazaes R, Iñiguez G, Cortes F, Avila A, Mericq V. Adre- narche in Prader-Willi syndrome appears not related to insulin sensi- tivity and serum adiponectin. Horm Res. 2007;67(3):152-158. 58. Michalakis K, Mintziori G, Kaprara A, Tarlatzis BC, Goulis DG. The complex interaction between obesity, metabolic syndrome and repro- ductive axis: a narrative review. Metabolism: clinical and experimental. 2013;62(4):457-478. 59. Machinal-Quelin F, Dieudonne MN, Pecquery R, Leneveu MC, Giudicelli Y. 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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 goverA. Arundhati Roy B. Jhumpa Lahiri C. Salman Rushdie D. Anita Desai ________________________________________ 2. The Lowland was published in: A. 2001 B. 2013 C. 2010 D. 2005 ________________________________________ 3. Which earlier work earned Lahiri the Pulitzer Prize? A. The Namesake B. Unaccustomed Earth C. Interpreter of Maladies D. The Lowland ________________________________________ 4. The novel is primarily about: A. Technology and modernity B. Immigration, family, and political violence C. Business rivalry D. Mythology and folklore ________________________________________ 5. The two central brothers in the novel are: A. Rahul and Anil B. Subhash and Udayan C. Gogol and Ashoke D. Amit and Nikhil ________________________________________ 6. Where did the brothers grow up? A. Mumbai B. Dhaka C. Calcutta D. Delhi ________________________________________ 7. Udayan becomes involved in: A. Peace activism B. Cinema C. Naxalite movement D. Business ________________________________________ 8. Subhash moves to: A. London B. Rhode Island C. Toronto D. Chicago ________________________________________ 9. Udayan is killed in: A. Jail B. A riot C. The lowland near his house D. A car accident ________________________________________ 10. Why does Subhash marry Gauri? A. Love B. To protect her and her unborn child C. Financial benefit D. Family pressure ________________________________________ 11. Gauri eventually: A. Becomes a politician B. Starts a business C. Leaves her family D. Returns to India ________________________________________ 12. Subhash raises Bela: A. With Gauri B. Alone C. With help from his parents D. In India ________________________________________ 13. Bela grows up believing: A. Udayan is her father B. Subhash is her father C. She has no father D. Her father died in war ________________________________________ 14. The setting of political unrest is linked to: A. Partition B. Naxalbari uprising C. Independence movement D. Civil War ________________________________________ 15. The narrative style uses: A. Magical realism B. Non-linear structure C. Poetry D. Second-person narration ________________________________________ 16. Gauriâs character represents: A. Traditional motherhood B. Obedient wife C. Intellectual autonomy and emotional detachment D. Political activism ________________________________________ 17. Belaâs character signifies: A. Rebellion against education B. Second-generation identity struggle C. Complete assimilation D. Materialistic living ________________________________________ 18. Memory in the novel functions as: A. A simple recollection B. A haunting presence affecting identity C. A forgotten history D. A symbolic decoration ________________________________________ 19. The lowland itself symbolizes: A. Wealth B. Stability C. Transitional, unstable space D. Escape ________________________________________ 20. Lahiriâs prose style can be described as: A. Flowery and ornate B. Minimalistic and restrained C. Dramatic and verbose D. Highly poetic ________________________________________ 21. Water imagery reflects: A. Joy and happiness B. Power and victory C. Memory and emotional fluidity D. Evil ________________________________________ 22. Which theory applies strongly to this novel? A. Structuralism B. Postcolonial hybridity C. Absurdism D. Modernism ________________________________________ 23. Postcolonial hybridity is linked to: A. Complete assimilation B. Identity in-between cultures C. Traditional values D. Language fluency alone ________________________________________ 24. Which character best reflects second-generation identity conflict? A. Gauri B. Bela C. Subhash D. Udayan ________________________________________ 25. What does Subhash struggle with most? A. Career failure B. Language C. Guilt and secrecy D. Wealth ________________________________________ 26. Udayanâs ideology centers on: A. Business growth B. Armed communist revolution C. Religious reform D. Education ________________________________________ 27. The novel shows how political violence leads to: A. Personal healing B. Economic prosperity C. Emotional trauma across generations D. Cultural unity ________________________________________ 28. Betrayal appears as: A. Only political B. Only emotional C. Both political and familial D. A background idea ________________________________________ 29. The genre of the text best fits: A. Fantasy B. Realistic political family saga C. Science fiction D. Thriller ________________________________________ 30. The narrative constantly shifts between: A. Dream and reality B. India and America C. Past and future India D. Fiction and nonfiction ________________________________________ 31. Homi Bhabhaâs "third space" represents: A. Physical land B. A zone of cultural in-betweenness C. A literal building D. A heavenlike vision ________________________________________ 32. Gauri symbolizes: A. Traditional widowhood B. Female agency vs social expectation C. Blind loyalty D. Economic dependence ________________________________________ 33. Bela unknowingly inherits: A. Udayanâs ideology B. Gauriâs academic passion only C. Subhashâs calmness D. Grandparentsâ wealth ________________________________________ 34. Lahiri uses silence to: A. Avoid details B. Deepen psychological complexity C. Reduce story relevance D. Simplify events ________________________________________ 35. A major structural device is: A. Letters B. Non-linear flashbacks C. Mythic storytelling D. Metafiction ________________________________________ 36. Which text offers a migrant theme comparison? A. The God of Small Things B. The White Tiger C. The Namesake D. Train to Pakistan ________________________________________ 38. The Naxalite movement first emerged in: A. Mumbai B. Naxalbari village C. Delhi D. Kerala ________________________________________ 39. Which theme repeats strongly? A. Celebration of success B. Silence and secrets C. Fantasy D. Heroism ________________________________________ 40. What does Bela do as an adult? A. Becomes a doctor B. Engages in environmental activism C. Joins corporate life D. Moves into politics ________________________________________ 41. The immigrant experience in the novel is portrayed as: A. Full belonging B. Alienation and partial belonging C. Achievement D. Liberation ________________________________________ 42. Which idea does Lahiri question through Gauri? A. Heroism B. Maternal expectation C. Religious devotion D. Wealth ________________________________________ 43. Subhash represents: A. Pure rebellion B. Survival and adaptation C. Anti-immigrant sentiment D. Total withdrawal ________________________________________ 44. Lahiriâs writing expects readers to: A. Passively accept the plot B. Read emotional subtext in silences C. Ignore symbols D. Only enjoy the story ________________________________________ 45. The lowland as a metaphor mainly signifies: A. Joy B. Unstable cultural ground C. Triumph D. Isolation from family ________________________________________ 46. Why is The Lowland considered significant? A. Its fantasy themes B. Its deep engagement with politics & identity C. Its humor D. Its romantic style ________________________________________ 47. Which comparative author also writes about diaspora identity? A. Chetan Bhagat B. Amitav Ghosh C. Premchand D. Ruskin Bond ________________________________________ 48. Udayanâs death drives the plot because: A. Family hides it B. It forces new relationships & trauma C. People forget him D. It has no consequence ________________________________________ 49. The narrative ends emphasizing: A. Closure and peace B. Lasting consequences of secrets C. National identity D. Religious conflict ________________________________________ 50. Scholars study this work because it explores: A. Only Indian history B. Trauma, diaspora, gender & politics C. Folk storytelling D. ComedySPANISH STUDENTS 10/22/25 In the sentence 'The author chose to juxtapose the wealthy neighborhood with the impoverished area to highlight social inequality,' what does 'juxtapose' most likely mean based on context clues? * 1 point to separate completely to describe in detail to criticize harshly to place side by side for comparison When reading 'This paradox confused everyone: the more he tried to save time, the less time he seemed to have,' what can you infer about a paradox? * 1 point a mathematical equation a simple solution a type of poem a contradictory statement that reveals truth The passage states: 'The author's use of symbolism was evident when the broken mirror represented the character's shattered dreams.' Based on this context, symbolism involves: * 1 point using objects to represent deeper meanings creating rhyming patterns writing in chronological order using literal descriptions only In the text 'Please elaborate on your answer by providing specific examples and detailed explanations,' the word 'elaborate' suggests the need to: * 1 point use simpler words change the topic add more detail make it shorter The critic wrote: 'The actor's performance captured every nuance of emotion, from subtle sadness to barely contained rage.' What does 'nuance' refer to in this context? * 1 point subtle variations in meaning simple emotions loud expressions obvious differences When the text says 'The implication of her silence was clear to everyone in the room, though she never spoke a word,' what does 'implication' mean? * 1 point a command given a direct statement a question asked a conclusion drawn indirectly The scientist stated: 'Based on our limited observations, our hypothesis suggests that plants grow faster with classical music.' What is a hypothesis? * 1 point a type of experiment a proven fact a final conclusion a possible explanation needing more evidence In 'Three witnesses were able to corroborate the defendant's alibi, strengthening his case significantly,' the word 'corroborate' most likely means: * 1 point to question or doubt to confirm or support to change the story to ignore completely The passage reads: 'The student needed to justify her controversial thesis with solid evidence and logical reasoning.' What does 'justify' mean here? * 1 point to make it longer to make excuses for to avoid explaining to prove something is reasonable When the text states 'The researcher was able to synthesize information from five different studies to create a comprehensive theory,' what does 'synthesize' involve? * 1 point copying one source exactly combining multiple sources to create something new rejecting all previous research focusing on only one idea When a reader encounters 'The symbolism in the novel was complex, with the recurring image of doors representing new opportunities throughout the story,' they should: * 1 point memorize all symbols skip symbolic passages look for deeper representational meanings focus only on the literal meaning If a teacher says 'Your essay needs more elaboration - expand on your main points with examples and analysis,' what critical thinking skill is being requested? * 1 point developing ideas with supporting details summarizing briefly using fewer examples changing the topic entirely In the passage 'The dark clouds gathering on the horizon seemed to foreshadow the troubles that would soon befall the village,' what literary technique is being demonstrated? * 1 point The author is using environmental details to hint at future plot developments The author is focusing on realistic weather descriptions The author is using weather to predict actual meteorological events The author is describing a coincidental weather pattern When analyzing 'Sarah knew the antagonist in her favorite novel wasn't just evilâhe represented the fear of change that many people experience,' what deeper understanding about antagonists is revealed? * 1 point Antagonists are always completely evil characters Antagonists can represent abstract concepts or human struggles Antagonists must be human characters Antagonists only exist to create action scenes In the sentence 'The protagonist's journey wasn't just about reaching the destinationâit was about discovering who she truly was,' what does this suggest about effective protagonists? * 1 point Protagonists must always succeed in their missions Protagonists should remain unchanged throughout the story Protagonists undergo both external and internal development Protagonists should focus only on external goals When the text states 'The word 'home' carried different connotations for each characterâwarmth and safety for some, confinement and obligation for others,' what critical reading skill is being highlighted? * 1 point Memorizing dictionary definitions Understanding that words have only one correct meaning Identifying grammatical structures Recognizing that word meanings can vary based on personal experience In 'While the denotation of 'snake' is simply a reptile, the author's use of it to describe the character suggests something far more sinister,' what analytical skill is required? * 1 point Understanding reptile biology Memorizing animal classifications Distinguishing between literal and figurative meanings Identifying sentence structure When examining 'The author's tone shifted from hopeful in the opening chapters to increasingly cynical as the story progressed,' what does this reveal about sophisticated writing? * 1 point Tone is unimportant in storytelling Tone changes reflect the author's developing attitude toward the subject Only the ending tone matters Authors should maintain the same tone throughout In analyzing 'The theme of the novel wasn't stated directly but emerged through the characters' repeated struggles with moral choices,' what does this demonstrate about themes? * 1 point Themes develop through patterns in the narrative Themes are only found in the conclusion Themes should always be explicitly stated Themes must be simple moral lessons When the passage reads 'From the character's nervous glances and hesitant speech, readers can infer that she's hiding something important,' what critical thinking process is being described? * 1 point Following explicit plot statements Memorizing character descriptions Making random guesses about character motivations Using textual evidence to draw logical conclusions In 'The ending was deliberately ambiguous, allowing readers to decide whether the character's actions were heroic or selfish,' what does this suggest about sophisticated literature? * 1 point Good stories always have clear, definitive endings Unclear endings indicate poor writing Ambiguity can enhance reader engagement and interpretation Authors should avoid confusing readers When analyzing 'The controversial decision to ban the book sparked debates about censorship versus protecting young readers,' what critical thinking skill is most important? * 1 point Choosing one side immediately Examining multiple perspectives before forming an opinion Avoiding difficult topics entirely Following popular opinion In 'Each character's perspective on the same event revealed how personal experiences shape our understanding of truth,' what deeper concept is being explored? * 1 point All perspectives are equally valid Perspective is unimportant in understanding events There is only one correct way to view any situation Personal background influences how we interpret events When the text states 'The community proved resilient, rebuilding not just their homes but their hope after the disaster,' what does this reveal about the concept of resilience? * 1 point Resilience encompasses both practical and emotional recovery Resilience is an innate trait that cannot be developed Resilience means avoiding all difficulties Resilience only involves physical recovery In analyzing 'The author's portrayal of the character's empathyâher ability to understand her enemy's pain even while fighting himâadded complexity to the conflict,' what does this suggest about empathy? * 1 point Empathy means agreeing with everyone Empathy makes people weak in conflicts Empathy should be avoided in difficult situations Empathy can coexist with opposition and create moral complexity When examining 'The character's integrity was tested when telling the truth would hurt people she loved,' what does this reveal about integrity? * 1 point Integrity means always following rules regardless of consequences Integrity means never causing any harm to others Integrity is only important in public situations Integrity involves making difficult moral choices even when costly In 'The student learned to advocate for her ideas by presenting evidence rather than just stating opinions,' what critical skill is being developed? * 1 point Supporting positions with logical reasoning and evidence Avoiding controversial topics entirely Learning to argue loudly and persistently Always agreeing with authority figures If you rewrote a scene from 'The Birchbark House' from Omakayas's grandmother's first-person perspective instead of Omakayas's, how would this most likely change the reader's understanding? * 1 point Nothing would change since they're both female characters The language would become more formal and difficult The story would become less interesting because adults are boring Readers would gain wisdom from experience but lose the innocence of childhood discovery In a plot diagram, the rising action serves which critical purpose beyond simply building toward the climax? * 1 point To provide background information about the setting To confuse readers so the ending is surprising To develop character relationships and establish stakes that make the climax meaningful To make the story longer and more detailed When analyzing the falling action in 'The Birchbark House,' which element would be most important to consider when writing an alternate version? * 1 point Whether the consequences of the climax align with the new direction you want the story to take Making sure it's shorter than the rising action Including a moral lesson for readers How quickly the conflicts get resolved In the exposition of a story, conflict serves which essential function that many readers don't realize? * 1 point To immediately grab attention with action scenes To provide comic relief before serious events To show off the author's writing skills To establish what the characters characterization/personality, which determines what they' must learn to overcome as they face more problemsLearning Narrative Text through Quizalize - Starter QuizWhy the Sun and Moon Live in the Sky This play is based on an African folktale that tells how the moon and sun ended up in the sky. Characters: Narrator Sun Moon, Sun's Wife Water Narrator: Long ago, Sun, Moon, and Water lived together on Earth. (Sun and Moon are eating breakfast at home.) Sun: I will visit my good friend Water today. Moon: That sounds enjoyable, but why doesn't Water ever visit us? Do you feel ashamed or embarrassed to invite Water here? Sun: No, I am proud of our house. I will invite Water today! (Sun visits Water at the beach.) Sun: Water, why don't you ever visit us? Water: Your house can't hold me and my family. Sun: That's nonsense! Moon and I will enlarge our house, so there will be plenty of room for everyone! Water: Then I will visit you. Sun: Wonderful! Please holler loudly, so I hear you when you arrive. Now I must dash home quickly to start the work. (Sun rushes home.) Narrator: Sun and Moon raced to make their home larger. They added rooms and raised the roof higher. The new house was completely different and had no similarities to their old home. They felt it was a victory, or a win, for now their friend could visit. Water: Sun and Moon, I have arrived! Sun: Isn't this the largest home you've seen? Moon: Sun, it's not polite to brag, so please don't boast to our guest. Water, come inside. Narrator: Water splashed through the door carrying colorful fish, frogs, and crabs. As the water began to rise, Sun and Moon climbed onto furniture. Then they scrambled onto the roof. Sun: Moon, I'm not sure about the wisdom of inviting Water. Perhaps this wasn't a smart idea! Moon: No, Sun, it was the right thing to do but we must fly to safety! Narrator: Sun and Moon flew to the sky, where they remain today and still shine down on Water.Here is a transcript of a video about Narrative Writing. Generate 25 questions. Intro to Narrative Writing What is Narrative Writing? You today, I want to introduce you to the basics of narrative writing. Narrative writing is writing that tells a story. It can be real or imagined, that is, nonfiction or fiction. It has a beginning, middle, and end. That is, it includes the basic elements of a plot exposition, rising action, conflict, climax, falling action, and resolution. And it's full of interesting details. The author's purpose in writing a narrative is to entertain the reader. There are three main types of narrative writing. The first is a personal narrative when a writer shares a true story from his or her own life. We could also say this type of narrative is autobiographical. The second type of narrative is biographical when a writer shares a true story from another person's life. The third type of narrative is fictional. When a writer tells an invented story, short stories, and novels are fictional narratives. The Process of Writing a Narrative While we could add to this list, there are five important parts of a narrative that I especially want you to remember as you write your own narrative. These parts of a narrative include setting, characters, plot, point of view, and dialogue. The first part of a narrative is the setting , where, and when the narrative takes place. The setting affects both the plot and characters in your narrative, so it's important to spend some time brainstorming where, when, and in what conditions your story takes place. The second part of a narrative is the characters , the people, animals or creatures involved in a story. Remember that your story must have a protagonist, the character facing the problem, and an antagonist the character or force causing the problem. Take some time while planning your narrative to focus on your characters beyond the characters names and roles they play in the story. Think about whether you'd like them to be flat with very few character traits or round with many character traits. Also think about which characters in your story will remain static or unchanged, and which characters will be dynamic, undergoing an important change in your narrative. The third part of a narrative is the plot , the sequence of events in a narrative. Take some time to think carefully through your story's plot. How will it begin and how will it end? What conflicts will your characters encounter? What is the climax or turning point of your story? How will the problems be solved? Creating a storyboard or labeling a plot diagram are both good tools for planning your story's plot. The fourth part of a narrative is the point of view , which is the perspective from which a narrative is told. You can choose to write your narrative in first person, writing a personal narrative from your own point of view, or you can choose a character in a fictional narrative to tell your story. Another option is to write your narrative in the third person point of view, telling the story from the perspective of an unseen narrator that is not a character in the story. Finally, the fifth part of a narrative is dialogue. The words the characters speak in your story dialogue can establish the setting, show characterization, foreshadow events, or advance the action in a narrative. Dialogue brings your narrative to life. It's important to review how to punctuate dialogue, following grammatical rules for using quotation marks, commas, and other N marks such as periods and question marks. As you begin writing your narrative, I'll help you break down each step of the process. But hopefully this introduction gives you a basic understanding of what narrative writing is, and hopefully it sparks some ideas for you to begin planning your own narrative.A BAD CASE OF THE STRIPES By David Shannon Parts(18): Camilla Narrator 1 Narrator 2 Narrator 3 Narrator 4 Mr. Harms Mother Father Dr. Bumble Old Woman Environmental Therapist Dr. Grop Dr. Gourd Dr. Sponge Mr. Mellon Dr. Cricket Dr. Young <><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><><> Narrator 1: A BAD CASE OF THE STRIPES By David Shannon Narrator 2: Camilla Cream loved lima beans. But she never ate them. Narrator 3: All of her friends hated lima beans, and she wanted to fit in. Camilla always worried about what other people thought of her. Narrator 4: Today she was fretting even more than usual. It was the very first day of school, and she couldn't decide what to wear. There were so many people to impress! Narrator 1: She tried on forty-two outfits, but none seemed quite right. She put on a pretty red dress and looked in the mirror. Then she screamed. Narrator 2: Her mother ran into the room, and she screamed, too. Mother: "Oh my heavens! You're completely covered with stripes!" Narrator 3: she cried. This was certainly true. Camilla was striped from head to toe. She looked like a rainbow. Narrator 4: Mrs. Cream felt Camilla's forehead. Mother: "Do you feel all right?" Narrator 1: she asked. Camilla: "I feel fine, but just look at me!" Narrator 2: Camilla answered. Mother: "You get back in bed this instant. You're not going to school today." Narrator 3: her mother ordered. Camilla was relieved. She didn't want to miss the first day of school, but she was afraid of what the other kids would say. And she had no idea what to wear with those crazy stripes. Narrator 4: That afternoon, Dr. Bumble came to examine Camilla. Dr. Bumble: "Most extraordinary! I've never seen anything like it! Are you having any coughing, sneezing, runny nose, aches, pains, chills, hot flashes, dizziness, drowsiness, shortness of breath, or uncontrollable twitching?" Narrator 1: he asked. Camilla: "No, I feel fine." Narrator 2: Camilla told him. Dr. Bumble: "Well then, I don't see any reason why she shouldn't go to school tomorrow. Here's some ointment that should help clear up those stripes in a few days. If it doesn't, you know where to reach me." Narrator 3: Dr. Bumble said, turning to Mrs. Cream. And off he went. Narrator 4: The next day was a disaster. Everyone at school laughed at Camilla. They called her "Camilla Crayon" and "Night of the Living Lollipop." Narrator 1: She tried her best to act as if everything were normal, but when the class said the Pledge of Allegiance, her stripes turned red, white, and blue, and she broke out in stars! Narrator 2: The other kids thought this was great. One yelled out, Narrator 3: "Let's see some purple polka dots!" Narrator 4: Sure enough, Camilla turned all purple polka-dotty. Someone else shouted, Narrator 1: "Checkerboard!" Narrator 4: and a pattern of squares covered her skin. Soon everyone was calling out different shapes and colors, and poor Camilla was changing faster than you can change channels on a T.V. Narrator 2: That night, Mr. Harms, the school principal, called. Mr. Harms: "I'm sorry, Mrs. Cream, I'm going to have to ask you to keep Camilla home from school. She's just too much of a distraction, and I've been getting phone calls from the other parents. They're afraid those stripes may be contagious." Narrator 3: he said. Camilla was so embarrassed. She couldn't believe that two days ago everyone liked her. Now, nobody wanted to be in the same room with her. Narrator 1: Her father tried to make her feel better. Father: "Is there anything I can get you, sweetheart?" Narrator 2: he asked. Camilla: "No, thank you," Narrator 3: sighed Camilla. What she really wanted was a nice plate of lima beans, but she had been laughed at enough for one day. Dr. Bumble: "Hmm, well, yes, I see. I think I'd better bring in the Specialists. We'll be right over.â Narrator 4: said Dr. Bumble to Mr. Cream on the phone. About an hour later, Dr. Bumble arrived with four people in long white coats. He introduced them to the Creams. Dr. Bumble: "This is Dr. Grop, Dr. Sponge, Dr. Cricket, and Dr. Young." Narrator 1: Then the Specialists went to work on Camilla. They squeezed and jabbed, tapped and tested. It was very uncomfortable. Dr. Grop: "Well, it's not the mumps." Dr. Sponge: "Or the measles." Dr. Cricket:"Definitely not chicken pox." Dr. Young: "Or sunburn." Narrator 2: replied the Specialists. Specialists:"Try these. Take one of each before bed." Narrator 4: said the specialists. They each handed her a bottle filled with different colored pills. Then they filed out the front door followed by Dr. Bumble. Narrator 1: That night, Camilla took her medicine. It was awful. Narrator 2: When she woke up the next morning, she did feel different, but when she got dressed, her clothes didn't fit right. She looked in the mirror, and there, staring back at her, was a giant, multi-colored pill with a face on it. Narrator 3: Dr. Bumble rushed over as soon as Mrs. Cream called. But this time, instead of the Specialists, he brought the Experts. Narrator 4: Dr. Gourd and Mr. Mellon were the finest scientific minds in the land. Once again, Camilla was poked and prodded, looked at and listened to. Narrator 1: The Experts wrote down lots of numbers. Then they huddled together and whispered. Dr. Gourd finally spoke. Dr. Gourd: "It might be a virus," Narrator 2: he announced with authority. Suddenly, fuzzy little virus balls appeared all over Camilla. Mr. Mellon: "Or possibly some form of bacteria," Narrator 3: said Mr. Mellon. Out popped squiggly little bacteria tails. Dr. Gourd: "Or it could be a fungus," Narrator 4: added Dr. Gourd. Instantly, Camilla was covered with different colored fungus blotches. The experts looked at Camilla, then each other. Experts: "We need to go over these numbers again back at the lab. Weâll call you when we know something," Narrator 1: said the Experts. But the Experts didn't have a clue, much less a cure. Narrator 2: By now, the T.V. news had found out about Camilla. Reporters from every channel were outside her house, telling the story of "The Bizarre Case of the Incredible Changing Kid." Narrator 3: Soon a huge crowd was camped out on the front lawn. Narrator 4: The Creams were swamped with all kinds of remedies from psychologists, allergists, herbalists, nutritionists, psychics, an old medicine man, a guru, and even a veterinarian. Narrator 1: Each so-called cure only added to poor Camilla's strange appearance until it was hard to even recognize her. She sprouted roots and berries and crystals and feathers and a long furry tail. But nothing worked. Narrator 2: One day, a woman who called herself an Environmental Therapist claimed she could cure Camilla. She said, Environmental Therapist: "Close your eyes, breathe deeply, and become one with your room." Camilla: "I wish you hadn't said that," Narrator 3: Camilla groaned. Slowly, she started to melt into the walls of her room. Her bed became her mouth, her nose was a dresser, and two paintings were her eyes. The therapist screamed and ran from the house. Mother: "What are we going to do? It just keeps getting worse and worse!" Narrator 4: cried Mrs. Cream. She began to sob. Narrator 1: At that moment, Mr. Cream heard a quiet little knock at the front door. He opened it, and there stood an old woman who was just as plump and sweet as a strawberry. Old Woman: "Excuse me, but I think I can help." Narrator 2: she said brightly. Narrator 3: She went into Camilla's room and looked around. Old Woman: "My goodness, what we have here is a bad case of the stripes. One of the worst I've ever seen!" Narrator 4: she said with a shake of her head. She pulled a container of small green beans from her bag. She said, Old Woman: "Here. These might do the trick." Mother: "Are those magic beans?" Narrator 1: asked Mrs. Cream. The old woman replied, Old Woman: "Oh my, no, there's no such thing. These are just plain old lima beans. I'll bet you'd like some, wouldn't you?" Narrator 2: she asked Camilla. Camilla wanted a big, heaping plateful of lima beans more than just about anything, but she was still afraid to admit it. She said, Camilla: "Yuck! No one likes lima beans, especially me!" Old Woman: "Oh, dear, I guess I was wrong about you." Narrator 3: said the old woman sadly. She put the beans back in her bag and started toward the door. Narrator 4: Camilla watched the old woman walk away. Those beans would taste so good. And being laughed at for eating them was nothing, compared to what she'd been going through. She finally couldn't stand it. Camilla: "Wait! The truth is...I really love lima beans." Narrator 1: she cried. The old woman smiled, popping a handful of beans into Camilla's mouth, and said, Old Woman: "I thought so." Camilla: "Mmmmmmm," Narrator 2: said Camilla. Suddenly the branches, feathers, and squiggly tails began to disappear.Then the whole room swirled around. When it stopped, there stood Camilla, and everything was back to normal. Camilla: "I'm cured!" Narrator 3: she shouted. The old woman said, Old Woman: "Yes, I knew the real you was in there somewhere." Narrator 4: She patted Camilla on the head and went outside and vanished into the crowd. Narrator 1: Afterward, Camilla wasn't quite the same. Narrator 2: Some of the kids at school said she was weird, but she didn't care a bit. Narrator 3: She ate all the lima beans she wanted, and she never had even a touch of stripes again.Make a quiz using the following words and definitions: 1. narrative a story 2. narrate to tell a story 3. pronounce to speak in a certain way; to say aloud 4. denounce to criticize; to blame 5. fabulous amazing; fantastic 6. fabled legendary; famous 7. mythical not existing in reality; made up 8. mythology a group of stories associated with a subject or culture 9. recount to tell; to describe 10. discount to put down; to say or believe something is not worth much 11. idealistic believing in the idea of perfection or a perfect world 12. ideal perfectly suitable 13. idealize to think of as perfect 14. conscience the part of the mind that tells the diference between right and wrong 15. scientifc based on proven facts 16. savvy cleverness; understanding 17. savor to take time to enjoy 18. certify to prove good or true; to declare correct 19. certainty something about which there is no doubt; a fact 20. concerted done together; combined 21. ascertain to fgure out through reasoning. Use all 21 words in the multiple choice quiz; create distractor items in the answer choices.