Does precocious puberty and its treatment cause the emotional and behavioural problems in children?

doi:10.21203/rs.3.rs-4835395/v1

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Does precocious puberty and its treatment cause the emotional and behavioural problems in children?

https://doi.org/10.21203/rs.3.rs-4835395/v1

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Central precocious puberty (CPP) occurs as a result of early activation of the hypothalamic-pituitary-gonadal axis. In recent years, especially after the COVID pandemic, presentations with signs of precocious puberty and cases requiring treatment have increased all over the world. Recent studies have showed that CPP patients are more likely to have social and psychiatric problems than their peers of the same age and gender. The aim of our study is to examine the psychiatric symptoms and quality of life of the children newly diagnosed with CPP and cases under treatment more than one year and to compare these symptoms with age and gender-matched healthy children. The research was planned as a cross-sectional study and included 47 female and 3 male patients (n = 50) who were followed up for CPP. The control group (CG) consisted of healthy children matched with the case group in terms of age and gender (n = 25). The case group was divided into two groups; patients who were newly diagnosed and did not receive treatment yet and patients who had been receiving treatment for at least one year. Sociodemographic form, Pediatric Quality of Life Inventory, Revised Child Anxiety and Depression Scale-Child Version (RCADS-CV), Strengths and Difficulties Questionnaire (SDQ), TURGAY DSM-IV-Based Child and Adolescent Behavior Disorders Screening and Rating Scale (T-DSM-IV-S) were applied to the children and their families. 50 cases diagnosed with CPP with a mean age of 8.95±1.07 years (25 at diagnosis, 25 on follow-up) and 25 healthy children with a mean age of 8.79±1.02 years were enrolled the study. 94% of CPP group (PG) (n = 47) and 84% of control group (CG) (n = 21) were girls. When the child and parent forms have evaluated; there was no significant difference between three groups in terms of quality of life (child and parent forms), anxiety and depression scores, strengths and difficulties scores. Similar results were obtained between three groups in terms of inattention and hyperactivity scores, oppositional defiance and conduct disorder scores according to the scale.

Conclusion: In the present study, psychiatric symptoms and quality of life were compared between the three groups and no significant difference was detected. While it is a favorable finding that there is no difference in terms of these symptoms in children with early adolescence, it is crucial to consider children with a chronic disease in a multidisciplinary approach and to assess the cases for the potential negative impacts on their quality of life.

precocious puberty

quality of life

affective reactivity

inattention and hyperactivity

Although it is predicted that children experiencing precocious puberty may experience depressive and anxiety-related symptoms, and their quality of life may be affected due to having a chronic disease, there are no consistent results in this regard.

What is new?

There is no difference in terms of psychiatric symptoms and quality of life in children who were diagnosed with precocious puberty and received treatment for a certain period of time after the diagnosis of PP compared to children without PP. Furthermore, our study is the first study comparing children with precocious puberty who received treatment with those who did not.

The onset of puberty symptoms at an early age has been frequently observed in recent years[1]. During the COVID-19 pandemic, the number of presentations with precocious puberty features and patients requiring treatment has increased in our country and all over the world[2], [3]. Precocious puberty (PP) is defined as the onset of physical signs of puberty before the age of 8 years in girls and 9 years in boys or the onset of menstruation before the age of 10 years[4]. Patients may present with early progression of secondary sexual characteristics, inappropriate body appearance and psychological behavioural abnormalities[5]. Rapid bone maturation due to precocious puberty may lead to short stature in adulthood[5]. Central precocious puberty (CPP) results from early activation of the hypothalamic-pituitary-gonadal axis[6]. GnRH analogs are used to treatment of central precocious puberty and are highly effective in suppressing the HPG axis[5]. While the primary medical reason for the treatment of CPP is to preserve adult height potential, a second commonly cited reason is to alleviate psychological distress associated with early pubertal development[7].

Adolescence and puberty is a period of major mental and psychological changes as well as biological changes[8]. While the structure of the body changes, region-specific, changes in brain structure, brain function and neurochemical transmission processes are also seen[9]. It is a challenge for the adolescent trying to adapt to his/her changing body and brain to complete his/her identity development and keep his/her social adaptive skills at a positive level in the process of individualization in order to adapt to these changes[10]. While even a normal course of adolescence can cause difficulties for the adolescents and their families, it has been found that children who experience precocious puberty are more likely to have social and psychiatric problems than their peers of the same age and gender[11].

Hormonal changes during puberty are known to increase the risk of developing emotional and behavioural problems[10]. In children who experience precocious puberty, the delay between physical and psychological maturity may also make them more vulnerable to psychopathologies[12]. Epidemiological studies have shown that early onset of puberty in girls is associated with earlier onset of sexuality, earlier age of pregnancy and lower educational attainment, regardless of cognitive ability and socioeconomic status[13]. Previous studies of children with CPP have reported irritability, aggression, depressive symptoms and anxiety-related symptoms[14]. In another study conducted in our country, while the depressive scores of the children were similar, significant difference was found only in terms of anxiety disorder[15]. In children, the impact of precocious puberty on quality of life has also been reported. While some studies found low quality of life, others found no difference in quality of life between the CPP group and healthy controls[1], [15], [16]

The aim of our study was to investigate psychiatric symptoms such as anxiety, depression and irritability and quality of life in children diagnosed with central precocious puberty and to compare these data with age- and sex-matched children without central precocious puberty.

The research was designed as a cross-sectional study. Written informed consent was obtained from the children and their parents before the study. The study protocol was approved by the Ethics Committee of Tekirdag Namık Kemal University, Faculty of Medical (2022.119.06.09) in light of the Helsinki Declaration. Detailed information about the study was given to the parents and children who were voluntary to participate in the study. Written informed consent was obtained from the healthy group and their parents.

Participants

Children diagnosed with CPP at the Pediatric Endocrinology Department of Tekirdag IFC City Hospital between December 2020 and April 2022 were included in the current study.

The study group included 47 female and 3 male patients (n = 50) who were followed up for CPP at the Pediatric Endocrinology Department of Tekirdag IFC City Hospital. The diagnosis of CPP was based on signs and symptoms of CPP, elevated level of basal or stimulated gonadotropin levels and advanced bone age. All patients and their families agreed to participate in the study and constituted the CPP group. The children's clinical data (physical examination and laboratory findings) were evaluated from the medical file records and scales were applied to the subjects. Children with CPP were divided into two groups as at diagnosis (Group PP1) and at follow-up and after more than one year of treatment (Group PP2).

The control group consisted of age and sex-matched children who were admitted to pediatric outpatient clinics of Tekirdag IFC City Hospital without any chronic disease and who volunteered to participate in the study. Twenty-five children and their families agreed to participate in the study. Twenty-one female and 4 male (n = 25) children constituted the Control Group (CG).

Exclusion criteria for both groups were the presence of intellectual disability, any neurological disorder, psychotic disorder, and autism spectrum disorder, as these individuals may have difficulty in completing the study procedure. Individuals with any chronic and/or severe medical illness were also excluded to eliminate any possible confounding effects.

Clinical Measures

The sociodemographic information of the children was obtained by using the sociodemographic information form developed by the researchers. In the clinical information form; auxological data, physical examination, the laboratory and radiological findings of the participants were evaluated.

The Strengths and Difficulties Questionnaire Children (SDQ-C) and Parent (SDQ-P) forms were used to assess the behavioural characteristics of the participants [17], [18]. The Turkish validity and reliability study was conducted by Guvenir et al. [19]. The questionnaire is a short behavioural screening questionnaire used to examine mental well-being. The SDQ examines 25 attributes, divided into 5 scales: Emotional problems, behavioural problems, Hyperactivity and inattention, Peer relationship problems, Prosocial behaviours.

Turgay DSM-IV-Based Child and Adolescent Behavior Disorders Screening and Rating Scale (T-DSM-IV-S) was developed by Turgay and adapted and translated into Turkish by Ercan

et al. [20]. The T-DSM-IV-S (parent and teacher forms) is based on the DSM-IV criteria and assesses hyperactivity-impulsivity (nine items), inattention (nine items), opposition–defiance disorder (eight items) and conduct disorder (15 items). The severity of each symptom is estimated on a fourpoint Likert-type scale (0 = not at all, 1 = just a little, 2 = quite a bit, and 3 = very much). Subscale scores on the T-DSM-IV-S are calculated by summing the item scores for each subscale.

The Revised Child Anxiety and Depression Scale-Child Version (RCADS-CV) is a self-report questionnaire that assesses the clinical symptoms of anxiety and depression based on DSM-IV criteria. The RCADS-CV has been shown to be a reliable and valid instrument in different cultures and languages as well as in Turkish [21]. It consists of 47 items with six subscales corresponding to generalised anxiety disorder (GAD), major depressive disorder (MDD), separation anxiety disorder (SAD), social phobia (SP), panic disorder (PD), and obsessive-compulsive disorder (OCD). It is a four-point Likert-type scale (0 = never, 1 = sometimes, 2 = often, and 3 = always). The general anxiety score is obtained by the sum of the first five sub-scales, and the internalisation score is obtained by the sum of all sub-scales. The scale has no cut-off score. In our study, RCADS-CV-children (RCADS-CV-C) and RCADS-CV-parent (RCADS-C-P) forms were used.

The Pediatric Quality of Life Inventory (PedsQL) developed by Varni et al. [22] in 1999, aims to evaluate the general quality of life in children aged 2–18 years. The scale consists of four subscales assessing physical, emotional, social, and school-related functioning. A validity and reliability study for the Turkish form of the inventory was conducted for 2–18 age group. PedsQL evaluates areas of functionality with 4 subheadings: 8 items are physical, 5 items are emotional, 5 items are social, and 5 items are school functionality, for a total of 23 items. Scoring is done in 3 areas: total physical health score, total psychosocial health score, which evaluates emotional, social and school functioning, and total score. It is accepted that the higher the total score, the higher the quality of life. The Turkish validity and reliability study was conducted by Memik et al [23]. In our study, the children (PedsQL-C) and parent forms (PedsQL-P) of PedsQL were used.

Statistical analyses

SPSS 25.0 (IBM Corporation, Armonk, New York, United States) was used in the analysis of the variables. First, preliminary analysis of the assumptions of parametric statistics was conducted. The Kolmogorov–Smirnov test was used to check the normal distribution of the variables. When the assumption of normality was met, parametric statistical tests were used. When the assumption of normality was not met, non-parametric statistical tests were used. The Student’s t-test or Mann–Whitney U- tests were used to asses differences between two groups according to the normal distribution of the measured parameters. Chi-square test was used to compare the categorical variables. Quantitative variables were expressed as mean (standard deviation), median (25th percentile / 75th percentile), while categorical variables were shown as number (n) and frequency (%). The variables were analyzed at 95% confidence level, and a p value less than 0.05 was considered as significant.

The group PP1 (mean age: 8.23 ± 0.91 years), PP2 (mean age: 9.68 ± 0.66years) and CG (mean age: 8,79 ± 1,02years) were not similar in age (p = 0), due to the difference between PP1 and PP2. All cases of the PP1 group (n = 25), 88% of the PP2 group (n = 22) and 84% of the CG (n:21) were female. The clinic characteristics of group PP1, PP2 and CG are summarised in Table 1. Pubertal stages were Tanner 2 in four of the patients, Tanner 3 in 13 of the patients, Tanner 4 in 20 of the patients and Tanner 5 in 13 of the patients. The 12% (n:3) and 13.6% (n:3) of the children had early menarche in group PP1 and PP2, respectively. The duration of GnRHa treatment in group PP2 ranged from 13 to 36 months. The mean duration of treatment was 14.42 ± 5.65 months.

Table 1

Sociodemographic and clinical features of PP and CG
	PP1 n:25	PP2 n:25	CG n:25
Age (year)	8.23 ± 0.91 (6.21–9.7)	9.68 ± 0.66 (7.7-10.68)	8.79 ± 1.02 (6.5–9.9)
Female/Male	25/0	22/3	21/4
Menarche at diagnosis	12% (n:3)	13.6% (n:3)	-
Data were presented as mean ± SD

The SDQ-C, SDQ-P, PedsQL-C and PedsQL-P scores are shown in Table 2. The three groups had similar scores in the SDQ-behavior, SDQ-emotional and total scores in the child and parent questionnaires (p = 0.812, p = 0.79, p = 0.959 respectively in the child questionnaires and p = 0.824, p = 0.852, p = 0.599 respectively in parent questionnaires). No significant differences were found between the groups in terms of PedsQL-total scores in the child and parent forms (p = 0.505, p = 0.992; respectively).

Table 2

SDQ-A, SDQ-P and PedsQL-A, PedsQL-P Scores
	PP1 n = 25	PP2 n = 25	CG n = 25	p value
SDQ-A emotional	2 (0,5 − 2,5)	1 (0–3)	1 (0–2)	0,790
SDQ-A behaviour	1 (0–2)	1 (0–2)	1 (0,5 − 2)	0,812
SDQ-A ADHD	4 (2–5)	4 (2–5)	4 (3–5)	0,585
SDQ-A peer	2 (0–2,5)	2 (0–3)	1 (0–2,5)	0,710
SDQ-A prosocial	9 (7,5–10)	8 (6–10)	9 (8–10)	0,917
SDQ-A total	10 (4–11)	8 (5–11)	8 (5,5–10)	0,959
SDQ-P- emotional	1 (0–3,5)	2 (1–2)	1 (0–2,5)	0,852
SDQ-P behavioural	1 (0,5 − 2)	1 (0–2)	1 (0–1,5)	0,824
SDQ-P ADHD	3 (2–5)	4 (2–5)	3 (2–5)	0,804
SDQ-P peer	2 (1–3)	1 (1–4)	1 (0–2,5)	0,406
SDQ-P total	9 (5,5–11,5)	8 (6–12)	7 (4–10,5)	0,599
PedsQL-C pyshical	84,375 (71,875 − 89,062)	78,125 (71,875 − 89,062)	81,25 (68,75–90,625)	0,928
PedsQL-C psychosocial	83,333 (75–92,5)	83,333 (77,5–93,333)	90 (83,33–95)	0,289
PedsQL-C total	83,437 (73,359 − 90,468)	82,968 (74,531 − 91,875)	87,812 (81,2591,718)	0,505
PedsQL-P pyschical	79,687 (61,718 − 91,406)	81,25 (71,875 − 90,625)	87,5 (64,843 − 100)	0,751
PedsQL-P psychosocial	84,166 (65,416 − 93,333)	85 (66,666 − 93,333)	82,5 (71,25–92,083)	0,987
PedsQL-P total	84,296 (63,710 − 91,445)	82,968 (67,812 − 91,406)	81,796 (69,804 − 90,976)	0,992
Data were presented as median (25-75th percentiles)
(SDQ-A): The Strengths and Difficulties Questionnaire-Adolescent; (SDQ-P): The Strengths and Difficulties Questionnaire-Parent; PedsQL-A: Pediatric Quality of Life Inventory -Adolescent Form; PedsQL-P: Pediatric Quality of Life Inventory-Parent Form

The RCADS-CV-C and RCADS-CV-P scores of PP1, PP2 and CG are shown in Table 3. No significant difference was found between groups in terms of RCADS-CV scores. Internalizing and anxiety scores were similar between groups for children (p = 0.987, p = 0.929 respectively) and parents (p = 0.942, p = 0.824 respectively).

Table 3

RCADS-CV-A and RCADS-CV-P scores
	PP1 n:25	PP2 n:25	CG n:25	p
RCADS-CV-C anx.dep. score	38 (33–45)	39 (30–47)	37 (32,5–46)	0,987
RCADS-CV-A anxiety score	39 (32–44)	40 (31–49)	38 (31,5–46,5)	0,929
RCADS-CV-P anx.dep. score	45,5 (42,75 − 55)	49 (41–55)	46 (42,5–55)	0,942
RCADS-CV-P anxiety score	45,5 (42–54,75)	48,5 (41,25–57)	46 (41,5–55,5)	0,824
Data were presented as median (25-75th percentiles)
RCADS-CV-A: Revised Child Anxiety and Depression Scale-Child Version-Adolescent Form
RCADS-CV-P: Revised Child Anxiety and Depression Scale-Child Version-Parent Form

The ARI-C and ARI-P scores of the groups are given in Table 4. The ARI scores were found to be similar between the three groups in children and parent forms (p = 0.581, 0.730 respectively).

Table 4

ARI-A, ARI-P and T-DSM-IV-S scores
	PP1 n: 25	PP2 n: 25	CG n: 25	p
ARI-C-total	5 (0–7)	2 (1–4,25)	1 (1–2)	0,581
ARI-P total	2 (0–6)	2 (0,5 − 3,5)	1 (0–2)	0,730
T-DSM-IV-S-IA	4,5 (3,25 − 9,5)	6 (0–10)	4 (1–6)	0,439
T-DSM-IV-S-HA	4 (1,25 − 6,5)	5 (1–11)	4 (2–7)	0,913
T-DSM-IV-S-ODD	4,5 (1–9,25)	3 (2–8)	3 (1–5)	0,892
T-DSM-IV-S-CD	0 (0–0)	0 (0–2)	0 (0–0)	0,359
T-DSM-IV-S-Total	14,5 (6–21)	15 (3–30)	17,5 (6,75 − 28,25)	0,903
Data were presented median (25-75th percentiles)
ARI-C: Affective Reactivity Index- Children Form; ARI-P: Affective Reactivity Index- Parent Form;
T-DSM-IV-S-IA: Turgay DSM-IV-Based Child and Adolescent Behavior Disorders Screening and Rating Scale-Inattention Score
T-DSM-IV-S-HA Turgay DSM-IV-Based Child and Adolescent Behavior Disorders Screening and Rating Scale- Hyperactivity
T-DSM-IV-S-ODD Turgay DSM-IV-Based Child and Adolescent Behavior Disorders Screening and Rating Scale-Oppositional Defiant Score
T-DSM-IV-S-CD Turgay DSM-IV-Based Child and Adolescent Behavior Disorders Screening and Rating Scale- Conduct Disorder Score

In the current study, we analysed behavioural and emotional problems, quality of life, anxiety, and depressive status of children with CPP (at diagnosis and at follow-up), and compared the results with age- and sex-matched healthy controls. In terms of behavioural and emotional problems, quality of life, anxiety and depressive status, the CPP groups did not differ from age-matched controls.

In contrast to previous reports on elevated behavioral and emotional problems in children with CPP[24], we found no significant differences in SDQ-A and SDQ-P scores between the three groups. In both groups with CPP, children and parents reported similar behavioural and emotional problems with CG. During puberty, it is known that psychological changes are known to follow physiological changes as a result of the activation of hypothalamic-pituitary axis[25]. As the children in the CPP group were younger and the possible effects of hormonal changes were treated in the early period, it is suggested that children diagnosed with CPP did not experience any emotional and behavioural differences. The fact that both parents and children consistently reported no emotional and behavioural changes, strengthens this conclusion.

In TURGAY scale which evaluates the symptoms of attention deficit hyperactivity, oppositional defiant disorder and conduct disorder, similar scores were found between the three groups. During adolescence, children experience some behavioural and emotional difficulties, increased risk-taking behaviour and impulsivity as well as difficulties in controlling anger[26]. In a cross-sectional study conducted in 2023, externalising behaviours were found to be more prevalent in female adolescents with CPP compared to the control group[27]. In another study, although the score assessing externalising behaviours was not considered to be clinically significant, it was found to be higher in adolescent girls compared to the control group. It was also suggested that the effect on behaviour emerged at a later age[28]. The findings of our study indicate that, although biological markers of adolescence have been observed in children, it is believed that their behavioural manifestations are more closely associated with their psychosocial developmental stage and chronological age than with this biological process. Furthermore, the data suggest that children do not exhibit behavioural patterns that are unique to the adolescent period.

The majority of studies conducted thus far on precocious puberty in children have focused on girls. In some of these studies, elevated rates of depression and anxiety have been observed in children experiencing precocious puberty[14], [29]. The onset of menarche has been shown as a reason for depressive symptoms[29]. Among anxiety disorders, social anxiety, which is associated with a lower self-image, has been reported to be more prevalent[15]. Conversely, similar to our study, some studies have reported that the groups diagnosed and treated with CPP did not exhibit any differences in terms of depressive and anxiety symptoms[30]. It is known that there should be a serious psychosocial stressor for the emergence of depression in childhood in association with the development of children's cognitive and emotional abilities[31]. Since the children in our study were relatively younger, it is thought that they did not differ from healthy children in terms of depressive and anxiety symptoms, even if they exhibited symptoms of adolescence.

It is established that children with a chronic disease experience a negative impact on their quality of life[32], [33]. There are limited studies that have analysed the quality of life of children with precocious puberty. In one of these studies, the CPP group included both treated and newly diagnosed children and no significant differences were identified in the quality of life of this group in comparison to healthy children[15]. In another study a total of 193 children were examined, including 59 children with CPP, 53 children with premature telarche, and 81 healthy children and their parents. No significant differences were found between the CPP, PT and control groups[1]. In our study, the quality of life of the group of children newly diagnosed with CPP and the group of children who had been receiving treatment for at least one year was found to be similar to that of healthy children according to both self-report and parental report. The favourable response to treatment and the absence of significant adverse effects during the treatment indicate that psychological well-being in children is associated with a high level of quality of life.

It should be noted that our study has some limitations. First of all, the limited sample size makes it difficult to generalise our results. Although children's psychiatric symptoms were assessed through scales, it is possible that structured psychiatric interviews for children might yield more accurate diagnoses of potential psychiatric disorders. A more detailed evaluation of children's physical characteristics such as height and weight, which change with the puberty process, could have provided a more accurate interpretation of the results. Furthermore, psychological problems that may arise in the longer term can be evaluated by longitudinal follow-up of the study groups.

In the present study, psychiatric symptoms and quality of life were compared between the three groups and no significant difference was detected. While it is a favorable finding that there is no difference in terms of these symptoms in children with early adolescence, it is crucial to consider children with a chronic disease in a multidisciplinary approach and to assess the cases for the potential negative impacts on their quality of life.

Funding:

The authors received no funding for the research.

Author Contribution

ÖK and GYA drafted the study protocol and wrote the manuscript. ÖK and GYA collected the data. ÖK and GYA revised the manuscript. All authors approved the final version.

Data Availability

All data generated or analyzed during this study are included in this article. Further inquiries can be directed to the corresponding author.

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Does precocious puberty and its treatment cause the emotional and behavioural problems in children?

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