Differences in sex hormones and brain morphology between females with offspring and nulliparous

doi:10.21203/rs.3.rs-3237537/v1

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Differences in sex hormones and brain morphology between females with offspring and nulliparous

https://doi.org/10.21203/rs.3.rs-3237537/v1

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Background

This study aims to investigate differences in sex hormone levels and brain morphology among women with offspring and nulliparous to explore the changes that the reproduction induces.

Methods

A total of 66 females of reproductive age range 20–40 years were enrolled, including 35 offspring women, and 31 nulliparous. Participants’ sex hormone levels were assessed. T1 structural images were obtained using a 3.0 Tesla MRI scanner, and voxel-based morphometry (VBM) was implemented to investigate gray matter changes between the two groups and extract brain volume including gray matter volume (GMV), white matter volume (WMV), cerebrospinal fluid (CSF).

Results

Analysis of sex hormones revealed no significant differences in E2 (z = − 0.28,p = 0.782), LH (z = − 0.62,p = 0.537), and P (z = − 1.34,p = 0.181), whereas significant differences were found in FSH (z = 3.86,p < 0.001), T (z = − 3.92,p < 0.001), and PRL (z = − 3.27, p = 0.018). Differences in brain volumes, including GMV (t = − 3.53,p = 0.001), CSF (t = − 2.39,p = 0.020), were observed. VBM analysis showed that compared with nulliparous women, those with offspring exhibited decreased cortical areas in the left superior frontal gyrus and right putamen, but no increased cortical areas were found.

Conclusion

Females of reproductive age in the 20–40 years group, compared with nulliparous female, sex hormones of female with offspring changed, and the volume of the cerebral cortex decreased, which indicated that females were developing in the direction of functional decline. Further research should explore the mechanism underlying these discrepancies, and their potential consequences for female health.

Female

Voxel-based morphometry

sex hormones

Reproduction

At present, sex hormones could have organizational effects on the developing brain and could initiate hormone transition periods, such as puberty and menopause, which are related to regeneration and development [1]. Throughout a woman’s life, hormone levels rise and fall differently through various stages, including pregnancy, postpartum, menopause, and perimenopause [2][3]. Periodic changes in sex hormone levels, particularly estrogen (E2), play a pivotal role in coordinating many aspects of fertility by altering the function of certain neuronal populations in the brain and regulating the activity of gonadotropins in the pituitary gland [4]. Although evidence shows that E2 can positively affect cognitive ability in animals and humans [5], sex hormones may lead to the occurrence of Alzheimer’s disease [6]. These hormones vary differentially and affect specific gonadal and non-gonadal target tissues/cells. For example, follicle-stimulating hormone (FSH) may contribute to the development of bone loss and obesity while increasing cardiovascular and cancer risk [7][8]. Sex hormones affect various cognitive abilities, including mood, verbal memory, working memory, spatial abilities, and visual–spatial sequencing [9].

The changes in gray matter volume (GMV) are complex, and they play a role in certain task states, functions, and emotions [10]. Some studies indicate that circulating sex hormones are related to GMV in young adult subjects [11]. Determining the organizing effect of steroid hormones on brain morphology is important, which may persist beyond puberty into young adulthood [12]. Different hormones act on targets in different parts of brain tissue; for example, classical nuclear receptors of progesterone (P) have been located in the frontal cortex, hypothalamus, thalamus, amygdala, hippocampus, cerebellum, and other regions in the rat brain [13]. Women with different emotional or cognitive function problems may experience changes in GMV [14]. The periods before and after reproduction are characterized by significant surroundings and role changes for female. However, only a few studies have examined whether these changes result in alterations in brain volume.

Substantial evidence shows that ovarian sex hormones, which demonstrate considerable variation throughout a female’s life span, play a significant role in altering brain morphology and function [15]. Nevertheless, research on the impact on hormonal fluctuations and brain morphology of female with offspring and nulliparous is insufficient; thus, this research primary aims to investigate the changes in hormonal fluctuations and brain morphology at two distinct stages among women.

Participants

The study protocol was a cross-sectional study research. All MR images were obtained with local research ethics committee permission from healthy women with offspring and nulliparous who had signed informed consent forms.

A total of 66 reproductive females aged from 20 to 40 years were enrolled, including 35 offspring women, and 31 nulliparous. Both groups had no prior history of psychiatric or neurological diseases. All participants underwent physical and neurological examinations, and they were interviewed by an obstetrician-gynecologist.

Data collection

Inclusion criteria

Women were selected in accordance with the following criteria. First, the age from 20 to 40 years old, women with offspring are those who have experienced pregnancy, childbirth, and child rearing, regardless of whether they have had a miscarriage. Nulliparous women are those who have never experienced pregnancy. Second, the selected women should have no prior history of hysterectomy/bilateral oophorectomy or psychiatric/neurological illnesses. Third, women should have no prior history of hormone and steroid treatment or oral contraception before study participation.

Measurement of serum sex hormones

We measured the level of E2, testosterone (T), prolactin (PRL), FSH, luteinizing hormone (LH), and P using chemiluminescent immunoassay and electrochemiluminescence immunoassay by using the E620 automatic analyzer. Hormonal measurements were conducted on the second day after the onset of menstruation (early follicular phase) for females with a normal menstrual cycle between 8:00 am to 9:30 am on an empty stomach.

Brain MRI acquisition and preprocessing

MRI examinations were performed using a 3T MRI scanner (Siemens MAGNETOM Prisma) with a 32-channel adult head coil. Brain images were acquired using the 3-dimensional T1-weighted magnetization-prepared rapid gradient echo, and the scan parameters were as follows: TR/TE, 2300/2.32 ms; FOV read, 256 mm; flip angle, 8°; slice thickness, 1 mm; voxel size, 1 mm × 1 mm × 1 mm; acquisition time, 3 min 54 s.

Voxel-based morphometry (VBM) was performed using Computational Anatomy Toolbox 12 (CAT12), which was based on Statistical Parametric Mapping program, version 12 (SPM12) in the Matlab. Several preprocessing steps were carried out on the images, including format conversion from the original DICOM format to the nifti format. The images were spatially registered to the Montreal Neurological Institute (MNI) space using the DARTEL method to improve accuracy. The images were segmented into GMV, white matter volume (WMV), and cerebrospinal fluid (CSF) to analyze their contributions to the overall brain structure. Next, we smoothed the gray matter images using an isotropic Gaussian kernel with a full width half maximum of 8 mm to improve the signal-to-noise ratio. Covariates such as total intracranial volume (TIV) and age were extracted and estimated to control for potential confounding effects. Finally, two independent sample t-tests were performed between groups.

Statistical analysis

All statistical analyses were performed using the statistical package for social sciences (SPSS ver.20). If the data conform to normal distribution, then such data are expressed by means and standard deviation (M ± SD) and analyzed using an independent two-sample t-test. If the data do not conform to normality, then such data are represented by M (Q1–Q3) and analyzed using Mann Whitney U test compared with the two groups. When the p-value < 0.05, a statistical difference is observed between the two groups. Morphological analysis of initial voxel threshold was set to 0.001 uncorrected, and the cluster size was set at 100 voxels. The results were considered significant only if the voxel-level family-wise-error rate corrected p-value was < 0.05.

Demographic and clinical information results

Table 1 shows the results of statistical analysis between the two groups, including demographic and clinical information of all the enrolled subjects. No significant differences in sex hormones were observed, including E2 (z = − 0.28, p = 0.782), LH (z = − 0.62, p = 0.537), and P (z = − 1.34, p = 0.181). By contrast, significant differences were observed in FSH (z = 3.86, p < 0.001), T (z = − 3.92, p < 0.001), and PRL (z = − 3.27, p = 0.018). The sex hormone levels between the two groups, the level of FSH for offspring women was higher than nulliparous, whereas T and PRL were lower.

No significant differences in WMV (t = 0.89, p = 0.378) and TIV (t = − 0.21, p = 0.838) were observed. On the contrary, significant differences in CSF (t = − 2.39, p = 0.020), CSFf (t = 2.98, p = 0.004), GMV (t = − 3.53, p = 0.001), GMVf (t = − 4.89, p < 0.001), and WMVf (t = 2.38, p = 0.020) were found. The CSF, CSF fraction, and WM fraction of the offspring group were larger than those of the nulliparous group. The GMV and GMVf of the offspring group were smaller than those of nulliparous females.

Table 1

The comparison of sex hormones and brain volume between groups
	Nulliparous(n = 31) (Age 20–40)	With offspring(n = 35) (Age 20–40)	z/t	P vaule
E2	31.55(23.11–34.98)	27.59(18.36–47.28)	-0.28	0.782
LH	6.31(4.77–8.18)	5.34(4.15–11.11)	-0.62	0.537
FSH	5.33(4.76–6.52)	7.83(6.56–11.26)	3.86	< 0.001
T	0.36(0.25–0.48)	0.18(0.08–0.30)	-3.92	< 0.001
P	0.53(0.29–0.68)	0.44(0.18–0.62)	-1.34	0.181
PRL	21.70(14.00-35.16)	13.71(9.45–21.21)	-2.37	0.018
GMV	655.00 ± 45.19	617.23 ± 41.78	-3.53	0.001
GMVf	47.89 ± 2.09	45.27 ± 2.23	-4.89	< 0.001
GSF	232.94 ± 37.94	257.23 ± 43.99	2.39	0.020
GSFf	16.98 ± 2.21	18.80 ± 2.68	2.98	0.004
WMV	481.32 ± 45.21	490.26 ± 36.45	0.89	0.378
WMVf	35.12 ± 1.35	35.93 ± 1.42	2.38	0.020
TIV	1369.45 ± 101.67	1364.63 ± 88.70	-0.21	0.838

GMV: gray matter volume; GMVf: gray matter volume fraction; CSF: cerebrospinal fluid; CSFf: cerebrospinal fluid fraction; WMV: white matter volume; WMVf: white matter volume fraction; TIV: total intracranial volume.

Gray matter volume changes

For GMV changes in the entire brain of women with offspring and the nulliparous group, two clusters were observed. Figure 1 and Fig. 2 show the locations of these clusters in the standard brain. Clusters with reduced GMV in the offspring group were located in the left superior frontal gyrus (SFG) and right putamen (FDR corrected, p < 0.05). Detailed information of brain regions with significant GMV differences is shown in Table 2.

Table 2

The results of voxel-based morphometry (VBM) analysis
Comparison	Region	Coordinates(mm)			p	t
Comparison	Region	x	y	z
Fertile with offspring < nulliparous female	Left superior frontal gyrus	-10	48	32	0.010	4.80
Fertile with offspring < nulliparous female	Right Lentiform Nucleus, Putamen	32	-2	0	0.000	4.67

In our study, we measured the differences in sex hormones and brain morphology between nulliparous and females with offspring and found significant differences in sex hormones; females who had offspring had higher FSH and lower T and PRL levels compared with those without nulliparous female. Brain volume analysis showed that the GMV of females with offspring was decreased compared with nulliparous female. In addition, the decreased volume was located in the left SFG and right putamen, whereas no regions of increased brain volume were observed in fertile women compared with nulliparous women.

Women experience significant changes in circulating hormone levels throughout their lives, including monthly fluctuations in the menstrual cycle, puberty, pregnancy, and menopause [16]. Sex steroids such as E2 and T are predominantly produced by the gonads. E2 is significant in adolescent growth [17]. Estrone and estradiol are the two majorly biologically active E2 in non-pregnant women. Pregnant women also produce significant quantities of estriol. During pregnancy, E2 and progesterone (P) levels increase steadily across the three trimesters and then rapidly return to baseline following parturition [18]. Notably, the occurrence of postmenopausal-like acidic FSH isoforms precedes the increase of FSH before menopause [19]. In short, women’s sex hormones undergo constant changes throughout different cycles.

Female sex hormones play a role in different areas of emotional processing [20]. Studies have shown that sex steroids play a role in the progression of specific forms of neurodegeneration. E2 and T were reported to be neuroprotective [21][22].Sex hormones can also act on organs outside the gonads, and PRL has broad potential in the treatment of metabolic and advanced liver diseases [23]. In addition, sex hormones play a fundamental role in contributing to specific cardiovascular and coronary risks [24]. Based on a previous report, sex hormones have an impact on obesity and metabolic obesity inflammation [25].

Our study indicates that hormonal differences exist between women who have given birth and those who have not. In particular, FSH levels increase, while T and PRL levels decrease in women who have given birth. FSH is critical for ovarian folliculogenesis and essential for female fertility. It binds to FSH receptors and regulates estrogen production in ovarian granulosa cells to orchestrate female reproductive physiology [26]. The increased FSH level in females with offspring may be due to a series of pregnancy processes in which the hormonal changes are complex, and FSH plays an important role in pregnancy [27]. Animal experimental studies have shown that the loss of FSH gene could lead to a decrease in placental blood flow, leading to a decrease in embryonic weight or death [28]. Therefore, FSH plays an important role in maintaining embryonic growth, with FSH increasing in the fertilized group compared with the unfertilized group, which may be due to an increase in FSH production that promotes placental growth during pregnancy. Some studies have reported the beneficial action of PRL on fertilization in various species [29]. The high PRL levels in nulliparous women of appropriate age may be due to preparation for future fertilization. Some studies indicate that T and PRL play a significant role in the formation of a zygote. The expression of post-ovulatory cumuli oophori containing unfertilized eggs is higher than that containing fertilized eggs, which is consistent with our results [30]. The group involved in our study focused on women of reproductive age between 20 and 40 years old, and the age span is relatively large. Whether age has an impact on sex hormone outcomes needs further research.

Our results demonstrated that the GMV of females with offspring was reduced compared with that of nulliparous females, and VBM analysis revealed that GMV was primarily located in the left SFG and right putamen region. The process of pregnancy, childbirth, and child rearing involves significant changes in women’s psychology because of the alterations in the surrounding environment, which leads to a decline in partial brain volume in the brain regions involved in social processes. The result indicates that pregnancy alters the GM structure of the human brain and provides initial support for adaptive processes that serve as the transition to motherhood [31]. Previous studies have reported that pregnant women experience persistent GMV reduction for at least 2 years, and the authors reported a long-term decrease in GMV, which was most pronounced in regions important for social cognition, namely, anterior midline and posterior midline structures, bilateral prefrontal cortex, and bilateral temporal cortex [31]. The cross-over relationship between GM volume changes during pregnancy and cognitive components of the human associative cortex [32] and the overlapping quantification between the results of Schurz et al.’s theory of mind meta-analysis confirmed the spatial similarity among genetic changes during pregnancy and the theory of mind network [33]. The left SFG is associated with learning, memory, and depression [34][35] and the right putamen is associated with anhedonia [36]. A decline in the brain volume of these regions in women who have given birth may indicate reduced function and susceptibility to affective disorders.

The difference in brain volume between nulliparous and females with offspring could be attributed to hormonal effects. Sex steroid hormones regulate neuronal morphology and number, and changes in endogenous or exogenous hormonal levels greatly affect the structure and function of the human brain [37]. Thus, sex steroid hormones served as an important regulator of neuronal morphology and number [38]. Different hormones act on different targets in the brain. Catenaccio et al. reviewed the association of sex hormones during hormonal transition periods and brain structure in women, including menstrual cycle, pregnancy, and menopausal transitions and found the most prominent effects of sex hormones on limbic brain structures [39]. Kim et al. [40] demonstrated that the serum estradiol level positively correlated with the GMV of the motor area (Mos), inferior frontal gyrus (IFG), and superior temporal gyrus (STG), and FSH negatively correlated with the GMV of the Mos, IFG, and STG. In general, the process of female childbirth and pregnancy is complex, and reproduction is related to many levels of neural changes, including regional changes in dendritic morphology, cell proliferation, and gene expression [41].

Previous studies have reported that hormones may cause changes in WMV [42], which is different from our results, and our findings showed no difference in WMV between the offspring and nulliparous female. However, a difference in GMVf was observed, which may be due to different subjects and insufficient sample size; thus, further investigation of this field is necessary. In addition, the relationship between age and brain volume has been reported [43]. Considering that the age of childbearing women is generally older than that of nlliparous women, age can lead to a decrease in cerebral cortex volume. We included age as a covariate in VBM analysis to minimize the inaccuracy arising from this factor.

Limitations

This study has several limitations that must be taken into consideration. First, the sample size utilized in this research is relatively small, with only 66 cases. Therefore, a larger and more comprehensive studies must be conducted to verify the reliability of our findings. Second, our research only included cases of women who have already given birth, and it did not consider the number of children and the time of reproduction. Thirdly, all the included age groups are between 20 and 40 years old, because this age group is the most fertile, so there is no subgroup comparison based on different ages, and the results may produce age differences. In the future, we will conduct more detailed research on this section. Finally, we control age and TIV as covariates in voxel-based morphological research, while we cannot entirely rule out their impact on the brain structure.

After conducting our study, we have identified notable variations in sex hormones and brain morphology between females with offspring and nulliparous. In particular, we observed a decrease in the cortex volume in the left SFG and right putamen regions using VBM analysis. These findings indicate that the considerable changes that arise during reproduction may reduce specific functions, which can affect women’s natural developmental course. Our results provide further insight into the complex relationship among hormones, brain structure, and behavior in female development.

Ethics approval and consent to participate

Approval was obtained from the ethics committee of Longgang Central Hospital of Shenzhen. Approval number:2023ECPJ045.

Data and materials availability

If necessary, we can provide corresponding data materials upon request.

Competing interests

No competing interests.

The authors did not receive support from any organization for the submitted work.

Funding

Not applicable.

Authors’ contributions

Huo Huiyan contributed to the study design and conceptualization. Yu Chunyan reviewed the literature. Sun Qiyuan performed the analysis. All authors provided technical support and critically reviewed the manuscript for its intellectual content. Zhang Lingyan had final responsibility to submit for publication. All authors read drafts of the paper and approved the final version.

Acknowledgements

The authors acknowledged all employees of the longgang central hospital imaging department for their support.

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No competing interests reported.

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Differences in sex hormones and brain morphology between females with offspring and nulliparous

Status:

Version 1

Abstract

Background

Methods

Results

Conclusion

Figures

Background

Methods

Participants

Data collection

Inclusion criteria

Measurement of serum sex hormones

Brain MRI acquisition and preprocessing

Statistical analysis

Results

Demographic and clinical information results

Gray matter volume changes

Disscussion

Limitations

Conclusion

Declarations

References

Additional Declarations

Status:

Version 1