1
Department of Clinical Nursing, Division of Health Sciences and Engineering, University of
Guanajuato, Guanajuato, Mexico
2
Department of Physical Engineering, Division of Sciences and Engineering, University of
Guanajuato, Guanajuato, Mexico
3
Industrial Technical Teaching Center (CETIS), Mexico & University of
Guadalajara., Guadalajara, Jalisco,
*4Department of Applied Science to Work, Division of Health Sciences, University of Guanajuato, Guanajuato, Mexico
Corresponding author details:
Maria-Raquel Huerta-Franco
Department of Applied Science to Work
Division of Health Sciences Campus Leon, University of Guanajuato Aquiles Serdán No. 924 Colonia Obregon
Guanajuato,Mexico
Copyright: © 2018 García-Campos ML, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 international License, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited.
Objective: The purpose of this study was to determine the relationship between mood, attitudes toward sexuality (ATS), feelings of empty nest syndrome (FENS), marital satisfaction (MS) and sex hormones in type 2 diabetic patients and non-diabetic subjects.
Research design and Methods: We studied 50 non-diabetic subjects (25 male, 25 female) and 50 type 2 diabetic subjects using a cross-sectional design (25 male, 25 female). Inclusion criteria for type 2 diabetic patients were determined according to the American Diabetes Association Criteria. Mood, FENS, ATS and MS were evaluated. Sex hormones and insulin levels were assessed using RIA kits.
Results: Type 2 diabetic women had a higher score of depression (p = 0.008) and anxiety (p = 0.01) than did both the control and diabetic men. Diabetic patients had significantly higher scores of sleep alterations (p = 0.03) and NSSD (p = 0.02) than the non-diabetic subjects. In female subjects, estrogens (E) were inversely related to anxiety (p = 0.02), and depression (p = 0.04) and directly to ATS (p = 0.002); dehydroepiandosterone sulfate was inversely related to MS (p < 0.001). In all male and the non-diabetic male free testosterone (FT) was inversely related to depression (p = 0.01 and p = 0.005, respectively) and anxiety (p = 0.005 and p < 0.001, respectively).
Conclusions: The diabetic and non-diabetic females had higher level of depression and
anxiety than did both the control and diabetic males. Diabetic males had higher scores of
sleep alterations and NSSD than control male. E in female and FT in males had an inverse
relationship with depression and anxiety. The role of sex hormones in mood alterations of
both diabetic and non-diabetic subjects should be further studied.
Mood; Attitudes; Sexuality; Marital satisfaction; Diabetes
Type 2 diabetic patients have a higher risk of mood alteration than do healthy control subjects [1-4]. While reports on mood alterations vary among different studies, in part due to the different methodologies used and to other aspects of to the subjects’ life situations [1-4], consistently a high proportion of women suffer physical and psychological symptoms, usually attributed to stage of the reproductive cycle [5,6]. The relationship between mood alterations and sex hormone levels in type 2 diabetic patients is not yet clear [1,3,5,6]. In type 2 diabetic and non-diabetic subjects it has been demonstrated that a short-term hypogonadism is enough to initiate symptoms of depression [7]. However, in O’Connor’s study [8], treatment with testosterone did not increase or change aggressive behavior nor did it induce any changes in non-aggressive or sexual behavior.
The basis for mood alterations in patients with type 2 diabetes is unknown, but it is likely complex, involving interactions among psychological, physical, endocrine, and genetic factors [3,6,9]. However, a clear evidence of the effects of sex steroids in the cognition and brain activity, have been demonstrated [10]: a) Estrogens facilitate cognitive function, acting in the hippocampus, and the prefrontal cortex through the formation of synapses using the genomic pathways; and the so-called fast, non-genomic pathways (through alpha- and beta-receptors bound to the membranes, and through G proteins coupled to the estrogen receptor). b) Estrogens promote the synthesis of neurotrophins, modulate cholinergic neurotransmitters, and dopaminergic, and protect the brain against stress, and inflammation. c) 17B-estradiol increases cognitive function in brain areas related to learning and memory (studies in animal models). d) 17B-estradiol in the prefrontal region of postmenopausal women improves cognitive function and working memory, and attention. e) Progesterone has trophic effects on the brain development from adolescence to adulthood. f) Together, estrogens and progesterone act on neuronal function, forming synapses, increasing synaptic transmission and through neuroprotective effects. g) Progesterone receptors have been identified in regions of cognitive function such as frontal cortex, hypothalamus, thalamus, hippocampus, amygdala, and cerebellum. Also, it has been demonstrated a positive relationship between FSH and cognition; higher levels of FSH have been associated to better cognition. So, gonadotropins may also play a role in mediating cognitive performance [10].
Due to the evidence presented previously and the lack of studies
in type 2 diabetics on the subject in question, the purpose of the
present study was to extend this finding by comparing mood and
sex hormone levels of type 2 diabetic male and female patients with
those of control healthy subjects.
Subjects were recruited after the protocol was approved by the Human Ethics Committee of our institution, and written informed consent was obtained from all participants. The study was conducted in accordance with the Declaration of Helsinki.
Somatic and psychological symptoms: Symptoms of depression were evaluated using the Hamilton Scale [14]. This scale included nine aspects of mood and sleep alteration. These included difficulties falling asleep, alterations in midnight sleep or alterations in early morning sleep. The NSSD were evaluated according to our previous studies [1,6,14], and included: digestive problems, loss of sexual interest, and recent loss of weight. Anxiety index was based on 16 symptoms, which included breathlessness, palpitations, tremors, agitation, fear, and others, as described by the Diagnostic and Statistical Manual of Mental Disorders (DSM-IV-TR) [15]. The FENS, as described in our previous work [6,14], included 11 binary questions.
Attitudes toward sexuality (ATS): This aspect was assessed with 13 questions as described in our previous work and evaluated the participant’s opinions on gender roles in society, such as the role of women as homemaker, the importance of physical attractiveness, and women’s role in initiating sexual activity when postmenopausal [6].
Self-Esteem: Patients’ sense of self worth was assessed using the Coppersmith test [14], previously validated on a Mexican population [16].
Marital Satisfaction: The marital satisfaction scale previously validated in our population by Pick and Andrade was used in this study [17]. This instrument includes 24 questions and assesses three aspects of the marital relationship: 1) satisfaction with marital interaction, 2) satisfaction with emotional characteristics of the spouse and 3) satisfaction with structural and organizational aspects of the spouse’s personality.
SECS = Socioeconomic Status; Waist: Hip = Waist to Hip Ratio; Abdomen: Hip = Abdomen to Hip Ratio; Systolic BP = Systolic
Blood Pressure; Diastolic BP = Diastolic Blood Pressure; FGL = Fasting Glucose; PGL = Postprandial Glucose; FI = Fasting Insulin;
PI = Postprandial Insulin; TCh = Total Cholesterol; TG = Tryglicerides; HDL = High density lipoproteins; VLDL = Very low-density
Lipoproteins; % Body fat = Body fat (percentage, considering the total body weight). Post-hoc Less Significant Differences Test: †p <
0.05; *p < 0.05; ‡p < 0.01; §p < 0.01; ||p < 0.001; ¶p < 0.001; #p < 0.001; **p < 0.001
Table 1: Shows significant differences in anthropometric and metabolic variables between diabetic patients and control subjects Mean
± SD
LH = Luteinizing Hormone; FSH = Follicle Stimulating Hormone; E = Estrogens; TT = Total Testosterone; FT = Free Testosterone; DHEASO4
= Dehydroepiandrosterone Sulfate Hormone; SHBG = Sex Hormone Binding Globulin; T = Student´s T test for Independent Samples
Table 2: Serum levels of sex hormones in diabetic patients and non-diabetic control subjects Mean ± SEM (Note that diabetic subjects
had significantly higher levels of both LH and SHBG)
ATS = Attitudes Toward Sexuality; FENS = Feelings of Empty Nest Syndrome; NSSD = Non- Specific Symptoms of Depression; LH = Luteinizing
Hormone; FSH = Follicle Stimulating Hormone; TT = Total Testosterone; FT = Free Testosterone; DHEA-SO4
= Dehydroepiandrosterone
Sulfate Hormone; SHBG = Sex Hormone Binding Globulin
Table 3: Results of forward stepwise Multiple Regression Analysis for Diabetic and Non-Diabetic Patients
In this study, we demonstrated the relationship between sex hormone levels and mood in diabetic patients and non-diabetic control subjects. Estrogen serum levels (in females) and free testosterone (in males) exhibited significant and inverse relationships with depression and anxiety. Some investigators explain the influence of sex hormones on mood in female subjects [11,18,19]. The explanation of these findings is that in female subjects with advancing age, sex hormone levels decrease and therefore affect change on specific regions of the brain [10,20]. In contrast, in men there is currently not enough information regarding the role androgens play in modulating change at the level of the central nervous system [21].
In this study we found that ATS show a direct relationship with the estrogen serum levels for diabetic and non-diabetic female subjects. However, testosterone and free testosterone had an indirect relationship with ATS in the control subjects. These results demonstrate that in the female subjects, those with higher estrogen serum levels had higher score of ATS, but the score decrease when free or total testosterone levels increased. Studies of the relationship of sex hormones and sexual desire in humans have produced varying and contradictory findings [21-23]. For example, it was demonstrated in two studies with a large sample size that estrogens had no effect on either sexual function [21] or on sexual satisfaction [22].
Although diabetes is related to psychological changes [9], we did not find significant differences in psychological evaluation scores between diabetic and non-diabetic females. However, diabetic males had significantly higher scores of sleep alteration and non-specific symptoms of depression (lost of sexual desire, weight loss, and loss of appetite), than non-diabetics males. Male diabetic subjects also had significantly higher LH and SHBG levels than non-diabetic males (p = 0.04 and p = 0.01, respectively). Iranzo et al. [24] did not find significant differences in androgen, LH, FSH, 17-B estradiol, SHBG, and prolactin serum leves between patients suffering idiopathic REM sleep disorder with healthy controls.
Recently, it has been demonstrated that metabolic variables play an important role in sleep disturbances [25]. In this study, we demonstrate three important findings that support this hypothesis: i) the male and female diabetic subjects show significantly higher triglyceride and VLDL serum levels than did the control group of female subjects; ii) diabetic males had significantly higher scores of sleep alterations and non-specific symptoms of depression than non-diabetics males; and iii) we observed an indirect relationship between HDL and sleep-alterations in the group of male subjects (diabetic and non diabetic) (β = 0.27, p = 0.008). The significance of this relationship held true when we analyzed only diabetic males (β = 0.41, p = 0.04).
In this study as well as in others [26,27], symptoms of depression and anxiety were significantly greater in females than in males. The reasons for this gender difference can be explained in different ways: i) in female subjects with advancing age, sex hormone levels decrease, and this could be related with alterations in cognition and brain activity [10]. These findings have not been well demonstrated in males [20]; and ii) the socio-cultural factors, education, and other circumstances that differentially effect males and females could explain the differences in psychological symptoms seen between genders [20]. Future studies will be necesary to evaluate the effects of the progression of the disease on sex hormone levels. With this information, we will be able to better understand the effects of diabetes on mood alterations and how these changes vary with gender [28,29].
Obesity is another variable associated with several psychological alterations, such as low self-esteem, depression and anxiety [14]. Consistent with this hypothesis, we found that in both diabetic and non-diabetic female subjects there is a significant inverse correlation between self-esteem and abdomen to hip ratio. For the diabetic males, we found an inverse correlation between BMI and NSSD. Although different investigators have demonstrated the relationship between obesity and psychological problems, there has not yet been any published data regarding the effects of obesity on the production of sex hormones, and the effects of these variables on the brains of diabetic patients. In this study we found that male subjects with higher BMI had lower levels of total testosterone. Testosterone also showed an inverse relationship with weight for non-diabetic males.
In type 2 diabetic males, a negative relationship was observed of
waist to hip ratio with estrogen serum levels (p = 0.002). However,
in type 2 diabetic female subjects, total testosterone (p = 0.001) and
DHEA-SO4
(p = 0.01) showed a direct relationship with weight. So,
it is important to clarify the role of weight, BMI and obesity in the
production of androgens in female diabetic subjects and estrogens
in the case of male diabetic subjects, and how these hormones levels
affect the central nervous system.
In conclusion, the diabetic and non-diabetic females had an
overall higher level of mood alteration than did the males from both
groups. Diabetic males had higher scores of sleep alteration and
non-specific symptoms of depression than did control males. The
estrogen serum levels in female and free testosterone in males had
inverse relationships to depression and anxiety. In both diabetic and
non-diabetic females, DHEA-SO4 had an inverse relationship with
marital satisfaction. More studies must be done to elucidate the role of sex hormones in mood alterations of both diabetic and nondiabetic subjects.
This work was supported in part by The Council of Science and
Technology of the State of Guanajuato, and by the Mexican Institute
of Social Security (IMSS), which provided economic support for the
involved student.
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