Abstract
We previously reported the association of positive psychosocial conditions with diabetic nephropathy (DN) in patients with type 2 diabetes in a cross-sectional setting. In the present study, we evaluated the association between six indicators related to psychosocial conditions and the progression of DN assessed by estimated glomerular filtration rate (eGFR) and albuminuria during 2-year observation period in 252 patients with type 2 diabetes. In unadjusted model, the subjects with higher happiness score attenuated reduced eGFR, and those with more social support attenuated increase in alubuminuria and decline eGFR. However, in adjusted model for happiness score and social support, only happiness score indicated the significant association with reduced eGFR. Gender-segregated analysis showed a significant association between happiness score and ΔeGFR in male but not in female subjects. On the other hand, decrease in eGFR was significantly attenuated in the subjects with more social support as compared to those with less social support in women but not in men. These results suggested that that psychosocial conditions could be related to the progression of DN, and that the psychosocial factors that influence in DN might differ between men and women, in Japanese patients with type 2 diabetes.
Electronic supplementary material
The online version contains supplementary material available at 10.1007/s13340-020-00479-x.
Keywords: Psychosocial factors, Social support, Diabetic nephropathy
Introduction
Many previous studies have shown that psychosocial condition affects health. Such relationship is also observed in patients with diabetes mellitus (DM). It was reported that affective disorders, including depression, induced poor adherence and reaction to medical treatment in patients with DM [1, 2] and that depression was associated with hyperglycemia [3]. On the other hand, social support has been reported to play an important role in maintaining health-promoting behaviors, including diet, physical activity, and medication compliance, which lead to good glycemic control [4, 5].
Similar associations have also been reported between psychosocial factors and macro- or microvascular diabetic complications [6, 7]. We had previously assessed the association between positive psychosocial conditions and diabetic nephropathy (DN) in Japanese patients with diabetes in a cross-sectional analysis of baseline data of an ongoing prospective observational study [8]. In the present study, we aimed to confirm the association between positive psychosocial condition and DN, by utilizing the longitudinal data of the above-mentioned project.
Materials and methods
Study design and study population
The subjects of the ongoing prospective observational study were recruited from Japanese type 2 diabetic patients at Osaka University Hospital in Osaka, Japan as previously reported [8]. The eligibility criteria were as follows: (1) diagnosed as type 2 diabetes based on the criteria of the Japan Diabetes Society; (2) ≥ 30 years, but < 80 years of age. In the present study, we used the baseline data and the second-year data for analysis. The progression of DN was evaluated using the change of estimated glomerular filtration rate (eGFR) and urinary albumin-to-creatinine ratio (UACR) during a 2-year observation period (value at the second year–value at baseline). Since UACR showed non-normal distribution, logarithmic transformation was performed.
Assessment of psychosocial conditions
Using an individual questionnaire, we assessed six indicators related to psychosocial conditions: happiness score, dispositional optimism, laughter frequency, self-awareness of stress, social network, and social support. Happiness score, a single-item score, was evaluated from 1 to 10, with 10 as the highest level of happiness. To evaluate dispositional optimism, the life orientation test-revised (LOT-R) was used [9]. The items of laughter frequency and self-awareness of stress were evaluated with four-level scales. Social network and support are broadly defined as the existence or connection of people on whom one can rely. To evaluate these items, the social network index (SNI) [10] and the ENRICHD social support instrument (ESSI) [11] were adopted, respectively. It has been confirmed that all of these six indicators reflect one factor; ‘positive psychosocial factors’ in our previous reports [8]. Happiness score and LOT-R were analyzed as continuous variables, and the others were divided into dichotomous variables. The details of these indicators were described in our previous report [8].
Statistical analysis
The rate of decline both eGFR and UACR was considered to be influenced by the initial values of those [12, 13]. The associations between psychosocial conditions and the progression of DN were assessed using Pearson’s correlation coefficient for continuous variables and analysis of co-variance for dichotomous variables. In the multivariate analysis, the baseline characteristics that were significantly associated with psychosocial factors were adopted as adjusted factors, and linear regression model was used. P value of less than 0.05 was considered to indicate significance. The statistical analyses were performed using SPSS version 22 (SPSS, Inc., Chicago, IL, USA).
Results
349 participants were initially enrolled, and the present analysis was conducted using the data from 252 participants excluding 97 participants because of missing UACR at baseline or second-year. Among them, 79 patients (31.3%) had been diagnosed as DN at baseline (Table 1). Over 2 years, only 35 participants (13.6%) advanced the stage of DN and no participants progressed to ESRD.
Table 1.
Baseline characteristics of study subjects
| Characteristic at baseline | |
|---|---|
| Sex (male) | 132 (52.4%) |
| Age | 66.3 ± 8.6 |
| Duration of diabetes (years) | 14.8 ± 12.4 |
| Body mass index (BMI) (kg/m2) | 25.5 ± 4.8 |
| Alcohol (once a week or more) (n = 250) | 84 (33.6%) |
| Current smoker (n = 251) | 30 (11.9%) |
| HbA1c (%) | 7.6 ± 1.3 |
| Creatinine (mg/dL) | 0.83 ± 0.27 |
| eGFR (ml/min/1.73 m2) | 67.8 ± 17.3 |
| Total cholesterol (mg/dL) | 188.7 ± 36.2 |
| Triglyceride (mg/dL) | 175 (83–165) |
| LDL cholesterol (mg/dL) | 106.2 ± 26.5 |
| HDL cholesterol (mg/dL) | 56.1 ± 16.7 |
| Hypertension | 173 (68.7%) |
| Dyslipidemia | 163 (64.7%) |
| Malignancy | 57 (22.6%) |
| Macroangiopathy | 48 (19.0%) |
| Nephropathy | – |
| Microalbuminuria | 58 (23.0%) |
| Macroalbuminuria and eGFR ≥ 30(ml/min/1.73 m2) | 18 (7.1%) |
| Macroalbuminuria and eGFR < 30(ml/min/1.73 m2) | 3 (1.2%) |
| Under dialysis | 0 (0%) |
| Retinopathy (n = 227) | 70 (30.8%) |
| Neuropathy (n = 238) | 95 (39.9%) |
| Medications | |
| Antidiabetics | 227 (90.1%) |
| Insulin | 83 (32.9%) |
| Antihypertensives | 160 (63.5%) |
| Renin–angiotensin system inhibitors | 136 (54.0%) |
| Lipid lowering drugs | 132 (52.4%) |
| Psychosocial factor | |
| Happiness score (range 1–10, higher = happier) | 7.4 ± 1.6 |
| Optimism: LOT-R (n = 247) (range 0–24, higher = greater optimism) | 13.8 ± 2.9 |
| Laughter frequency (n = 249) | |
| Non-everyday laughter | 147 (59.0%) |
| Almost-everyday laughter | 102 (41.0%) |
| Self-awareness of stress (n = 251) | |
| More stress (“always” and “often”) | 76 (30.2%) |
| Less stress (“sometimes” and “rarely”) | 175 (69.8%) |
| Social network: SNI (n = 247) | |
| Low connection (SNI score: 0 and 1) | 110 (44.5%) |
| High connection (SNI score: 2–4) | 137 (55.5%) |
| Social support: ESSI (n = 247) | |
| Less support (ESSI score: 5–26) | 130 (52.6%) |
| More support (ESSI score: 27 to 31) | 117 (47.4%) |
Values are shown as mean ± SD, median (interquartile), or number (percentage). Macrovascular disease includes ischemic heart disease, cerebrovascular disease, and peripheral artery disease. Microalbuminuria was defined as UACR ≥ 30 and < 300 mg/gCr, and macroalbuminuria was defined as UACR ≥ 300 mg/gCr
HbA1c hemoglobin A1c; eGFR estimated glomerular filtration rate; LDL-C low-density lipoprotein cholesterol; HDL-C high-density lipoprotein cholesterol; UACR urinary albumin-to-creatinine ratio; SNI The social network index; ESSI The ENRICHD social support instrument
Happiness score was significantly associated with ΔeGFR (r = 0.17, p = 0.006): decrease in eGFR was attenuated in the subjects with higher happiness score. There was no significant association between happiness score and ΔLg(UACR) (r = 0.05, p = 0.439). Decrease in eGFR was also attenuated in the subjects with more social support as compared to those with less social support (− 1.8 ± 8.5 ml/min/1.73 m2 vs. − 4.4 ± 9.8 ml/min/1.73 m2, p = 0.010). Increase in the Lg(UACR) was also attenuated in the subjects with more social support as compared to those with less social support (0.09 ± 0.53 vs. 0.19 ± 0.56, p = 0.040) (Table 2). The other 4 indicators of psychosocial conditions were not significantly associated with the progression of DN.
Table 2.
Associations between indices of psychosocial conditions and the progression of diabetic nephropathy
| ΔeGFR | ΔLg (UACR) | |||
|---|---|---|---|---|
| r | p value | r | p value | |
| Happiness score (range 1–10, higher = happier) | 0.17 | 0.006 | 0.05 | 0.439 |
| Optimism: LOT-R (n = 247) (range 0–24, higher = greater optimism) | 0.08 | 0.232 | − 0.01 | 0.863 |
| ΔeGFR | p value (difference between groups) | ΔLg(UACR) | p value (difference between groups) | |
|---|---|---|---|---|
| Laughter frequency (n = 249) | ||||
| Non-every day laughter | − 3.0 ± 8.6 | 0.828 | 0.03 ± 0.57 | 0.098 |
| Almost-every day laughter | − 3.2 ± 9.4 | 0.17 ± 0.55 | ||
| Self-awareness of stress (n = 251) | ||||
| More stress (“always” and “often”) | − 5.0 ± 10.0 | 0.097 | 0.12 ± 0.57 | 0.667 |
| Less stress (“sometimes” and “rarely”) | − 2.3 ± 8.8 | 0.15 ± 0.55 | ||
| Social network: SNI (n = 247) | ||||
| Low connection (SNI score: 0 and 1) | − 3.3 ± 8.1 | 0.960 | 0.85 ± 0.55 | 0.418 |
| High connection (SNI score: 2–4) | − 3.1 ± 10.2 | 0.18 ± 0.57 | ||
| Social support: ESSI (n = 247) | ||||
| Less support (ESSI score: 5–26) | − 4.4 ± 9.8 | 0.010 | 0.19 ± 0.56 | 0.040 |
| More support (ESSI score: 27–31) | − 1.8 ± 8.5 | 0.09 ± 0.53 |
Values are shown as mean ± SD, median (interquartile). Δ values express the difference between second-year values and baseline. Analysis using Pearson’s correlation coefficient was performed to evaluate the association between the change of eGFR and Lg(UACR) for continuous variables, Happiness score, and optimism (LOTR). The association between the progression of nephropathy and the dichotomous items such as laughter frequency, self-awareness of stress, social network, and social support were assessed using covariate analysis. p value of less than 0.05 was considered to indicate significance
Happiness score was significantly associated with age and body mass index (BMI). Social support was significantly associated with sex: females showed a higher proportion of receiving more social support (Table 3). In addition, happiness score was also significantly associated with mean plasma glucose level (r = − 0.17, p = 0.009) and mean BMI (r = − 0.15, p = 0.016) at baseline and second year, but not with mean blood pressure (r = − 0.05, p = 0.421) and mean HbA1c (r = − 0.08, p = 0.205). On the other hand, social support did not show any significant association with these factors (data not shown).
Table 3.
Associations between baseline characteristics and happiness score and social support score
| Happiness score (n = 252) | Social support (n = 247) | ||||
|---|---|---|---|---|---|
| r | p value | Less-support (n = 130) | More-support (n = 117) | p value | |
| Sex (male) | − 0.08 | 0.232 | 78 (60.0%) | 51 (43.6%) | 0.010 |
| Age (years) | 0.14 | 0.023 | 66.6 ± 9.3 | 65.8 ± 7.9 | 0.462 |
| Duration of diabetes (years) | − 0.04 | 0.527 | 15.9 ± 11.1 | 14.6 ± 8.8 | 0.321 |
| Body mass index (kg/m2) | − 0.15 | 0.019 | 25.3 ± 5.4 | 25.9 ± 4.2 | 0.382 |
| HbA1c (%) | − 0.08 | 0.198 | 7.6 ± 1.4 | 7.6 ± 1.3 | 0.966 |
| Hypertension | − 0.05 | 0.418 | 93 (71.5%) | 78 (66.7%) | 0.407 |
| Dyslipidemia | − 0.03 | 0.655 | 78(60.0%) | 83(70.9%) | 0.072 |
| Renin-angiotensin system inhibitor | − 0.08 | 0.211 | 70 (53.8%) | 64 (54.7%) | 0.893 |
| Current smoker | − 0.05 | 0.411 | 17 (13.1%) | 11 (9.5%) | 0.376 |
| Alcohol (once a week or more) | 0.00 | 0.997 | 49 (38.0%) | 34 (29.3%) | 0.152 |
Values are shown as mean ± SD, median (interquartile), or number (percentage). The less support group comprised the patients with ESSI score from 5 to 26, and the more support group comprised those with ESSI score from 27 to 31. The association of happiness score and participants’ characteristics were assessed using Pearson’s coefficient. Differences in parameters between the less support group and more support group were analyzed using t test for continuous variables and Chi-square test for dichotomous items. p value of less than 0.05 was considered to indicate significance
Multivariate analysis revealed that happiness score was an independent determinant of the ΔeGFR (β = 0.16, p = 0.008), even after adjusting for baseline eGFR, age, sex, and BMI. Social support was also significantly associated with both secular change of eGFR (β = 0.14, p = 0.021), and that of Lg(UACR) (β = − 0.13, p = 0.040), after adjusting for baseline eGFR or Lg(UACR), age, sex, and BMI. If both happiness score and social support were included in the models as explanatory variables, there remained only a significant association between happiness score and ΔGFR (β = 0.13, p = 0.0497) (Table 4).
Table 4.
Effect of happiness score and social support on the progression of diabetic nephropathy
| Happiness score | Social support | |||||||
|---|---|---|---|---|---|---|---|---|
| ΔeGFR | ΔLg (UACR) | ΔeGFR | ΔLg (UACR) | |||||
| β | p value | β | p value | β | p value | β | p value | |
| Model 1 | 0.16 | 0.010 | − 0.09 | 0.112 | 0.16 | 0.010 | − 0.12 | 0.040 |
| Model 2 | 0.17 | 0.005 | − 0.10 | 0.087 | 0.16 | 0.011 | − 0.12 | 0.040 |
| Model 3 | 0.16 | 0.008 | − 0.10 | 0.086 | 0.14 | 0.021 | − 0.13 | 0.040 |
| Model 4 | 0.13 | 0.0497 | − 0.06 | 0.340 | 0.10 | 0.139 | − 0.10 | 0.112 |
Multivariate linear regression models were used for analysis
Model 1: Adjusted for eGFR at baseline for ΔeGFR; and Lg(UACR) at baseline for ΔLg(UACR)
Model 2: Adjusted for eGFR, age, and BMI at baseline for ΔeGFR; and Lg(UACR), age, and BMI at baseline for ΔLg(UACR)
Model 3: Adjusted for eGFR, age, and BMI at baseline, and sex for ΔeGFR; and Lg(UACR), age, and BMI at baseline, and sex for ΔLg(UACR)
Model 4. Added both happiness score and social support to Model 3 as adjustment factors
p value of less than 0.05 was considered to indicate significance. β means standardized partial regression coefficient
Gender-segregated analysis showed a significant association between happiness score and ΔeGFR (r = 0.24, p = 0.006) in male but not in female subjects (Supplementary Table 2). On the other hand, decrease in eGFR was significantly attenuated in the subjects with more social support as compared to those with less social support (− 4.6 ± 9.1 ml/min/1.73 m2 vs. − 0.7 ± 8.4 ml/min/1.73 m2, p = 0.011) in women but not in men. (Supplementary Table 2). Multivariate models including both happiness score and social support as explanatory variables showed similar results: happiness score was significantly associated with ΔGFR in men (β = 0.22, p = 0.016) and social support was significantly associated with ΔGFR in women (β = 0.19, p = 0.043) (Supplementary Table 4). The same analysis was performed only in patients with diabetic nephropathy stage 1 or stage 2 (n = 231), and similar results were obtained (data not shown).
Discussion
Based on second-year follow-up data of our previous study, this study demonstrated that lower happiness score was associated with the reduced eGFR, and that poor social supports was associated with decline in eGFR and increase in alubuminuria. After adjusted for both happiness score and social support each other, happiness score was still associated with reduced eGFR but social support was no longer associated with the reduced eGFR or alubuminuria progression. These results did not contradict previous reports. Depression was reported to associate with a greater prevalence of microalbuminuria [14], in other hands, Campbell et al. reported that reduced eGFR was associated with depression [15]. Moreover, Takasaki et al. reported that advanced stages of nephropathy were incrementally associated with higher prevalence and more severe depression [16]. These previous reports would support the idea that depression would influence progression of DN, while they were cross-sectional study. In addition, it has been also reported that social support significantly associated with the progression of DN among patients with diabetes but without macroalubuminuria [17].
Notably, in gender-segregated analysis, a significant association between happiness score and reduced eGFR was confirmed in men but not in women. On the other hand, a significant association between social support and reduced eGFR was confirmed in women but not in men. The impact of psychosocial factors on diseases could be differed by gender [7, 18]. Women is more likely to integrate social and emotional aspect and used more internalizing defenses than men and used coping strategies that flexibly integrated intra-and interpersonal aspects of conflict situations [19] Gender differences in the neuroendocrine and cardiovascular response to psychological stress may contribute to the gender differences in the progression of diseases associated with hypothalamic–pituitary–adrenal axis reactivity such as diabetes, hypertension, and cardio-renal disease. For example, men had significantly greater cortisol responses compared to women [20].
Although the mechanisms that link psychosocial conditions with progression of DN remain unclear, we assumed two scenarios in reference to prior reports. First, it could be hypothesized that the pathway from psychosocial conditions to the progression of DN is mediated by medical adherence. Generally, patients with lifestyle-related diseases, including DM, are required to engage in health-promoting behaviors such as recommended diet, physical activity, and good medication compliance. Marquez et al. reported that social support affected medical adherence that led to weight loss in obese patients with type 2 DM [4]. Shao et al. also reported that better social support was related to better medical adherence, which in turn led to good glycemic control in diabetic patients [5]. In addition, patients with positive psychosocial condition understand the importance of good health behavior well, and feel maintaining a healthy lifestyle to be less troublesome as compared to patients without positive psychosocial condition [21, 22].
In contrast, depressed patients with diabetes reported less adherence with oral antidiabetic, antihypertensive, and lipid-lowering drugs compared to the nondepressed patients with diabetes [23]. In our study, most of the subjects were prescribed antidiabetic drugs and more than half of them were prescribed antihypertensive and/or lipid-lowering drugs, while associations between psychosocial factors and medical adherence were not precisely examined. Therefore, it is possible that patients with better psychosocial factors may have better medication compliance, which could lead to the attenuation of the progression of DN.
Second, inflammation, which plays a crucial role in the pathogenesis of DN [24, 25], might link psychosocial conditions and progression of DN. It was reported that people with better social support showed lower levels of serum inflammatory markers [26], but that those with stressful situation and pessimism had increased levels of serum inflammatory markers [27, 28]. In this context, hypothalamic–pituitary–adrenal axis reaction to mental stress could be considered as one of the mediators between psychosocial conditions and inflammation [27]. Unfortunately, however, serum levels of inflammatory markers were not evaluated in this study.
Several limitations of the present study should be discussed. First of all, the present research was designed as an observational study, not interventional study, and, therefore, we could not evaluate the causal relation between psychosocial factors and DN strictly. Second, this analysis was examined using the baseline and second-year data of an ongoing project, planned as a 4-year observation study. This 2-year observation period might be short for evaluating the association with psychosocial conditions and the progression of DN. Finally, the number of study participants was relatively small, and all of them were recruited from a single institution, and thus we cannot deny the presence of selection bias.
Notwithstanding these limitations, this study showed the possibility that positive psychosocial conditions could be related to the progression of DN, and that the psychosocial factors that influence in DN might differ between men and women, in Japanese patients with type 2 diabetes. Further examination is required to establish the causal pathway between psychosocial conditions and DN.
Supplementary Information
Below is the link to the electronic supplementary material.
Acknowledgements
The authors thank all the clinical staff who participated in this trial.
Compliance with ethical standards
Conflict of interest
All authors declare no conflicts of interest.
Ethical approval
All procedure followed were accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and/or with Helsinki Declaration of 1964 and later versions.
Informed consent
Informed consent or substitute for it was obtained from all patients for being included in the study. The study protocol was approved by the Ethics committee of Osaka University Hospital (Approval date: Aug. 22, 2014, No. 14117).
Footnotes
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