Abstract
Objectives
The aim of this study was to investigate the association between subjective memory complaints (SMCs) and depressive symptoms, with and without adjustment for genetic and family environmental factors.
Methods
We conducted a cross-sectional study using twins and measured SMCs and depressive symptoms as outcomes and explanatory variables, respectively. First, we performed regression analyses using generalized estimating equations to investigate the associations between SMCs and depressive symptoms without adjustment for genetic and family environmental factors (individual-level analyses). We then performed regression analyses for within-pair differences using monozygotic (MZ) and dizygotic (DZ) twin pairs and MZ twin pairs to investigate these associations with adjustment for genetic and family environmental factors by subtracting the values of one twin from those of co-twin variables (within-pair level analyses). Therefore, differences between the associations at individual- and within-pair level analyses suggested confounding by genetic factors.
Results
We included 556 twins aged ≥20 years. In the individual-level analyses, SMCs were significantly associated with depressive symptoms in both males and females [standardized coefficients: males, 0.23 (95 % CI 0.08–0.38); females, 0.35 (95 % CI 0.23–0.46)]. In the within-pair level analyses using MZ and same-sex DZ twin pairs, SMCs were significantly associated with depressive symptoms. In the within-pair level analyses using the MZ twin pairs, SMCs were significantly associated with depressive symptoms [standardized coefficients: males, 0.32 (95 % CI 0.08–0.56); females, 0.24 (95 % CI 0.13–0.42)].
Conclusions
This study suggested that SMCs were significantly associated with depressive symptoms after adjustment for genetic and family environmental factors.
Keywords: Subjective memory complaints, Depressive symptoms, Twin study
Introduction
Subjective memory complaints (SMCs) have been defined as the subjective awareness of memory loss, which may or may not be memory deficits, measured using standard neuropsychological tests [1, 2]. In fact, a review article that evaluated whether the associations between SMCs and memory as evaluated by standard neuropsychological tests were significant or not has been controversial [2]. SMCs can be considered an important symptom because they have been associated with a low quality of life [3], low daily living activity [3], impaired higher-level functional capacities [4], mild cognitive impairment [5], and dementia [1, 2].
In addition, previous studies have reported that SMCs were significantly associated with depression or depressive symptoms [2, 6–11]. Depression may be affected by genetic and family environmental factors [12], which suggests that the association between SMCs and depressive symptoms is confounded by these factors. However, previous studies did not adjust for these factors. A twin study may allow for adjustments in the genetic and family environmental factors because monozygotic (MZ) twin pairs share almost the same factors [13, 14]. Understanding this association after adjustments for these factors using twin subjects could lead to important considerations for the prevention of SMCs.
The aim of the present study was to investigate the associations between SMCs and depressive symptoms with and without adjustment for genetic and family environmental factors using twin pairs.
Materials and methods
Study design and participants
This study was completed at the Osaka University Center for Twin Research that was founded in 2009 in Japan [15]. We recruited twin participants using several methods, such as newspaper advertisements and posters in hospitals and universities. The inclusion criteria for participation in the present study were: (a) twin pairs who had participated in a cross-sectional, comprehensive medical examination between January 2009 and December 2014, (b) twin pairs aged ≥20 years, (c) being either monozygotic (MZ) twins, or same-sex dizygotic (DZ) twins, and (d) twin pairs who had participated in memory assessment. We excluded twin pairs whose zygosity was unknown and who were different-sex DZ twins. Informed consent in written form was obtained from all individual participants included in the study. The consent procedure and the present study were approved by the Institutional Review Board for Clinical Research Osaka University Hospital and Research Ethics Committee Osaka University; the study was performed in accordance with the principles of the Helsinki Convention.
The zygosity of the twin pairs was determined using 15 loci from the short tandem repeat (STR) markers [16]. A completely concordant twin pair within these STRs was identified as a MZ twin pair. To assess whether the DNA was identical, all other twin pairs underwent DNA microsatellite analyses; this measured concordance of the DNA markers (any pair with one discordant marker was identified as DZ, while any pair with seven concordant markers was identified as MZ).
Measurements
Subject memory complaints
The SMCs were assessed through a single self-reported question referring to previous review articles [1, 2]: “Please tell us how you would have answered the following question during the past week: Do you consider yourself as being forgetful?” The responses were graded with a graduated response ranging from 0 (not at all) to 4 (extremely) points. The single self-reported question was included in the Japanese version of the Profile of Mood States (POMS)-Brief [17]. Therefore, high scores indicated severe SMCs. SMCs were used as the quantitative variable in the analyses.
Depressive symptoms
Depressive symptoms were measured using the Depression–Dejection scale, which is a subscale of the Japanese version of POMS-Brief [17]. This subscale comprised five self-report items that were scored using a Likert-type scale and grading that spanned from 0 (not at all) to 4 (extremely) points. Therefore, the total score for the Depression–Dejection scale ranged from 0 to 20 points; a high score on this scale indicated highly depressive symptoms. Depression status measured using the Depression–Dejection scale of the Japanese version of POMS has been reported to be associated with major depressive disorder [18]. The depressive symptoms were used as the quantitative variable in the analyses.
Possible confounders
We used the following information as possible confounders: (a) age, (b) educational level, (c) short-term memory, (d) current medication use for depression, (e) current smoking status, (f) marital status, (g) history of hypertension or diabetes, and (h) alcohol intake. We organized the educational levels as primary school, junior high school, senior high school, junior college or vocational school, university, and graduate school. We classified junior college or vocational school, university, and graduate school as high educational level. We identified short-term memory as the memory evaluated using the Logical Memory I component of the Wechsler Memory Scale-Revised (WMS-R) [19, 20]. For the current smoking status, we asked the participants to respond to the following statements: (1) I smoke every day, (2) I do not smoke, or (3) I do not smoke now but I smoked previously. Furthermore, we classified the participants who responded to (1) as current smokers. Marital status was dichotomized into current marriage and others. Alcohol intake was evaluated using a brief-type self-administered diet history questionnaire (BDHQ) [21]. Alcohol intake was adjusted for energy intake using the residual method [21]. Age, short-term memory, and alcohol intake were used as quantitative variables in these analyses, whereas the educational level, current medication use for depression, current smoking status, marital status, and history of hypertension or diabetes were used as categorical variables.
Statistical analysis
We investigated the crude association between SMCs and each possible confounder using generalized estimating equations (GEEs). Subsequently, we performed three-step regression analyses with the individual-level analyses using the MZ and same-sex DZ twins, within-pair analyses using the MZ twin pairs and same-sex DZ twin pairs, and within-pair analyses using only the MZ twin pairs to investigate the association between SMCs and depressive symptoms with and without adjustment for genetic and family environmental factors [13]. We used the SMCs as the outcome variables and the depressive symptoms as the predictive variables.
First, we completed the individual-level analyses using GEE with exchangeable working correlations, since the GEE can adjust for the clustering of twins within a pair [13, 14, 22]. Therefore, the GEE analyses can be used to evaluate the twins as individuals (individual-level analyses). The possible confounders were sequentially adjusted by the residual method using the GEE with exchangeable working correlations in the following order: older age (1-year increments), educational level, short-term memory, current medication use for depression, current smoking status, marital status, history of hypertension or diabetes, and alcohol intake.
Second, we adjusted for possible confounding variables, some genetic factors, and almost all family environmental factors during the regression analyses of the within-pair differences for the MZ and DZ twin pairs [13]. In further regression analyses, the within-pair differences for MZ twin pairs only were used to adjust for possible confounding variables and almost all the potentially confounding genetic and family environmental factors [13]. The within-pair difference values for each twin pair were adjusted for their shared factors, including genetic and family environmental factors, by subtracting the values of one twin from those of the co-twin variables [13, 14]. The within-pair difference values for each MZ twin pair were adjusted for almost all genetic and family environmental factors because MZ twin pairs shared these factors [13, 14]. Thus, we examined the within-pair effects after the adjustment for genetic and family environmental factors (within-pair level analyses).
We interpreted the results from the three-step analyses as follows. The differences between the associations found in the individual-level and within-pair level analyses using the MZ and same-sex DZ twin pairs suggested the presence of confounding by shared factors such as genetic and family environmental factors [13, 14]. The differences between the associations found in the within-pair level analyses using the MZ and same-sex DZ twin pairs and using MZ twin pair suggested confounding by almost all genetic factors [13, 14]. When these associations were similar, the findings indicated no confounding by genetic and family environmental factors [13, 14].
We presumed a normal distribution and obtained standardized coefficients and 95 % confidence intervals (CIs). All analyses performed were stratified by sex because the mean of the ages was different between males and females. We used the “geepack” package version 1.2.0 [23] from the R statistics software version 3.1.2 [24]. To manage any missing data, we used list-wise case deletion; a case deletion with a missing rate of 10 % or less was considered suitable [25].
Results
In this study, 594 twins participated in a cross-sectional, comprehensive medical examination between January 2009 and December 2014. Among them, we evaluated 556 twins aged ≥20 years, which included 250 MZ twin pairs (360 females and 140 males) and 28 same-sex DZ twin pairs (32 females and 24 males) in accordance with the eligibility criteria (93.6 %). The overall rate for missing data was 7.19 %. The descriptive statistics are summarized in Table 1. The association between SMCs and each possible confounder is shown in Table 2. In males, SMCs were associated with only current medication use. In females, SMCs were associated with only smoking status. Figure 1 shows histogram of SMCs in male, and Fig. 2 shows histogram of SMCs in females.
Table 1.
Characteristics of the participants
| Variables | Male (n = 164) | Female (n = 392) |
|---|---|---|
| Age, year, mean (SD) | 59.91 (19.82) | 47.24 (17.00) |
| Subjective memory complains, mean (SD) | 1.54 (1.20) | 1.07 (1.02) |
| Depressive symptoms, mean (SD) | 2.86 (3.30) | 2.50 (2.96) |
| Short-term memory, mean (SD) | 15.46 (7.19) | 20.05 (7.00) |
| Alcohol intake (g/day), mean (SD) | 17.9 (26.8) | 4.4 (10.7) |
| Current medication use for depression [n (%)] | 1 (0.61) | 6 (1.53) |
| Educational level | ||
| Primary school [n (%)] | 7 (4.27) | 2 (0.51) |
| Junior high school [n (%)] | 17 (10.37) | 21 (5.36) |
| Senior high school [n (%)] | 53 (32.32) | 111 (28.32) |
| Junior college or vocational school [n (%)] | 1 (0.61) | 59 (15.05) |
| University [n (%)] | 72 (43.90) | 180 (45.92) |
| Graduate school [n (%)] | 7 (4.27) | 7 (1.79) |
| Smoking status [n (%)] | 29 (17.7) | 15 (3.8) |
| Marital status [n (%)] | 41 (25) | 162 (41.3) |
| History of hypertension [n (%)] | 31 (18.9) | 38 (9.7) |
| History of diabetes [n (%)] | 11 (6.7) | 12 (3.0) |
SD standard deviation
Table 2.
Standardized coefficients for the crude association between subjective memory complaints and each possible confounder using GEE
| Males | Females | |
|---|---|---|
| Standardized coefficients (95 % CI) |
Standardized coefficients (95 % CI) |
|
| Age | 0.09 (−0.12 to 0.29) | 0.11 (−0.01 to 0.22) |
| Educational levela | 0.03 (−0.28 to 0.34) | −0.20 (−0.44 to 0.22) |
| Current medication use for depressionb | −0.59 (−0.70 to −0.47) | 0.47 (−0.26 to 1.20) |
| Short-term memory | 0.04 (−0.13 to 0.22) | −0.02 (−0.14 to 0.09) |
| Smoking statusc | 0.1 (−0.36 to 0.56) | −0.65 (−0.84 to −0.47) |
| Marital statusd | −0.02 (−0.42 to 0.38) | −0.14 (−0.36 to 0.07) |
| History of hypertension or diabetes | 0.30 (−0.03 to 0.62) | −0.31 (−0.07 to 0.68) |
| Alcohol intake | −0.05 (−0.20 to 0.11) | <0.001 (−0.10 to 0.11) |
SMCs are used as outcome, and each possible confounder is used as explanatory variable in the analyses
Standardized coefficients range from −1 to 1 and show how much the standard deviation (SD) of SMCs change per 1-SD increase in each possible confounder
GEE generalized estimating equations, CI confidence interval
aJunior college or vocational school, university, and graduate school = 1; primary school, junior high school, and senior high school = 0
bCurrent medication use = 1
cCurrent smoker = 1
dCurrent marriage = 1, other = 0
Fig. 1.
Histogram of SMCs in male
Fig. 2.
Histogram of SMCs in female
Tables 3 and 4 show results of analyses for associations between SMCs and depressive symptoms. For the individual-level analyses, depressive symptoms were significantly associated with SMCs after adjustment for possible confounders in both males and females (Model 9 of Tables 3, 4). For the within-pair level analyses using the MZ and DZ twin pairs, depressive symptoms were significantly associated with SMCs in both males and females (Model 10 of Tables 3, 4). For the within-pair level analyses using only MZ twin pairs, depressive symptoms were significantly associated with SMCs in both males and females (Model 11 of Tables 3, 4).
Table 3.
Standardized coefficients for the association between subjective memory complaints and depressive symptoms by individual level analyses using GEE and within-pair level analyses in males (n = 146)
| Standardized coefficients | 95 % CIs | |
|---|---|---|
| Individual-level analyses | ||
| Model 1 | 0.21 | (0.05–0.36) |
| Model 2 | 0.22 | (0.06–0.38) |
| Model 3 | 0.22 | (0.05–0.38) |
| Model 4 | 0.22 | (0.06–0.39) |
| Model 5 | 0.22 | (0.06–0.38) |
| Model 6 | 0.21 | (0.05–0.38) |
| Model 7 | 0.21 | (0.05–0.37) |
| Model 8 | 0.22 | (0.06–0.38) |
| Model 9 | 0.23 | (0.08–0.38) |
| Within-pair level analyses | ||
| Model 10 | 0.31 | (0.09–0.53) |
| Model 11 | 0.32 | (0.08–0.56) |
Subjective memory complaints are outcomes. Depressive symptoms are the predictor
Standardized coefficients range from −1 to 1 and show how much the standard deviation (SD) of SMCs change per 1-SD increase in depressive symptoms
GEE generalized estimating equations, CI confidence interval
Model 1: Crude association
Model 2: Adjusted for age
Model 3: Adjusted for age and educational level
Model 4: Adjusted for age, educational level, and short-term memory
Model 5: Adjusted for age, educational level, short-term memory, and current medication use for depression
Model 6: Adjusted for age, educational level, short-term memory, current medication use for depression, and smoking
Model 7: Adjusted for age, educational level, short-term memory, current medication use for depression, smoking, and marital status
Model 8: Adjusted for age, educational level, short-term memory, current medication use for depression, smoking, marital status, and hypertension or diabetes
Model 9: Adjusted for age, educational level, short-term memory, current medication use for depression, smoking, marital status, hypertension or diabetes, and alcohol intake
Model 10: Adjusted for age, educational level, short-term memory, current medication use for depression, smoking, marital status, hypertension or diabetes, alcohol intake, and some genetic factors and almost all family environmental factors using within-pair differences for a monozygotic or dizygotic twin pair (72 monozygotic and dizygotic twin pairs)
Model 11: Adjusted for age, educational level, short-term memory, current medication use for depression, smoking, marital status, hypertension or diabetes, alcohol intake, and almost all genetic and family environmental factors using within-pair differences for a monozygotic twin pair (62 monozygotic twin pairs)
Table 4.
Standardized coefficients for the association between subjective memory complaints and depressive symptoms by individual level analyses using GEE and within-pair level analyses in females (n = 352)
| Standardized coefficients | 95 % CIs | |
|---|---|---|
| Individual-level analyses | ||
| Model 1 | 0.33 | (0.22–0.44) |
| Model 2 | 0.36 | (0.25–0.47) |
| Model 3 | 0.36 | (0.25–0.47) |
| Model 4 | 0.36 | (0.25–0.47) |
| Model 5 | 0.35 | (0.23–0.46) |
| Model 6 | 0.35 | (0.23–0.46) |
| Model 7 | 0.35 | (0.24–0.46) |
| Model 8 | 0.35 | (0.23–0.46) |
| Model 9 | 0.35 | (0.23–0.46) |
| Within-pair level analyses | ||
| Model 10 | 0.27 | (0.13–0.42) |
| Model 11 | 0.24 | (0.09–0.39) |
Subjective memory complaints are outcomes. Depressive symptoms are the predictor
Standardized coefficients range from −1 to 1 and show how much the standard deviation (SD) of SMCs change per 1-SD increase in depressive symptoms
GEE generalized estimating equations, CI confidence interval
Model 1: Crude association
Model 2: Adjusted for age
Model 3: Adjusted for age and educational level
Model 4: Adjusted for age, educational level and short-term memory
Model 5: Adjusted for age, educational level, short-term memory, and current medication use for depression
Model 6: Adjusted for age, educational level, short-term memory, current medication use for depression, and smoking
Model 7: Adjusted for age, educational level, short-term memory, current medication use for depression, smoking, and marital status
Model 8: Adjusted for age, educational level, short-term memory, current medication use for depression, smoking, marital status, and hypertension or diabetes
Model 9: Adjusted for age, educational level, short-term memory, current medication use for depression, smoking, marital status, hypertension or diabetes, and alcohol intake
Model 10: Adjusted for age, educational level, short-term memory, current medication use for depression, smoking, marital status, hypertension or diabetes, alcohol intake, and some genetic factors and almost all family environmental factors using within-pair differences for a monozygotic or dizygotic twin pair (173 monozygotic and dizygotic twin pairs)
Model 11: Adjusted for age, educational level, short-term memory, current medication use for depression, smoking, marital status, hypertension or diabetes, alcohol intake, and almost all genetic and family environmental factors using within-pair differences for a monozygotic twin pair (159 monozygotic twin pairs)
Discussion
While investigating the association between SMCs and depressive symptoms without adjustment for genetic and family environmental factors, we first found that depressive symptoms were significantly associated with SMCs in males and females. Second, during the investigation of the association between SMCs and depressive symptoms with adjustment for genetic and family environmental factors using a genetically informative sample of twins, we found that depressive symptoms were significantly associated SMCs after adjustment for almost all genetic and family environmental factors. These results suggested that depressive symptoms were associated with SMCs after adjustment for genetic and family environmental factors.
The results of the individual analyses in the present study were similar to those from previous studies that had investigated the association between SMCs and depression or depressive symptoms [2, 6–11]. These previous studies did not make adjustments for genetic and family environmental factors, although depression can be affected by genetic factors [12]. We established a significant association between SMCs and depressive symptoms with adjustment for genetic and family environmental factors in the present study using a genetically informative sample of twin pairs.
The present study also showed that SMCs were significantly associated with depressive symptoms after adjustment for memory scores as evaluated by a standard neuropsychological test. The results of the present study also confirmed the results of previous studies that had demonstrated that SMCs were significantly associated with depressive symptoms rather than these memory scores [6, 7]. A previous study by Antikainen et al. [10] showed that SMCs were significantly associated with both depressive symptoms and memory scores in a cross-sectional study. This previous study did not investigate this association between the SMCs and the depressive symptoms after adjustment for the memory score. It is unknown whether SMCs were significantly associated with short-term memory. In any case, the aim of the present study was not to investigate this association between SMCs and memory scores; it was designed to investigate the association between SMCs and depressive symptoms.
There may be several mechanisms for the association between SMCs and depressive symptoms. First, previous studies showed that low physical activity was associated with SMCs in subjects who were 18 years or older [26] and with depressive symptoms [27]. Therefore, low physical activity might influence the association between SMCs and depressive symptoms. Second, previous studies showed that a low educational level was also associated with SMCs in subjects who were 18 years or older [26] and with depressive symptoms [28]. Therefore, a low educational level may have an impact on this association. The present study showed a significant association between SMCs and depressive symptoms with adjustment for educational level. However, this study could not reveal effects of educational level on the association between SMCs and depressive symptoms; further studies are required to clarify these effects. Third, previous studies indicated that psychological stress was associated with SMCs [29] and depression [30]. Therefore, psychological stress may also have an impact on this association. Considering those previous studies and the results of our study, the association between SMCs and depressive symptoms may be caused by these mechanisms with adjustment for genetic and family environmental factors. The present study did not reveal the mechanisms because of the cross-sectional nature of our study. However, the results of the present study do warrant further research to investigate the mechanisms of the association between SMCs and depressive symptoms.
A notable strength of this study is that it is based on a genetically informative sample, which allowed us to investigate the association between traits after adjustment for genetic and family environmental factors. However, this study had several limitations. First, the present study did not identify any causal relationships due to the cross-sectional design. Second, the analyses of the present study were unable to adjust for gene–environmental interactions. However, we were able to adjust for almost all other genetic effects by using the genetically informative sample of the MZ twin pairs. Third, to measure SMCs, the present study used a single question with a graded response instead of a questionnaire which previous studies had used [6, 8, 10, 11]. However, previous review articles have showed that many studies used a simple one question to measure SMCs [1, 2]; a single question may be convenient in clinical situations. Our findings require further studies investigating the association between depressive symptoms and SMCs, as assessed by validated methods or the gold standard with adjustment for genetic and family environmental factors. Finally, we have adjusted for possible confounders, but residual confounders may be present. Further studies adjusting other confounders are required.
In conclusion, the present study showed that depressive symptoms were significantly associated with a high SMC score before and after adjustment for possible confounders, including genetic and family environmental factors, in both males and females. The findings of the present study suggested that preventing or effectively managing depressive symptoms might improve subjective memory complaints regardless of genetic and family environmental factors.
Acknowledgments
We would like to thank all the participants of the study. This work was supported by University Grants from Japanese Ministry of Education, Culture, Sports, Science and Technology (MEXT), MEXT KAKENHI Grant No. 26293151, and JSPS KAKENHI Grant No. 15J03698.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
Footnotes
Osaka Twin Research Group: Kazuo Hayakawa, Yoshinori Iwatani, Jun Hatazawa, Shiro Yorifuji, Chika Honda, Mikio Watanabe, and Kayoko Omura, Center for Twin Research, Osaka University Graduate School of Medicine.
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