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Associations between dietary oleic acid and linoleic acid and depressive symptoms in perimenopausal women: The Study of Women's Health Across the Nation
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Associations Between Dietary Oleic Acid and Linoleic Acid and Depressive Symptoms in Perimenopausal Women: The Study of Women’s Health Across the Nation Di Li , Yongqing Tong , Yan Li PII: DOI: Reference:
S0899-9007(19)30185-6 https://doi.org/10.1016/j.nut.2019.110602 NUT 110602
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Nutrition
Received date: Revised date: Accepted date:
21 April 2019 24 August 2019 5 October 2019
Please cite this article as: Di Li , Yongqing Tong , Yan Li , Associations Between Dietary Oleic Acid and Linoleic Acid and Depressive Symptoms in Perimenopausal Women: The Study of Women’s Health Across the Nation, Nutrition (2019), doi: https://doi.org/10.1016/j.nut.2019.110602
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Highlights:
National wide sample of perimenopausal women in the US
Oleic acids and linoleic acids are related to depressive symptoms
Lower oleic acids and linoleic acids intakes were less likely to be depressive
Oleic acids and linoleic acids are positively associated with CES-D score
Associations Between Dietary Oleic Acid and Linoleic Acid and Depressive Symptoms in Perimenopausal Women: The Study of Women’s Health Across the Nation Running Title: Oleic acid,
Linoleic acid and Depressive Symptoms Di Li1, Yongqing Tong1, Yan Li1*
1
Department of Clinical Laboratory, Renmin Hospital of Wuhan University, Wuhan 430060, China
First Author
Full name: Di Li Institute: Renmin Hospital of Wuhan University Department: Department of Clinical Laboratory University/Hospital: Renmin Hospital of Wuhan University Street Name & Number: Zhangzhidong Road, Wuchang district City, State, Postal code, Country: Wuhan, Hubei, 430060, China Tel: +8613871888108 Fax: NA E-mail: [email protected],
Second Author
Full name: Yongqing Tong Institute: Renmin Hospital of Wuhan University Department: Department of Clinical Laboratory University/Hospital: Renmin Hospital of Wuhan University Street Name & Number: Zhangzhidong Road, Wuchang district City, State, Postal code, Country: Wuhan, Hubei, 430060, China Tel: +8613638685578 Fax: NA E-mail: [email protected],
*Corresponding Author
Full name: Yan Li Institute: Renmin Hospital of Wuhan University Department: Department of Clinical Laboratory University/Hospital: Renmin Hospital of Wuhan University Street Name & Number: Zhangzhidong Road, Wuchang district City, State, Postal code, Country: Wuhan, Hubei, 430060, China Tel: +8613886079252 Fax: NA E-mail: [email protected]
Associations Between Dietary Oleic Acid and Linoleic Acid and
Depressive Symptoms in Perimenopausal Women: The Study of Women’s Health Across the Nation Abstract Background: To study the association of oleic acid and linoleic acid intake from diet with depressive symptoms in perimenopausal women. Methods: Cross-sectional study used data from the Study of Women’s Health Across the Nation (SWAN). Linear regression, logistic regression and restricted cubic spline models were performed to examine the association oleic acid and linoleic acid intake with depression. Results: A total of 2793 women aged 42-52 years were included in the present study. Oleic acid and linoleic acid intake were positively associated with CES-D scores in unadjusted and age-, race/ethnicity-, total family income- and education-adjusted linear regression model. The fully adjusted regression coefficients were β=0.089 and β=0.145 for oleic acid and linoleic acid intake, respectively. oleic acid and linoleic acid intake were positively associated with depressive symptoms (CES-D score ≥16) in unadjusted and age-, race/ethnicity-, total family income- and education-adjusted logistic regression model. The fully adjusted Odds ratios (ORs) with 95% confidence intervals (CIs) of depressive symptoms were 1.994 (1.298-3.063) and 1.592 (1.047-2.421) for the highest versus lowest quartile of oleic acid and linoleic acid intake, respectively. Conclusion: Oleic acid and linoleic acid intake may be positively associated with depressive symptoms in perimenopausal women. Key words: Oleic acid; Linoleic acid; Depressive symptoms; Cross-sectional study Introduction
Depression is a common disease worldwide, producing the most of decrement in health compared with other chronic diseases such as diabetes, asthma, arthritis and angina[1]. Depression is associated with disease burden, health care costs and disability. It is expected to be the world’s second leading cause of disease burden and the leading cause of disability by 2030[2, 3]. Early intervention make depression treatable; Nevertheless, long-term treatment rises numerous side effect[4]. Therefore, it is necessary to explore the effective preventive methods and modifiable risk factors for depression. Steady accumulation research efforts have been done in past decades; Nevertheless, the etiology of depression has not been understood fully. Growing interest in the last few years has focused on the association between depression and dietary factors. The elevated incidence of numerous health conditions, including depression, during past century has been guessed as being associated with dietary factors[5]. Indeed, dietary factors, such as fruits, vegetables[6], coffee[7] and fish[8] have been linked to development of depression. Additionally, it is indicated in several studies that fatty acids were related to depression. This was reflected in studies exploring the association between the omega-3 fatty acids and depression[9, 10]. Accumulating results from clinical observations also confirmed the important role of other types of fatty acids, such as oleic fatty acids and linoleic fatty acid, in maintaining mental health[11, 12]. The Western diet has been characterized by increasing consumption of seed oils whose unsaturated fatty acids are predominantly oleic acid and linoleic acid[13]. Evidence from metabolic, biochemical and epidemiological studies confirmed that oleic acid has a beneficial effect against several health conditions, such as cardiovascular diseases[14] and cancer[15]. Oleic acid was also associated with reduced likelihood of depression among adults[16]. The beneficial effect of oleic acid may
partly result from its ability to attenuates inflammatory gene expression[17]. Prospective study suggested that dietary linoleic fatty acid was positively associated with depressed mood among general population[16]. Evidence from experimental studies observed an overproduction of pro-inflammatory cytokines from linoleic-rich diet among depressed patients[18, 19]. The overproduction of pro-inflammatory cytokines may partly explain the associations between linoleic acid and depression. Indeed, inflammation induce depressive symptoms by impacting diverse mood-related processes. Elevated inflammatory signaling dysregulates neurotransmitter metabolism, impairs neuronal health, and alters neural activity in mood-relevant brain regions[18]. Inflammatory factors can alter production, metabolism, and transport of neurotransmitters that synergistically affect mood, including serotonin, glutamate and dopamine[20]. However, epidemiological studies investigating the association between oleic acid and linoleic acid intake and depression in perimenopausal women are lacked. The present study included midlife women from the Study of Women’s Health Across the Nation (SWAN). Midlife women are a special group in the study of depression. On the one hand, depression is more prevalence in women[21]. On the other hand, women in the midlife period may experience dynamic and numerous alterations in circumstances and social roles, such as the death of a loved one, marital disruption, financial issues, children returning to or leaving the home and caring for aging parents, which may lead to depressive symptoms or major depression[22]. The alterations in health behaviors and health status that happen during later midlife also lead to the development of depression among women[23, 24]. Moreover, longitudinal researches have provided evidence that menopausal transition associated with risk of depressive symptoms or major depression[25]. The central nervous system has several estrogen receptors, and alterations
in estrogen during menopausal transition affect levels of norepinephrine, dopamine and serotonin via unblocking of binding sites, enhancement of neurotransmitter and degradation of catabolic enzymes[26]. While perimenopausal period is potent confound, it is necessary to explore the effective preventive methods and modifiable risk factors for depression in perimenopausal women. Accordingly, in our study, analyses were performed on a subsample of Study of Women’s Health Across the Nation (SWAN) to explore the associations of oleic acid and linoleic acid intake and depression in perimenopausal women.
Methods
Data collection and study population The present study uses the baseline data from Study of Women’s Health Across the Nation (SWAN), a longitudinal, multicenter and population-based study of the natural history of the late midlife women. The cohort was recruited with a telephone screening interview to determine individual eligibility between 1995 and 1997. Community-based samples of participants were selected at seven sites across the US using a variety of sampling frames and recruitment strategies. Non-Hispanic white participants and participants from specified minority groups (Chinese in the Oakland region; Japanese in Los Angeles; Hispanic in Newark; and black in Pittsburgh, Chicago, Boston and the Detroit area). 16,065 women completed the screening interview. A total of 3302 women were eligible and included in the SWAN cohort. Women who met the eligibility criteria were 42-52 years old, had an intact uterus and at least one intact ovary, had not used of
reproductive hormones in the previous 3 months and had had at least one menstrual period. The study protocol was approved by the institutional review boards at all sites, and informed consent was received from all individual at each visit. The protocol contained extensive self-reported health, lifestyle, physical, reproductive psychosocial and psychological symptoms. Thirty-eight women were excluded due to missing information for calculating the CES-D score. A total of 326 women were excluded due to use of antidepressant. A total of 145 women without oleic acid or linoleic acid data were excluded. The final cohort in our study included 2793 women who provided dietary oleic acid and linoleic acid intake data and depression symptom data without use of antidepressant.
Depression assessment Depressive symptoms were assessed in the SWAN study with the 20-item Center for Epidemiological Studies Depression Scale (CES-D), a measure widely used in epidemiologic study and well-validated with reliability in ethnically diverse data. The standard cut-off point for CES-D is 16, and a score of 16 or higher has been defined as high levels of depressive symptomatology[27].
Dietary intake assessment Daily dietary intake was obtained via a modified 1995 Block Food Frequency Questionnaire (FFQ)[28, 29] with 103 food items, on the basis of responses of Caucasians and African Americans in the Second National Health and Nutrition Examination Survey (NHANES)[28, 30, 31]. Nutrients (included oleic acid and linoleic acid) intake was computed based on a database of
food composition from United States Department of Agriculture data (USDA)[32] link to the food frequency data.
Covariates Demographic
characteristics
included
age,
ethnicity
(Black/African
American,
Chinese/Chinese American, Japanese/Japanese American, Caucasian/White Non-Hispanic and Hispanic), total family income (less than $19,999, $20,000 to $49,999, $50,000 to $99,999 and $50,000 or more) and education (less than high school, high school graduate, some college/technical school, college graduate and postgraduate). Life style characteristic included physical activity, smoke and body mass index (BMI). Mean index of physical activity was calculated based on frequency of household/childcare activities, nonsports leisure time and sports activities[33]. Age assessment was based on self-reported date of birth. Race/ethnicity identification was based on the self-reported identification. BMI was calculated as weight (kg) divided by height (meters) squared. Height and weight were measured using standardized protocols.
Statistical analysis SPSS (version 20.0) and R (version 3.5.2 basic) were used to analyze the data. All continuous variables represent a non-normal distribution according to Kolmogorov-Smirnov test, and described by the median with the interquartile range. Chi-square tests and Mann-Whitney U test were used to compare the percentages of categorical variables and averages of continuous variables between women with low (<16) versus high (≥16) CES-D scores. Linear regression was
used to examine the relationship between oleic acid and linoleic acid intake and CES-D scores. oleic acid and linoleic acid intake were categorized by quartiles (quartile 4: ≥75th percentile, quartile 3: ≥50th to 75th percentile, quartile 2: ≥25th to 50th percentile, quartile 1: <25th percentile). Logistic regression was performed to examine the associations between oleic acid and linoleic acid intake and depressive symptoms (CES-D scores≥16), with the quartile 1 as the reference category. The crude model had no adjustment. Model 1 was adjusted for age, race/ethnicity, total family income and education, and model 2 was adjusted for age, race/ethnicity, total family income, education, physical activity, current smoker, menopausal status and BMI. Tests for linear trend were performed by entering the median value of each category of oleic acid and linoleic acid as a continuous variable in the models. To further investigate the relationship between oleic acid and linoleic acid intake and depression symptoms, restricted cubic spline analysis was conducted in a fully adjusted model with knots at the 5th, 15th, 75th, 95th percentiles of the distribution with 10th as a reference knot.
Results Table 1 presents the characteristics of the 2793 women across CES-D scores. Women in the total sample were approximately 46 years old and predominantly white and overweight. Women with depressive symptoms (CES-D scores≥16) had higher dietary oleic acid and linoleic acid intake compared to women without depressive symptoms (CES-D scores < 16). Table 2 presents the multivariate-adjusted liner associations between oleic acid and linoleic acid intake and CES-D scores. The crude regression coefficient with the 95% confidence intervals (CIs) of CES-D scores indicated that oleic acid and linoleic acid intake were positively associated
with CES-D scores. After adjustment for age, race, total family income and education in model 1, higher oleic acid and linoleic acid intake were significantly related to higher depressive symptoms. This association remained statistically significant and was little changed with fully controlling for age, race/ethnicity, total family income, education, physical activity, current smoker, menopausal status and BMI in model 2 (β=0.089, P<0.001; β=0.145, P<0.001, respectively). Table 3 presented odds ratios (ORs) and the 95% CI of depressive symptoms (CES-D score ≥16) across quartiles of oleic acid and linoleic acid intake. The crude model indicated that dietary oleic acid and linoleic acid intake were positively associated with depressive symptoms. After adjustment for age, race, total family income and education in model 1, the results were similar to those of the crude model. This association remained statistically significant and was changed little when fully controlling for age, race/ethnicity, total family income, education, physical activity, current smoker, menopausal status and BMI in model 2. The fully adjusted ORs (95% CI) of depressive symptoms were 1.994 (1.298-3.063) and 1.592 (1.047-2.421) in the highest versus lowest quartile of oleic acid and linoleic acid intake, respectively. Fig. 1 depicts the results of the restricted cubic spline analyses. The results showed that dietary oleic acid and linoleic acid intake were positively associated with risk of elevated CES-D score (≥16), suggesting of line-shaped association.
Discussion In the present study, we used SWAN 1995-1997 data and included 2793 participants aged 42-52 years to evaluate the associations of oleic acid and linoleic acid intake with depressive symptoms. The results of this study found that CES-D score was positively associated with oleic
acid and linoleic acid intake, and these positive associations of oleic acid and linoleic acid intake remained statistically significant after controlling for potential confounders. Similar positive associations were observed between oleic acid and linoleic acid intake and depressive symptoms (CES-D score ≥16) women in unadjusted model, age-, race/ethnicity-, total family income- and education-adjusted model and the fully adjusted model. To the best of our knowledge, this is the first time to investigate the associations between oleic acid and linoleic acid intake and depressive symptoms in perimenopausal women. Mechanically, neuronal differentiation relies on synthesis of oleic acid [34]. High oleic acid diet can specifically decrease sensitivity of enteric and vagal neuronal indicating that decreased sensitivity to gastric and satiation inhibitory effects of oleic acid may mediated via specific reduction by fatty acid[35]. The hypothalamus and other regions link the sensing of fatty acids to the adjustment of behavior and metabolism. The oleic acid can reduce expression of hypothalamic neuropeptide Y[36]. Fatty acid composition of hippocampus and brain in cognitive impaired rats involve alterations in oleic acid[37]. The amounts of linoleic acid needed in the diet to elaborate membrane function and structures in brain, have been determined[38]. Evidence from mice showed that imbalance between alpha-linolenic acid (18:3n-3, ALA) and linoleic acid (18:2n-6, LA) induce anxious behavior in offspring[39]. The alpha-linolenic acid deficiency has been associated with the increased risk of mood disorders while increased linoleic acid results in abnormal anxiety and depressive -related behaviors[40, 41]. Therefore, a LA excess/ALA deficient dietary condition is suggested to cause mood disorders[42]. The Western diet has been characterized by increasing consumption of seed oils whose unsaturated fatty acids are predominantly oleic acid and linoleic acid[13]. Evidence from
metabolic, biochemical and epidemiological studies confirmed that oleic acid has a beneficial effect against several health conditions, such as cardiovascular diseases[14] and cancer[15]. Higher oleic acid was also associated with reduced likelihood of depression among adults while higher linoleic and oleic fatty acid may increase the risk of depression[16]. However, the previous evidences have been performed in general. It remains unknown whether oleic acid or linoleic acid intake impacts depression in perimenopausal women. Various factor such as age, sex and menopausal status could confound the associations found in earlier studies. The present study extends the previous studies and provides reliable evidence that dietary oleic acid or linoleic acid intake are positively associated with depressive symptoms. That is consistent with previous results which indicated that linoleic acid may enhance the risk of depression in general population[16]. However, higher oleic acid was reported to be associated with reduced likelihood of depression. The different population in our study may contribute to this contradictory result. Our research has several strengths and limitations. The major strength of our research is the use of a national wide sample of perimenopausal women in the US. Additionally, the positively associations between oleic acid and linoleic acid intake and depressive symptoms remained significant after full adjustment for confounders. Unfortunately, there are still some limitations in our research. On the one hand, the cross-sectional design of this study is the major limitation. Because a cross-sectional is hard to make causal inference. Thus, reverse causality, depressive symptoms may result in decreased food intake resulting in the reduced oleic acid and linoleic acid intake. On the other hand, lacking biological detection is another limitation. It is desirable to investigate the fatty acids detected in adipose tissue, which can accurately reflect long-term dietary intake of fatty acids due to the low turnover in adipose tissue[43]. Collection of daily
dietary information relied on the participant’s ability to remember. That might cause recall bias. Additionally, memory may be affected by depressive symptoms. That might potentially differential assessment error. Conclusion Our results show that oleic acid and linoleic acid intake may be positively associated with depressive symptoms in perimenopausal women. Nevertheless, the causality of our findings could not be determined due to a cross-sectional design. Prospective studies are needed to verify our findings.
Author Statement Contributors Yan Li and Yongqing Tong designed study; Di Li collected and analyse data; Di Li wrote the manuscript; Yan Li and Yongqing Tong appraise and revise the manuscript.
s
Acknowledgements
We thank all individuals who were responsible for the planning and administering of SWAN and making the datasets of SWAN available on their website. We also acknowledge the reviewers and editors for view our work.
Funding Our study was supported by the National Natural Science Foundation of China (No. 81772265).
Conflicts of interest The authors have declared no conflicts of interest.
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Table 1 Characteristics of participants by CES-D score, represented by Medians and Interquartile Range (IQR). Variable
Total n=2793
CES-D score<16 n=2182
CES-D score≥16 n=611
p value
Age (year)
46 (44-48)
46 (44-48)
45 (43-47)
0.004
Black/African American
788 (28.2%)
596 (27.3%)
192 (31.4%)
Chinese/Chinese American
233 (8.3%)
202 (9.3%)
31 (5.1%)
Japanese/Japanese American
235 (8.4%)
199 (9.1%)
36 (5.9%)
1298 (46.5%)
1043 (47.8%)
255 (41.7%)
239 (8.6%)
142 (6.5%)
97 (15.9%)
Race/ethnicity(%)
Caucasian/White Non-Hispanic Hispanic
<0.001
<0.001
Education Less than High School
200 (7.2%)
119 (5.5%)
81 (13.3%)
High School Graduate
479 (17.3%)
345 (16.0%)
134 (22.1%)
Some College/Technical School
875 (31.6%)
671 (31.1%)
204 (33.6%)
College Graduate
565 (20.4%)
465 (21.5%)
100 (16.5%)
Postgraduate
646 (23.4%)
558 (25.9%)
88 (14.5%) <0.001
Total family income Less Than $19,999
370 (13.6%)
219 (10.3%)
151 (25.8%)
$20,000 to $49,999
928 (34.1%)
710 (33.3%)
218 (37.3%)
$50,000 to $99,999
1020 (37.5%)
840 (39.4%)
180 (30.8%)
$100,000 or More
400 (14.7%)
364 (17.1%)
36 (6.2%)
2.6 (2.0-3.4)
2.6 (2.0-3.4)
2.2 (1.6-3.0)
Physical activity
<0.001
Current smoker no
683 (60.0%)
548 (64.0%)
135 (47.9%)
yes
455 (40.0%)
308 (36.0%)
147 (52.1%)
Menopausal Status
<0.001
<0.001
Early Peri-menopausal
1250 (45.5%)
934 (43.5%)
316 (52.6%)
Pre-menopausal
1502 (54.5%)
1217 (56.5%)
285 (47.4%)
BMI (kg/m )
26.51 (22.85-31.95)
26.22 (22.70-31.32)
27.84 (23.36-33.56)
<0.001
Dietary Oleic Acid intake (g/d)
23.92 (17.28-32.36)
23.41 (16.98-31.37)
26.26 (18.99-35.96)
<0.001
11.32 (7.91-16.16)
11.15 (7.77-15.50)
12.33 (8.38-17.88)
<0.001
7 (3-14)
5 (2-9)
22 (18-29)
<0.001
2
Dietary Linoleic Acid intake (g/d) CES-D score
BMI: body mass index; CES-D: Center for Epidemiological Studies Depression
Table 2 Associations of CES-D scores with dietary oleic acid intake and linoleic acid intake (regression coefficient and 95% confidence intervals). Crude no adjustment Oleic Acids intake (g/d)
Linoleic Acids intake (g/d)
Standard Error
β (95%CI)
p value
Standard Error
β (95%CI)
p value
Crude
0.014
0.095 (0.069-0.122)
<0.001
0.026
0.131 (0.079-0.183)
<0.001
Model1
0.014
0.078 (0.051-0.104)
<0.001
0.026
0.136 (0.084-0.188)
<0.001
Model2
0.021
0.089 (0.047-0.131)
<0.001
0.041
0.145 (0.064-0.225)
<0.001
Model 1 adjusted for age, race/ethnicity, total family income and education Model 2 adjusted for age, race/ethnicity, total family income, education, physical activity, current smoker, menopausal status and BMI
Table 3 Weighted odds ratios (95% confidence intervals) of depressive symptoms (CES-D score ≥16) across quartiles of oleic acid intake and linoleic acid intake. Intake cut off
Cases/parti cipants
Crude
Model 1
Model 2
Oleic acids intakes (g/d) Quartile 1 (low)
< 17.28
192/698
1.000 (ref.)
1.000 (ref.)
1.000 (ref.)
Quartile 2
17.28 to < 23.92
154/700
1.174 (0.898-1.535)
1.169 (0.882-1.549)
1.637 (1.025-2.614)
Quartile 3
23.92 to < 32.36
141/697
1.306 (1.003-1.700)
1.245 (0.941-1.646)
1.569 (1.002-2.458)
≥32.36
124/698
1.756 (1.360-2.268)
1.592 (1.213-2.091)
1.994 (1.298-3.063)
<0.001
<0.001
0.004
Quartile 4 (high) P-trend Linoleic acids intakes (g/d) Quartile 1 (low)
< 7.905
188/698
1.000 (ref.)
1.000 (ref.)
1.000 (ref.)
Quartile 2
7.905 to < 11.32
150/697
1.043 (0.800-1.359)
1.046 (0.791-1.383)
0.947 (0.598-1.501)
Quartile 3
11.32 to < 16.16
139/700
1.154 (0.889-1.498)
1.282 (0.973-1.689)
1.351 (0.875-2.087)
≥16.16
134/698
1.552 (1.206-1.996)
1.638 (1.248-2.150)
1.592 (1.047-2.421)
<0.001
<0.001
0.008
Quartile 4 (high) P-trend
Test for trend based on variable containing median value for each quintile. Crude no adjustment
Model 1 adjusted for age, race/ethnicity, total family income and education Model 2 adjusted for age, race/ethnicity, total family income, education, physical activity, current smoker, menopausal status and BMI
Fig. 1. Restricted cubic spline model of the odds ratios of high CES-D score (≥16) with oleic acid intake and linoleic acid intake. Adjusted for age, race/ethnicity, total family income, education, physical activity, current smoker, menopausal status and BMI. The dashed lines represent the 95% confidence intervals.
Graphical abstract
Associations Between Dietary Oleic Acid and Linoleic Acid and Depressive Symptoms in Perimenopausal Women: The Study of Women’s Health Across the Nation Di Li , Yongqing Tong , Yan Li PII: DOI: Reference:
S0899-9007(19)30185-6 https://doi.org/10.1016/j.nut.2019.110602 NUT 110602
To appear in:
Nutrition
Received date: Revised date: Accepted date:
21 April 2019 24 August 2019 5 October 2019
Please cite this article as: Di Li , Yongqing Tong , Yan Li , Associations Between Dietary Oleic Acid and Linoleic Acid and Depressive Symptoms in Perimenopausal Women: The Study of Women’s Health Across the Nation, Nutrition (2019), doi: https://doi.org/10.1016/j.nut.2019.110602
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Highlights:
National wide sample of perimenopausal women in the US
Oleic acids and linoleic acids are related to depressive symptoms
Lower oleic acids and linoleic acids intakes were less likely to be depressive
Oleic acids and linoleic acids are positively associated with CES-D score
Associations Between Dietary Oleic Acid and Linoleic Acid and Depressive Symptoms in Perimenopausal Women: The Study of Women’s Health Across the Nation Running Title: Oleic acid,
Linoleic acid and Depressive Symptoms Di Li1, Yongqing Tong1, Yan Li1*
1
Department of Clinical Laboratory, Renmin Hospital of Wuhan University, Wuhan 430060, China
First Author
Full name: Di Li Institute: Renmin Hospital of Wuhan University Department: Department of Clinical Laboratory University/Hospital: Renmin Hospital of Wuhan University Street Name & Number: Zhangzhidong Road, Wuchang district City, State, Postal code, Country: Wuhan, Hubei, 430060, China Tel: +8613871888108 Fax: NA E-mail: [email protected],
Second Author
Full name: Yongqing Tong Institute: Renmin Hospital of Wuhan University Department: Department of Clinical Laboratory University/Hospital: Renmin Hospital of Wuhan University Street Name & Number: Zhangzhidong Road, Wuchang district City, State, Postal code, Country: Wuhan, Hubei, 430060, China Tel: +8613638685578 Fax: NA E-mail: [email protected],
*Corresponding Author
Full name: Yan Li Institute: Renmin Hospital of Wuhan University Department: Department of Clinical Laboratory University/Hospital: Renmin Hospital of Wuhan University Street Name & Number: Zhangzhidong Road, Wuchang district City, State, Postal code, Country: Wuhan, Hubei, 430060, China Tel: +8613886079252 Fax: NA E-mail: [email protected]
Associations Between Dietary Oleic Acid and Linoleic Acid and
Depressive Symptoms in Perimenopausal Women: The Study of Women’s Health Across the Nation Abstract Background: To study the association of oleic acid and linoleic acid intake from diet with depressive symptoms in perimenopausal women. Methods: Cross-sectional study used data from the Study of Women’s Health Across the Nation (SWAN). Linear regression, logistic regression and restricted cubic spline models were performed to examine the association oleic acid and linoleic acid intake with depression. Results: A total of 2793 women aged 42-52 years were included in the present study. Oleic acid and linoleic acid intake were positively associated with CES-D scores in unadjusted and age-, race/ethnicity-, total family income- and education-adjusted linear regression model. The fully adjusted regression coefficients were β=0.089 and β=0.145 for oleic acid and linoleic acid intake, respectively. oleic acid and linoleic acid intake were positively associated with depressive symptoms (CES-D score ≥16) in unadjusted and age-, race/ethnicity-, total family income- and education-adjusted logistic regression model. The fully adjusted Odds ratios (ORs) with 95% confidence intervals (CIs) of depressive symptoms were 1.994 (1.298-3.063) and 1.592 (1.047-2.421) for the highest versus lowest quartile of oleic acid and linoleic acid intake, respectively. Conclusion: Oleic acid and linoleic acid intake may be positively associated with depressive symptoms in perimenopausal women. Key words: Oleic acid; Linoleic acid; Depressive symptoms; Cross-sectional study Introduction
Depression is a common disease worldwide, producing the most of decrement in health compared with other chronic diseases such as diabetes, asthma, arthritis and angina[1]. Depression is associated with disease burden, health care costs and disability. It is expected to be the world’s second leading cause of disease burden and the leading cause of disability by 2030[2, 3]. Early intervention make depression treatable; Nevertheless, long-term treatment rises numerous side effect[4]. Therefore, it is necessary to explore the effective preventive methods and modifiable risk factors for depression. Steady accumulation research efforts have been done in past decades; Nevertheless, the etiology of depression has not been understood fully. Growing interest in the last few years has focused on the association between depression and dietary factors. The elevated incidence of numerous health conditions, including depression, during past century has been guessed as being associated with dietary factors[5]. Indeed, dietary factors, such as fruits, vegetables[6], coffee[7] and fish[8] have been linked to development of depression. Additionally, it is indicated in several studies that fatty acids were related to depression. This was reflected in studies exploring the association between the omega-3 fatty acids and depression[9, 10]. Accumulating results from clinical observations also confirmed the important role of other types of fatty acids, such as oleic fatty acids and linoleic fatty acid, in maintaining mental health[11, 12]. The Western diet has been characterized by increasing consumption of seed oils whose unsaturated fatty acids are predominantly oleic acid and linoleic acid[13]. Evidence from metabolic, biochemical and epidemiological studies confirmed that oleic acid has a beneficial effect against several health conditions, such as cardiovascular diseases[14] and cancer[15]. Oleic acid was also associated with reduced likelihood of depression among adults[16]. The beneficial effect of oleic acid may
partly result from its ability to attenuates inflammatory gene expression[17]. Prospective study suggested that dietary linoleic fatty acid was positively associated with depressed mood among general population[16]. Evidence from experimental studies observed an overproduction of pro-inflammatory cytokines from linoleic-rich diet among depressed patients[18, 19]. The overproduction of pro-inflammatory cytokines may partly explain the associations between linoleic acid and depression. Indeed, inflammation induce depressive symptoms by impacting diverse mood-related processes. Elevated inflammatory signaling dysregulates neurotransmitter metabolism, impairs neuronal health, and alters neural activity in mood-relevant brain regions[18]. Inflammatory factors can alter production, metabolism, and transport of neurotransmitters that synergistically affect mood, including serotonin, glutamate and dopamine[20]. However, epidemiological studies investigating the association between oleic acid and linoleic acid intake and depression in perimenopausal women are lacked. The present study included midlife women from the Study of Women’s Health Across the Nation (SWAN). Midlife women are a special group in the study of depression. On the one hand, depression is more prevalence in women[21]. On the other hand, women in the midlife period may experience dynamic and numerous alterations in circumstances and social roles, such as the death of a loved one, marital disruption, financial issues, children returning to or leaving the home and caring for aging parents, which may lead to depressive symptoms or major depression[22]. The alterations in health behaviors and health status that happen during later midlife also lead to the development of depression among women[23, 24]. Moreover, longitudinal researches have provided evidence that menopausal transition associated with risk of depressive symptoms or major depression[25]. The central nervous system has several estrogen receptors, and alterations
in estrogen during menopausal transition affect levels of norepinephrine, dopamine and serotonin via unblocking of binding sites, enhancement of neurotransmitter and degradation of catabolic enzymes[26]. While perimenopausal period is potent confound, it is necessary to explore the effective preventive methods and modifiable risk factors for depression in perimenopausal women. Accordingly, in our study, analyses were performed on a subsample of Study of Women’s Health Across the Nation (SWAN) to explore the associations of oleic acid and linoleic acid intake and depression in perimenopausal women.
Methods
Data collection and study population The present study uses the baseline data from Study of Women’s Health Across the Nation (SWAN), a longitudinal, multicenter and population-based study of the natural history of the late midlife women. The cohort was recruited with a telephone screening interview to determine individual eligibility between 1995 and 1997. Community-based samples of participants were selected at seven sites across the US using a variety of sampling frames and recruitment strategies. Non-Hispanic white participants and participants from specified minority groups (Chinese in the Oakland region; Japanese in Los Angeles; Hispanic in Newark; and black in Pittsburgh, Chicago, Boston and the Detroit area). 16,065 women completed the screening interview. A total of 3302 women were eligible and included in the SWAN cohort. Women who met the eligibility criteria were 42-52 years old, had an intact uterus and at least one intact ovary, had not used of
reproductive hormones in the previous 3 months and had had at least one menstrual period. The study protocol was approved by the institutional review boards at all sites, and informed consent was received from all individual at each visit. The protocol contained extensive self-reported health, lifestyle, physical, reproductive psychosocial and psychological symptoms. Thirty-eight women were excluded due to missing information for calculating the CES-D score. A total of 326 women were excluded due to use of antidepressant. A total of 145 women without oleic acid or linoleic acid data were excluded. The final cohort in our study included 2793 women who provided dietary oleic acid and linoleic acid intake data and depression symptom data without use of antidepressant.
Depression assessment Depressive symptoms were assessed in the SWAN study with the 20-item Center for Epidemiological Studies Depression Scale (CES-D), a measure widely used in epidemiologic study and well-validated with reliability in ethnically diverse data. The standard cut-off point for CES-D is 16, and a score of 16 or higher has been defined as high levels of depressive symptomatology[27].
Dietary intake assessment Daily dietary intake was obtained via a modified 1995 Block Food Frequency Questionnaire (FFQ)[28, 29] with 103 food items, on the basis of responses of Caucasians and African Americans in the Second National Health and Nutrition Examination Survey (NHANES)[28, 30, 31]. Nutrients (included oleic acid and linoleic acid) intake was computed based on a database of
food composition from United States Department of Agriculture data (USDA)[32] link to the food frequency data.
Covariates Demographic
characteristics
included
age,
ethnicity
(Black/African
American,
Chinese/Chinese American, Japanese/Japanese American, Caucasian/White Non-Hispanic and Hispanic), total family income (less than $19,999, $20,000 to $49,999, $50,000 to $99,999 and $50,000 or more) and education (less than high school, high school graduate, some college/technical school, college graduate and postgraduate). Life style characteristic included physical activity, smoke and body mass index (BMI). Mean index of physical activity was calculated based on frequency of household/childcare activities, nonsports leisure time and sports activities[33]. Age assessment was based on self-reported date of birth. Race/ethnicity identification was based on the self-reported identification. BMI was calculated as weight (kg) divided by height (meters) squared. Height and weight were measured using standardized protocols.
Statistical analysis SPSS (version 20.0) and R (version 3.5.2 basic) were used to analyze the data. All continuous variables represent a non-normal distribution according to Kolmogorov-Smirnov test, and described by the median with the interquartile range. Chi-square tests and Mann-Whitney U test were used to compare the percentages of categorical variables and averages of continuous variables between women with low (<16) versus high (≥16) CES-D scores. Linear regression was
used to examine the relationship between oleic acid and linoleic acid intake and CES-D scores. oleic acid and linoleic acid intake were categorized by quartiles (quartile 4: ≥75th percentile, quartile 3: ≥50th to 75th percentile, quartile 2: ≥25th to 50th percentile, quartile 1: <25th percentile). Logistic regression was performed to examine the associations between oleic acid and linoleic acid intake and depressive symptoms (CES-D scores≥16), with the quartile 1 as the reference category. The crude model had no adjustment. Model 1 was adjusted for age, race/ethnicity, total family income and education, and model 2 was adjusted for age, race/ethnicity, total family income, education, physical activity, current smoker, menopausal status and BMI. Tests for linear trend were performed by entering the median value of each category of oleic acid and linoleic acid as a continuous variable in the models. To further investigate the relationship between oleic acid and linoleic acid intake and depression symptoms, restricted cubic spline analysis was conducted in a fully adjusted model with knots at the 5th, 15th, 75th, 95th percentiles of the distribution with 10th as a reference knot.
Results Table 1 presents the characteristics of the 2793 women across CES-D scores. Women in the total sample were approximately 46 years old and predominantly white and overweight. Women with depressive symptoms (CES-D scores≥16) had higher dietary oleic acid and linoleic acid intake compared to women without depressive symptoms (CES-D scores < 16). Table 2 presents the multivariate-adjusted liner associations between oleic acid and linoleic acid intake and CES-D scores. The crude regression coefficient with the 95% confidence intervals (CIs) of CES-D scores indicated that oleic acid and linoleic acid intake were positively associated
with CES-D scores. After adjustment for age, race, total family income and education in model 1, higher oleic acid and linoleic acid intake were significantly related to higher depressive symptoms. This association remained statistically significant and was little changed with fully controlling for age, race/ethnicity, total family income, education, physical activity, current smoker, menopausal status and BMI in model 2 (β=0.089, P<0.001; β=0.145, P<0.001, respectively). Table 3 presented odds ratios (ORs) and the 95% CI of depressive symptoms (CES-D score ≥16) across quartiles of oleic acid and linoleic acid intake. The crude model indicated that dietary oleic acid and linoleic acid intake were positively associated with depressive symptoms. After adjustment for age, race, total family income and education in model 1, the results were similar to those of the crude model. This association remained statistically significant and was changed little when fully controlling for age, race/ethnicity, total family income, education, physical activity, current smoker, menopausal status and BMI in model 2. The fully adjusted ORs (95% CI) of depressive symptoms were 1.994 (1.298-3.063) and 1.592 (1.047-2.421) in the highest versus lowest quartile of oleic acid and linoleic acid intake, respectively. Fig. 1 depicts the results of the restricted cubic spline analyses. The results showed that dietary oleic acid and linoleic acid intake were positively associated with risk of elevated CES-D score (≥16), suggesting of line-shaped association.
Discussion In the present study, we used SWAN 1995-1997 data and included 2793 participants aged 42-52 years to evaluate the associations of oleic acid and linoleic acid intake with depressive symptoms. The results of this study found that CES-D score was positively associated with oleic
acid and linoleic acid intake, and these positive associations of oleic acid and linoleic acid intake remained statistically significant after controlling for potential confounders. Similar positive associations were observed between oleic acid and linoleic acid intake and depressive symptoms (CES-D score ≥16) women in unadjusted model, age-, race/ethnicity-, total family income- and education-adjusted model and the fully adjusted model. To the best of our knowledge, this is the first time to investigate the associations between oleic acid and linoleic acid intake and depressive symptoms in perimenopausal women. Mechanically, neuronal differentiation relies on synthesis of oleic acid [34]. High oleic acid diet can specifically decrease sensitivity of enteric and vagal neuronal indicating that decreased sensitivity to gastric and satiation inhibitory effects of oleic acid may mediated via specific reduction by fatty acid[35]. The hypothalamus and other regions link the sensing of fatty acids to the adjustment of behavior and metabolism. The oleic acid can reduce expression of hypothalamic neuropeptide Y[36]. Fatty acid composition of hippocampus and brain in cognitive impaired rats involve alterations in oleic acid[37]. The amounts of linoleic acid needed in the diet to elaborate membrane function and structures in brain, have been determined[38]. Evidence from mice showed that imbalance between alpha-linolenic acid (18:3n-3, ALA) and linoleic acid (18:2n-6, LA) induce anxious behavior in offspring[39]. The alpha-linolenic acid deficiency has been associated with the increased risk of mood disorders while increased linoleic acid results in abnormal anxiety and depressive -related behaviors[40, 41]. Therefore, a LA excess/ALA deficient dietary condition is suggested to cause mood disorders[42]. The Western diet has been characterized by increasing consumption of seed oils whose unsaturated fatty acids are predominantly oleic acid and linoleic acid[13]. Evidence from
metabolic, biochemical and epidemiological studies confirmed that oleic acid has a beneficial effect against several health conditions, such as cardiovascular diseases[14] and cancer[15]. Higher oleic acid was also associated with reduced likelihood of depression among adults while higher linoleic and oleic fatty acid may increase the risk of depression[16]. However, the previous evidences have been performed in general. It remains unknown whether oleic acid or linoleic acid intake impacts depression in perimenopausal women. Various factor such as age, sex and menopausal status could confound the associations found in earlier studies. The present study extends the previous studies and provides reliable evidence that dietary oleic acid or linoleic acid intake are positively associated with depressive symptoms. That is consistent with previous results which indicated that linoleic acid may enhance the risk of depression in general population[16]. However, higher oleic acid was reported to be associated with reduced likelihood of depression. The different population in our study may contribute to this contradictory result. Our research has several strengths and limitations. The major strength of our research is the use of a national wide sample of perimenopausal women in the US. Additionally, the positively associations between oleic acid and linoleic acid intake and depressive symptoms remained significant after full adjustment for confounders. Unfortunately, there are still some limitations in our research. On the one hand, the cross-sectional design of this study is the major limitation. Because a cross-sectional is hard to make causal inference. Thus, reverse causality, depressive symptoms may result in decreased food intake resulting in the reduced oleic acid and linoleic acid intake. On the other hand, lacking biological detection is another limitation. It is desirable to investigate the fatty acids detected in adipose tissue, which can accurately reflect long-term dietary intake of fatty acids due to the low turnover in adipose tissue[43]. Collection of daily
dietary information relied on the participant’s ability to remember. That might cause recall bias. Additionally, memory may be affected by depressive symptoms. That might potentially differential assessment error. Conclusion Our results show that oleic acid and linoleic acid intake may be positively associated with depressive symptoms in perimenopausal women. Nevertheless, the causality of our findings could not be determined due to a cross-sectional design. Prospective studies are needed to verify our findings.
Author Statement Contributors Yan Li and Yongqing Tong designed study; Di Li collected and analyse data; Di Li wrote the manuscript; Yan Li and Yongqing Tong appraise and revise the manuscript.
s
Acknowledgements
We thank all individuals who were responsible for the planning and administering of SWAN and making the datasets of SWAN available on their website. We also acknowledge the reviewers and editors for view our work.
Funding Our study was supported by the National Natural Science Foundation of China (No. 81772265).
Conflicts of interest The authors have declared no conflicts of interest.
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Table 1 Characteristics of participants by CES-D score, represented by Medians and Interquartile Range (IQR). Variable
Total n=2793
CES-D score<16 n=2182
CES-D score≥16 n=611
p value
Age (year)
46 (44-48)
46 (44-48)
45 (43-47)
0.004
Black/African American
788 (28.2%)
596 (27.3%)
192 (31.4%)
Chinese/Chinese American
233 (8.3%)
202 (9.3%)
31 (5.1%)
Japanese/Japanese American
235 (8.4%)
199 (9.1%)
36 (5.9%)
1298 (46.5%)
1043 (47.8%)
255 (41.7%)
239 (8.6%)
142 (6.5%)
97 (15.9%)
Race/ethnicity(%)
Caucasian/White Non-Hispanic Hispanic
<0.001
<0.001
Education Less than High School
200 (7.2%)
119 (5.5%)
81 (13.3%)
High School Graduate
479 (17.3%)
345 (16.0%)
134 (22.1%)
Some College/Technical School
875 (31.6%)
671 (31.1%)
204 (33.6%)
College Graduate
565 (20.4%)
465 (21.5%)
100 (16.5%)
Postgraduate
646 (23.4%)
558 (25.9%)
88 (14.5%) <0.001
Total family income Less Than $19,999
370 (13.6%)
219 (10.3%)
151 (25.8%)
$20,000 to $49,999
928 (34.1%)
710 (33.3%)
218 (37.3%)
$50,000 to $99,999
1020 (37.5%)
840 (39.4%)
180 (30.8%)
$100,000 or More
400 (14.7%)
364 (17.1%)
36 (6.2%)
2.6 (2.0-3.4)
2.6 (2.0-3.4)
2.2 (1.6-3.0)
Physical activity
<0.001
Current smoker no
683 (60.0%)
548 (64.0%)
135 (47.9%)
yes
455 (40.0%)
308 (36.0%)
147 (52.1%)
Menopausal Status
<0.001
<0.001
Early Peri-menopausal
1250 (45.5%)
934 (43.5%)
316 (52.6%)
Pre-menopausal
1502 (54.5%)
1217 (56.5%)
285 (47.4%)
BMI (kg/m )
26.51 (22.85-31.95)
26.22 (22.70-31.32)
27.84 (23.36-33.56)
<0.001
Dietary Oleic Acid intake (g/d)
23.92 (17.28-32.36)
23.41 (16.98-31.37)
26.26 (18.99-35.96)
<0.001
11.32 (7.91-16.16)
11.15 (7.77-15.50)
12.33 (8.38-17.88)
<0.001
7 (3-14)
5 (2-9)
22 (18-29)
<0.001
2
Dietary Linoleic Acid intake (g/d) CES-D score
BMI: body mass index; CES-D: Center for Epidemiological Studies Depression
Table 2 Associations of CES-D scores with dietary oleic acid intake and linoleic acid intake (regression coefficient and 95% confidence intervals). Crude no adjustment Oleic Acids intake (g/d)
Linoleic Acids intake (g/d)
Standard Error
β (95%CI)
p value
Standard Error
β (95%CI)
p value
Crude
0.014
0.095 (0.069-0.122)
<0.001
0.026
0.131 (0.079-0.183)
<0.001
Model1
0.014
0.078 (0.051-0.104)
<0.001
0.026
0.136 (0.084-0.188)
<0.001
Model2
0.021
0.089 (0.047-0.131)
<0.001
0.041
0.145 (0.064-0.225)
<0.001
Model 1 adjusted for age, race/ethnicity, total family income and education Model 2 adjusted for age, race/ethnicity, total family income, education, physical activity, current smoker, menopausal status and BMI
Table 3 Weighted odds ratios (95% confidence intervals) of depressive symptoms (CES-D score ≥16) across quartiles of oleic acid intake and linoleic acid intake. Intake cut off
Cases/parti cipants
Crude
Model 1
Model 2
Oleic acids intakes (g/d) Quartile 1 (low)
< 17.28
192/698
1.000 (ref.)
1.000 (ref.)
1.000 (ref.)
Quartile 2
17.28 to < 23.92
154/700
1.174 (0.898-1.535)
1.169 (0.882-1.549)
1.637 (1.025-2.614)
Quartile 3
23.92 to < 32.36
141/697
1.306 (1.003-1.700)
1.245 (0.941-1.646)
1.569 (1.002-2.458)
≥32.36
124/698
1.756 (1.360-2.268)
1.592 (1.213-2.091)
1.994 (1.298-3.063)
<0.001
<0.001
0.004
Quartile 4 (high) P-trend Linoleic acids intakes (g/d) Quartile 1 (low)
< 7.905
188/698
1.000 (ref.)
1.000 (ref.)
1.000 (ref.)
Quartile 2
7.905 to < 11.32
150/697
1.043 (0.800-1.359)
1.046 (0.791-1.383)
0.947 (0.598-1.501)
Quartile 3
11.32 to < 16.16
139/700
1.154 (0.889-1.498)
1.282 (0.973-1.689)
1.351 (0.875-2.087)
≥16.16
134/698
1.552 (1.206-1.996)
1.638 (1.248-2.150)
1.592 (1.047-2.421)
<0.001
<0.001
0.008
Quartile 4 (high) P-trend
Test for trend based on variable containing median value for each quintile. Crude no adjustment
Model 1 adjusted for age, race/ethnicity, total family income and education Model 2 adjusted for age, race/ethnicity, total family income, education, physical activity, current smoker, menopausal status and BMI
Fig. 1. Restricted cubic spline model of the odds ratios of high CES-D score (≥16) with oleic acid intake and linoleic acid intake. Adjusted for age, race/ethnicity, total family income, education, physical activity, current smoker, menopausal status and BMI. The dashed lines represent the 95% confidence intervals.
Graphical abstract