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Association between mental health status and bone mineral density: Analysis of the 2008-2010 Korea national health and nutrition examination survey

  • Changtae Hahn,

    Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Visualization, Writing – original draft, Writing – review & editing

    Affiliation Department of Psychiatry, Daejeon St. Mary’s Hospital, College of Medicine, Catholic University of Korea, Deajeon, Republic of Korea

  • Ji Hoon Oh,

    Roles Formal analysis, Methodology

    Affiliation Department of Psychiatry, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

  • Soo-Hyun Joo,

    Roles Conceptualization, Data curation, Investigation, Methodology, Project administration, Resources, Software, Validation

    Affiliation Department of Psychiatry, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

  • Jo-Eun Jeong,

    Roles Conceptualization, Data curation, Investigation, Methodology, Project administration, Software, Validation

    Affiliation Department of Psychiatry, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

  • Jeong-Ho Chae,

    Roles Investigation, Resources, Supervision, Validation

    Affiliation Department of Psychiatry, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

  • Chang-Uk Lee,

    Roles Investigation, Resources, Supervision, Validation

    Affiliation Department of Psychiatry, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

  • Tae-Suk Kim

    Roles Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Visualization, Writing – review & editing

    bluenote@catholic.ac.kr

    Affiliation Department of Psychiatry, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

Association between mental health status and bone mineral density: Analysis of the 2008-2010 Korea national health and nutrition examination survey

  • Changtae Hahn, 
  • Ji Hoon Oh, 
  • Soo-Hyun Joo, 
  • Jo-Eun Jeong, 
  • Jeong-Ho Chae, 
  • Chang-Uk Lee, 
  • Tae-Suk Kim
PLOS
x

Abstract

The current study aimed to investigate the association between mental health status and bone mineral density (BMD) using data from the Korean National Health and Nutrition Examination Survey (KNHANES) 2008–2010. We enrolled 15,876 South Korean participants (4,010 postmenopausal females, 4,836 premenopausal females, and 7,016 males, all aged 20 years or older). BMD was measured using dual-energy radiography absorptiometry at the femoral neck (NK), lumbar spine (LSP), and total femur (TFM). Mental health status data were obtained from a self-report questionnaire that assessed psychological stress, depressed mood, and suicidal ideation. Psychological stress was negatively correlated with BMD in the LSP, NK, and TFM for the male group. Depressed mood was associated with lower BMD in the LSP, NK and TFM for the premenopausal female group, and in the LSP for the male group. Suicidal ideation was associated with lower BMD in the NK and TFM for the male group. Mental health problems were associated with lower BMD, especially in premenopausal females and males. Future investigations should focus on the shared pathophysiology between mental health problems and BMD, and the interrelationship between increased BMD and recovery from mental health problems.

Introduction

In the past decade, mental illnesses have received worldwide attention as a major public health problem.[1] Several investigators reported that mental health problems were significantly associated with poor quality of life,[2] and various mental disorders were related to functional impairment.[3,4] Mental health illnesses are fairly common; approximately 25% of all individuals experience mental health problems at some point in their lifetime.[5] Therefore, patients with physical diseases could have a concurrent mental health disease, whether the two types of disease were independent or interrelated. It is certain that physical and mental disease comorbidity could cause an increased disease burden, not only in terms of effect accumulation on functional impairment severity, but also due to increased health care expenses. Furthermore, from a clinician’s perspective, physical and mental disease comorbidity leads to greater therapeutic challenges and poorer outcomes than if each problem existed independently.[5]

Several investigators found that various mental health problems were significantly associated with physical diseases, particularly chronic conditions, including cardiovascular disease, chronic obstructive pulmonary disease (COPD), and diabetes.[68] Osteoporosis is a metabolic bone disease characterized by loss of bone mass and bone tissue microarchitectural deterioration. Osteoporosis is a major health problem that can lead to fragile fractures and increased fracture risk. It is a chronic, prevalent, and debilitating disease that strongly influences morbidity, mortality and quality of life.[9] In this context, several investigators have been concerned that osteoporosis and mental disorders might share a common denominator which indicates the possibility of a mutual relationship. Several studies found that major depressive disorder was associated with lower bone mineral density and that lower bone mineral density in subjects with depression increased fracture risk.[912] In addition, some investigators observed that postmenopausal osteoporosis has a specific relationship with depression, [13,14] and several studies explored the shared pathophysiology between osteoporosis and depression.[13,1520]

In the present study, we aimed to evaluate the association between lower bone mineral density and mental health problems among Korean adults who participated in the Korean National Health and Nutrition Examination Survey (KNHANES, 2008–2010). We hypothesized that mental health problems, including psychological stress and depressive symptoms, as well as lower bone mineral density, would be significantly correlated with one another after controlling for essential demographic data that could present potential risk factors for lower bone mineral density and mental health problems. This study examined relatively extensive demographic data that could identify potential risk factors for lower bone mineral density and/or depression, relative to the above-mentioned studies. Furthermore, we also focused on mental health problems, such as psychological stress and suicidal ideation, as well as depression, the primary focus of previous studies.

Materials and methods

Subjects and data collection

The current study analyzed data from the KNHANES (2008–2010), which was a cross-sectional, nationwide, population-based survey conducted by the Division of Chronic Disease Surveillance of the Korean Center for Disease Control and Prevention from 2008 to 2010. The KNHANES is composed of three different surveys on the health and nutrition of the Korean population: a health interview survey, physical examination, and nutrition survey.[21] Health interviews and physical examinations were performed at mobile exam centers, and nutrition data were collected through visits to subject households. The survey acquired a representative national sample from the Korean population using a stratified, multistage, clustered probability sampling design. KNHANES is available to researchers as an open material on the website. (knhanes.cdc.go.kr)

From 2008 to 2010, 29,235 individuals participated in the KNHANES. The present study included 15,876 of the original participants. Among participants whose BMD was measured in the KNHANES (2008–2010), the present study included only those aged 20 years or older. We then divided participants into three groups: males, premenopausal females, and postmenopausal females. Since menopause has been related to decreased bone mineral density at various skeletal sites and men do not undergo menopause, our three-group classification sought to clarify the substantive correlation between bone mineral density and mental health while simultaneously considering hormonal changes in females and gender differences.

We excluded subjects with missing data on essential analytic variables, such as bone mineral density (BMD) and the mental health questionnaire. The Institutional Review Board of the Centers for Disease Control and Prevention in Korea approved use of KNHANES (2008–2010) data. All participants of the KNHANES used in the current study provided written informed consent.

Bone mineral density measurement

A trained radiographer in a mobile examination center using dual-energy radiography absorptiometry (DXA; DISCOVERY-W fan-beam densitometer; Hologic, Bedford, MA, USA) measured BMD at the femoral neck, lumbar spine, and total femur. This device used Hologic Discovery software, version 3.1. Accuracy was evaluated by performing double scans on 30 random samples. Coefficients of variation (CVs) for accurate BMD assessment were 1.9% for the lumbar spine, 2.5% for the femur neck, and 1.8% for the total femur. Calibration was performed daily. We analyzed lumbar spine, femur neck, and total femur BMD.

Mental health measures

Mental health data were obtained from a self-report mental health questionnaire administered under the supervision of a researcher. Mental health surveys were divided into questions from three domains: stress, depression, and suicidal ideation and attempts. Stress level stress was assessed by asking, "What are your stress levels?” Possible responses included none, mild, moderate, or severe. We divided research participants into two groups based on reported stress levels (none to mild and moderate to severe). Depressive symptoms were assessed by asking, "Have you felt any sadness or hopelessness that has interfered with your daily life for two or more continuous weeks during the past year?" Participants were placed into a dichotomous category according to their answer, "yes" or "no." Watkins and colleagues evaluated the validity of this indicator for depressive symptoms. [22] Suicidal ideation was assessed by asking, "Did you ever think about committing suicide?" Participants were divided into two groups according to their answer, "yes" or "no." Gaynes and colleagues reported that this assessment method was a useful predictor of suicidal attempts in a survey of suicidal risk. [23]

Statistical analysis

We presented data as mean ± standard error (SE) for continuous variables or as percentages (SE) for categorical variables. Analysis of variance was used for continuous variables, and a Chi-square test was applied to categorical variables to quantify differences in participant characteristics. A multi-variable logistic regression model was employed to analyze the relationship between mental health measures and BMD for every increment of 0.1 g/cm2. Model 1 was adjusted for age and body mass index (BMI). Model 2 was adjusted for model 1 covariates, as well as cigarette smoking, alcohol intake, regular exercise, education and income. Model 3 was adjusted for model 2 covariates, as well as metabolic syndrome, diabetes mellitus (DM), and hypertension (HTN). Analysis of covariance was used to compare BMD between postmenopausal, premenopausal and male groups covaried according to the three mental health domains of stress, depression, and suicidal ideation. Stress level was organized into two groups (none and mild vs moderate and severe). Depressive symptoms and suicidal ideation were organized into dichotomous categories (yes or no). The Statistical Analysis System (SAS) software package version 9.2 for Windows (SAS Institute Inc., Cary, NC, USA) was used to accommodate the complex sampling design and weighting inherent in the KNHANES, and to provide approximations for the entire Korean population. All statistical tests were two-tailed, and a p < 0.05 was considered statistically significant.

Results

Table 1 presents study population sociodemographic characteristics (postmenopausal female, premenopausal female, and male groups). Mean age was 62.8±0.2 years for postmenopausal females, 35.3±0.2 years for premenopausal females, and 43.7±0.3 years for males. Table 1 shows BMD values for the three groups (lumbar spine (LSP), total femur (TFM), and femoral neck (NK)). Table 1 shows body mass index (BMI), waist circumference, sleep duration, smoking, drinking, exercise, education, income, residence, metabolic syndrome, DM, and HTN for the three study groups. Table 1 contains information about covariates that should be considered.

Table 2 presents differences in mental health status between the postmenopausal female, premenopausal female and male groups. The proportion of postmenopausal females, premenopausal females, and males who reported moderate to severe stress was 29±0.9%, 34±0.8%, and 27.1±0.7% (p = 0.0001), respectively. Depressed mood for two or more continuous weeks was reported by 22.1±0.8% of postmenopausal females, 16.4±0.6% of premenopausal females, and 9.2±0.4% of males (p < .0001). Suicidal ideation was reported by 27.4±1% of postmenopausal females, 18.5±0.7% of premenopausal females, and 10.6±0.4% of males (p < .0001).

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Table 2. Participants with positive responses to mental health questionnaires.

https://doi.org/10.1371/journal.pone.0187425.t002

Analysis of covariance (ANCOVA) was used to compare BMD between postmenopausal, premenopausal and male groups covaried according to the three mental health domains of stress, depression, and suicidal ideation. And the results of ANCOVA showed statistically significant differences. Table 3 presents results from the multivariate logistic regressions analyzing the relationship between BMD and mental health among postmenopausal females, premenopausal females, and males. Moderate to severe stress was correlated with decreased BMD at the LSP, NK, and TFM in the male group after adjusting for age and BMI (Model 1). For the male group, after adjusting for age and BMI, smoking, drinking, exercise, education and income (Model 2), the correlation between moderate to severe stress and decreased BMD remained significant, as well as after adjusting for age and BMI, smoking, drinking, exercise, education, income, metabolic syndrome, DM and HTN (Model 3). These covariates have been linked to BMD in previous studies analyzing KNHANES data. [2426] Through the stepwise analysis (Model 1, 2, 3), we considered the importance of selecting covariates which was controversial and difficult tasks. Depressed mood was associated with lower BMD at the LSP and NK among premenopausal females in Models 1 and 2. In Model 3, depressed mood showed a negative correlation with BMD at the LSP, NK and TFM in premenopausal females, and at the LSP for males. Suicidal ideation was related to lower BMD at the TFM in postmenopausal females, at the LSP and NK in premenopausal females, and at the NK and TFM in males in Model 1. In Model 2, suicidal ideation was associated with lower BMD at the LSP and NK in premenopausal females and at the NK and TFM in males. In Model 3, suicidal ideation was correlated with lower BMD at the NK and TFM in males.

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Table 3. The relationship between mental health status and bone mineral density of postmenopausal females, premenopausal females and males.

https://doi.org/10.1371/journal.pone.0187425.t003

Discussion

Several previous studies have demonstrated the relationship between BMD and mental health. [920] However, these studies included a relatively small number of participants, and they concentrated primarily on depression, [912,27,28] although Guo and colleagues reported an association between osteoporosis and various psychiatric disorders (depression, bipolar disorder, schizophrenia, and Alzheimer's disease).[29] Thus, our study intended to explore the relationship between BMD and various mental health problems (stress, depressive symptoms and suicidal ideation). Furthermore, we considered the level of stress that individuals experienced, even if it was a subclinical state. In addition, we used representative data from KNHANES conducted from 2008 to 2010, which allowed us to include a large number of participants.

This study’s findings indicated that various psychological symptoms were associated with BMD at three sites (LSP, NK, and TFM) in postmenopausal females, premenopausal females and males.

We observed that moderate to severe psychological stress was associated with lower BMD at the LSP, NK and TFM in the male group, while there was no correlation between stress and BMD in postmenopausal or premenopausal females (Table 3). Psychological stress can lead to alterations in the secretion of many hormones, including cortisol, catecholamines, vasopressin, gonadotropins, thyroid hormones, growth hormone, prolactin and insulin.[30] Furthermore, several investigators have suggested that psychological stress could result in decreased testosterone secretion. [17,18] The hypothalamic-pituitary-adrenal axis, which is influenced by psychological stress, could effect inhibitory action on the hypothalamic-pituitary-gonadal (HPG) axis. Inhibition of the HPG axis results in decreased testosterone secretion.[31] A lower serum testosterone concentration is associated with decreased BMD, resulting in osteoporosis. [32] Our findings were consistent with the studies described above. Furthermore, our observation of the association between psychological stress and BMD after adjusting for age and BMI, smoking, drinking, exercise, education, income, metabolic syndrome, DM and HTN (Model 3) suggests a primary role for biological factors, including hormonal alterations.

Depressed mood was associated with lower BMD at the LSP and NK in premenopausal females in Models 1 and 2. In Model 3, depressed mood was correlated with decreased BMD at the LSP, NK and TFM in premenopausal females, and at the LSP in males (Table 3). Depressed mood was also closely associated with BMD in the premenopausal female group, although the BMD at the LSP in the male group was related to depressed mood. Although stress could affect biological alterations, including decreased female sex hormones in women [33], our findings indicate that stress, which might be subjective or subclinical, had little influence on BMD alteration in the female groups. However, depressed mood, which can be more severe than subjective or subclinical stress, can cause biological alterations, including hormonal changes. Considerable psychological burdens, like depressed mood, could influence the abundant state of female sex hormones and lead to biological alterations, including decreased estrogen, which results in lower BMD. Depressed mood was not associated with BMD in the postmenopausal female group, although it was in the premenopausal female group. The reason lies in that dramatic hormonal changes over a woman’s life course, such as menopause, could have a greater influence on BMD than psychological changes, like depressed mood. Furthermore, notably lower estrogen levels in the postmenopausal female group could make these women less sensitive to depressed mood. Therefore, our findings indicate that the postmenopausal female and male groups had similar patterns in the association between depressed mood and BMD alteration. In addition, we could hypothesize that the alteration of male sex hormones was less sensitive than it of female sex hormones to the depressed mood at least. It is interesting that subjective or subclinical stress was closely associated with lower BMD in the male group, unlike the association between BMD and depressed mood.

Suicidal ideation, one of the most severe mental health problems, was related to lower BMD at the TFM in postmenopausal females, at the LSP and NK in premenopausal females, and at the NK and TFM in males in Model 1. It might be that suicidal ideation affects female and male sex hormonal changes and decreased BMD in spite of lower hormonal levels, like in the case of postmenopausal females. However, in Model 2, suicidal ideation was associated with lower BMD at the LSP and NK in premenopausal females and at the NK and TFM in males. In Model 3, suicidal ideation was correlated with lower BMD at the NK and TFM in males. Several investigators found that there were gender differences in the effects of various demographic and risk factors for suicidal ideation.[3436] Indeed, in Model 3, which was adjusted for age, BMI, smoking, drinking, exercise, education, income, metabolic syndrome, DM and HTN, suicidal ideation was correlated with lower BMD in males. Suicidal ideation could be the cumulative product of various mental health problems, although stress and depressed mood were relatively singular and homogenous expressions of mental health problems. Such a severe mental health problem could be correlated with lower BMD in males and females (Model 1). However, our findings showed that menopause could have a significant impact on lower BMD and that severe psychopathology, such as suicidal ideation, was not significantly associated with decreased BMD (Model 2). Furthermore, suicidal ideation, a severe psychopathology, was correlated with lower BMD in males compared to females. (Model 3)

This study has several limitations. First, this study investigated individuals from only one Asian country, although we analyzed a comparatively large sample. Second, this cross-sectional study was not able to establish causation between mental health and BMD. Third, there was no information about whether participants received psychiatric treatment, including psychiatric medications. Fourth, we could not determine if decreased BMD, which was associated with mental health problems, represented a clinically significant decrease, such as osteomalacia or osteoporosis. Fifth, we investigated the relationship between mental health status and BMD among three groups (postmenopausal females, premenopausal females and males). Such a design might be advantageous in terms of considering menopause. But women have been divided into two categories according to pre- and postmenopausal with a discrepancy of mean age in-between the two female groups although we adjusted for age statistically. Sixth, KNHANES mental health data were composed of self-report scale. Therefor we should considered limitations in terms of their reliability and validity. Lastly, we did not assess male and female sex hormone levels, such as estrogen and testosterone. Therefore, additional longitudinal studies regarding various mental health problems and BMD should be conducted in other races or countries. Furthermore, follow-up studies should include various medical examinations and histories.

In conclusion, evidence from this study indicates that mental health problems were associated with lower BMD, especially among premenopausal females and males. Future investigations should focus on the shared pathophysiology between mental health problems and BMD, and the interrelationship between increased BMD and recovery from mental health problems.

Acknowledgments

The authors wish to acknowledge the financial support of the Catholic Medical Center Research Foundation made in the program year of 2014, 2016 and thank the Korean Center for Disease Control and Prevention, which conducted the KNHANES studies, and the subjects who participated in the KNHANES. We also thank Kyungdo Han for statistical analyses.

References

  1. 1. Abma F, van der Klink JJL, Terwee C, Amick B, Bültmann U (2012) Evaluation of the measurement properties of self-reported health-related work-functioning instruments among workers with common mental disorders. Scandinavian journal of work, environment & health 38: 5–18.
  2. 2. Connell J, Brazier J, O'Cathain A, Lloyd-Jones M, Paisley S (2012) Quality of life of people with mental health problems: a synthesis of qualitative research. Health Qual Life Outcomes 10: 138. pmid:23173689
  3. 3. Evans VC, Iverson GL, Yatham LN, Lam RW (2014) The relationship between neurocognitive and psychosocial functioning in major depressive disorder: a systematic review. J Clin Psychiatry 75: 1359–1370. pmid:25551235
  4. 4. Iosifescu DV (2012) The relation between mood, cognition and psychosocial functioning in psychiatric disorders. Eur Neuropsychopharmacol 22 Suppl 3: S499–504.
  5. 5. Doherty A, Gaughran F (2014) The interface of physical and mental health. Social psychiatry and psychiatric epidemiology 49: 673–682. pmid:24562320
  6. 6. Charlson FJ, Moran AE, Freedman G, Norman RE, Stapelberg NJ, et al. (2013) The contribution of major depression to the global burden of ischemic heart disease: a comparative risk assessment. BMC Med 11: 250. pmid:24274053
  7. 7. Hasan SS, Clavarino AM, Mamun AA, Doi SA, Kairuz T (2013) Population impact of depression either as a risk factor or consequence of type 2 diabetes in adults: a meta-analysis of longitudinal studies. Asian J Psychiatr 6: 460–472. pmid:24309855
  8. 8. Panagioti M, Scott C, Blakemore A, Coventry PA (2014) Overview of the prevalence, impact, and management of depression and anxiety in chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis 9: 1289–1306. pmid:25419126
  9. 9. Aloumanis K, Mavroudis K (2013) The "depressive" face of osteoporosis and the "osteoporotic" face of depression. Hormones 12: 350–362. pmid:24121377
  10. 10. Lee C, Liao C-H, Lin C-L, Liang J-A, Sung F-C, et al. (2015) Increased risk of osteoporosis in patients with depression: a population-based retrospective cohort study. Mayo Clinic proceedings 90: 63–70. pmid:25572194
  11. 11. Cizza G (2011) Major depressive disorder is a risk factor for low bone mass, central obesity, and other medical conditions. Dialogues Clin Neurosci 13: 73–87. pmid:21485748
  12. 12. Cizza G, Primma S, Coyle M, Gourgiotis L, Csako G (2010) Depression and osteoporosis: a research synthesis with meta-analysis. Horm Metab Res 42: 467–482. pmid:20455194
  13. 13. Bab IA, Yirmiya R (2010) Depression and bone mass. Ann N Y Acad Sci 1192: 170–175. pmid:20392233
  14. 14. Reginster JY, Deroisy R, Paul I, Hansenne M, Ansseau M (1999) Depressive vulnerability is not an independent risk factor for osteoporosis in postmenopausal women. Maturitas 33: 133–137. pmid:10597877
  15. 15. Bab I, Yirmiya R (2010) Depression, selective serotonin reuptake inhibitors, and osteoporosis. Curr Osteoporos Rep 8: 185–191. pmid:20809204
  16. 16. Cizza G, Nguyen VT, Eskandari F, Duan Z, Wright EC, et al. (2010) Low 24-hour adiponectin and high nocturnal leptin concentrations in a case-control study of community-dwelling premenopausal women with major depressive disorder: the Premenopausal, Osteopenia/Osteoporosis, Women, Alendronate, Depression (POWER) study. J Clin Psychiatry 71: 1079–1087. pmid:20492842
  17. 17. Cizza G, Primma S, Csako G (2009) Depression as a risk factor for osteoporosis. Trends Endocrinol Metab 20: 367–373. pmid:19747841
  18. 18. Mezuk B, Eaton WW, Golden SH (2008) Depression and osteoporosis: epidemiology and potential mediating pathways. Osteoporos Int 19: 1–12.
  19. 19. Vrkljan M, Thaller V, Lovricevic I, Gacina P, Resetic J, et al. (2001) Depressive disorder as possible risk factor of osteoporosis. Coll Antropol 25: 485–492. pmid:11811278
  20. 20. Cizza G, Ravn P, Chrousos GP, Gold PW (2001) Depression: a major, unrecognized risk factor for osteoporosis? Trends Endocrinol Metab 12: 198–203. pmid:11397644
  21. 21. Park H (2013) The Korea national health and nutrition examination survey as a primary data source. KJFM 34(2):79–79. pmid:23560205
  22. 22. Watkins C, Daniels L, Jack C, Dickinson H, van Den Broek M (2001) Accuracy of a single question in screening for depression in a cohort of patients after stroke: comparative study. BMJ 323: 1159. pmid:11711407
  23. 23. Gaynes BN, West SL, Ford CA, Frame P, Klein J, et al. (2004) Screening for suicide risk in adults: a summary of the evidence for the U.S. Preventive Services Task Force. Ann Intern Med 140: 822–835. pmid:15148072
  24. 24. Choi HS, Park JH, Kim SH, Shin S, Park MJ (2017) Strong familial association of bone mineral density between parents and offspring: KNHANES 2008–2011. Osteoporos Int 28: 955–964. pmid:27747365
  25. 25. Lim Y, Chun S, Lee JH, Baek KH, Lee WK, et al. (2016) Association of bone mineral density and diabetic retinopathy in diabetic subjects: the 2008–2011 Korea National Health and Nutrition Examination Survey. Osteoporos Int 27: 2249–2257. pmid:26883444
  26. 26. Jang KM, Cho KH, Lee SH, Han SB, Han KD, et al. (2015) Tooth loss and bone mineral density in postmenopausal South Korean women: The 2008–2010 Korea National Health and Nutrition Examination Survey. Maturitas 82: 360–364. pmid:26278872
  27. 27. Calarge C, Butcher B, Burns T, Coryell W, Schlechte J, et al. (2014) Major depressive disorder and bone mass in adolescents and young adults. Journal of bone and mineral research 29: 2230–2237. pmid:24723424
  28. 28. Lee CW, Liao CH, Lin CL, Liang JA, Sung FC, et al. (2015) Increased risk of osteoporosis in patients with depression: a population-based retrospective cohort study. Mayo Clin Proc 90: 63–70. pmid:25572194
  29. 29. Guo P, Wang S, Zhu Y, Shen X, Jin X, et al. (2012) Prevalence of osteopenia and osteoporosis and factors associated with decreased bone mineral density in elderly inpatients with psychiatric disorders in Huzhou, China. Shanghai Arch Psychiatry 24: 262–270. pmid:25328349
  30. 30. Ranabir S, Reetu K (2011) Stress and hormones. Indian journal of endocrinology and metabolism 15: 18–22. pmid:21584161
  31. 31. Nargund V (2015) Effects of psychological stress on male fertility. Nature reviews. Urology 12: 373–382. pmid:26057063
  32. 32. Tsujimura A (2013) The Relationship between Testosterone Deficiency and Men's Health. The World Journal of Men's Health 31: 126–135. pmid:24044107
  33. 33. Cameron JL (1997) Stress and behaviorally induced reproductive dysfunction in primates. Seminars in reproductive endocrinology 15: 37–45. pmid:9065976
  34. 34. Xu H, Zhang W, Wang X, Yuan J, Tang X, et al. (2015) Prevalence and influence factors of suicidal ideation among females and males in Northwestern urban China: a population-based epidemiological study. BMC Public Health 15: 961. pmid:26404535
  35. 35. Kim SM, Han DH, Trksak GH, Lee YS (2014) Gender differences in adolescent coping behaviors and suicidal ideation: findings from a sample of 73,238 adolescents. Anxiety Stress Coping 27: 439–454. pmid:24344782
  36. 36. Park S (2013) Gender-specific factors of suicide ideation among adolescents in the Republic of Korea: a nationally representative population-based study. Arch Psychiatr Nurs 27: 253–259. pmid:24070995