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NDT Advance Access originally published online on November 22, 2006
Nephrology Dialysis Transplantation 2007 22(3):857-861; doi:10.1093/ndt/gfl666
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© The Author [2006]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

The association of higher depressive symptoms and sexual dysfunction in male haemodialysis patients

Yu-Sen Peng1, Chih-Kang Chiang1,2, Kung-Yu Hung1,2, Shou-Shang Chiang3, Chia-Sheng Lu4, Chwei-Shiun Yang5, Kwan-Dun Wu2, Chin-Ching Yang6, Ru-Ping Lin7, Chee-Jen Chang8,*, Tun-Jun Tsai2,* and Wang-Yu Chen2

1Department of Internal Medicine, Far Eastern Memorial Hospital, 2National Taiwan University Hospital, 3Shin-Kong Wu Ho-Su Memorial Hospital, 4En Chu Kong Hospital, 5Cathay General Hospital, 6Taipei Municipal Ho-Ping Hospital, 7Da-Chien General Hospital and 8Graduate Institute of Basic Medical Science Chang Gung University, Taiwan, ROC

Correspondence and offprint requests to: Tun-Jun Tsai, PhD, Division of Nephrology, Department of Internal Medicine, National Taiwan University Hospital, No. 7, Chung-Shan South Road, Taipei 10016, Taiwan ROC. Email: paul{at}ha.mc.ntu.edu.tw Chee-Jen Chang, PhD, Graduate Institute of Basic Medical Science, Chang Gung University, No. 5, Fu-Hsing Street, Kuei Shan Hsiang, Tao-Yuan, Taiwan, ROC. Email: cjchang{at}mail.cgu.edu.tw



   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 
Background. The prevalence of sexual dysfunction among male haemodialysis patients is high. Sexual dysfunction is composed of both physiological and psychological factors. However, the role of pyschological depression is still obscure.

Methods. A multicentre cross-sectional study of 411 male haemodialysis patients was conducted to define the determinants of sexual dysfunction. Mid-week pre-dialytic biochemical and haematological parameters were obtained. All patients were required to complete three questionnaires by themselves: (i) the International Index of Erectile Function (IIEF, Chinese version); (ii) the Beck Depression Inventory (BDI, Chinese version) and (iii) the 36-item Short Form Health Survey Questionnaire (SF-36, Taiwan Standard Version 1.0).

Results. In total, 154 male patients completed the IIEF questionnaire. Their mean age was 50.2 ± 10.7 years. A linear multivariable regression analysis demonstrated advanced age, diabetes and the presence of depressive symptoms to be independently associated with sexual dysfunction. Subjects with sexual dysfunction had significantly lower quality of life scores.

Conclusions. The presence of depressive symptoms, highly prevalent in haemodialysis patients, is an independent factor of sexual dysfunction in male haemodialysis patients. In a comprehensive approach to the management of sexual dysfunction, a thorough evaluation of psychological depression must be included.

Keywords: depression; haemodialysis; quality of life; sexual dysfunction



   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 Acknowledgements
 References
 
Sexual dysfunction is highly prevalent in male end-stage renal disease (ESRD) patients on haemodialysis [1]. It is well known that sexual dysfunction is composed of both physiological and psychological factors. Furthermore, sexual dysfunction can cause marked distress and interpersonal difficulties [2]. In prior studies of sexual dysfunction in male ESRD patients, the focus has been on erectile dysfunction and associated physiological factors. Psychological depression is highly prevalent in ESRD patients [3]. However, there have been no studies addressing the psychological factors of sexual dysfunction in male ESRD patients. The association of psychological depression and sexual dysfunction deserves further exploration.

By use of self-reported questionnaires, we conducted a study to identify the possible association of depressive symptoms and sexual dysfunction in male chronic haemodialysis patients. In an effort to construct a comprehensive survey, we used the complete form of the International Index of Erectile Function (IIEF), not the short form, IIEF-5, to evaluate sexual function. Additionally, we tried to explore the impact of sexual dysfunction on quality of life (QOL). The 36-item Short Form Health Survey Questionnaire (SF-36) was applied.



   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 Acknowledgements
 References
 
Subjects
A total of 411 male patients with ESRD receiving haemodialysis at 14 hospitals or dialysis centres in northern Taiwan were included in this study. All patients had been receiving haemodialysis for more than 3 months before this study. They had no evidence of active psychiatric disease, infection, uncontrolled congestive heart failure (more severe than New York Heart Association functional class II), or acute complications from uraemia at the time of the study. The patients who were taking antipsychotic or antidepressant medications were excluded. Other exclusion criteria included refusing to join this study, cognitive impairment, history of alcohol or substance abuse, having dual sexual roles with multiple partners in their homosexual lives, and poorly controlled diabetes mellitus (post-prandial blood sugar higher than 300 mg/dl persistently in the last 1 month).

Biochemical and haematological parameters were obtained by mid-week pre-dialysis blood samples within 1 month of this study. Other clinical variables, including marital status, duration on haemodialysis, primary renal disease, coexistent diseases and medications in use, were also documented. Patients were defined to have cardiovascular disease if any one of the following conditions existed: angiography- demonstrated coronary or peripheral artery diseases, left ventricular ejection fraction <30% revealed by echocardiogram, previous myocardial infarction, or stroke history.

Questionnaires
After written informed consent was obtained, each patient was asked to complete three questionnaires on his own: (i) the complete form of the IIEF to assess sexual function; (ii) the Beck Depression Inventory (BDI, Chinese Version) to rate the severity of depressive symptoms, and (iii) the SF-36, Taiwan Standard Version 1.0, to perform a survey for QOL.

The IIEF is a self-administered questionnaire, which has been used to assess sexual function in the normal and ESRD populations [1,4]. The IIEF is a 15-item, validated instrument designed to measure sexual function in males. The index is comprised of five domains including erectile function, orgasmic function, sexual desire, intercourse satisfaction and overall satisfaction. Each item of the IIEF is scored on a 5- or 6-point categorical scale, with higher scores indicating more favourable outcomes, the scores ranging from 1 (almost never/never) to 5 (almost always/always). Scores for each domain vary, and the total score range is from 5 to 75. In the IIEF questionnaire, questions 1–5 and 15 address erectile function with a maximum score of 30, questions 9 and 10 orgasmic function with a maximum score of 10, questions 11 and 12 sexual desire with a maximum score of 10, questions 6–8 intercourse satisfaction with a maximum score of 15, and questions 13 and 14 addressing overall satisfaction with a maximum score of 10.

The BDI is a standard self-administered questionnaire and has been used in the screening and assessment of depression in ESRD patients [5]. BDI scores of 14–19 represent a mild degree of depression, 20–28 a moderate degree and 29–60 a severe degree of depression. The SF-36 is an instrument commonly utilized to measure QOL in the general and uraemic populations [6,7]. It includes eight domains: physical function (PF), role physical (RP), bodily pain (BP), general health (GH), vitality, social functioning (SF), role emotional (RE) and mental health (MH). The range of score in each domain is 0–100. Low scores in the eight domains indicate lower QOL. These eight scales have been compressed into two primary summary scales: the physical component scale and the mental component scale. Because there are no standard steps of transformation and aggregation of scale scores in the Chinese population, we did not transform the SF-36 scores to the summary scales.

This study was approved by the Ethical Committee of Hospitals and monitored by the Institutional Review Board.

Statistics
The patients’ characteristics were presented as mean ± SD. The Kolmogorov–Smirnov test and Shapiro–Wilk test of normality were used for data distribution analysis. Chi-square test and t-test were used to detect the difference of demographic and clinical characteristics between the study and non-responding group. Spearman's rho correlation test was used in screening the independent variables of sexual function scores. If P-values were <0.10, the variables were included in further regression analysis. Stepwise multivariable linear regression analysis with both backward elimination and forward selection were employed to evaluate any association between sexual function scores as the outcome variable and multiple independent variables. A two-tailed P-value <0.05 was considered statistically significant. For studying the association between the scores of sexual function and QOL, stepwise multivariable linear regression was used for analysis. All calculations were performed using a standard statistical package (SPSS 10.0 for Windows; SPSS Inc., Chicago, IL).



   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 Acknowledgements
 References
 
A total of 154 patients completed the IIEF questionnaire, with a response rate of 37.5%, and were enrolled into further analysis. There were 234 (56.9%) patients who did not engage in sexual activity anymore, and 23 (5.6%) patients refused the survey. The mean age of enrolled patients was 50.2 ± 10.7 years. They had been receiving haemodialysis 50.0 ± 46.7 (range 3.2–198.8) months before the study. Thirty-seven (24.0%) patients had diabetes mellitus (DM), and 48 (31.1%) patients had hypertension. Four (2.6%) patients received ß-blocker treatment. Other clinical characteristics are listed in Table 1. The mean total IIEF score for all patients was 49.1 ± 17.6. The score distribution of each sexual function domain is listed in Table 2.


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  		Table 1. Demographic and clinical characteristics of patients

 

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  		Table 2. The score distribution of each sexual function domain

 
The clinical parameters associated with sexual dysfunction
In bivariate analysis, advanced age and diabetes were both strongly associated with dysfunction in the total score and each domain (P < 0.005). Except for overall satisfaction, pre-dialytic serum creatinine levels were associated with other domains and the total score (P < 0.005). The history of cardiovascular disease was found to be associated with dysfunction in the domains of orgasmic function, overall satisfaction and the total score (P = 0.046, 0.025 and 0.023, respectively). Lower serum albumin was associated only with the lower score in the domain of intercourse satisfaction (P = 0.036). The association of adequacy of dialysis and sexual function was also analysed. However, by bivariate analysis, urea clearance (Kt/V) was not found to be associated with dysfunction in any domain. Higher scores on the BDI were significantly associated with lower scores in each domain and the total score (P < 0.001).

By multivariable linear regression analysis, age, diabetes and higher BDI scores were found to be independent factors of dysfunction in each sexual function domain (Table 3). In the domain of erectile function, the score decreased by 0.328 for one year increase in age, decreased 0.348 if BDI score increased by 1 and decreased 4.705 if the patient had diabetes. By comparing the ß-coefficient values, we could conclude that the age still played a more important role than depressive symptoms and DM in the erectile dysfunction. Although unadjusted analyses suggested that history of cardiovascular disease, lower serum albumin and pre-dialytic serum creatinine levels were significantly associated with sexual dysfunction, none were associated with sexual dysfunction after adjustment for age, BDI scores and diabetes history.


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  		Table 3. Multple linear regression model of individual sexual function domains

 
Association of sexual dysfunction and decreased quality of life
Multiple linear regression analysis was used to examine the association between various measures of QOL, sexual dysfunction, BDI scores and other clinical variables (Table 4). After adjustment, we found that patients with lower sexual desire, intercourse satisfaction, orgasmic function or total scores had significantly lower scores in the domain of SF (P < 0.001, <0.001, <0.001 and =0.003, respectively). A score increase of 1 in the domain of social functioning predicted the score increase of 0.022, 0.034 and 0.033 in the domain of sexual desire, intercourse satisfaction and orgasmic function, respectively. Better erectile function scores predicted higher scores in the domain of RP (P = 0.026).


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  		Table 4. Association between male sexual function and quality of life

 


   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
Acknowledgements
 References
 
Consistent with previous studies of male haemodialysis patients [1], our study revealed diabetes and increasing age as being associated with erectile dysfunction. We further demonstrated that elderly patients had lower scores in the domains of sexual desire, intercourse satisfaction and orgasmic function, but not in overall satisfaction. This implies that elderly patients considered sexual dysfunction as a part of ‘aging degeneration’ but not ‘disease’. They did not have high expectations towards sexual activity, so they were satisfied with their present condition. On the other hand, in spite of lower scores in the domains of erectile function, intercourse satisfaction and orgasmic function, diabetes did not cause lower sexual desire. Such results correspond with previous research, where diabetes impairs neurogenic and endothelium-mediated relaxation of penile smooth muscle [8]. The demand of sexual activity is not impaired with diabetes.

The most unique finding in our study was the higher self-reported depressive symptoms among the dialysis population with sexual dysfunction. This association is particularly interesting. Several questions arise from our observations.

First, do higher depressive symptoms cause decreased libido? Depression is characterized by loss of interest, reduction in energy, lowered-esteem and inability to experience pleasure. All such symptoms produce difficulties in maintaining adequate sexual relationships. Social withdrawal further impairs the ability to form and maintain intimate relationships. So loss of sexual desire is very common in depressed patients. Such association has been also disclosed in many studies [9].

Second, can higher depressive symptoms directly cause organic disorders, such as erectile or orgasmic dysfunction? Empirically, depressive symptoms limit sexual foreplay and intimacy, so they can certainly interfere with the ability to be sexually aroused and successfully achieve erections and orgasms. In the general population, the results of studies on relationships between erectile dysfunction and depression are conflicting [10,11]. In a study of haemodialysis patients, erectile dysfunction was not found to be associated with depression [12]. Such conflicting findings may be attributed to the different methods of defining psychological depression. On the other hand, because most antidepressant drugs have adverse effects on erectile function, it is difficult to interpret the effect of depression treatment on erectile dysfunction in the intervention studies. Whether depressive symptoms can cause such organic disorders is speculative now; further study is needed.

Third, does sexual dysfunction cause depressive symptoms? Sexual dysfunction can erode one's sense of self-esteem and lead to emotional and marital tension, so it has great impact on the mood. In a 12-week, randomized, double-blind, placebo-controlled study of population with mild to moderate depressive symptoms [13], therapy of erectile dysfunction with sildenafil was disclosed to lead to marked improvement in depressive symptoms and QOL. This is strong evidence towards proving that sexual dysfunction attributes to depressive symptoms.

Fourth, a common factor may simultaneously cause the development of depressive symptoms and sexual dysfunction. It is well known that the major physiological factors of erectile dysfunction are vasculogenic and neurogenic disorders. Psychological depression has been shown to be a significant, independent risk factor for the development of symptomatic ischaemic heart disease in other healthy individuals [14,15]. A number of plausible biobehavioural mechanisms linking depression and ischaemic heart disease have been identified, including treatment adherence, lifestyle factors, traditional risk factors, alterations in the autonomic nervous system and hypothalamic pituitary adrenal axis functioning, platelet activation and inflammation [14,16,17]. On the other hand, peripheral neuropathy may cause physical disability, pain and limitation in daily activity. It deeply impairs patients’ QOL and leads to psychological depression. In diabetics, the association between peripheral neuropathy, sexual dysfunction and psychological depression had been proved [18]. Cardiovascular disorders and peripheral neuropathy may be both common factors of depression and sexual dysfunction.

Fifth, previous studies had provided evidence towards the association of sexual dysfunction and QOL [12,19], although the role of psychological depression has never been clarified. After adjusting the BDI scores, we demonstrated the independent association of sexual dysfunction and QOL in male haemodialysis patients. To improve QOL, the management of sexual dysfunction should be based on both psychological and physiological interventions.

There are three major limitations in our study. First, our study shows only an association between depressive symptoms and sexual dysfunction, but cannot interpret which is primary. The second is the selection bias which, inherent in any survey-based study, introduced by patients’ self-selection in responding to our survey [20]. It is impossible to know how much difference existed between the responders and non-responders. The third is that our study used self-reported questionnaires to identify depressive symptoms only. The exact screening threshold of these questionnaires may be controversial. In today's clinical practice, it is necessary to conduct structured psychiatric interviews with patients exhibiting depressive symptoms on screening to characterize the severity of their depression.

Sexual dysfunction is a multifactor condition and strongly associated with QOL. The presence of higher depressive symptoms, highly prevalent in haemodialysis patients, has been proved to be independently associated with sexual dysfunction in this study. In the comprehensive management of sexual dysfunction of male haemodialysis patients, thorough evaluation of psychological depression must be included.



   Acknowledgements
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
References
 
The authors would like to thank the Ta-Tung Kidney Foundation and the Mrs Hsiu-Chin Lee Kidney Research Fund for grant support of this study.

Conflicts of interest statement. None declared.



   Notes
 
*The authors wish it to be known that, in their opinion the authors Chee-Jen Chang and Tun-Jun Tsai contributed equally to this work. Back



   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 

  1. Rosas SE, Joffe M, Franklin E, et al. (2001) Prevalence and determinants of erectile dysfunction in hemodialysis patients. Kidney Int 59:2259–2266.[Web of Science][Medline]
  2. Shabsigh R, Klein LT, Seidman S, et al. (1998) Increased incidence of depressive symptoms in men with erectile dysfunction. Urology 52:848–852.[CrossRef][Web of Science][Medline]
  3. Kimmel PL. (2000) Psychosocial factors in adult end-stage renal disease patients treated with hemodialysis: correlates and outcomes. Am J Kidney Dis 35:[Suppl 1], S132–S140.[Web of Science][Medline]
  4. Rosen RC, Rilewy A, Wagner G, et al. (1997) The international index of erectile function (IIEF): a multidimensional scale for assessment of erectile dysfunction. Urology 49:822–830.[CrossRef][Web of Science][Medline]
  5. Kimmel PL, Peterson RA, Weihs KL, et al. (2000) Multiple measurements of depression predict mortality in a longitudinal study of chronic hemodialysis outpatients. Kidney Int 57:2093–2098.[CrossRef][Web of Science][Medline]
  6. Lowrie EG, Curtin RB, LePain N, et al. (2003) Medical outcomes study short form-36: a consistent and powerful predictor of morbidity and mortality in dialysis patients. Am J Kidney Dis 41:1286–1292.[CrossRef][Web of Science][Medline]
  7. Chen YC, Hung KY, Kao TW, et al. (2000) Relationship between dialysis adequacy and quality of life in long-term peritoneal dialysis patients. Periton Dialysis Int 20:534–540.
  8. Ledda A. (2000) Diabetes, hypertension and erectile dysfunction. Curr Med Res Opin 16:[Suppl 1], S17–20.
  9. Baldwin DS. (2001) Depression and sexual dysfunction. Brit Med Bull 57:81–99.[Abstract/Free Full Text]
  10. Mallis D, Moysidis K, Nakopoulou K, et al. (2005) Psychiatric morbidity is frequently undetected in patients with erectile dysfunction. J Urol 174:1913–1916.[CrossRef][Web of Science][Medline]
  11. Kantor J, Bilker WB, Glasser DB, et al. (2002) Prevalence of erectile dysfunction and active depression: an analytic cross-sectional study of general medical patients. Am J Epidemiol 156:1035–1042.[Abstract/Free Full Text]
  12. Rosas SE, Joffe M, Franklin E, et al. (2003) Association of decreased quality of life and erectile dysfunction in hemodialysis patients. Kidney Int 64:232–238.[CrossRef][Web of Science][Medline]
  13. Seidman SN, Roose SP, Menza MA, et al. (2001) Treatment of erectile dysfunction in men with depressive symptoms: results of a placebo-controlled trial with sildenafil citrate. Am J Psychiatry 158:1623–1630.[Abstract/Free Full Text]
  14. Lett HS, Blumenthal JA, Babyak MA, et al. (2004) Depression as a risk factor for coronary artery disease: evidence, mechanisms, and treatment. Psychosom Med 66:305–315.[Abstract/Free Full Text]
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  16. Shimbo D, Chaplin W, Crossman D, et al. (2005) Role of depression and inflammation in incident coronary heart disease events. Am J Cardiol 96:1016–1021.[CrossRef][Web of Science][Medline]
  17. Kalender B, Ozdemir AC, Koroglu G. (2006) Association of depression with markers of nutrition and inflammation in chronic kidney disease and end-stage renal disease. Nephron Clin Pract 102:c115–121.[CrossRef][Web of Science][Medline]
  18. Koo JR, Yoon JW, Kim SG, et al. (2003) Association of depression with malnutrition in chronic hemodialysis patients. Am J Kid Dis 41:1037–1042.[CrossRef][Web of Science][Medline]
  19. Turk S, Guney I, Altintepe L, et al. (2004) Quality of life in male hemodialysis patients. Role of erectile dysfunction. Nephron Clin Pract 96:c21–27.[CrossRef][Web of Science][Medline]
  20. Wolchik HA, Braver SL, Jensen K. (1985) Volunteer bias in erotica research. Effect of intrussiveness of measure and sexual background. Arch Sex Behav 14:93–107.[CrossRef][Web of Science][Medline]
Received for publication: 9. 8.06
Accepted in revised form: 16.10.06


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