Association among hypogonadism, quality of life and erectile ...

International Journal of Impotence Research (2007) 19, 69–75 & 2007 Nature Publishing Group All rights reserved 0955-9930/07 $30.00 www.nature.com/ijir

ORIGINAL ARTICLE

Association among hypogonadism, quality of life and erectile dysfunction in middle-aged and aged male in Taiwan TIS Hwang1,2,3, H-C Lo4, T-F Tsai1 and H-Y Chiou4 1 Division of Urology, Department of Surgery, Shin Kong Wu Ho-Su Memorial Hospital, Taipei, Taiwan; 2Department of Urology, Taipei Medical University, Taipei, Taiwan; 3Department of Urology, School of Medicine, Fu Jen Catholic University, Hsin Chuang, Taipei, Taiwan and 4School of Public Health, Taipei Medical University, Taipei, Taiwan

The association between hypogonadism, quality of life (QoL), and erectile dysfunction (ED) among the middle-aged and aged male in Taiwan is evaluated. A total of 680 study subjects aged X40 years old were recruited from Northern (n ¼ 276), Middle (n ¼ 238), and Southern (n ¼ 202) Taiwan, respectively. ED was diagnosed by score of International Index of Erectile Function (IIEF-5). Taiwan version questionnaire for QoL includes domain 1 (physical domain), domain 2 (psychological domain), domain 3 (social relationship domain), and domain 4 (environmental domain) was used to measure QoL. Blood hormones, including FSH, LH, Prolactin, SHBG, total testosterone (TT), calculated free testosterone (cFT), and bioavailable testosterone (Bio-T), were determined. Logistic regression analysis was used to estimate crude and multivariate-adjusted odds ratio of risk factors and its 95% confidence interval. A significantly inverse association between concentration of serum cFT and Bio-T, and severity of ED was observed. Scores of QoL of Domain 1–4 were significantly decreased with the increament of severity of ED. Significant correlations were found between IIEF scores and four domains of QoL, respectively. After adjustment for age, cFT and Bio-T, study subjects with ED (IIEFp21) would have significantly high risk of low level of QoL in four domains. In conclusion, a significant association between low levels of serum calculated cFT, Bio-T, and severity of ED was found. In addition, abnormal erectile function significantly associated with low level of QoL in four domains. International Journal of Impotence Research (2007) 19, 69–75. doi:10.1038/sj.ijir.3901480; published online 11 May 2006 Keywords: hypogonadism; men’s health; quality of life; erectile dysfunction; aged male

Introduction According to the recommendations of the First International Consultation on erectile dysfunction (ED) co-sponsored by World Health Organization (WHO), ED is defined as ‘the consistent or recurrent inability to attain and/or to maintain a penile erection sufficient for sexual performance’.1 Although ED is a benign disorder, it is related to physical and psychological health and has a significant impact on the quality-of-life (QoL) of both the sufferers and their families.2 Erectile dysfunction is commonly associated with aging. Therefore, age-related factors are the most

Correspondence: Dr H-Y Chiou, School of Public Health, Taipei Medical University, No. 250, Wu-Hsing Street, Taipei 110, Taiwan. E-mail: [email protected] Received 23 January 2006; revised 7 March 2006; accepted 10 March 2006; published online 11 May 2006

commonly cited causes of ED, including hormonal derangement, diabetes, vascular insufficiency, neural damage from surgery, side effects of drug and radiation therapy, and psychogenic factors.3,4 Androgens are essential in the maintenance of libido and have an important role in regulating penile smooth muscle function in man.5 It is reported that hypogonadism in the aged group with the highest prevalence of ED (middle-age and beyond) is higher than initially suspected.6 The data of Massachusetts Male Aging Study (MMAS) show that total testosterone declined at the rate of 0.8% per year,7 whereas both free and albumin-bound testosterone declined at about 1.4–2% per year of aging.7,8 Of the sex hormone levels, the changes in free testosterone correlate most closely with aging and have the closest correlation with sexual activity.9 However, the association between sex hormone levels and ED in epidemiology in Taiwan is still to be examined through an epidemiological study of large samples. Quality of life, a multidimensional construct, is primarily based on a person’s subjective appraisal of

Association among hypogonadism, QoL and ED TIS Hwang et al 70

physical, psychological function, social interaction and somatic sensation.10 Quality of life measures provide valuable information in evaluating the progression of disease and the efficacy of medical interventions, as well as in helping to construct a comprehensive health profile of older people after illness.11 Thus, it is reasonable to assess the effect of ED on older people by means of QoL measures. So far the association between QoL and ED, especially in Asian population, is seldom studied. To shed new lights on this rarely explored field, the aim of this study is to investigate the association among testosterone levels, QoL and ED to explore the impact of these factors on ED in Taiwanese men.

Materials and methods Study subjects In August 2004, a community survey of ED was carried out through five medical centers in northern, middle and southern Taiwan. Thousand residents in community household registry files of catchment areas of these medical centers were collected as study population and were also informed to participate in this study. A total of 748 participants aged more than 40 years of age were recruited. These participants were collected from five medical centers: Shin Kong Wu Ho-Su Memorial Hospital (n ¼ 276) of northern Taiwan, China Medical University Hospital (n ¼ 179) and Taichung Veterans General Hospital (n ¼ 59) of central Taiwan, and Kaohsiung Veterans General Hospital (n ¼ 75) and Kaohsiung Medical University Hospital (n ¼ 159) of southern Taiwan. Response rate of this study was 74.8%. Among these participants, 68 were excluded owing to the affection with hyperprolactinemia or hormone medication (supplementation or deprivation) or failure to answer the question on ED. Studies of the remaining 680 participants were used in this analysis.

Data collection The information is collected through a standardized self-completed questionnaire. The data include demographic characteristics (age, marital status and education), lifestyle factors (cigarette smoking, alcohol drinking) and disease record. Questionnaires of International Index of Erectile Function (IIEF-5)12 and Saint Louis Hypogonadism13 are used to measure the level of erectile function and hypogonadism. Saint Louis Hypogonadism questionnaire includes 10 questions, which is designed to screen hypogonadism prevalence in aging men. Participants whose answers are positive to the first and the eighth questions are recognized as hypogonadism. Likewise, those answers are negative to the first and the eighth questions but give three positive International Journal of Impotence Research

answers out of the remaining eight questions are also recognized as hypogonadism. Of commonly used QoL instruments, the brief version of the World Health Organization’s Quality of life (WHOQOLBREF) is developed on a theoretical model and is suitable for different local cultures.14 As detailed in the Appendix, the Taiwanese-adapted WHOQOLBREF15 comprises 26 items translated from the original WHOQOL-BREF with two additional items of local importance, which is used to assess the changes in QoL in this study. In addition, QoL questionnaire of Taiwan version including domain 1 (physical domain), domain 2 (psychological domain), domain 3 (social relationship domain) and domain 4 (environmental domain) is used to measure QoL. Namely, the last two questions in the Taiwanese-adapted WHOQOL-BREF concern overall QoL. The remaining 26 items, according to the WHOQOL group, can be appropriately grouped into four major domains. The first group including Q3, Q4, Q10, Q15, Q16, Q17 and Q18 is physical domain; the second group including Q5, Q6, Q7, Q11, Q19 and Q26 is psychological domain; the third group including Q20, Q21, Q22 and Q27 is social relationships domains and the last group including Q8, Q9, Q12, Q13, Q14, Q23, Q24, Q25 and Q28 is environmental domain. Score of each question ranges from 1 to 5, with a higher score indicating a better QoL. Scores of each domain are standardized to a scale ranging from 4 to 20. Definition of erectile function The total score of IIEF-5 items is 25. In regard to the ED assessment, score more than 21 is recognized as healthy without ED, score between 17 and 21 as mild ED, 12 and 16 as moderate-mild ED, 8 and 11 as moderate ED and less than 7 is categorized as severe ED. Hormone measurement One sample including 8 ml of non-fasting blood samples was drawn by venipuncture from the antecubital vein through each study subjects who agreed to participate in the study by signing an IRB agreement form. All samples were collected at 9–12 in the morning and are then centrifuged and stored at 201C until analysis. Serum hormones, including follicle stimulating hormone, luteinizing hormone, Prolactin, total testosterone (TT), sex hormone binding globulin (SHBG), calculated free testosterone (cFT), bioavailable testosterone (Bio-T), are determined. Calculated free testosterone was calculated by SHBG and Bio-T was calculated by albumin and testosterone using method of international society for the study of the aging male web. The serum levels of TT more than 11 nmol/l, cFT more than 0.23 nmol/l and Bio-T more than 5 nmol/l are recognized as normal.16

Association among hypogonadism, QoL and ED TIS Hwang et al

Statistical analysis The completed questionnaire data were keyed in Microsoft Excel database. All analyses were performed with the SAS package (version 8.1, SAS Institute, Cary, NC, USA), and data were considered statistically significant at Po0.05. The statistical significance was assessed by the w2 test for categorical variables and by analysis of variance (ANOVA) for continuous variables. Duncan’s test was used to test the difference between two levels of specific hormone by severity of ED, as well as comparison of QoL. Logistic regression analysis was used to estimate crude and multivariate-adjusted odds ratio of risk factors and its 95% confidence interval.

Results Table 1 shows the risks of characteristics of study population. The study population recruited represents an unselected group of men who come from communities in Taiwan. They are more than 40 years of age. In this study, the ED prevalence of them is 77.94% and the ED prevalence for participants older than 65 is 89.96%. The study subjects aged more than 65 years old have the risk for development of ED (IIEFp21), 3.5 times higher than those of the younger ones as the referent group. Study

subjects with lower education level (p6 years) have significantly increased risk for development of ED, 2.7 times higher than those of higher education level (X13 years). In addition, those who had insomnia of at least once per month have significant higher risk of ED. However, marital status, current smoking and alcohol consumption do not show significant associations with risk of ED. As shown in Table 2, a significantly inverse association among concentration of serum cFT, Bio-T and severity of ED is observed. Scores of QoL of domain 1, domain 2, domain 3 and domain 4 are significantly decreased with increse in severity of ED. The association between ED and biochemical markers of hypogonadism is shown in Table 3. Those with abnormal serum cFT and Bio-T has significantly increased risk for development of ED; the biological gradient is shown among the group with most severity of ED. After adjustment for age, education and insomnia, significantly multivariateadjusted risks of ED are observed among study subjects with abnormal level of serum cFT and BioT, showing odds ratio of 1.5, 2.1 and 3.0, respectively, for IIEFp21, 11 and 7 for cFT and that of 1.7, 2.6 and 3.9 for Bio-T. Four scatter plots between IIEF and four domains of QoL are shown in Figure 1 (panels a–d). There are significant correlations between IIEF scores and scores of four domains of QoL. It would imply that

71

Table 1 Risk of characteristics of study subjects (IIEFp21 vs IIEF421) P

ORa (95% CI)

324 (71.84) 206 (89.96)

o0.0001

1.0 3.5 (2.2–5.7)***

130 (23.38) 18 (17.14)

426 (76.62) 87 (82.86)

0.1619

1.0 1.5 (0.9–2.5)

Education (years) X13 7–12 p6

78 (27.37) 57 (20.00) 11 (11.96)

207 (72.63) 228 (80.00) 81 (88.04)

0.0446 0.0037

1.0 1.5 (1.0–2.2)* 2.7 (1.4–5.4)**

Smoking (current) No Yes

119 (22.16) 29 (21.17)

418 (77.84) 108 (78.83)

0.8023

1.0 1.1 (0.7–1.7)

Alcohol consumption (current) No Yes

108 (21.26) 34 (22.82)

400 (78.74) 115 (77.18)

0.6844

1.0 0.9 (0.6–1.4)

Insomnia Normal At least once a week

130 (24.95) 12 (10.62)

391 (75.05) 101 (89.38)

0.0014

1.0 2.8 (1.5–5.3)**

IIEF421 N (%)

IIEFp21 N (%)

Age (years) o65 X65

127 (28.16) 23 (10.04)

Marital status Couples Others

Abbreviations: CI, Confidence interval; IIEF, International Index of Erectile Function; OR, Odds ratio. a Crude odds ratio. *Po0.05; **Po0.01; ***Po0.001.

International Journal of Impotence Research


Table 2 Hormone level and QoL score of study subjects categorized by erectile function status IIEF421 (n ¼ 150) 17pIIEFp21 (n ¼ 235) 12pIIEFp16 (n ¼ 130) 8pIIEFp11 (n ¼ 54) IIEFp7 (n ¼ 111) Mean7s.d. Mean7s.d. Mean7s.d. Mean7s.d. Mean7s.d. Age TT (nmol/l) CFT (nmol/l) Bio-T (nmol/l) Domain 1 Domain 2 Domain 3 (tw) Domain 4 (tw)

56.6178.06 16.3775.44 0.2970.09a 6.8472.17a 15.9771.92a 15.1072.05a 14.9872.10a 15.0571.92a

57.5378.52 15.9275.13 0.2870.09a 6.6572.11a 14.5771.80b 13.6972.01b 13.6271.93b 13.9571.91b

61.4378.60 15.9375.29 0.2770.09a 6.5472.03a 13.9071.93c 13.3071.99b,c 13.0971.81b,c 13.7671.81b,c

64.0278.62 15.2574.51 0.2470.07b 5.8471.74b 13.7772.11c 12.9572.37c,d 12.6171.75c 13.2572.09c,d

68.0178.47 15.7876.04 0.2370.07b 5.4771.66b 13.1572.34d 12.4272.65d 11.8272.30d 12.9672.31d

P

0.7408 o0.0001 o0.0001 o0.0001 o0.0001 o0.0001 o0.0001

Abbreviations: Bio-T, boiavailable testosterone; cFT, calculated free testosterone; IIEF, International Index of Erectile Function; QoL, quality-of-life; TT, total testosterone. a,b,c,d Based on Duncan test, a significant difference between two levels of a specific hormone by erectile function will be observed of the two hormone levels with different characters, as well as comparison of QoL. Table 3 Odds ratio for study groups in different IIEF scores Cutoff

TT (nmol/l) cFT (nmol/l) Bio-T (nmol/l)

o11 o0.23 o5

0pIIEFp21

0pIIEFp11

0pIIEFp7

OR (95% CI)

ORa (95% CI)

OR (95% CI)

ORa (95% CI)

OR (95% CI)

ORa (95% CI)

1.1 (0.7–1.7) 2.0 (1.3–3.1)** 2.4 (1.4–3.9)***

1.2 (0.7–1.9) 1.5 (1.0–2.4) þ 1.7 (1.0–2.9)*

1.1 (0.6–2.0) 3.3 (2.0–5.4)*** 3.9 (2.2–6.7)***

1.3 (0.6–2.7) 2.1 (1.1–3.8)* 2.6 (1.3–4.9)*

1.3 (0.7–2.3) 3.4 (2.0–5.7)*** 4.3 (2.4–7.7)***

2.4 (1.0–5.5)* 3.0 (1.5–6.2)** 3.9 (1.8–8.5)***

Abbreviations: Bio-T, boiavailable testosterone; cFT, calculated free testosterone; CI, confidence interval; IIEF, International Index of Erectile Function; OR, odds ratio; TT, total testosterone. IIEF421 as a referent group. a Adjusted for age, education and insomnia. *Po0.05; **Po0.01; ***Po0.001.

Figure 1 Scatter plots between international index of erectile function (IIEF) and four domains of quality of life. (a) Domain 1: physical; (b) Domain 2: psychological; (c) Domain 3: social relationship; (d) Domain 4: environmental.

study subjects with ED would have low level of QoL in four domains. As shown in Table 4, study subjects whose scores of QoL are less than median value (domain 1:15, domain 2:14, domain 3(tw):14, domain 4(tw):13.8) of the scores are diagnosed as low level of QoL in International Journal of Impotence Research

each domain. Compared with normal erectile function (IIEF421) as referent group, significantly high risks of low-level QoL in four domains are found among study subjects with ED (IIEF%21), showing odds ratios of 6.0, 3.8, 3.7 and 3.4, respectively, for domains 1–4.


Table 4 Multivariate-adjusted ORs and 95% CIs of low level of four domains of QoL by IIEFp21

IIEFp21

Domain 1a OR (95% CI)

Domain 2a OR (95% CI)

Domain 3 (tw)a OR (95% CI)

Domain 4 (tw)a OR (95% CI)

6.0 (4.0–9.2)***

3.8 (2.5–5.8)***

3.7 (2.4–5.6)***

3.4 (2.2–5.0)***

Abbreviations: CI, Confidence interval; IIEF, International Index of Erectile Function; OR, odds ratio; QoL, quality-of-life. Adjustment for age, cFT, Bio-T. a Low level of QoL: domain 1o15, domain 2o14, domain 3 (tw)o14 and domain 4 (tw)o13.8. *Po0.05; **Po0.01; ***Po0.001.

Discussion The MMAS shows the ED prevalence among 1290 healthy men aged 40–70 years was 52%.17 In France, 31.6% of men aged 40 years and above have problems of essentially mild or moderate severity of ED.18 In addition, the prevalence of ED is 37.5% in Thailand.19 Another study in Taiwan they found that the prevalence of ED on 5939 urological patients aged from 20 to 93 years is 71%.20 Our study is the first community-based study in Taiwan. Owing to different age ranges and races, and IIEF-recognized ED, this study observes that Taiwan has a higher prevalence of ED than that of the MMAS study. In MMAS, psychological factors are strongly associated with ED, which included depression, low levels of dominance and anger either expressed outward or directed inward.17 Quality-of-life, itself a multidimensional construct, is primarily based on a person’s subjective appraisal of physical, psychological function, social interaction and somatic sensation.10 We observe that all of the average values of physical, psychological, social relationship and environment domains decrease with increasing severity of ED status. Furthermore, study subjects with ED would have significantly increased risks for the development of low level of QoL in these four domains. A similar result was also reported by a study carried out in Spain.21 In that study, a significantly negative association between physical summary component of health-related quality of life (HRQoL) and ED was observed. In addition, a multicenter clinical study has also found a significant correlation between improvement of erectile function and psychological manifestations in ED patients treated with a 10-week, open-label and flexible-dose of sildenafil (50 mg, adjustable to 25 or 100 mg).22 The association between smoking and ED is controversial. It indicates that smokers do not have significant risk of ED.23,24 However, in another study, ex- and current smokers are at greater risk of ED.25 There is no association between alcohol abuse and ED,26 but a slight association between alcohol consumption and risk of ED was observed in MMAS subjects.17 In this study, we acknowledge that the impact of smoking and alcohol on ED is not strong. In addition, we notice that study subjects with

higher education level have lower risk of ED, and those with insomnia at least once a week have higher risk of ED. Testosterone is the major circulating androgen in the male. The decrease of its serum level may be manifested clinically in various ways, including psychological symptoms of fatigue, depression and alterations in mood and cognition and in sexual symptoms of decreased libido and ED.27 It circulates as unbound or free testosterone (FT) in a small proportion. Both FT and testosterone nonspecifically bound to albumin, called as Bio-T, which reflects the physiological activity of testosterone.27 Currently, the most reliable and widely accepted indicators of hypogonadism are low serum Bio-T or cFT.28 The serum level of total testosterone in healthy men and patients with ED do not show any difference.29 In our study, we also observed nonsignificant association between severity of ED and total testosterone, except severe ED (IIEF%7). This finding might be explained by aging men with highlevel SHBG, as SHBG increases 0.86 nmol/l per year. A multiple logistic regression model of the study finds out that total testosterone does not show a statistically significant association with ED, after adjustment for age and SHBG. The IIEF-5 score for erectile function increases significantly with increase in Bio-T.27 Our study shows that the serum levels of cFT and Bio-T both decrease with severity of ED status, but total testosterone does not. This finding suggests that study subjects with hypogonadism would have greater ED risk. Furthermore, this study secures the significant association between hypogonadism and ED risk. In conclusion, low levels of serum cFT, and Bio-T are significantly associated with severity of ED. Furthermore, significant associations between abnormal erectile function and low levels of QoL in four domains are also observed.

Acknowledgments This study is in part financially supported by the Taiwanese Association of Andrology. With a collective collaboration, Drs HS Chiang, CR Yang, HC Wu, TL Wu, and SP Huang contributed to collect part of study subjects. International Journal of Impotence Research


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15 The WHOQOL-Taiwan Group. Introduction to the development of the WHOQOL-Taiwan version. Chin J Public Health (Taipei) 2000; 19: 315–324. 16 Morales A, Buvat J, Gooren LJ, Guay AT, Kaufma JM, Tan HM et al Endocrine aspects of sexual dysfunction in men. J Sexual Med 2004; 1: 69–81. 17 Feldman HA, Goldstein I, Hatzichristou DG, Krane RJ, McKinlay JB. Impotence and its medical and psychosocial correlates: results of the Massachusetts Male Aging Study. J Urol 1994; 151: 54–61. 18 Francois G, Marie CM, Anne T, Caroline R, Michel M, Patrick T. Prevalence of erectile dysfunction in France: results of an epidemiological survey of a representative sample of 1004 men. Eur Urol 2002; 42: 382–389. 19 Kongkanand A, Thai erectile dysfunction epidemiological study group. Prevalence of erectile dysfunction in Thailand. Int J Androl 2000; 23: 77–80. 20 Chen K, Wu C, Chiang H. Prevalence of erectile dysfunction in Taiwanese males: a statistical analysis of 5939 urological patients. New Taipei J Med 2001; 3: 239–244. 21 Sanchez-cruz JJ, Cabrera-Leon A, Martin-Morales A, Fernandez A, Burgos R, Rejas J. Male erectile dysfunction and healthrelated quality of life. Eur Urol 2003; 44: 245–253. 22 Althof SE, Cappelleri JC, Shpilsky A, Stecher V, Diuguid C, Sweeney M et al Treatment responsiveness of the self-esteem and relationship questionnaire in erectile dysfunction. Urology 2003; 61: 888–892. 23 Mak R, Backer G, Kornitzer M, Meyer J. Prevalence and correlates of erectile dysfunction in a population-based study in Belgium. Eur Urol 2002; 41: 132–138. 24 Moreira EJ, Lobo C, Diament A, Nicolosi A, Glasser DB. Incidence of erectile dysfunction in men 40 to 69 years old: results from a population-based cohort study in Brazil. Uology 2003; 61: 431–436. 25 Mirone V, Imbimbo C, Bortolotti A, Cintio ED, Colli E, Landoni M. Cigarette smoking as risk factor for erectile dysfunction: results from an Italian epidemiological study. Eur Urol 2002; 41: 294–297. 26 Okulate G, Olayinka O, Dogunro AS. Erectile dysfunction: prevalence and relationship to depression, alcohol abuse and panic disorder. Gen Hosp Psychiatry 2003; 25: 209–213. 27 Tsujimura A, Matsumiya K, Matsuoka Y, Takahashi T, Koga M, Iwasa A. Bioavailable testosterone with age and erectile dysfunction. J Urol 2003; 170: 2345–2347. 28 Morales A, Lunenfeld B. Investigation, treatment and monitoring of late-onset hypoganadism in males. Official recommendations of the International Society for the Study of the Aging Male. Aging Male 2002; 5: 74–86. 29 Derouet H, Lehmann J, Stamm B, Luhl C, Romer D, Georg T. Age dependent secretion of LH and ACTH in healthy men and patients with erectile dysfunction. Eur Urol 2002; 41: 144–154.

Appendix A WHOQOL-BREF: Taiwanese-adapted version Q1 Q2 Q3 Q4 Q5 Q6 Q7 Q8 Q9 Q10

How would you rate your quality of life? How satisfied are you with your health? To what extent do you feel that physical pain prevents you from doing what you need to do? How much medical treatment do you need to function in your daily life? How much do you enjoy life? To what extent do you feel your life to be meaningful? How well are you able to concentrate? How safe do you feel in your daily life? How healthy is your physical environment? Do you have enough energy for everyday life?


Association among hypogonadism, QoL and ED TIS Hwang et al

Q11 Q12 Q13 Q14 Q15 Q16 Q17 Q18 Q19 Q20 Q21 Q22 Q23 Q24 Q25 Q26 Q27 Q28

Are you able to accept your bodily appearance? Do you have enough money to meet your needs? How available to you is the information that you need in your day-to-day life? To what extent do you have the opportunity for leisure activities? How well are you able to get around? How satisfied are you with your sleep? How satisfied are you with your ability to perform your daily living activities? How satisfied are you with your capacity for work? How satisfied are you with yourself? How satisfied are you with your personal relationships? How satisfied are you with your sex life? How satisfied are you with the support you get from your friends? How satisfied are you with the conditions of your living place? How satisfied are you with your access to health services? How satisfied are you with your transport? How often do you have negative feelings such as a blue mood, despair, anxiety, or depression? Do you feel respected by others? (additional questionnaire for Taiwan version) Are you usually able to get the things you like to eat? (additional questionnaire for Taiwan version)

75
