ANDROLOGY
ISSN: 2047-2919
ORIGINAL ARTICLE
Correspondence: Cheng-liang Xiong, Family Planning Institute, Tongji Medical College, Hangkong Road 13, Wuhan 430030, China. E-mail: [email protected]
Keywords: AMS, ageing male, androgen deficiency, reliability, validation
The ageing males’ symptoms scale for Chinese men: reliability, validation and applicability of the Chinese version 1
Received: 19-Feb-2013 Revised: 31-Aug-2013 Accepted: 16-Sep-2013
X-b. Kong, 1H-t. Guan, 1H-g. Li, 2Y. Zhou and 1C-l. Xiong
1 Family Planning Institute, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China, and 2Statistic Department, Zunyi Medical College, Zunyi, China
doi: 10.1111/j.2047-2927.2013.00145.x
SUMMARY In this study, the ageing males’ symptoms (AMS) scale was translated into Chinese following methodological recommendations for linguistic and cultural adaptation. This study aimed to confirm the reliability, validation and applicability of the simplified Chinese version of the scale (CN-AMS) in older Chinese men, a free health screening for men older than 40 years was conducted. All participants completed a health questionnaire, which consisted of personal health information, AMS scale, the generic quality of life (QoL) instrument SF36 and the Beck Depression Inventory (BDI). The fasting blood samples of participants were collected on the day of completing the health questionnaire. Serum total testosterone (TT), albumin and sex hormone-binding globulin levels were measured and the level of free testosterone was calculated (calculated free testosterone, CFT). A total of 244 men (mean age: 52 7.3 years, range: 40–79 years) were involved in the investigation and provided informed consent before their participation. The reliability of CN-AMS was analysed as internal consistency reliability (Cronbach’s alpha was 0.91) as well as a 4-week-interval test–retest stability (Pearson’s correlation was 0.83) and found to be good. The validation of CN-AMS was analysed as the internal structure analysis (Pearson’s correlation between total score and each item score r = 0.48–0.75), total-domain-correlation (among the three domains r = 0.47–0.68, p < 0.01; domains with the total score r = 0.81–0.88, p < 0.01), and cross-validation with other scales (with SF36 r = 0.59, p < 0.01; with BDI r = 0.50, p < 0.01). Androgen deficiency (AD) was defined as the presence of three sexual symptoms (decreased frequency of morning erections, sexual thoughts and erectile dysfunction) in combination with TT < 11 nmol/L and CFT < 220 pmol/L, and the sensitivity and specificity for CN-AMS was 68.8 and 6.8% respectively. The CN-AMS had sufficient sensitivity in screening AD of older men, but the low specificity made it unsuitable to be adopted as the diagnostic criteria. The scanning capability of AMS scale for AD has the downward trend with ageing and a hypothesis is proposed to give a possible reason for the new finding.
INTRODUCTION The number and proportion of older people in China are growing rapidly. This is not only mainly attributable to the One-Child Policy, but also to an overall increase in life expectancy. As the proportion of ageing males keeps rising, people have been paying more attention to improving the quality of life of ageing males in recent years. late-onset hypogonadism (LOH), also referred to as age-associated testosterone deficiency syndrome, TDS is a clinical and biochemical syndrome associated with advancing age and characterized by a range of symptoms attributed to a deficiency in serum testosterone levels, as they fall below the young healthy adult male reference range (Wang et al., 2009). This condition may result in significant detriment to quality of life and adversely 856
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affects the function of multiple organ systems. These changes include a diminished sexual function and libido, reduced muscle mass and strength, lack of energy and endurance, increased visceral adiposity, and mild-to-moderate depression along with some impairment in cognitive function (reviewed in Schreiber & Ziemer, 2008). To measure health-related quality of life (HRQoL) and symptoms of ageing men, the ageing males’ symptoms (AMS) scale was developed (Heinemann et al., 1999). This questionnaire contains 17 items ranging from the general feeling of well-being to the specific decrease in libido. The AMS scale has become the most widely used scale to measure HRQoL and symptoms in ageing males and is used in many countries across the world (www.aging-males-symptoms-scale.info/languages.htm). In this © 2014 American Society of Andrology and European Academy of Andrology
ANDROLOGY
THE AMS SCALE’S APPLICABILITY FOR CHINESE MEN
study, the AMS scale was translated into simplified Chinese and an attempt was made to validate its use in ageing males.
MATERIALS AND METHODS Gathering of personal health information Basic information All participants filled the table of basic information including age, educational level, marital status and employment status. Medical history Late-onset hypogonadism is the only one possible explanation of age-related complaints, other causes such as liver disease, kidney disease and depression must be ruled out (Bhasin & Basaria, 2011). Therefore, the relative medical history of each participant was recorded in his health questionnaire by the andrologist. Physical examination result During health screening, the results of physical examination were recorded in the attached table of the health questionnaire including height, body mass, chest circumference, abdomen circumference, blood pressure and electrocardiogram. Laboratory test result The serum test results were attached to the health questionnaire, which included: sexual hormone (TT, SHBG, albumin,
oestradiol (E2), luteinizing hormone (LH), calculated free testosterone (CFT)), insulin, serum glucose, liver function and renal function. Translation of CN-AMS scale The English version of the scale was downloaded from a website (http://www.aging-males-symptoms-scale.info/documents/ AMS_English.pdf) and translated into Chinese (Table 1) following the recommended translation process (Sperber et al., 1994). Hormone assays The fasting blood samples of the participants were collected between 08.00 h and 09.00 h on the day of screening. This time frame was chosen to minimize the natural diurnal variation in hormone levels (Ho & Beckett, 2011). The TT, albumin and SHBG levels were measured and the level of CFT was calculated according to the Vermeulen formula (Vermeulen et al., 1999). Serum albumin was measured using a Roche Cobas c 311 analyser with an interassay coefficient of variation (CV) of 1.5% and an intra-assay CV of 1.2%. TT levels (detectable range, 0.1– 16 ng/mL; interassay CV of 7.1%; intra-assay CV of 3.9%, total CV < 8.1%), and SHBG levels (detectable range, 0.2–200 nmol/L; total CV < 7%) were measured by a Beckman Access Immunoassay system. Considering the reference value of TT in our laboratory (range: 10.41–19.78 nmol/L), TT < 11 nmol/L and CFT < 220 pmol/L was adopted as the lower threshold (Wu et al., 2010). Participants involved in the investigation provided informed consent before their participation. All of them could
Table 1 AMS Questionnaire Which of the following symptoms apply to you at this time? Please, mark the appropriate box for each symptom. For symptoms that do not apply, please mark “none”. Symptoms
Score = Decline in your feeling of general well-being (general state of health, subjective feeling) Joint pain and muscular ache (lower back pain, joint pain, pain in a limb, general back ache) Excessive sweating (unexpected/sudden episodes of sweating, hot flushes independent of strain) Sleep problems (difficulty in falling asleep, difficulty in sleeping through, waking up early and feeling tired, poor sleep, sleeplessness) 5. Increased need for sleep, often feeling tired 6. Irritability (feeling aggressive, easily upset about little things, moody) 7. Nervousness (inner tension, restlessness, feeling fidgety) 8. Anxiety (feeling panicky) 9. Physical exhaustion / lacking vitality (general decrease in performance, reduced activity, lacking interest in leisure activities, feeling of getting less done, of achieving less, of having to force oneself to undertake activities) 10. Decrease in muscular strength (feeling of weakness) 11. Depressive mood (feeling down, sad, on the verge of tears, lack of drive, mood swings, feeling nothing is of any use) 12. Feeling that you have passed your peak 13. Feeling burnt out, having hit rock-bottom 14. Decrease in beard growth 15. Decrease in ability/frequency to perform sexually 16. Decrease in the number of morning erections 17. Decrease in sexual desire/libido (lacking pleasure in sex, lacking desire for sexual intercourse) Have you got any other major symptoms? If Yes, please describe: THANK YOU VERY MUCH FOR YOUR COOPERATION 1. 2. 3. 4.
© 2014 American Society of Andrology and European Academy of Andrology
None
Mild
Moderate
Severe
Extremely severe
1 □ □ □ □
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Yes
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No
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X-b. Kong et al. Table 2 Characteristics of the participants (n = 244) N (%)
Parameter Age (years) BMI (kg/m2) Underweight (BMI < 18.5) Normal weight (18.5 ≤ BMI < 25) Overweight (25 ≤ BMI < 30) Obesity (BMI ≥ 30) Smoking Alcohol drinking Co-morbidities Diabetes mellitus Hypertension Cardiovascular disease Endocrinology TT (nmol/L) CFT (pmol/L) SHBG (nmol/L) Albumin (g/L) FSH (IU/L) LH (IU/L) LOH suspects LOH patients
Mean SD
Range
52 7.3 24.5 2.9
40–79 17.9–38.3
16.2 4.6 299.0 88.9 42.1 20.5 50.7 3.9 8.9 5.7 4.6 2.3
7.5–32.1 152–678 11.1–118.7 41.8–65.9 2.1–45.0 1.4–15.4
3 (1.2) 145 (59.4) 86 (35.2) 10 (4.1) 118 (48.4) 57 (23.4) 10 (4.1) 60 (24.6) 8 (3.3)
16 (6.6) 4 (1.6)
BMI, body mass index; TT, total testosterone; CFT, calculated free testosterone; SHBG, sex hormone-binding globulin; FSH, follicle-stimulating hormone; LH, luteinizing hormone; LOH, late-onset hypogonadism.
communicate verbally and had no psychotic or cognitive disorders. This study was approved by the ethical committee of Tongji Medical College. Data analysis In this study, the statistical analyses were performed using PASW Statistics 18.0 (SPSS Inc., Chicago, IL, USA). The data were expressed as mean SD.
RESULTS Overall, 244 male participants (mean age: 52 7.3 years, range: 40–79 years) were involved in the final analysis. The other participants were excluded because of unsuitable age, medication or other such reasons that influence the hormone analysis, and the results are not shown in this article. The baseline characteristics and endocrine parameter of the participants are summarized in Table 2. In the first hormone analysis, 16 participants were suspected to be androgen deficient (AD) patients with testosterone levels under the lower threshold. All of the 16 participants accepted the hormone analysis again and AD was found in four men finally. In the reliability analysis, 27 younger men (mean age: 25.1 4.3 years, range: 22–36 years) were involved in the control group. The internal consistency was measured with Cronbach’s alpha coefficient (a) for the total score as well as the Table 3 Results of internal consistency and test–retest study Group
N Total score Psychological score Somatic score Sexual score
Young male group
Ageing male group
Consistency (a)
Test–retest (r)
Consistency (a)
Test–retest (r)
27 0.86 0.62 0.75 0.78
27 0.91 0.75 0.90 0.94
244 0.91 0.88 0.83 0.85
46 0.83 0.74 0.82 0.79
a, Cronbach’s alpha coefficient; r, Pearson’s correlation coefficient.
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three subscales (Table 3). The a value of the ageing male group for total score and subscales (psychological/somatic/sexual) were 0.91, 0.88, 0.83 and 0.85 respectively. The test–retest correlation coefficients (Pearson’s correlation coefficient, r) of the total score and three subscales are also summarized in Table 3. For the ageing male group, the Pearson’s correlation coefficients for the total score and three subscales (psychological/somatic/sexual) were 0.83, 0.74, 0.82 and 0.79 respectively. Interestingly, for the psychological subscale, the Cronbach’s alpha coefficient for the young male group is obviously lower than the result of ageing men group. However, for the sexual subscale, the retest reliability of young male group is better than that of ageing men group. In the validation analysis, an inter-item correlation matrix was made (Table 4). The Pearson correlation coefficient (r) for the agreement between the total score and each item score was analysed. In this study, items’ r value with the total score ranged from 0.48 to 0.75. Items 3 and 14 showed poor correlation with the total score and other items. Item 14 belonged to the sexual subscale but had insufficient correlation with the other items of the subscale (r = 0.27–0.37). Another structural validity aspect is the total-domain correlation (Table 5). The lower correlation among the three subscales (r = 0.53–0.68) as compared with the correlation of subscales with the total score (r = 0.81–0.88) was noticed. In the cross-validation analysis, the AMS scale, generic QoL instrument SF36 and Beck Depression Inventory (BDI) were applied at the same time in the 244 participants (Table 6). The AMS total score and the SF36 (include the physical subscale and mental subscale) were significantly inversely correlated (r = 0.59; p < 0.01). The correlation between the AMS scale and BDI was also significant (r = 0.50; p < 0.01). In this study, the lower threshold of the serum testosterone level was defined as TT < 11 nmol/L and CFT < 220 pmol/L. The sensitivity and specificity of CN-AMS for screening the low serum testosterone level were 68.8 and 6.8% respectively (Table 7).
DISCUSSION In this study, the AMS scale was translated into simplified Chinese and an attempt was made to validate its use in the ageing males. The reliability analysis results were in agreement with other studies that were reported (Schreiber & Ziemer, 2008). In the validity analysis, item 14 (Decrease of beard growth) showed poor correlation with the AMS scale and sexual subscale. It suggested that item 14 could be deleted from the scale. In the study, item 3 (excessive sweating) also showed very low correlation with the scale, as far as we know, which had not been reported by other studies. However, the result was based on small numbers and needs to be confirmed. To validate the AMS scale‘s applicability for screening AD in ageing males, the distribution characteristic of AMS score was analysed (Tables 8 and 9). To find the distribution pattern more intuitively, a bar chart was made based on the data of Tables 8 and 9 (Fig. 1). As seen in Fig. 1, little severity appeared in the thirties and the maximum probability in the fifties. The moderate severity appeared in the forties and reached maximum probability in the fifties. The trends of both these were downward between the © 2014 American Society of Andrology and European Academy of Andrology
ANDROLOGY
THE AMS SCALE’S APPLICABILITY FOR CHINESE MEN Table 4 Inter-item correlation matrix (n = 244) Item no.
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 Total
1.00 0.581 0.239 0.424 0.585 0.438 0.310 0.273 0.382 0.400 0.341 0.374 0.305 0.059 0.313 0.272 0.317 0.587
0.581 1.00 0.205 0.381 0.500 0.328 0.287 0.272 0.352 0.364 0.155 0.249 0.214 0.115 0.347 0.303 0.341 0.543
0.239 0.205 1.00 0.328 0.299 0.357 0.425 0.354 0.258 0.324 0.286 0.283 0.296 0.250 0.201 0.170 0.218 0.482
0.424 0.381 0.328 1.00 0.486 0.364 0.385 0.449 0.546 0.463 0.398 0.381 0.345 0.157 0.350 0.183 0.298 0.629
0.585 0.500 0.299 0.486 1.00 0.579 0.517 0.485 0.516 0.460 0.394 0.400 0.349 0.233 0.365 0.278 0.347 0.693
0.438 0.328 0.357 0.364 0.579 1.00 0.591 0.630 0.536 0.517 0.518 0.265 0.381 0.266 0.266 0.223 0.272 0.660
0.310 0.287 0.425 0.385 0.517 0.591 1.00 0.756 0.534 0.410 0.602 0.349 0.535 0.410 0.296 0.157 0.305 0.686
0.273 0.272 0.354 0.449 0.485 0.630 0.756 1.00 0.594 0.411 0.707 0.372 0.522 0.371 0.269 0.144 0.283 0.688
0.382 0.352 0.258 0.546 0.516 0.536 0.534 0.594 1.00 0.659 0.568 0.542 0.545 0.340 0.391 0.324 0.374 0.752
0.400 0.364 0.324 0.463 0.460 0.517 0.410 0.411 0.659 1.00 0.394 0.476 0.502 0.390 0.373 0.309 0.344 0.694
0.341 0.155 0.286 0.398 0.394 0.518 0.602 0.707 0.568 0.394 1.00 0.552 0.718 0.330 0.301 0.238 0.362 0.692
0.374 0.249 0.283 0.381 0.400 0.265 0.349 0.372 0.542 0.476 0.552 1.00 0.652 0.345 0.480 0.360 0.494 0.686
0.305 0.214 0.296 0.345 0.349 0.381 0.535 0.522 0.545 0.502 0.718 0.652 1.00 0.418 0.368 0.269 0.439 0.697
0.059 0.115 0.250 0.157 0.233 0.266 0.410 0.371 0.340 0.390 0.330 0.345 0.418 1.00 0.366 0.266 0.369 0.507
0.313 0.347 0.201 0.350 0.365 0.266 0.296 0.269 0.391 0.373 0.301 0.480 0.368 0.366 1.00 0.764 0.895 0.711
0.272 0.303 0.170 0.183 0.278 0.223 0.157 0.144 0.324 0.309 0.238 0.360 0.269 0.266 0.764 1.00 0.805 0.597
0.317 0.341 0.218 0.298 0.347 0.272 0.305 0.283 0.374 0.344 0.362 0.494 0.439 0.369 0.895 0.805 1.00 0.722
Pearson correlation coefficient (r) for the agreement between the total score and each item.
Table 5 Sub-scores and total score correlation (n = 244)
Total Psychological Somatic Sexual
Table 9 Distribution characteristic of the AMS score (ageing group)
Total
Psychological
Somatic
Sexual
Age range
1 0.831* 0.882* 0.807*
0.831* 1 0.679* 0.472*
0.882* 0.679* 1 0.529*
0.807* 0.472* 0.529* 1
N 244 Severity, n (%) Negative 71 (29.1) Little 104 (42.6) Moderate 58 (23.8) Severity 11 (4.5)
*Correlation is significant at the 0.01 level (two-tailed).
Total
40–
50–
60–
70–
110
72
30
32
16 (22.2) 32 (44.4) 20 (27.8) 4 (5.5)
8 (26.7) 12 (40.0) 5 (16.7) 5 (16.7)
11 (34.4) 13 (40.6) 7 (21.9) 1 (3.1)
36 (32.7) 47 (42.7) 26 (23.6) 1 (0.9)
Table 6 Cross-validation analysis Total score SF36 BDI
Psychological
0.584* 0.470*
Somatic
0.509* 0.545*
Sexual
0.596* 0.403*
Figure 1 Distribution of the ageing males’ symptoms (AMS) score.
0.368* 0.263*
*Correlation is significant at the 0.01 level (two-tailed).
Table 7 Sensitivity and specificity of CN-AMS (n = 244)
N AMS negatives AMS positives Sensitivity (%)
Normal
LOH suspects
Sum
228 66 162 68.8
16 5 11 Specificity (%)
244 71 173 6.8
LOH, late-onset hypogonadism.
Table 8 Distribution characteristic of the AMS score (young group) Age range
Total
20–
30–
N Severity, n (%) Negative Little Moderate Severity
40
23
17
36 (90) 4 (10) 0 (0) 0 (0)
23 (100) 0 (0) 0 (0) 0 (0)
13 (76.5) 4 (23.5) 0 (0) 0 (0)
This analysis included the above-mentioned 27 young men and 13 participants were excluded from the ageing group because of being younger than 40 years.
fifties and the sixties and upward between the sixties and the seventies. A severe severity condition appeared in the forties with a very low probability and became maximum in the sixties. It is a well-known fact that the gonadal function of men will decrease with ageing and the probability of AD and LOH should © 2014 American Society of Andrology and European Academy of Andrology
have the upward trend (Araujo et al., 2007). However, the upward trend of the negative probability since the fifties and the downward trend of the severe probability since the sixties were obviously contrary to the fact (Fig. 2). To make this contrary phenomenon easier to understand, a hypothesis is proposed wherein the serum testosterone level falls below the defined threshold value (For example, TT < 11 nmol/ L and CFT < 220 pmol/L), the AMS scale score has enough correlation with the fluctuation of serum testosterone (free Andrology, 2014, 2, 856–861
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X-b. Kong et al. Figure 2 Probability of androgen deficiency (AD) and late-onset hypogonadism (LOH) (T < 10.4 nmol/L) (Araujo et al., 2007).
Another proof is the distribution characteristic of the free testosterone level with ageing in Japanese men (Namiki et al., 2008). The fluctuation amplitude of the free testosterone level kept decreasing with ageing (Fig. 3). The hypothesis based on known facts gives a possible reason for the contrary phenomenon between the probability of AD and that of AMS with ageing. To confirm the hypothesis, further investigation is required. In summary, the CN-AMS was developed and was self-administered by older participants. It has sufficient sensitivity in screening AD of older men, but the low specificity has made it unsuitable to be adopted as the diagnostic criteria. The scanning capability of the AMS scale for AD has the downward trend with ageing and a hypothesis is proposed to give a possible reason for the new finding.
ACKNOWLEDGEMENTS
Figure 3 Distribution of free testosterone with ageing (Namiki et al., 2008).
This study was supported by the Ministry of Science and Technology of the People’s Republic of China (2012BAI32B03). We are thankful to the participants of the study. Jiawei Zhang, Daoan Wang and Hongyan Li are thanked for the assistance in the recruitment of study participants, and Hui Zhou and Shuang Chen for laboratory assistance in hormone assays. The reviewers and editors are thanked for suggestions and critical comments to the manuscript.
AUTHOR CONTRIBUTIONS Study design: X-b.K., H-g.L.; Clinical data acquisition, patient recruitment: H-t.G.; Association study execution: C-l.X., H-g.L., H-t.G.; Statistical data analysis: Y.Z., X-b.K.; Critical discussion on data interpretation: C-l.X., X-b.K.; Manuscript drafting: X-b.K.; Comments to early versions of the manuscript: C-l.X., H-g.L.; Critical revision for important intellectual content: X-b.K. All authors have approved the final version of the manuscript.
DISCLOSURE Table 10 Correlation between AMS score, age and testosterone level (n = 244) Age Total Psychological Somatic Sexual
0.077 0.016 0.056 0.113
T
CFT 0.023 0.050 0.010 0.005
0.022 0.055 0.018 0.116
*Correlation is significant at the 0.01 level (two-tailed).
testosterone especially) level. When the fluctuation amplitude of testosterone level keeps descending with ageing, the scanning capability of the AMS scale for AD has the downward trend. There are proofs of this hypothesis. One proof is that the scale score improved significantly after the administration of androgen replacement therapy in LOH patients (Moore et al., 2004; Taniguchi et al., 2011), although there was no significant correlation between AMS score and age or testosterone levels which have been confirmed in other studies (T’Sjoen et al., 2004; Basar et al., 2005). In the study, the correlation between AMS score and testosterone level or age was analysed and no significant correlation was found (Table 10). 860
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None of the authors have financial and/or personal relationships with people or organizations that could inappropriately influence (bias) their work. The corresponding author had full access to all the data in the study and has the final responsibility for the decision to submit the manuscript for publication.
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THE AMS SCALE’S APPLICABILITY FOR CHINESE MEN Namiki M, Akaza H, Shimazui T, Ito N, Iwamoto T, Baba K, Kumano H, Koh E, Tsujimura A, Matsumiya K, Horie S, Maruyama O, Marumo K, Yanase T, Kumamoto Y; Working Committee on Clinical Practice Guidelines for Late-onset Hypogonadism; Japanese Urological Association/Japanese Society for Study of Aging Male. (2008) Clinical practice manual for late-onset hypogonadism syndrome. Int J Urol 15, 377–388. Schreiber G & Ziemer M. (2008) The aging male – diagnosis and therapy of late-onset hypogonadism. J Dtsch Dermatol Ges 6, 273–280. Sperber AD, Devellis RF & Boehlecke B. (1994) Cross-cultural translation: methodology and validation. J Cross Cult Psychol 25, 501–524. Taniguchi H, Kawa G, Kinoshita H & Matsuda T. (2011) Change of aging males’ symptoms (AMS) rating scale in Japanese late-onset hypogonadism (LOH) patients administered androgen replacement therapy. J Men‘s Health 8, 67–70. T’Sjoen G, Goemaere S, De Meyere M & Kaufman JM. (2004) Perception of males’ aging symptoms, health and well-being in elderly
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ANDROLOGY community-dwelling men is not related to circulating androgen levels. Psychoneuroendocrinology 29, 201–214. Vermeulen A, Verdonck L & Kaufman JM. (1999) A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab 84, 3666–3672. Wang C, Nieschlag E, Swerdloff R, Behre HM, Hellstrom WJ, Gooren LJ, Kaufman JM, Legros JJ, Lunenfeld B, Morales A, Morley JE, Schulman C, Thompson IM, Weidner W, Wu FC. (2009) Investigation, treatment, and monitoring of late-onset hypogonadism in males: ISA, ISSAM, EAU, EAA, and ASA recommendations. Eur Urol 55, 121–130. Wu FC, Tajar A, Beynon JM, Pye SR, Silman AJ, Finn JD, O’Neill TW, Bartfai G, Casanueva FF, Forti G, Giwercman A, Han TS, Kula K, Lean ME, Pendleton N, Punab M, Boonen S, Vanderschueren D, Labrie F, Huhtaniemi IT; EMAS Group. (2010) Identification of late-onset hypogonadism in middle-aged and elderly men. N Engl J Med 363, 123–135.
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ORIGINAL ARTICLE
Correspondence: Cheng-liang Xiong, Family Planning Institute, Tongji Medical College, Hangkong Road 13, Wuhan 430030, China. E-mail: [email protected]
Keywords: AMS, ageing male, androgen deficiency, reliability, validation
The ageing males’ symptoms scale for Chinese men: reliability, validation and applicability of the Chinese version 1
Received: 19-Feb-2013 Revised: 31-Aug-2013 Accepted: 16-Sep-2013
X-b. Kong, 1H-t. Guan, 1H-g. Li, 2Y. Zhou and 1C-l. Xiong
1 Family Planning Institute, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China, and 2Statistic Department, Zunyi Medical College, Zunyi, China
doi: 10.1111/j.2047-2927.2013.00145.x
SUMMARY In this study, the ageing males’ symptoms (AMS) scale was translated into Chinese following methodological recommendations for linguistic and cultural adaptation. This study aimed to confirm the reliability, validation and applicability of the simplified Chinese version of the scale (CN-AMS) in older Chinese men, a free health screening for men older than 40 years was conducted. All participants completed a health questionnaire, which consisted of personal health information, AMS scale, the generic quality of life (QoL) instrument SF36 and the Beck Depression Inventory (BDI). The fasting blood samples of participants were collected on the day of completing the health questionnaire. Serum total testosterone (TT), albumin and sex hormone-binding globulin levels were measured and the level of free testosterone was calculated (calculated free testosterone, CFT). A total of 244 men (mean age: 52 7.3 years, range: 40–79 years) were involved in the investigation and provided informed consent before their participation. The reliability of CN-AMS was analysed as internal consistency reliability (Cronbach’s alpha was 0.91) as well as a 4-week-interval test–retest stability (Pearson’s correlation was 0.83) and found to be good. The validation of CN-AMS was analysed as the internal structure analysis (Pearson’s correlation between total score and each item score r = 0.48–0.75), total-domain-correlation (among the three domains r = 0.47–0.68, p < 0.01; domains with the total score r = 0.81–0.88, p < 0.01), and cross-validation with other scales (with SF36 r = 0.59, p < 0.01; with BDI r = 0.50, p < 0.01). Androgen deficiency (AD) was defined as the presence of three sexual symptoms (decreased frequency of morning erections, sexual thoughts and erectile dysfunction) in combination with TT < 11 nmol/L and CFT < 220 pmol/L, and the sensitivity and specificity for CN-AMS was 68.8 and 6.8% respectively. The CN-AMS had sufficient sensitivity in screening AD of older men, but the low specificity made it unsuitable to be adopted as the diagnostic criteria. The scanning capability of AMS scale for AD has the downward trend with ageing and a hypothesis is proposed to give a possible reason for the new finding.
INTRODUCTION The number and proportion of older people in China are growing rapidly. This is not only mainly attributable to the One-Child Policy, but also to an overall increase in life expectancy. As the proportion of ageing males keeps rising, people have been paying more attention to improving the quality of life of ageing males in recent years. late-onset hypogonadism (LOH), also referred to as age-associated testosterone deficiency syndrome, TDS is a clinical and biochemical syndrome associated with advancing age and characterized by a range of symptoms attributed to a deficiency in serum testosterone levels, as they fall below the young healthy adult male reference range (Wang et al., 2009). This condition may result in significant detriment to quality of life and adversely 856
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affects the function of multiple organ systems. These changes include a diminished sexual function and libido, reduced muscle mass and strength, lack of energy and endurance, increased visceral adiposity, and mild-to-moderate depression along with some impairment in cognitive function (reviewed in Schreiber & Ziemer, 2008). To measure health-related quality of life (HRQoL) and symptoms of ageing men, the ageing males’ symptoms (AMS) scale was developed (Heinemann et al., 1999). This questionnaire contains 17 items ranging from the general feeling of well-being to the specific decrease in libido. The AMS scale has become the most widely used scale to measure HRQoL and symptoms in ageing males and is used in many countries across the world (www.aging-males-symptoms-scale.info/languages.htm). In this © 2014 American Society of Andrology and European Academy of Andrology
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THE AMS SCALE’S APPLICABILITY FOR CHINESE MEN
study, the AMS scale was translated into simplified Chinese and an attempt was made to validate its use in ageing males.
MATERIALS AND METHODS Gathering of personal health information Basic information All participants filled the table of basic information including age, educational level, marital status and employment status. Medical history Late-onset hypogonadism is the only one possible explanation of age-related complaints, other causes such as liver disease, kidney disease and depression must be ruled out (Bhasin & Basaria, 2011). Therefore, the relative medical history of each participant was recorded in his health questionnaire by the andrologist. Physical examination result During health screening, the results of physical examination were recorded in the attached table of the health questionnaire including height, body mass, chest circumference, abdomen circumference, blood pressure and electrocardiogram. Laboratory test result The serum test results were attached to the health questionnaire, which included: sexual hormone (TT, SHBG, albumin,
oestradiol (E2), luteinizing hormone (LH), calculated free testosterone (CFT)), insulin, serum glucose, liver function and renal function. Translation of CN-AMS scale The English version of the scale was downloaded from a website (http://www.aging-males-symptoms-scale.info/documents/ AMS_English.pdf) and translated into Chinese (Table 1) following the recommended translation process (Sperber et al., 1994). Hormone assays The fasting blood samples of the participants were collected between 08.00 h and 09.00 h on the day of screening. This time frame was chosen to minimize the natural diurnal variation in hormone levels (Ho & Beckett, 2011). The TT, albumin and SHBG levels were measured and the level of CFT was calculated according to the Vermeulen formula (Vermeulen et al., 1999). Serum albumin was measured using a Roche Cobas c 311 analyser with an interassay coefficient of variation (CV) of 1.5% and an intra-assay CV of 1.2%. TT levels (detectable range, 0.1– 16 ng/mL; interassay CV of 7.1%; intra-assay CV of 3.9%, total CV < 8.1%), and SHBG levels (detectable range, 0.2–200 nmol/L; total CV < 7%) were measured by a Beckman Access Immunoassay system. Considering the reference value of TT in our laboratory (range: 10.41–19.78 nmol/L), TT < 11 nmol/L and CFT < 220 pmol/L was adopted as the lower threshold (Wu et al., 2010). Participants involved in the investigation provided informed consent before their participation. All of them could
Table 1 AMS Questionnaire Which of the following symptoms apply to you at this time? Please, mark the appropriate box for each symptom. For symptoms that do not apply, please mark “none”. Symptoms
Score = Decline in your feeling of general well-being (general state of health, subjective feeling) Joint pain and muscular ache (lower back pain, joint pain, pain in a limb, general back ache) Excessive sweating (unexpected/sudden episodes of sweating, hot flushes independent of strain) Sleep problems (difficulty in falling asleep, difficulty in sleeping through, waking up early and feeling tired, poor sleep, sleeplessness) 5. Increased need for sleep, often feeling tired 6. Irritability (feeling aggressive, easily upset about little things, moody) 7. Nervousness (inner tension, restlessness, feeling fidgety) 8. Anxiety (feeling panicky) 9. Physical exhaustion / lacking vitality (general decrease in performance, reduced activity, lacking interest in leisure activities, feeling of getting less done, of achieving less, of having to force oneself to undertake activities) 10. Decrease in muscular strength (feeling of weakness) 11. Depressive mood (feeling down, sad, on the verge of tears, lack of drive, mood swings, feeling nothing is of any use) 12. Feeling that you have passed your peak 13. Feeling burnt out, having hit rock-bottom 14. Decrease in beard growth 15. Decrease in ability/frequency to perform sexually 16. Decrease in the number of morning erections 17. Decrease in sexual desire/libido (lacking pleasure in sex, lacking desire for sexual intercourse) Have you got any other major symptoms? If Yes, please describe: THANK YOU VERY MUCH FOR YOUR COOPERATION 1. 2. 3. 4.
© 2014 American Society of Andrology and European Academy of Andrology
None
Mild
Moderate
Severe
Extremely severe
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X-b. Kong et al. Table 2 Characteristics of the participants (n = 244) N (%)
Parameter Age (years) BMI (kg/m2) Underweight (BMI < 18.5) Normal weight (18.5 ≤ BMI < 25) Overweight (25 ≤ BMI < 30) Obesity (BMI ≥ 30) Smoking Alcohol drinking Co-morbidities Diabetes mellitus Hypertension Cardiovascular disease Endocrinology TT (nmol/L) CFT (pmol/L) SHBG (nmol/L) Albumin (g/L) FSH (IU/L) LH (IU/L) LOH suspects LOH patients
Mean SD
Range
52 7.3 24.5 2.9
40–79 17.9–38.3
16.2 4.6 299.0 88.9 42.1 20.5 50.7 3.9 8.9 5.7 4.6 2.3
7.5–32.1 152–678 11.1–118.7 41.8–65.9 2.1–45.0 1.4–15.4
3 (1.2) 145 (59.4) 86 (35.2) 10 (4.1) 118 (48.4) 57 (23.4) 10 (4.1) 60 (24.6) 8 (3.3)
16 (6.6) 4 (1.6)
BMI, body mass index; TT, total testosterone; CFT, calculated free testosterone; SHBG, sex hormone-binding globulin; FSH, follicle-stimulating hormone; LH, luteinizing hormone; LOH, late-onset hypogonadism.
communicate verbally and had no psychotic or cognitive disorders. This study was approved by the ethical committee of Tongji Medical College. Data analysis In this study, the statistical analyses were performed using PASW Statistics 18.0 (SPSS Inc., Chicago, IL, USA). The data were expressed as mean SD.
RESULTS Overall, 244 male participants (mean age: 52 7.3 years, range: 40–79 years) were involved in the final analysis. The other participants were excluded because of unsuitable age, medication or other such reasons that influence the hormone analysis, and the results are not shown in this article. The baseline characteristics and endocrine parameter of the participants are summarized in Table 2. In the first hormone analysis, 16 participants were suspected to be androgen deficient (AD) patients with testosterone levels under the lower threshold. All of the 16 participants accepted the hormone analysis again and AD was found in four men finally. In the reliability analysis, 27 younger men (mean age: 25.1 4.3 years, range: 22–36 years) were involved in the control group. The internal consistency was measured with Cronbach’s alpha coefficient (a) for the total score as well as the Table 3 Results of internal consistency and test–retest study Group
N Total score Psychological score Somatic score Sexual score
Young male group
Ageing male group
Consistency (a)
Test–retest (r)
Consistency (a)
Test–retest (r)
27 0.86 0.62 0.75 0.78
27 0.91 0.75 0.90 0.94
244 0.91 0.88 0.83 0.85
46 0.83 0.74 0.82 0.79
a, Cronbach’s alpha coefficient; r, Pearson’s correlation coefficient.
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three subscales (Table 3). The a value of the ageing male group for total score and subscales (psychological/somatic/sexual) were 0.91, 0.88, 0.83 and 0.85 respectively. The test–retest correlation coefficients (Pearson’s correlation coefficient, r) of the total score and three subscales are also summarized in Table 3. For the ageing male group, the Pearson’s correlation coefficients for the total score and three subscales (psychological/somatic/sexual) were 0.83, 0.74, 0.82 and 0.79 respectively. Interestingly, for the psychological subscale, the Cronbach’s alpha coefficient for the young male group is obviously lower than the result of ageing men group. However, for the sexual subscale, the retest reliability of young male group is better than that of ageing men group. In the validation analysis, an inter-item correlation matrix was made (Table 4). The Pearson correlation coefficient (r) for the agreement between the total score and each item score was analysed. In this study, items’ r value with the total score ranged from 0.48 to 0.75. Items 3 and 14 showed poor correlation with the total score and other items. Item 14 belonged to the sexual subscale but had insufficient correlation with the other items of the subscale (r = 0.27–0.37). Another structural validity aspect is the total-domain correlation (Table 5). The lower correlation among the three subscales (r = 0.53–0.68) as compared with the correlation of subscales with the total score (r = 0.81–0.88) was noticed. In the cross-validation analysis, the AMS scale, generic QoL instrument SF36 and Beck Depression Inventory (BDI) were applied at the same time in the 244 participants (Table 6). The AMS total score and the SF36 (include the physical subscale and mental subscale) were significantly inversely correlated (r = 0.59; p < 0.01). The correlation between the AMS scale and BDI was also significant (r = 0.50; p < 0.01). In this study, the lower threshold of the serum testosterone level was defined as TT < 11 nmol/L and CFT < 220 pmol/L. The sensitivity and specificity of CN-AMS for screening the low serum testosterone level were 68.8 and 6.8% respectively (Table 7).
DISCUSSION In this study, the AMS scale was translated into simplified Chinese and an attempt was made to validate its use in the ageing males. The reliability analysis results were in agreement with other studies that were reported (Schreiber & Ziemer, 2008). In the validity analysis, item 14 (Decrease of beard growth) showed poor correlation with the AMS scale and sexual subscale. It suggested that item 14 could be deleted from the scale. In the study, item 3 (excessive sweating) also showed very low correlation with the scale, as far as we know, which had not been reported by other studies. However, the result was based on small numbers and needs to be confirmed. To validate the AMS scale‘s applicability for screening AD in ageing males, the distribution characteristic of AMS score was analysed (Tables 8 and 9). To find the distribution pattern more intuitively, a bar chart was made based on the data of Tables 8 and 9 (Fig. 1). As seen in Fig. 1, little severity appeared in the thirties and the maximum probability in the fifties. The moderate severity appeared in the forties and reached maximum probability in the fifties. The trends of both these were downward between the © 2014 American Society of Andrology and European Academy of Andrology
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THE AMS SCALE’S APPLICABILITY FOR CHINESE MEN Table 4 Inter-item correlation matrix (n = 244) Item no.
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 Total
1.00 0.581 0.239 0.424 0.585 0.438 0.310 0.273 0.382 0.400 0.341 0.374 0.305 0.059 0.313 0.272 0.317 0.587
0.581 1.00 0.205 0.381 0.500 0.328 0.287 0.272 0.352 0.364 0.155 0.249 0.214 0.115 0.347 0.303 0.341 0.543
0.239 0.205 1.00 0.328 0.299 0.357 0.425 0.354 0.258 0.324 0.286 0.283 0.296 0.250 0.201 0.170 0.218 0.482
0.424 0.381 0.328 1.00 0.486 0.364 0.385 0.449 0.546 0.463 0.398 0.381 0.345 0.157 0.350 0.183 0.298 0.629
0.585 0.500 0.299 0.486 1.00 0.579 0.517 0.485 0.516 0.460 0.394 0.400 0.349 0.233 0.365 0.278 0.347 0.693
0.438 0.328 0.357 0.364 0.579 1.00 0.591 0.630 0.536 0.517 0.518 0.265 0.381 0.266 0.266 0.223 0.272 0.660
0.310 0.287 0.425 0.385 0.517 0.591 1.00 0.756 0.534 0.410 0.602 0.349 0.535 0.410 0.296 0.157 0.305 0.686
0.273 0.272 0.354 0.449 0.485 0.630 0.756 1.00 0.594 0.411 0.707 0.372 0.522 0.371 0.269 0.144 0.283 0.688
0.382 0.352 0.258 0.546 0.516 0.536 0.534 0.594 1.00 0.659 0.568 0.542 0.545 0.340 0.391 0.324 0.374 0.752
0.400 0.364 0.324 0.463 0.460 0.517 0.410 0.411 0.659 1.00 0.394 0.476 0.502 0.390 0.373 0.309 0.344 0.694
0.341 0.155 0.286 0.398 0.394 0.518 0.602 0.707 0.568 0.394 1.00 0.552 0.718 0.330 0.301 0.238 0.362 0.692
0.374 0.249 0.283 0.381 0.400 0.265 0.349 0.372 0.542 0.476 0.552 1.00 0.652 0.345 0.480 0.360 0.494 0.686
0.305 0.214 0.296 0.345 0.349 0.381 0.535 0.522 0.545 0.502 0.718 0.652 1.00 0.418 0.368 0.269 0.439 0.697
0.059 0.115 0.250 0.157 0.233 0.266 0.410 0.371 0.340 0.390 0.330 0.345 0.418 1.00 0.366 0.266 0.369 0.507
0.313 0.347 0.201 0.350 0.365 0.266 0.296 0.269 0.391 0.373 0.301 0.480 0.368 0.366 1.00 0.764 0.895 0.711
0.272 0.303 0.170 0.183 0.278 0.223 0.157 0.144 0.324 0.309 0.238 0.360 0.269 0.266 0.764 1.00 0.805 0.597
0.317 0.341 0.218 0.298 0.347 0.272 0.305 0.283 0.374 0.344 0.362 0.494 0.439 0.369 0.895 0.805 1.00 0.722
Pearson correlation coefficient (r) for the agreement between the total score and each item.
Table 5 Sub-scores and total score correlation (n = 244)
Total Psychological Somatic Sexual
Table 9 Distribution characteristic of the AMS score (ageing group)
Total
Psychological
Somatic
Sexual
Age range
1 0.831* 0.882* 0.807*
0.831* 1 0.679* 0.472*
0.882* 0.679* 1 0.529*
0.807* 0.472* 0.529* 1
N 244 Severity, n (%) Negative 71 (29.1) Little 104 (42.6) Moderate 58 (23.8) Severity 11 (4.5)
*Correlation is significant at the 0.01 level (two-tailed).
Total
40–
50–
60–
70–
110
72
30
32
16 (22.2) 32 (44.4) 20 (27.8) 4 (5.5)
8 (26.7) 12 (40.0) 5 (16.7) 5 (16.7)
11 (34.4) 13 (40.6) 7 (21.9) 1 (3.1)
36 (32.7) 47 (42.7) 26 (23.6) 1 (0.9)
Table 6 Cross-validation analysis Total score SF36 BDI
Psychological
0.584* 0.470*
Somatic
0.509* 0.545*
Sexual
0.596* 0.403*
Figure 1 Distribution of the ageing males’ symptoms (AMS) score.
0.368* 0.263*
*Correlation is significant at the 0.01 level (two-tailed).
Table 7 Sensitivity and specificity of CN-AMS (n = 244)
N AMS negatives AMS positives Sensitivity (%)
Normal
LOH suspects
Sum
228 66 162 68.8
16 5 11 Specificity (%)
244 71 173 6.8
LOH, late-onset hypogonadism.
Table 8 Distribution characteristic of the AMS score (young group) Age range
Total
20–
30–
N Severity, n (%) Negative Little Moderate Severity
40
23
17
36 (90) 4 (10) 0 (0) 0 (0)
23 (100) 0 (0) 0 (0) 0 (0)
13 (76.5) 4 (23.5) 0 (0) 0 (0)
This analysis included the above-mentioned 27 young men and 13 participants were excluded from the ageing group because of being younger than 40 years.
fifties and the sixties and upward between the sixties and the seventies. A severe severity condition appeared in the forties with a very low probability and became maximum in the sixties. It is a well-known fact that the gonadal function of men will decrease with ageing and the probability of AD and LOH should © 2014 American Society of Andrology and European Academy of Andrology
have the upward trend (Araujo et al., 2007). However, the upward trend of the negative probability since the fifties and the downward trend of the severe probability since the sixties were obviously contrary to the fact (Fig. 2). To make this contrary phenomenon easier to understand, a hypothesis is proposed wherein the serum testosterone level falls below the defined threshold value (For example, TT < 11 nmol/ L and CFT < 220 pmol/L), the AMS scale score has enough correlation with the fluctuation of serum testosterone (free Andrology, 2014, 2, 856–861
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X-b. Kong et al. Figure 2 Probability of androgen deficiency (AD) and late-onset hypogonadism (LOH) (T < 10.4 nmol/L) (Araujo et al., 2007).
Another proof is the distribution characteristic of the free testosterone level with ageing in Japanese men (Namiki et al., 2008). The fluctuation amplitude of the free testosterone level kept decreasing with ageing (Fig. 3). The hypothesis based on known facts gives a possible reason for the contrary phenomenon between the probability of AD and that of AMS with ageing. To confirm the hypothesis, further investigation is required. In summary, the CN-AMS was developed and was self-administered by older participants. It has sufficient sensitivity in screening AD of older men, but the low specificity has made it unsuitable to be adopted as the diagnostic criteria. The scanning capability of the AMS scale for AD has the downward trend with ageing and a hypothesis is proposed to give a possible reason for the new finding.
ACKNOWLEDGEMENTS
Figure 3 Distribution of free testosterone with ageing (Namiki et al., 2008).
This study was supported by the Ministry of Science and Technology of the People’s Republic of China (2012BAI32B03). We are thankful to the participants of the study. Jiawei Zhang, Daoan Wang and Hongyan Li are thanked for the assistance in the recruitment of study participants, and Hui Zhou and Shuang Chen for laboratory assistance in hormone assays. The reviewers and editors are thanked for suggestions and critical comments to the manuscript.
AUTHOR CONTRIBUTIONS Study design: X-b.K., H-g.L.; Clinical data acquisition, patient recruitment: H-t.G.; Association study execution: C-l.X., H-g.L., H-t.G.; Statistical data analysis: Y.Z., X-b.K.; Critical discussion on data interpretation: C-l.X., X-b.K.; Manuscript drafting: X-b.K.; Comments to early versions of the manuscript: C-l.X., H-g.L.; Critical revision for important intellectual content: X-b.K. All authors have approved the final version of the manuscript.
DISCLOSURE Table 10 Correlation between AMS score, age and testosterone level (n = 244) Age Total Psychological Somatic Sexual
0.077 0.016 0.056 0.113
T
CFT 0.023 0.050 0.010 0.005
0.022 0.055 0.018 0.116
*Correlation is significant at the 0.01 level (two-tailed).
testosterone especially) level. When the fluctuation amplitude of testosterone level keeps descending with ageing, the scanning capability of the AMS scale for AD has the downward trend. There are proofs of this hypothesis. One proof is that the scale score improved significantly after the administration of androgen replacement therapy in LOH patients (Moore et al., 2004; Taniguchi et al., 2011), although there was no significant correlation between AMS score and age or testosterone levels which have been confirmed in other studies (T’Sjoen et al., 2004; Basar et al., 2005). In the study, the correlation between AMS score and testosterone level or age was analysed and no significant correlation was found (Table 10). 860
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None of the authors have financial and/or personal relationships with people or organizations that could inappropriately influence (bias) their work. The corresponding author had full access to all the data in the study and has the final responsibility for the decision to submit the manuscript for publication.
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