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The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 63:426-431 (2008)
© 2008 The Gerontological Society of America

A Short Version of the ADAM Questionnaire for Androgen Deficiency in Chinese Men

Leung-Wing Chu, Sidney Tam, Annie W. C. Kung, Tai-Pong Lam, Antoinette Lee, Rachel L. C. Wong, Sue Lo, Susan Fan, Chun-Pong Chung, John E. Morley and Karen S. L. Lam

Divisions of 1 Geriatric Medicine and 2 Division of Clinical Biochemistry, Queen Mary Hospital, Hong Kong.
3 Endocrinology and Metabolism, Department of Medicine, Queen Mary Hospital, Faculty of Medicine, the University of Hong Kong.
4 Research Centre of Heart, Brain, Hormone & Healthy Aging
5 Family Medicine Unit, Department of Medicine, Faculty of Medicine, the University of Hong Kong.
6 Department of Psychiatry, Faculty of Medicine, the University of Hong Kong.
7 Family Planning Association of Hong Kong.
8 Division of Geriatric Medicine, Saint Louis University Medical School, St. Louis, Missouri.

Address correspondence to Leung-Wing Chu, MBBS, FRCP, FRCP, Division of Geriatric Medicine, Department of Medicine, Queen Mary Hospital, University of Hong Kong, 102 Pokfulam Road, Hong Kong SAR. E-mail: lwchu{at}hkucc.hku.hk


   Abstract
Top
 Abstract
Methods
 Results
 Discussion
 References
 
Background. A 10-question screening questionnaire for androgen deficiency in aging men (ADAM) was reported in previous white but not Chinese populations. We therefore investigated the validity of a Chinese version of the Saint Louis University ADAM questionnaire to screen for androgen deficiency in Chinese men.

Methods. This was a cross-sectional study. Seven hundred ninety-six ambulatory community-based Chinese men, 18–89 years old, were recruited from October 2003 through June 2006. Self-administered Chinese ADAM questionnaire and morning blood samples for serum total testosterone (TT) and bioavailable testosterone (BT) levels were collected from all participants. Low serum BT levels (androgen deficiency) were defined as <5th percentile of serum BT levels in young healthy Chinese men (18–29 years).

Results. The Chinese ADAM questionnaire had good internal consistency (Cronbach {alpha} = 0.74) and test–retest reliability (Pearson correlation coefficient, r = 0.86; p <.001, two-tailed). As a screening test for low serum BT levels, the Chinese ADAM questionnaire has a high sensitivity of 88% but low specificity of 32%. In 6 of the 10 questions, the mean serum BT levels were significantly lower in those who answered positively than in those who answered negatively. Using a cut-off score of ≥2, a six-question short Chinese ADAM questionnaire demonstrated sensitivity, specificity, and positive and negative predictive values of 86%, 40%, 46%, and 82%, respectively.

Conclusion. We have validated a full Chinese version and developed a shortened version of the ADAM questionnaire, and demonstrated that they are sensitive but not specific screening tests for androgen deficiency in Chinese men.

Key Words: Testosterone • Aging • Androgen deficiency • ADAM questionnaire • Chinese • Men

ANDROGEN deficiency in aging men had been well reported in both cross-sectional (1–13) and longitudinal (14–17) studies, which showed much greater declines in serum free or bioavailable testosterone (BT) than total testosterone (TT) levels. In particular, the age-related decline in serum BT or free testosterone (FT) levels was associated with symptoms, including decreases in libido (18–20), muscle strength (21,22), functional decline (23,24), and cognitive impairment (25–28). Moreover, most of these symptoms showed improvement after testosterone replacement therapy (25–31).

Morley and colleagues (19,20) validated a 10-question screening questionnaire for androgen deficiency in aging men (ADAM) in two studies of white men. This St. Louis University ADAM questionnaire contained questions covering areas on libido, energy, strength/endurance, height loss, enjoyment of life, sadness in mood, erectile dysfunction, sports performance, sleepiness after dinner, and work performance. Serum BT levels were used as the biochemical gold standard in these studies (19,20), and mean serum BT, but not TT, levels were significantly lower in those who answered positively, when compared to those who answered negatively, in 8 of the 10 questions (20). In the first study, the Saint Louis University ADAM questionnaire had 88% sensitivity and 60% specificity in detecting androgen deficiency by the low serum BT level (<71 ng/dL) standard (19). In the second study, the sensitivity and specificity of this questionnaire were 97% and 30%, respectively (20).

It would be important to confirm whether the Saint Louis University ADAM questionnaire could also be usefully employed to screen for androgen deficiency in Chinese men. We therefore set out to investigate, in this study, the validity of a Chinese version of the ADAM questionnaire to detect androgen deficiency among Chinese men.


   METHODS
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 Abstract
 Methods
Results
 Discussion
 References
 
Translation and Back-Translation of the Chinese Version of the ADAM Questionnaire
The Saint Louis University questionnaire was translated from English into Chinese by a bilingual professional translator. The Chinese version's content validity was assessed by a panel of geriatricians, endocrinologists, a clinical psychologist, and gynecologists, and amendments were made as indicated. This draft Chinese ADAM questionnaire was then back-translated to English independently by three bilingual professionals (two doctors and one professional translator). The three back-translated English versions were then assessed and compared with the original English version by the original author (J.E.M.), who commented that the back-translated English versions were very similar in meaning to the original English version. The final version of the Chinese ADAM questionnaire was administered to 22 Chinese men (mean age 34 ± 10.6 years; range 22–68 years) and then again within 7 days to assess the test–retest reliability.

Participants
This was a cross-sectional study of ambulatory community-based Chinese men recruited from staff volunteers in hospitals, men attending a "well men clinic" for preventive health assessment, older men from social centers for elderly persons, and men from a university-based family medicine clinic. The inclusion criteria included Chinese ethnicity, ability to walk, living in the community, age between 18 and 90 years, and ability to provide written informed consent. The exclusion criteria included the presence of cancer; known hypogonadism, dementia, and/or depression; renal, respiratory, heart, and/or liver failure; and the use of sex hormone or any steroid compound or medications that would impact erectile function or libido. The study complied with the Declaration of Helsinki, and the research protocol was approved by the Ethics Committee of the University of Hong Kong.

Baseline Assessment
All eligible participants who fulfilled the inclusion and exclusion criteria were invited to attend an interview. Sociodemographic data and past medical history were collected. The Chinese ADAM questionnaire (yes/no format) was self-administered.

Serum Testosterone Assays
A fasting blood sample for serum TT and BT levels was collected from every participant between 9:00 AM and 11:00 AM. Serum TT and BT levels were determined, using 125I-labeled testosterone antibody radioimmunoassay (RIA) kits (Diagnostic Products Corporation, Los Angeles, CA) in the neat and ammonium sulfate-treated samples, respectively. BT was measured after ammonium sulfate precipitation. Assays were done in duplicate, and the mean values were adopted for analysis. Serum was treated with 50% saturated ammonium sulfate for 15 minutes at 4°C. After centrifugation at 2000 g for 10 minutes at 4°C, the BT in the supernatant was measured. The analytical sensitivities of BT and TT were both 0.14 nmol/L. The intraassay coefficients of variance were 6.36% at 0.7 nmol/L and 4% at 55.4 nmol/L. The interassay coefficients of variation were 6.97% at 2.63 nmol/L and 7.3% at 45.0 nmol/L. In a previous study, Morley and colleagues (32) had reported good correlation of serum BT levels by assay and that obtained by the equilibrium dialysis. From our own sample of healthy Chinese men, the reference range of serum TT and BT levels in young healthy Chinese men (18–29 years) were 11.4–35.0 nmol/L and 2.4–10.2 nmol/L nmol/L, respectively (our unpublished data, 2006).

Statistical Analyses
The internal consistency of the Chinese ADAM questionnaire on the whole sample (n = 796) was assessed by the Cronbach {alpha} under scale reliability analyses. The test–retest reliability of the Chinese ADAM questionnaire was analyzed by using the Pearson correlation coefficient of the two scores on 22 Chinese men, and the differences between the two scores were compared by the paired t test and also assessed by Bland–Altman plots.

Descriptive analyses were done for all participants. The relationships of serum TT and BT levels with age were analyzed by using Pearson correlation analyses. Low BT levels were defined as below the 5th percentile of serum BT levels in young Chinese men (18–29 years). Participants were stratified into two groups by their serum BT levels into the low (<2.405 nmol/L or <69.4 ng/dL) and non-low BT (≥2.405 nmol/L or ≥69.4 ng/dL) groups. A positive Saint Louis ADAM questionnaire was defined as a positive answer to question 1, question 7, or to three of the other questions (19,20). The sensitivity, specificity, positive predictive value (+PV), and negative predictive value (–PV) of the Chinese version of the Saint Louis University ADAM questionnaire to detect men with low versus non-low BT levels was calculated. Similarly, the sensitivity, specificity, +PV, and –PV of each question in the Chinese ADAM questionnaire was calculated. For each individual question, we compared serum BT and TT levels between those who answered positively ("yes") and those who answered negatively ("no") with an independent t test. Those questions that displayed significant differences in serum BT levels between the two answer groups were selected to form a short version of the Chinese ADAM questionnaire. In each question, a positive answer scored one point and a negative answer scored zero points. Receiver operating characteristic (ROC) curve and area under curve (AUC) analyses, sensitivity, specificity, +PV, and –PV for different cut-off scores to detect low BT levels were performed for both the full and short versions. SPSS for Windows (version 13.0; SPSS Inc., Chicago, IL) was used for data analyses, whereas the MedCalc for Windows (version 7.0; Frank Schoonjans, Mariakerke, Belgium) was used for the Bland–Altman plots and ROC curve analyses.


   RESULTS
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 Abstract
 Methods
 Results
Discussion
 References
 
Reliability of the Chinese ADAM Questionnaire
The internal consistency of the Chinese ADAM questionnaire was good with a Cronbach {alpha} of 0.74 (n = 796). The test–retest reliability of the Chinese ADAM questionnaire (n = 22) was also good (Pearson correlation coefficient or r = 0.86, p <.001, two-tailed) with no significant difference between the test and retest ADAM scores (mean ± standard error of the mean 2.32 ± 0.36 vs 2.45 ± 0.45; p =.56, paired t test, two-tailed). Moreover, the Bland–Altman plots showed that most plots (21 of 22) of the difference between the two scores against the test–retest average scores were within the mean ± 1.96 standard deviation range with no systematic bias.

Participants
From October 2003 through June 2006, 796 ambulatory, community-living Chinese men were recruited. The proportions of men in the 18–39, 40–59, and 60–89 year age groups were 19.7%, 41.6%, and 35.6%, respectively. The baseline characteristics of the participants are described in Table 1. Serum BT levels had a strong negative correlation, whereas serum TT levels had a weak negative correlation with age (BT: r = –0.69, p <.001; TT: r = –0.10, p =.004).


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  		Table 1. Baseline Characteristics of Participants (N = 796).

 
Overall, 37.6% and 75.7% of the participants had low serum BT levels and a positive ADAM questionnaire, respectively, and both of them showed an age-associated increase in prevalence. Even in young Chinese men (18–29 years), 35.8% displayed a positive ADAM questionnaire despite a corresponding low prevalence of 3.8% in the low serum BT level group (Table 2). The Chinese ADAM questionnaire had a good sensitivity of 88%, a low specificity of 32%, and +PVs and –PVs of 44% and 81%, respectively (Table 3). In the ROC curve analysis, the AUC was 0.636 (95% confidence interval [CI], 0.602–0.670).


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  		Table 2. Prevalence of Low Serum Bioavailable Testosterone Levels and Positive Chinese ADAM Questionnaire in Chinese Men (N = 796).

 

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  		Table 3. Screening for Androgen Deficiency by the Chinese ADAM Questionnaire and Its Individual Question in Chinese Men (N = 796).

 
The prevalence of positive answers ("yes") for each question varied widely. Participants were stratified into two groups by their serum BT levels into low (<2.405 nmol/L or 69.4 ng/dL) or non-low BT (≥2.405 nmol/L or ≥69.4 ng/dL) groups. The top four questions with high sensitivity (approximately 70%) to detect low BT levels were "decreased in strength," "lack in energy," "less strong erection," and "decreased libido," which also had high prevalence of positive answers. However, these questions only had low to satisfactory specificity (35%–62%). The +PV (61%) was the highest for the "lost height" question, although this question also had the lowest sensitivity (28%) and prevalence of positive answers (17.1%) (Table 3).

Serum BT levels were significantly lower in those who answered positively than in those who answered negatively, in 6 of the 10 questions. The 6 questions were "decreased in strength," "lack in energy," "less strong erection," "lost height," "decreased libido," and "deterioration in work performance." In contrast, serum TT levels displayed no significant differences between the positive and negative answer groups in all but one (decreased libido) of the questions (Table 4). Using these six questions, we evaluated the properties of a six question, short Chinese ADAM questionnaire in detecting low serum BT levels in our participants. ROC curve analysis showed that the AUC was 0.69 (95% CI, 0.66–0.72), and a cut-off score of ≥2 had sensitivity, specificity, and +PVs and –PVs of 86%, 40%, 46%, and 82%, respectively (Table 5). The AUC of the short version was higher than that of the full 10-question Chinese ADAM questionnaire (AUC = 0.636; 95% CI, 0.602–0.670; Table 3). Compared to those of the full ADAM questionnaire, the short form of the questionnaire had lower positive rates, which were actually closer to the positive rates of low serum BT levels in most age groups (18–29, 30–39, 40–49, 50–59, 60–69, and 70–79) (Tables 2 and 6).


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  		Table 4. Serum Bioavailable Testosterone (BT) Levels of Participants with Positive and Negative Answers to the Chinese ADAM Questionnaire (N = 796).

 

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  		Table 5. Short Chinese ADAM Questionnaire to Screen for Androgen Deficiency in Chinese Men (N = 796).

 

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  		Table 6. Prevalence of Low Serum Bioavailable Testosterone (BT) Levels and Positive Short Chinese ADAM Questionnaire in Chinese Men (N = 796).

 

   DISCUSSION
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 Methods
 Results
 Discussion
References
 
To our knowledge, there is no validated Chinese questionnaire available for the screening of androgen deficiency in Chinese men. Morley and colleagues (19,20), Heineman and colleagues (33), and Smith and colleagues (34) recently reported three questionnaires—the Saint Louis University ADAM, the Aging Male Survey (AMS), and the Massachusetts Male Aging Study (MMAS)—and found that the ADAM questionnaire had the highest sensitivity, compared to the AMS and MMAS (20). In the present study, we found the translated Chinese ADAM questionnaire had good content validity, internal consistency (as reflected by a Cronbach {alpha} of 0.74), and test–retest reliability, as well as a high sensitivity of 88%, similar to the original Saint Louis University ADAM questionnaire. In the present study, we used a serum BT level of 2.405 nmol/L (69.4 ng/dL) as the cut-off for androgen deficiency; this corresponded closely to the cut-off of 71 ng/dL in the original Saint Louis ADAM questionnaire validation study (19).

Based on the findings of a low frequency of low serum BT in men younger than 40 years, there was a low chance of having low serum BT levels in the 18–29 and 30–39 age groups. The need for the use of a screening questionnaire in these age groups was low. In contrast, there was a very high prevalence of low serum BT levels in the 80- to 89-year-olds (i.e., 98% low serum BT levels), and most of these men could be assumed to have low BT levels. The need for the use of a screening questionnaire in these age groups was also low. Between the ages of 40 and 79 years, the prevalence of low BT ranged from 14% to 81%. The ADAM questionnaire could be used to screen for low BT in the subgroups of 40- to 49-year-olds, 50- to 59-year-olds, 60- to 69-year-olds, and 70- to 79-year-olds. A repeated analyses of the ADAM questionnaire on the men 40–79 years old (n = 594) showed similar sensitivity, specificity, +PV, and –PV of 89%, 23%, 46%, and 74%, respectively, with those of the whole group.

The drawback of the Chinese ADAM questionnaire was its relatively low specificity of 32%. A low specificity was also found with the original Saint Louis University ADAM questionnaire (19) and the AMS (33). This is because a number of these symptoms in the questionnaire can be caused by depression and other diseases, apart from androgen deficiency in men (19,20,33,34). In the present study, we found the questions "decrease in strength," "lack in energy," "decreased ability to play sports," and "falling asleep after dinner" had the lowest individual specificity, ranging from 35% to 54%.

Except for question 1 on "decreased libido," there were no significant differences in the mean serum TT levels between those who gave positive answers and those who gave negative answers for all the other nine questions. In contrast, strongly statistically significant differences in the mean serum BT levels were observed between those who gave positive answers and those who gave negative answers in six questions, including "decreased in strength," "lack in energy," "less strong erection," "lost height," "decreased libido," and "deterioration in work performance." These findings agreed largely with a previous study (20), which showed significant differences in serum BT but not TT levels between the two groups in 8 of 10 questions including the six questions in our present study. However, two of those eight questions (i.e., "decreased ability to play sports" and "falling asleep after dinner") did not show any significant difference between the two answer groups in our study. This difference between our study and that of Morley and colleagues (19) might be related to some cultural differences in "sports activity" and "after dinner activity" between men in Chinese and Western societies.

We then developed a short six-question Chinese ADAM questionnaire that consisted of the six questions with a significant relationship with serum BT levels. This short version showed sensitivity, specificity, and +PVs and –PVs of 86%, 40%, 46%, and 82%, respectively, comparable to those of the 10-question version. Moreover, the short ADAM questionnaire had higher AUC and lower positive rates, which were closer to the positive rates of low serum BT levels in most age groups (i.e., 18–29, 30–39, 40–49, 50–59, 60–69, and 70–79), than the full version (Tables 2 and 6). We therefore recommend using this short Chinese version for screening purposes in Hong Kong Chinese men. The obvious benefit is a decrease in the test administration time without compromising its sensitivity and specificity. For confirmation of androgen deficiency, we recommend morning serum BT level determinations in those men who are screened positive by the questionnaire. In the recent consensus recommendation for the investigation, treatment and monitoring of late-onset hypogonadism endorsed by the International Society of Andrology (ISA), International Society for the Study of the Aging Male (ISSAM) and European Association of Urology (EAU), measured or calculated serum FT or BT levels are also recommended to confirm the diagnosis in aging men who have androgen deficiency symptoms if the serum TT levels are either borderline or normal (35–37). As week-to-week variation in serum testosterone levels may occur, and we recommend a repeated blood sampling 1–2 weeks later for morning serum BT level if the first serum BT level is within normal limits (32).

Conclusion
We have validated a Chinese version of the ADAM questionnaire, developed a shortened version of it, and shown that both are suitable for use as screening tests of androgen deficiency in Chinese men from 40 to 79 years old.


   Acknowledgments
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 Methods
 Results
 Discussion
 References
 
This work was funded by the Training and Research Assistance Scheme (TRAS) of the QMH Charitable Trust and by the CRCG Small Projects Fund of the University of Hong Kong.

Disclaimer: John E. Morley provides consultation for Organon, Mattern Pharmaceuticals, Solvay, and Schering.


   Footnotes
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Decision Editor: Luigi Ferrucci, MD, PhD

Received April 2, 2007

Accepted July 16, 2007


   References
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 Discussion
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