Association of hypogonadism symptoms and serum hormones in aging males
Guoqing Liang
Department of Urology, Tianjin Medical University General Hospital, Tianjin, China
Search for more papers by this authorYuxuan Song
Department of Urology, Tianjin Medical University General Hospital, Tianjin, China
Search for more papers by this authorLi Liu
Department of Urology, Tianjin Medical University General Hospital, Tianjin, China
Search for more papers by this authorKechong Zhou
Department of Urology, Tianjin Medical University General Hospital, Tianjin, China
Search for more papers by this authorJia Tian
Department of Urology, Tianjin Medical University General Hospital, Tianjin, China
Search for more papers by this authorJianhui Li
Department of Reproductive Epidemiology and Social Science, NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Fudan University, Shanghai, China
Search for more papers by this authorHuijuan Shi
Department of Reproductive Epidemiology and Social Science, NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Fudan University, Shanghai, China
Search for more papers by this authorQianxi Zhu
Department of Reproductive Epidemiology and Social Science, NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Fudan University, Shanghai, China
Search for more papers by this authorJun Wang
Department of Urology, The First People’s Hospital of Jiashan, Zhejiang, China
Search for more papers by this authorJunbiao Zheng
Department of Urology, The First People’s Hospital of Jiashan, Zhejiang, China
Search for more papers by this authorXiaohua Yu
Department of Urology, The First People’s Hospital of Jiashan, Zhejiang, China
Search for more papers by this authorShucheng Zhang
Department of Cell Biology, National Research Institute of Family Planning, Beijing, China
Search for more papers by this authorZheng Li
Department of Andrology, Shanghai general Hospital, Shanghai Jiaotong University, Shanghai, China
Search for more papers by this authorCorresponding Author
Xiaoqiang Liu
Department of Urology, Tianjin Medical University General Hospital, Tianjin, China
Correspondence
Xiaoqiang Liu, Department of Urology, Tianjin Medical University General Hospital, 154 Anshan Road, Heping District, Tianjin 300052, China.
Email: [email protected]
Search for more papers by this authorGuoqing Liang
Department of Urology, Tianjin Medical University General Hospital, Tianjin, China
Search for more papers by this authorYuxuan Song
Department of Urology, Tianjin Medical University General Hospital, Tianjin, China
Search for more papers by this authorLi Liu
Department of Urology, Tianjin Medical University General Hospital, Tianjin, China
Search for more papers by this authorKechong Zhou
Department of Urology, Tianjin Medical University General Hospital, Tianjin, China
Search for more papers by this authorJia Tian
Department of Urology, Tianjin Medical University General Hospital, Tianjin, China
Search for more papers by this authorJianhui Li
Department of Reproductive Epidemiology and Social Science, NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Fudan University, Shanghai, China
Search for more papers by this authorHuijuan Shi
Department of Reproductive Epidemiology and Social Science, NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Fudan University, Shanghai, China
Search for more papers by this authorQianxi Zhu
Department of Reproductive Epidemiology and Social Science, NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Fudan University, Shanghai, China
Search for more papers by this authorJun Wang
Department of Urology, The First People’s Hospital of Jiashan, Zhejiang, China
Search for more papers by this authorJunbiao Zheng
Department of Urology, The First People’s Hospital of Jiashan, Zhejiang, China
Search for more papers by this authorXiaohua Yu
Department of Urology, The First People’s Hospital of Jiashan, Zhejiang, China
Search for more papers by this authorShucheng Zhang
Department of Cell Biology, National Research Institute of Family Planning, Beijing, China
Search for more papers by this authorZheng Li
Department of Andrology, Shanghai general Hospital, Shanghai Jiaotong University, Shanghai, China
Search for more papers by this authorCorresponding Author
Xiaoqiang Liu
Department of Urology, Tianjin Medical University General Hospital, Tianjin, China
Correspondence
Xiaoqiang Liu, Department of Urology, Tianjin Medical University General Hospital, 154 Anshan Road, Heping District, Tianjin 300052, China.
Email: [email protected]
Search for more papers by this authorGuoqing Liang, Yuxuan Song, Li Liu and Kechong Zhou contributed equally to this work
Abstract
The association between hypogonadism symptoms and the levels of serum hormones are still in debate. To investigate the relationship between hypogonadism symptoms and serum hormones in middle-aged and elderly Chinese men, this community-based cross-sectional study was conducted based on a total of 965 ageing men. The ageing males’ symptom (AMS) scale, International Index of Erectile Function-5 (IIEF-5), International Prostate Symptom Score (IPSS) questionnaires and related variables were assessed. Blood tests for total testosterone (TT), sex hormone-binding globulin (SHBG) and luteinising hormone (LH) were performed. Serum level of free testosterone (FT) and bioavailable testosterone (Bio-T) was calculated. The mean age was 56.34 ± 8.85 years. Total AMS score was significantly associated with all five serum hormones (LH: p < 0.001; SHBG: p < 0.001; TT: p =.043; FT: p = 0.007; Bio-T: p < 0.001). We identified sexual and somatic symptoms were obviously related to five serum hormones, while psychological symptoms seemed to have no association with serum hormones. After adjusting for age and BMI, multiple linear regression analysis indicated that LH had positive correlations with total AMS score, somatic and sexual symptom score (p < 0.05). In conclusion, LH and SHBG had the strongest correlation hypogonadism and might be used as early predictors for symptomatic hypogonadism in the near future.
Open Research
DATA AVAILABILITY STATEMENT
Data available on request from the authors.
REFERENCES
- Bansal, V. P. (2013). Andropause a clinical entity. Journal of Universal College of Medical Sciences, 1(2), 54–68. https://doi.org/10.3126/jucms.v1i2.8413
10.3126/jucms.v1i2.8413 Google Scholar
- Bhasin, S., Brito, J. P., Cunningham, G. R., Hayes, F. J., Hodis, H. N., Matsumoto, A. M., Snyder, P. J., Swerdloff, R. S., Wu, F. C., & Yialamas, M. A. (2018). Testosterone therapy in men with hypogonadism. An endocrine society clinical practice guideline. The Journal of Clinical Endocrinology and Metabolism, 103(5), 1715–1744. https://doi.org/10.1210/jc.2018-00229
- Boyce, M. J., Baisley, K. J., Clark, E. V., & Warrington, S. J. (2004). Are published normal ranges of serum testosterone too high? Results of a cross-sectional survey of serum testosterone and luteinizing hormone in healthy men. BJU International, 94(6), 881–885. https://doi.org/10.1111/j.1464-410X.2004.05051.x
- Bozkurt, O., Bolat, D., Demir, O., Ucer, O., Şahin, A., Ozcift, B., Pektaş, A., Turan, T., Gümüş, B. H., Can, E., Bolukbasi, A., Erol, H., & Esen, A. (2013). Erectile function and late-onset hypogonadism symptoms related to lower urinary tract symptom severity in elderly men. Asian Journal of Andrology, 15(6), 785–789. https://doi.org/10.1038/aja.2013.44
- Crawford, E. D., Poage, W., Nyhuis, A., Price, D. A., Dowsett, S. A., Gelwicks, S., & Muram, D. (2015). Measurement of testosterone: How important is a morning blood draw? Current Medical Research and Opinion, 31(10), 1911–1914. https://doi.org/10.1185/03007995.2015.1082994
- Fabbri, E., An, Y., Gonzalez-Freire, M., Zoli, M., Maggio, M., Studenski, S. A., Egan, J. M., Chia, C. W., & Ferrucci, L. (2016). Bioavailable testosterone linearly declines over a wide age spectrum in men and women from the baltimore longitudinal study of aging. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 71(9), 1202–1209. https://doi.org/10.1093/gerona/glw021
- Feldman, H. A., Longcope, C., Derby, C. A., Johannes, C. B., Araujo, A. B., Coviello, A. D., Bremner, W. J., & McKinlay, J. B. (2002). Age trends in the level of serum testosterone and other hormones in middle-aged men: longitudinal results from the massachusetts male aging study. The Journal of Clinical Endocrinology & Metabolism, 87(2), 589–598. https://doi.org/10.1210/jcem.87.2.8201
- Frost, M., Wraae, K., Nielsen, T. L., Hougaard, D. M., Brixen, K., Hagen, C., & Andersen, M. (2013). Similar reference intervals for total testosterone in healthy young and elderly men: Results from the Odense Androgen Study. Clinical Endocrinology, 78(5), 743–751. https://doi.org/10.1111/cen.12042
- Giovanni, C., Giulia, R., Linda, V., Edoardo, M., & Mario, M. (2012). How to recognize late-onset hypogonadism in men with sexual dysfunction. Asian Journal of Andrology, 14(2), 251–259. https://doi.org/10.1038/aja.2011.138
- Habous, M., Tealab, A., Ali, M., Raheem, A. A., Ralph, D., & Binsaleh, S. (2017). Obesity is an independent risk factor for low serum testosterone in adult males. Journal of Men's Health, 11(5), 30–34.
- Harman, S. M., Metter, E. J., Tobin, J. D., Pearson, J., & Blackman, M. R. (2001). Longitudinal effects of aging on serum total and free testosterone levels in healthy men. The Journal of Clinical Endocrinology & Metabolism, 86(2), 724–731. https://doi.org/10.1210/jcem.86.2.7219
- Hsu, B., Cumming, R. G., Naganathan, V., Blyth, F. M., Le Couteur, D. G., Hirani, V., Waite, L. M., Seibel, M. J., & Handelsman, D. J. (2016). Temporal changes in androgens and estrogens are associated with all-cause and cause-specific mortality in older men. The Journal of Clinical Endocrinology & Metabolism, 101(5), 2201–2210. https://doi.org/10.1210/jc.2016-1025
- Huhtaniemi, I. (2014). Late-onset hypogonadism: Current concepts and controversies of pathogenesis, diagnosis and treatment. Asian Journal of Andrology, 16(2), 192. https://doi.org/10.4103/1008-682X.122336
- Kai, S., Guo-Qing, L., Xiang-Feng, C., Ping, P., Wen-Liang, Y., Shi-Jun, Z., Bo, W., Ying-Hao, S., & Zheng, L. (2012). Survey for late-onset hypogonadism among old and middle-aged males in Shanghai communities. Asian Journal of Andrology, 14(2), 338–340. https://doi.org/10.1038/aja.2011.171
- Khera, M., Adaikan, G., Buvat, J., Carrier, S., El-Meliegy, A., Hatzimouratidis, K., McCullough, A., Morgentaler, A., Torres, L. O., & Salonia, A. (2016). Diagnosis and treatment of testosterone deficiency: recommendations from the fourth international consultation for sexual medicine (ICSM 2015). Journal of Sexual Medicine, 13(12), 1787–1804. https://doi.org/10.1016/j.jsxm.2016.10.009
- Kim, J. W., Bae, Y. D., Ahn, S. T., Kim, J. W., Kim, J. J., & Moon, D. G. (2018). Androgen receptor CAG repeat length as a risk factor of late-onset hypogonadism in a korean male population. Sexual Medicine, 6(3), 203–209. https://doi.org/10.1016/j.esxm.2018.04.002
- Kong, X., Guan, H., Li, H., Zhou, Y., & Xiong, C. (2014). The ageing males' symptoms scale for Chinese men: Reliability, validation and applicability of the Chinese version. Andrology, 2(6), 856–861. https://doi.org/10.1111/j.2047-2927.2013.00145.x
- Li, J., Yu, X., Zheng, J., Zhao, J., Wang, J., Shen, Y., Li, Y., Yu, J., Li, D., Xu, J., & Zhu, Q. (2016). The reproductive health indices and sex hormone levels in middle-aged and elderly Chinese men. The Aging Male, 19(3), 143–147. https://doi.org/10.1080/13685538.2016.1188068
- Lunenfeld, B., Mskhalaya, G., Zitzmann, M., Arver, S., Kalinchenko, S., Tishova, Y., & Morgentaler, A. (2015). Recommendations on the diagnosis, treatment and monitoring of hypogonadism in men. The Aging Male, 18(1), 5–15. https://doi.org/10.3109/13685538.2015.1004049
- Marco, M., Alessia, F., Alessandra, G., Guido, D. D., Roberta, M., Carla, P., Valentina, V., Renato, P., Uberto, P., & Flaminia, F. (2017). Parallel diurnal fluctuation of testosterone, androstenedione, dehydroepiandrosterone and 17OHprogesterone as assessed in serum and saliva: Validation of a novel liquid chromatography-tandem mass spectrometry method for salivary steroid profiling. Clinical Chemistry and Laboratory Medicine, 55(9), 1315-1323. https://doi.org/10.1515/cclm-2016-0805
- Mario, G., Olivier, B., Pierre-Olivier, T., Fahima, N., Julie, D., & Mario, T. (2016). Modeling testosterone circadian rhythm in hypogonadal males: Effect of age and circannual variations. The AAPS Journal, 18(1) , 217–227. https://doi.org/10.1208/s12248-015-9841-6
- Orwoll, E., Lambert, L. C., Marshall, L. M., Phipps, K., Blank, J., Barrett-Connor, E., Cauley, J., Ensrud, K., & Cummings, S. (2006). Testosterone and estradiol among older men. The Journal of Clinical Endocrinology & Metabolism, 91(4), 1336–1344. https://doi.org/10.1210/jc.2005-1830
- Park, H. M., Kim, E. S., & Won, Y. (2020). Relationship between testosterone deficiency and the cardiovascular risk factors, diabetes, and hypertension. Journal of Men's Health, 16(4), 97–106.
- Peel, A., Martin, S., Vincent, A., Turnbull, D., Wang, X., McGee, M., Jesudason, D., Chambers, S., & Wittert, G. (2020). Testosterone and self-perceived masculinity in an australian cohort of community-dwelling men. Journal of Men's Health, 16(4), 28–44.
- Pye, S. R., Huhtaniemi, I. T., Finn, J. D., Lee, D. M., O'Neill, T. W., Tajar, A., Bartfai, G., Boonen, S., Casanueva, F. F., Forti, G., Giwercman, A., Han, T. S., Kula, K., Lean, M. E., Pendleton, N., Punab, M., Rutter, M. K., Vanderschueren, D., & Wu, F. C. W. (2014). Late-onset hypogonadism and mortality in aging men. The Journal of Clinical Endocrinology & Metabolism, 99(4), 1357–1366. https://doi.org/10.1210/jc.2013-2052
- Saalu, L. C., & Abraham, O. A. (2013). Andropause (male menopause): Valid concepts, fables and controversies. Journal of Basic Medical Sciences, 1, 33–37.
- Saleh, B. O., & Majeed, M. J. (2013). Andropause phenomenon by measurement of serum free testosterone concentration in Iraqi healthy men. Age Related Study. Saudi Medical Journal, 34(10), 1026.
- Samaras, N., Frangos, E., Forster, A., Lang, P. O., & Samaras, D. (2012). Andropause: A review of the definition and treatment. European Geriatric Medicine, 3(6), 368–373. https://doi.org/10.1016/j.eurger.2012.08.007
- Samipoor, F., Pakseresht, S., Rezasoltani, P., & Mehrdad, M. (2018). The association between hypogonadism symptoms with serum testosterone, FSH and LH in men. The Aging Male, 21(1), 1–8. https://doi.org/10.1080/13685538.2017.1382468
- Shigehara, K., Kato, Y., Kawaguchi, S., Ijima, M., Izumi, K., Kadono, Y., Konaka, H., Namiki, M., & Mizokami, A. (2020). Short-term effects of testosterone replacement therapy on risk predictors for arteriosclerosis among men with late-onset hypogonadism: A case–control study. Journal of Men's Health, 16(4), 65–71.
- Sungmin, K., Jun, P. H., & Cheol, P. N. (2013). Serum total testosterone level and identification of late-onset hypogonadism: A community-based study. Korean Journal of Urology, 54(9), 619. https://doi.org/10.4111/kju.2013.54.9.619
- Svartberg, J., Midtby, M., Bønaa, K. H., Sundsfjord, J., Joakimsen, R. M., & Jorde, R.(2003). The associations of age, lifestyle factors and chronic disease with testosterone in men: The Tromsø Study. European Journal of Endocrinology, 149(2).
- Tajar, A., Huhtaniemi, I. T., O'Neill, T. W., Finn, J. D., Pye, S. R., Lee, D. M., Bartfai, G., Boonen, S., Casanueva, F. F. F., Forti, G., Giwercman, A., Han, T. S., Kula, K., Labrie, F., Lean, M. E. J., Pendleton, N., Punab, M., Vanderschueren, D., & Wu, F. C. W. (2012). Characteristics of androgen deficiency in late-onset hypogonadism: Results from the european male aging study (EMAS). The Journal of Clinical Endocrinology & Metabolism, 97(5), 1508–1516. https://doi.org/10.1210/jc.2011-2513
- Tang, W. H., Zhuang, X. J., Shu, R. M., Guan, D., Ji, Y. D., Zhang, B. L., Wang, C. G., Zhuang, L. H., Yang, Z., Hong, K., Ma, L. L., Jiang, H., Zhou, S. J., & Gu, Y. Q. (2015). The prevalence of erectile dysfunction among subjects with late-onset hypogonadism: A population-based study in China. International Journal of Clinical and Experimental Medicine, 8(8), 13901–13910.
- Travison, T. G., Araujo, A. B., Kupelian, V., O’Donnell, A. B., & McKinlay, J. B., (2007). The relative contributions of aging, health, and lifestyle factors to serum testosterone decline in men. The Journal of Clinical Endocrinology & Metabolism, 92(2), 549–555. https://doi.org/10.1210/jc.2006-1859
- Wei, C., Zhi-Yong, L., Lin-Hui, W., Qin-Song, Z., Hui-Qing, W., & Ying-hao, S. (2013). Are the Aging Male's Symptoms (AMS) scale and the Androgen Deficiency in the Aging Male (ADAM) questionnaire suitable for the screening of late-onset hypogonadism in aging Chinese men? The Aging Male : the Official Journal of the International Society for the Study of the Aging Male, 16(3), 92–96. https://doi.org/10.3109/13685538.2013.805319
- Wittert, G. (2014). The relationship between sleep disorders and testosterone in men. Asian Journal of Andrology, 16(2), 262. https://doi.org/10.4103/1008-682X.122586
- Wu, F. C. W., Tajar, A., Beynon, J. M., Pye, S. R., Silman, A. J., Finn, J. D., O'Neill, T. W., Bartfai, G., Casanueva, F. F., Forti, G., Giwercman, A., Han, T. S., Kula, K.,Lean, M. E. J., Pendleton, N., Punab, M., Boonen, S., Vanderschueren, D., Labrie, F., & Huhtaniemi, I. T. (2010). Identification of late-onset hypogonadism in middle-aged and elderly men. New England Journal of Medicine, 363(2), 123–135. https://doi.org/10.1056/NEJMoa0911101
- Yang, Q. T., Wu, K. S., Li, Z. J., Li, W. C., Lu, L., Wu, H. Q., Zhuang, Y. Y., & Sui, X. X. (2018). Risk factors for late-onset hypogonadism. Andrologia, 50(6), e13016. https://doi.org/10.1111/and.13016
- Yeap, B. B., Almeida, O. P., Hyde, Z., Norman, P. E., Chubb, S. A. P., Jamrozik, K., & Flicker, L. (2007). In men older than 70 years, total testosterone remains stable while free testosterone declines with age. The Health in Men Study. European Journal of Endocrinology, 156(5), 585–594. https://doi.org/10.1530/EJE-06-0714
- Yu, X., Zhao, J., Zhang, S., Li, J., Zheng, J., Li, Z., Liang, G., Shi, H., Zhou, W., & Zhu, Q. (2017). The impact of age, BMI and sex hormone on aging males’ symptoms and the international index of erectile function scores. The Aging Male, 20(4), 235–240. https://doi.org/10.1080/13685538.2017.1361399
- Zarotsky, V., Huang, M. Y., Carman, W., Morgentaler, A., Singhal, P. K., Coffin, D., & Jones, T. H. (2014). Systematic literature review of the risk factors, comorbidities, and consequences of hypogonadism in men. Andrology, 2(6), 819–834. https://doi.org/10.1111/andr.274