Benign prostatic hyperplasia: A new metabolic disease?

Journal of Endocrinological Investigation

Volumn 37, Issue 4, 2014, Pages 313-322

  Vignozzi, L ^a   Rastrelli, G ^a   Corona, G ^b   Gacci, M ^c   Forti, G ^a   Maggi, M ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b BELLARIA HOSPITAL   (Italy)

^c UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Dyslipidemia; Hyperestrogenism; Hypogonadism; Inflammation; Metabolic syndrome

Indexed keywords

ESTRADIOL; SEX HORMONE; TESTOSTERONE; TOLL LIKE RECEPTOR;

ANTIGEN PRESENTING CELL; BACTERIAL INFECTION; BLADDER NECK; GONADAL DISEASE; HUMAN; HYPERCHOLESTEROLEMIA; HYPERESTROGENISM; HYPOGONADISM; HYPOTHESIS; INFLAMMATION; LOWER URINARY TRACT SYMPTOM; LYMPHOID TISSUE; MEDLINE; METABOLIC DISORDER; METABOLIC SYNDROME X; OBSERVATIONAL STUDY; ORGAN GROWTH; PATHOGENESIS; PROSTATE; PROSTATE HYPERTROPHY; REVIEW; VIRUS INFECTION; AGED; BLADDER; COMPLICATION; MALE; MICROBIOLOGY; MIDDLE AGED; OVERACTIVE BLADDER; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROSTATIC HYPERPLASIA; PROSTATITIS; VERY ELDERLY;

AGED; AGED, 80 AND OVER; BACTERIAL INFECTIONS; ESTRADIOL; HUMANS; HYPERCHOLESTEROLEMIA; HYPOGONADISM; MALE; METABOLIC SYNDROME X; MIDDLE AGED; PROSTATE; PROSTATIC HYPERPLASIA; PROSTATITIS; TESTOSTERONE; TOLL-LIKE RECEPTORS; URINARY BLADDER; URINARY BLADDER, OVERACTIVE; VIRUS DISEASES;

EID: 84897818874     PISSN: 03914097     EISSN: 17208386     Source Type: Journal    
DOI: 10.1007/s40618-014-0051-3     Document Type: Review

References (75)

1. Maggi M, Crescioli C, Morelli A, Colli E, Adorini L (2006) Preclinical evidence and clinical translation of benign prostatic hyperplasia treatment by the vitamin D receptor agonist BXL-628 (Elocalcitol). J Endocrinol Invest 29:665-674
2. Adorini L, Penna G, Fibbi B, Maggi M (2010) Vitamin D receptor agonists target static, dynamic, and inflammatory components of benign prostatic hyperplasia. Ann N Y Acad Sci 1193:146-152
3. Berry SJ, Coffey DS, Walsh PC, Ewing LL (1984) The development of human benign prostatic hyperplasia with age. J Urol 132:474-479
4. Abrams P (1999) LUTS, BPH, BPE, BPO: a plea for the logical use of correct terms. Rev Urol 1:65
5. Andersson KE, Arner A (2004) Urinary bladder contraction and relaxation: physiology and pathophysiology. Physiol Rev 84:935-986
6. Fibbi B, Penna G, Morelli A, Adorini L, Maggi M (2010) Chronic inflammation in the pathogenesis of benign prostatic hyperplasia. Int J Androl 33:475-488
7. Corona G, Baldi E, Maggi M (2011) Androgen regulation of prostate cancer: where are we now? J Endocrinol Invest 34:232-243
8. Behre HM, Bohmeyer J, Nieschlag E (1994) Prostate volume in testosterone-treated and untreated hypogonadal men in comparison to age-matched normal controls. Clin Endocrinol (Oxf) 40:341-349
9. Hunter J (1976) Observations on the glands situated between the rectum and bladder, called vesiculae seminales. In: Palmer JF (ed) Collected works of John Hunter, vol 4. Langman, London, p 31
10. Zuckerman S (1936) The endocrine control of the prostate: (section of urology). Proc R Soc Med 29:1557-1568
11. Wilson JD (1972) Recent studies on the mechanism of action of testosterone. N Engl J Med 287:1284-1291
12. Emberton M, Fitzpatrick JM, Rees J (2011) Risk stratification for benign prostatic hyperplasia (BPH) treatment. BJU Int 10:876-880
13. Gravas S, Oelke M (2010) Current status of 5alpha-reductase inhibitors in the management of lower urinary tract symptoms and BPH. World J Urol 28:9-15
14. Corona G, Rastrelli G, Maseroli E et al (2012) Inhibitors of 5α-reductase-related side effects in patients seeking medical care for sexual dysfunction. J Endocrinol Invest 35:915-920
15. Lenzi A, Balercia G, Bellastella A et al (2009) Epidemiology, diagnosis, and treatment of male hypogonadotropic hypogonadism. J Endocrinol Invest 32:934-938
16. Liu CC, Huang SP, Li WM et al (2007) Relationship between serum testosterone and measures of benign prostatic hyperplasia in aging men. Urology 70:677-680
17. Martin S, Lange K, Haren MT, Taylor AW, Wittert G, Members of the Florey Adelaide Male Ageing Study (2013) Risk factors for progression and improvement of lower urinary tract symptoms (LUTS) in a prospective cohort of men. J Urol doi: 10.1016/j. juro.2013.06.018. (Epub ahead of print)
18. Isaacs JT (1983) Changes in dihydrotestosterone metabolism and the development of benign prostatic hyperplasia in the aging beagle. J Steroid Biochem 18:749-757
19. Bartsch W, Klein H, Schiemann U, Bauer HW, Voigt KD (1990) Enzymes of androgen formation and degradation in the human prostate. Ann N Y Acad Sci 595:53-66
20. Corona G, Lee DM, Forti G, EMAS Study Group et al (2010) Age-related changes in general and sexual health in middle-aged and older men: results from the European Male Ageing Study (EMAS). J Sex Med 7:1362-1380
21. Marks LS, Mazer NA, Mostaghel E et al (2006) Effect of testosterone replacement therapy on prostate tissue in men with late-onset hypogonadism: a randomized controlled trial. JAMA 296:2351-2361
22. Tenover JS (1992) Effects of testosterone supplementation in the aging male. J Clin Endocrinol Metab 75:1092-1098
23. Holmäng S, Mårin P, Lindstedt G, Hedelin H (1993) Effect of long-term oral testosterone undecanoate treatment on prostate volume and serum prostate-specific antigen concentration in eugonadal middle-aged men. Prostate 23:99-106
24. Shigehara K, Sugimoto K, Konaka H et al (2011) Androgen replacement therapy contributes to improving lower urinary tract symptoms in patients with hypogonadism and benign prostate hypertrophy: a randomised controlled study. Aging Male 14:53-58
25. Haider A, Gooren LJ, Padungtod P, Saad F (2009) Concurrent improvement of the metabolic syndrome and lower urinary tract symptoms upon normalisation of plasma testosterone levels in hypogonadal elderly men. Andrologia 41:7-13
26. Kalinchenko S, Vishnevskiy EL, Koval AN, Mskhalaya GJ, Saad F (2008) Beneficial effects of testosterone administration on symptoms of the lower urinary tract in men with late-onset hypogonadism: a pilot study. Aging Male 11:57-61
27. Pearl JA, Berhanu D, François N et al (2013) Testosterone supplementation does not worsen lower urinary tract symptoms. J Urol doi:10.1016/j.juro.2013.05.111. (Epub ahead of print)
28. Ko YH, du Moon G, Moon KH (2013) Testosterone replacement alone for testosterone deficiency syndrome improves moderate lower urinary tract symptoms: one year follow-up. World J Men's Health 31:47-52
29. Karazindiyanoǧlu S, Cayan S (2008) The effect of testosterone therapy on lower urinary tract symptoms/bladder and sexual functions in men with symptomatic late-onset hypogonadism. Aging Male 11:146-149
30. Morgentaler A, Traish AM (2009) Shifting the paradigm of testosterone and prostate cancer: the saturation model and the limits of androgen-dependent growth. Eur Urol 55:310-320
31. Rastrelli G, Corona G, Vignozzi L et al (2013) Serum PSA as a predictor of testosterone deficiency. J Sex Med doi:10.1111/jsm.12266. (Epub ahead of print)
32. Comeglio P, Morelli A, Cellai I et al (2013) Opposite effects of tamoxifen on metabolic syndrome-induced bladder and prostate alterations: a role for GPR30/GPER? Prostate doi:10.1002/pros. 22723. (Epub ahead of print)
33. Nicholson TM, Ricke WA (2011) Androgens and estrogens in benign prostatic hyperplasia: past, present and future. Differentiation 82:184-199
34. Chavalmane AK, Comeglio P, Morelli A et al (2010) Sex steroid receptors in male human bladder: expression and biological function. J Sex Med 7:2698-2713
35. Robinette CL (1988) Sex-hormone-induced inflammation and fibromuscular proliferation in the rat lateral prostate. Prostate 12:271-286
36. Harris MT, Feldberg RS, Lau KM, Lazarus NH, Cochrane DE (2000) Expression of proinflammatory genes during estrogen-induced inflammation of the rat prostate. Prostate 44:19-25
37. Schatzl G, Brössner C, Schmid S et al (2000) Endocrine status in elderly men with lower urinary tract symptoms: correlation of age, hormonal status, and lower urinary tract function. The Prostate Study Group of the Austrian Society of Urology. Urology 55:397-402
38. Rohrmann S, Nelson WG, Rifai N et al (2007) Serum sex steroid hormones and lower urinary tract symptoms in third National Health and Nutrition Examination Survey (NHANES III). Urology 69:708-713
39. Partin AW, Oesterling JE, Epstein JI, Horton R, Walsh PC (1991) Influence of age and endocrine factors on the volume of benign prostatic hyperplasia. J Urol 145:405-409
40. Meikle AW, Stephenson RA, McWhorter WP, Skolnick MH, Middleton RG (1995) Effects of age, sex steroids, and family relationships on volumes of prostate zones in men with and without prostate cancer. Prostate 26:253-259
41. Hammarsten J, Damber JE, Karlsson M et al (2009) Insulin and free oestradiol are independent risk factors for benign prostatic hyperplasia. Prostate Cancer Prostatic Dis 12:160-165
42. Miwa Y, Kaneda T, Yokoyama O (2008) Association between lower urinary tract symptoms and serum levels of sex hormones in men. Urology 72:552-555
43. St Sauver JL, Jacobson DJ, McGree ME et al (2011) Associations between longitudinal changes in serum estrogen, testosterone, and bioavailable testosterone and changes in benign urologic outcomes. Am J Epidemiol 173:787-796
44. Martin S, Lange K, Haren MT, Taylor AW, Wittert G, Members of the Florey Adelaide Male Ageing Study (2013) Risk factors for progression and improvement of lower urinary tract symptoms (LUTS) in a prospective cohort of men. J Urol doi:10.1016/j.juro.2013.06.018. (Epub ahead of print)
45. Kastner P, Krust A, Turcotte B et al (1990) Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. EMBO J 9:1603-1614
46. Gronemeyer H, Meyer ME, Bocquel MT, Kastner P, Turcotte B, Chambon P (1991) Progestin receptors: isoforms and antihormone action. J Steroid Biochem Mol Biol 40:271-278
47. Ing NH, Tornesi MB (1997) Estradiol up-regulates estrogen receptor and progesterone receptor gene expression in specific ovine uterine cells. Biol Reprod 56:1205-1215
48. Vignozzi L, Morelli A, Sarchielli E et al (2012) Testosterone protects from metabolic syndrome-associated prostate inflammation: an experimental study in rabbit. J Endocrinol 212:71-84
49. Morelli A, Comeglio P, Filippi S et al (2012) Testosterone and farnesoid X receptor agonist INT-747 counteract high fat dietinduced bladder alterations in a rabbit model of metabolic syndrome. J Steroid Biochem Mol Biol 132:80-92
50. Di Carlo E, Magnasco S, D'Antuono T, Tenaglia R, Sorrentino C (2007) The prostate-associated lymphoid tissue (PALT) is linked to the expression of homing chemokines CXCL13 and CCL21. Prostate 67:1070-1080
51. Kohnen PW, Drach GW (1979) Patterns of inflammation in prostatic hyperplasia: a histologic and bacteriologic study. J Urol 121:755-760
52. Theyer G, Kramer G, Assmann I et al (1992) Phenotypic characterization of infiltrating leukocytes in benign prostatic hyperplasia. Lab Invest 66:96-107
53. Steiner GE, Stix U, Handisurya A et al (2003) Cytokine expression pattern in benign prostatic hyperplasia infiltrating T cells and impact of lymphocytic infiltration on cytokine mRNA profile in prostatic tissue. Lab Invest 83:1131-1146
54. Steiner GE, Newman ME, Paikl D et al (2003) Expression and function of pro-inflammatory interleukin IL-17 and IL-17 receptor in normal, benign hyperplastic, and malignant prostate. Prostate 56:171-182
55. Penna G, Fibbi B, Amuchastegui S et al (2009) Human benign prostatic hyperplasia stromal cells as inducers and targets of chronic immuno-mediated inflammation. J Immunol 182:4056-4064
56. Vignozzi L, Cellai I, Santi R et al (2012) Antiinflammatory effect of androgen receptor activation in human benign prostatic hyperplasia cells. J Endocrinol 214:31-43
57. Vignozzi L, Gacci M, Cellai I et al (2013) Fat boosts, while androgen receptor activation counteracts, BPH-associated prostate inflammation. Prostate 73:789-800
58. Roehrborn CG, Nuckolls JG, Wei JT, Steers W, BPH Registry and Patient Survey Steering Committee (2007) The benign prostatic hyperplasia registry and patient survey: study design, methods and patient baseline characteristics. Br J Urol 100:813-819
59. Nickel JC, Roehrborn CG, O'Leary MP, Bostwick DG, Somerville MC, Rittmaster RS (2008) The relationship between prostate inflammation and lower urinary tract symptoms: examination of baseline data from the REDUCE trial. Eur Urol 54:1379-1384
60. Hochreiter WW, Duncan JL, Schaeffer AJ (2000) Evaluation of the bacterial flora of the prostate using a 16S rRNA gene based polymerase chain reaction. J Urol 163:127-130
61. Sfanos KS, Sauvageot J, Fedor HL, Dick JD, De Marzo AM, Isaacs WB (2008) A molecular analysis of prokaryotic and viral DNA sequences in prostate tissue from patients with prostate cancer indicates the presence of multiple and diverse microorganisms. Prostate 68:306-320
62. Wang S, Mao Q, Lin Y et al (2012) Body mass index and risk of BPH: a meta-analysis. Prostate Cancer Prostatic Dis 15:265-272
63. Lotti F, Corona G, Colpi GM et al (2011) Elevated body mass index correlates with higher seminal plasma interleukin 8 levels and ultrasonographic abnormalities of the prostate in men attending an andrology clinic for infertility. J Endocrinol Invest 34:e336-e342
64. Lotti F, Maggi M (2013) Interleukin 8 and the male genital tract. J Reprod Immunol doi:10.1016/j.jri.2013.02.004. (Epub ahead of print)
65. Giovannucci E, Rimm EB, Liu Y et al (2003) Body mass index and risk of prostate cancer in U.S. health professionals. J Natl Cancer Inst 95:1240-1244
66. Parsons JK, Carter HB, Partin AW et al (2006) Metabolic factors associated with benign prostatic hyperplasia. J Clin Endocrinol Metab 91:2562-2568
67. Rohrmann S, Smit E, Giovannucci E, Platz EA (2004) Associations of obesity with lower urinary tract symptoms and noncancer prostate surgery in the third National Health and Nutrition Examination Survey. Am J Epidemiol 159:390-397
68. Corona G, Rastrelli G, Morelli A, Vignozzi L, Mannucci E, Maggi M (2011) Hypogonadism and metabolic syndrome. J Endocrinol Invest 34:557-567
69. De Nunzio C, Aronson W, Freedland SJ, Giovannucci E, Parsons JK (2012) The correlation between metabolic syndrome and prostatic diseases. Eur Urol 61:560-570
70. Gacci M, Vignozzi L, Sebastianelli A et al (2013) Metabolic syndrome and lower urinary tract symptoms: the role of inflammation. Prostate Cancer Prostatic Dis 16:101-106
71. Lotti F, Corona G, Vignozzi L et al (2013) Metabolic syndrome and prostate abnormalities in male subjects of infertile couples. Asian J Androl (accepted)
72. Filippi S, Vignozzi L, Morelli A et al (2009) Testosterone partially ameliorates metabolic profile and erectile responsiveness to PDE5 inhibitors in an animal model of male metabolic syndrome. J Sex Med 6:3274-3288
73. Morelli A, Comeglio P, Filippi S et al (2013) Mechanism of action of phosphodiesterase type 5 inhibition in metabolic syn-drome- associated prostate alterations: an experimental study in the rabbit. Prostate 73:428-441
74. Vignozzi L, Gacci M, Cellai I et al (2013) PDE5 inhibitors blunt inflammation in human BPH: a potential mechanism of action for PDE5 inhibitors in LUTS. Prostate 73:1391-1402
75. Morelli A, Sarchielli E, Comeglio P et al (2013) Metabolic syndrome induces inflammation and impairs gonadotropinreleasing hormone neurons in the preoptic area of the hypothalamus in rabbits. Mol Cell Endocrinol doi:10.1016/j.mce.2013.09.017. (Epub ahead of print)