Review Article

Systematic Literature Review of the Epidemiology of Nongenetic Forms of Hypogonadism in Adult Males

Table 3

Prevalence of hypogonadism among patients with specific conditions.

Author, year, and study nameCountry and years of data collectedStudy population Definition of hypogonadism usedPrevalence (%) among patients with disease of interest

Type 2 diabetes mellitus (T2DM)
Kapoor et al., 2007 [56]UK/not specifiedPrimary care retinopathy Screening service and medical clinic355 men with T2DMTT < 8 nmol/L
TT 8–12 nmol/L
17
25
Biswas et al., 2012 [25]UK/not specifiedMedical clinic329
T2DM ( )
T1DM ( )
controls ( )
TT < 11.9 nM 45
Chen et al., 2006 [29]Australia/NZ/1992 to 2000Population-based195
T2DM ( )
Non-T2DM ( )
TT < 8.0 nmol/L14.3
Corona et al., 2006 [36]Italy/not specifiedMedical clinic1246
T2DM ( )
TT < 10.4 nmol/L24.5
Anderson et al., 2012 [23]UK/January 2008–June 2009Medical clinic 387
T2DM ( )
T1DM ( )
TT < 8.0 nmol/L
TT 8–11.99 nmol/L
4.4
32.1
Talukder et al., 2010 [87]India/May 2008–April 2009Medical clinic 420
T2DM ( )
non-T2DM ( )
Symptoms/signs of hypogonadism and TT ≤ 12 nmol/L 34.7
Dhindsa et al., 2004 [40]US/not specifiedMedical clinic103
men with T2DM
TT < 300 ng/dL33
Grossmann et al., 2008 [48]Australia/not specifiedMedical clinic 649
T2DM ( )
T1DM ( )
TT < 10 nmol/L43
Grossmann et al., 2009 [47]Australia/2005Medical clinic 464 men with T2DM TT < 10 nmol/L43
La Vignera et al., 2009 [61]Italy/not specifiedMedical clinic 110 men with T2DM TT < 231 ng/mL 10
Ogbera et al., 2011 [71]Nigeria/December 2009 to May 2010Medical clinic203 men with T2DMTT < 8 nmol/L36
Hackett et al., 2009 [50]UK/September 2007 and May 2008Medical clinic 488 men with T2DM TT < 8 nmol/LTT 8–12 nmol/L 15.5
33.8
Ganesh et al., 2009 [45] India/not specifiedMedical clinic 100 men with T2DMcFT < 64.8 pg/mL (0.225 nmol/L)15

T2DM + obesity or metabolic syndrome (MetS)
Ogbera 2011 [70]Nigeria/December 2009 to May 2010Medical clinic203 men with T2DM
+ MetS ( )
T2DM + TT < 12 nmol/L36
T2DM + MetS43
T2DM + MetS + low TT47
Dhindsa et al., 2010 [39]US/not specifiedMedical clinic1849FT < 300 ng/dL or 10.4 nmol/L:
Obesity + T2DM ( )Obesity and T2DM51
Obesity ( )Obese31

Obesity
Hofstra et al., 2008 [54]The Netherlands/not specifiedMedical clinic160 obese males TT < 11 nmol/L57.7
Pellitero et al., 2012 [74]Spain/not specifiedClinical research center33 obese malesTT < 300 ng/dL 78.8
TT < 200 ng/dL + FT <65 pg/mL100
TT < 300 but >200 ng/dL23.1
FT low and TT > 300 ng/dL 3.85
Allan et al., 2006 [22]Australia/May 2001–February 2003Community-based223 TT < 8 nmol/L plus symptoms
Obese ( )Obese15
Nonobese ( )Nonobese 3

MetS
Laaksonen et al., 2005 [62]Finland/1987–2001Population-based854 men with MetS TT < 11 nmol/L10.7
Singh et al., 2011 [83]India/not specifiedMedical clinic95 men with MetS FT < 0.225 nmol/L30.2
Caldas et al., 2009 [27]Brazil/January 2003 to March 2007Medical clinic80 men with MetS TT < 300 ng/dL 30.0

Cardiac disease
Jankowska et al., 2006 [55]Poland/October 2001 to November 2002Medical clinic574
CHF ( )
health controls ( )
Serum TT and FT levels at or below the 10th percentile of healthy peers13–39 (by age)
Wang et al., 2010 [94]China/March 1, 2005, to May 31, 2007Medical clinic175 men with CHF Serum levels at or below the 10th percentile of healthy peers 21.7
Serra et al., 2012 [84]Italy/not specifiedMedical clinic52 male heart transplantation recipients TT < 10.4 nmol/L34.6
Florvaag et al., 2012 [44]Germany/not specified Medical clinic137 male heart failure patients Free testosterone (age-related cut-off values)39
Malkin et al., 2010 [67]UK/June 2000 and June 2002Medical clinic930 men with coronary disease TT < 8.1 nmol/L16.9
Wehr et al., 2010 [95]Germany/1997 to 2000Medical clinic2299 men who were routinely referred for coronary angiography T < 11.3 nmol/L18
Lerchbaum et al., 2012 [65]Germany/1997–2000 Medical clinic2069 men with coronary disease TT < 11.3 nM18.4

Erectile dysfunction (ED)
Köhler et al., 2008 [59]US/1987 to 2002Chart review2794 men presenting for ED evaluation TT < 300 ng/dL23
Bunch et al., 2002 [26]US/1996 to 1999Chart review501 men with ED TT < 300 ng/dL44
Corona et al., 2009 [33]Italy/not specifiedChart review2302 men with ED TT < 12 nmol/L + symptoms28.1
Arafa et al., 2012 [24]Egypt/not specifiedMedical clinic212 men T2DM + ED TT < 300 ng/dL + symptoms41
Guay et al., 2010 [49]US/July 1995 to July 1997Chart review 990 with men ED 10.4 nmol/L + symptoms36.3
Makhlouf et al., 2008 [66]US/July 2001 to June 2003Medical clinic157 men with ED TT < 300 mg/dL36
Corona et al., 2007 [35]Italy/not specifiedMedical clinic1134 men with ED TT < 10.4 nmol/L16.9
Corona et al., 2010 [37]Italy/2000 to 2007 Medical clinic1687 men with ED TT 230–300 ng/dL no symptoms13.3
Corona et al., 2009 [34]Italy/January 2001 to April 2008Medical clinic1093 men with ED
Somani et al., 2010 [85]UK/March 2007–August 2008Medical clinic124 men with ED Low TT (not further defined)23.4
Corona et al., 2010 [32]Italy/January 2001–April 2009Medical chart review 3712 men with sexual dysfunction TT <8 nmol/L + symptoms7.5
Tan et al., 2011 [88]Multiethnic Asia/Pacific/2003Medical chart review1046
ED ( )
TT < 10.4 nmol/L20.4
Hamidi et al., 2012 [52]Iran/November 2009 to August 2010Medical clinic241 men with EDFT < 5 ng/dL36.5

HIV
Klein et al., 2005 [58]US/not specifiedCommunity-based502 (had or at risk of HIV) TT < 300 ng/dL45.6
Crum-Cianflone et al., 2007 [38]US/September 2004 to May 2005HIV medical clinic 300 HIV+ TT < 300 ng/dL 17
Wahlstrom et al., 2000 [93]US/not specifiedObservational study20 HIV+T ≤ 410 ng/dL25
Collazos et al., 2009 [31]Spain/not specifiedMedical chart review188 HIV+ T < 2.6 ng/mL3.7
Wunder et al., 2007 [96]Switzerland/not specifiedCohort study139 HIV+ FT below the age-adjusted normal limits70
Wagner et al., 1995 [92]US/not specifiedStudy setting (baseline data)234 HIV+ TT ≤ 400 ng/dL 38
Rietschel et al., 2000 [78]US/November 1997–April 1999Cohort study90 HIV+ Low TT/FT19

Respiratory disease
Laghi et al., 2005 [64]US/not specifiedCohort study 101 men with COPDFT < 50 pg/mL37.6
Kirbas et al., 2007 [57]Turkey/November 2004 to July 2006Medical clinic 96 men with obstructive sleep apneaTT < 2.62 ng/mL19.8
Halabi et al., 2011 [51]US/not specifiedMedical clinic 104 men with COPD FT < 35 pg/mL for patients <70 years; FT < 30 pg/mL for patients ≥70 years 33.6

Depression
Hintikka et al., 2009 [53]Finland/1998, 1999, 2001, and 2005Population-based116
with and without psychological symptoms
FT < 160 pmol/L plus BDI scores:
+depressive symptoms28.8
−depressive symptoms10.5
McIntyre et al., 2006 [68]Canada/not specifiedMedical clinic94 men with and without depressionTT < 12.14 nmol/L:
Men with depression34
Men without depression6

Cancer
Tromp et al., 2011 [91]The Netherlands/2008Medical clinics 565 male 5-year survivors of childhood cancerT < 11.0 nmol/L12.4
Lackner et al., 2007 [63] Austria/not specifiedMedical clinic 68 men with testicular cancerT < 3.0 ng/mL + symptoms33.8
Pühse et al., 2011 [75]Germany/2004 Medical clinic376 men with testicular germ-cell cancer (TGCC) TT 2.84 ng/mL or 9.85 nmol/L ~25
Fleishman et al., 2010 [43]US/July 2007 through July 2009Medical clinic428 male patients with nontestosterone-related cancer TT < 300 ng/dL48
Salonia et al., 2011 [80]Italy/June 2006 and June 2008Medical clinic673 prostate cancer patientsTT < 3 ng/mL 21.4%
Greenfield et al., 2007 [46]US/not specifiedMedical clinic389 cancer survivorsTT < 10 nmol/L 13.6
Rajagopal et al., 2004 [76]US/not specifiedChart review40 cancer survivors<345 ng/dL
All65
On opioids90
Not on opioids40
Schatzl et al., 2001 [82]Austria/January 1999–April 2000Medical clinic156 men with prostate cancerTT <3.0 ng/mL 33.3
Romerius et al., 2009 [79]Sweden/2004–2006Medical clinic 292 men with history of childhood treatment of cancer or brain tumor T < 10 nmol/L 23

Rheumatoid arthritis (RA)
Tengstrand et al., 2002 [89]Sweden/not specifiedMedical clinic104 patients with RA<6.5 nmol/L–8.1 nmol/L
(age dependent)
31.7

Osteoporosis
Fink et al., 2006 [42]US/March 2000 to April 2002Medical clinics3674 men with osteoporosis TT < 200 ng/dL6.9
Clapauch et al., 2008 [30] Brazil/January 2005Medical clinic216 men with osteoporosiscFT < 6.5 ng/dL + symptoms25

Chronic kidney disease (CKD)
Yilmaz et al., 2011 [97]Turkey/March 2006 to June 2010Medical clinic239 men with CKDTT 10 nmol/L33
Carrero et al., 2011 [28]Sweden/June 1999 and October 2007Medical clinics260 men with ESRDTT < 10 nmol/L44
Kyriazis et al., 2011 [60]Greece/October 2005 and December 2006Medical clinic111 male hemodialysis patientsTT < 8 nmol/L49
Albaaj et al., 2006 [21]UK/not specifiedMedical clinic214 male patients with CKD or ESRDTT < 10 nmol/L26.2

Myopathies
Travison et al., 2008 [90]Canada/3-year studyMedical clinic59 men with myopathies10–30 nmol/L54
Durga et al., 2011 [41]US/July 2006 to April 2007Medical clinic60 men with spinal cord injuriesTT < 325 ng/dL43.3
Okun et al., 2002 [73]US/not specifiedMedical clinic68 men with PDFT < 70 pg/mL 35
Abbasi et al., 1994 [20]US/not specifiedMedical clinic102 men with poststroke hemiplegiaTT < 2.5 percentile of the healthy old men17

Miscellaneous diseases
Schatzl et al., 2000 [81]Austria/October 1998 to May 1999Medical clinic312 men with lower urinary tract symptomsT < 3 ng/mL22.1
Rhoden et al., 2005 [77]Brazil/January 2000 to December 2001Medical clinic746 urological patientsTT < 13.87 nmol/L24.5
Taddesse et al., 2012 [86]US/September 21 to December 21, 2010Medical clinic34 men with sickle cellT ≤ 250 ng/dL24
Okun et al., 2004 [72]US/not specifiedChart review118 men with PD + AD PD + T < 325 ng/mL
AD + T < 325 ng/mL
35
38
Moreno et al., 2009 [69]US/January 2006 to January 2008Medical chart review121 men with Peyronie's disease TT < 300 ng/dL29.5

CHD: chronic heart failure; CKD: chronic kidney disease; ED: erectile dysfunction; ESRD: end stage renal disease; MetS: metabolic syndrome; RA: rheumatoid arthritis; T2DM: type 2 diabetes mellitus; PD: Parkinson’s disease; AD: Alzheimer’s disease.