The scope was to determine the incidence of ED and evaluate the correlations of ED and LUTS among adult Nigerian male patients who presented with LUTS at the urology clinics of N.A.U.T.H. The prevalence of common associated co- morbidities and effect on Quality of Life (QoL) was also assessed.
The limitations:
The IPSS and IIEF were designed to be self-administered. However, many of the subjects were illiterate and semiliterate, thus the researcher resorted to slight modification of the IIEF without alteration in its main structure. The researcher also assisted in the filling of the questionnaire. This could introduce observer bias to the study.
In the study, the co-morbidities were self-reported. No attempts were made to validate respondents’ answers with their medical records. Also, single screening for conditions like diabetes and hypertension may not be enough to exclude them. These medical conditions may be asymptomatic and unknown to the subject and thus may be underreported
The study population was also selective. Thus the findings may not be directly applicable to the general population.
26
CHAPTER FOUR RESULTS
A total of 110 patients were studied. The age ranged from 43 years to 80 years with a mean age of 65.8 ± 7.95 years. The peak age group was in age range 71 to 75 years with 34 patients. Other basic characteristics of the patients were also noted (Table 1, Figure 3).
Table 1 Baseline characteristics of patients (n = 110).
Characteristics Range Mean ± SD
Age (yrs) 43.0-80.0 65.8 ± 7.95
Height (m) 1.60-1.81 1.68 ± 0.04
Weight (Kg) 46.0-98.0 69.61 ± 10.66
BMI (Kg/m2) 16.9-34.72 24.59 ± 3.55
SBP (mmHg) 110.0-192.0 141.6 ± 19.98
DBP (mmHg) 60.0-110.0 81.45 ± 10.86
Figure 3: The distribution of LUTS according to age groups (n=110).
n=6 n=34
n=22
n=14 n=24
n=2 n=4 n=4
0 5 10 15 20 25 30 35
40-45 46-50 51-55 56-60 61-65 66-70 71-75 76-80 AGE GROUPS (YRS)
FREQUENCY(%)
27
Body mass index (BMI) ranged from 16.9 to 34.7 with mean BMI of 24.59 ± 3.55. The peak BMI was within the 18.5 to 24.9 group representing 47.3% (Figure 4). This means that most of the patients had normal body weight.
Figure 4: The incidence of LUTS according to the level of adiposity (n=110).
Ninety-four patients (85.5%) were married and had their wives alive while 16 patients (14.5%) were widowed. One hundred and eight (98.2%) were Christians while 2 (1.8%) were traditionalists. Sixty (54.5%), 20 (18.2%) and 30 (27.3%) patients had up to primary, secondary and post secondary levels of education respectively. Thus there is a tendency towards illiteracy or semi-illiteracy. The life-style patterns of the patients are also represented in table 2.
n=6 n=46
n=52
n=6 0
5 10 15 20 25 30 35 40 45 50
<18 18-24.9 25-29.9 30-34.9
ADIPOSITY LEVEL BY BMI (KG/M2)
FREQUENCY(%)
28
Table 2 Frequencies of other characteristics and life-style of patients
Frequency Percentage
Marital Status Married Widowed Total
94 16 110
85.5*
14.5 100 Religion
Christianity Traditionalist Total
108 2 110
98.2*
1.8 100 Highest Level of
Education Primary Secondary Post-secondary Total
60 20 30 110
54.5*
18.2 27.3 100 Smoking Habit
Smokers Non-smokers Total
8 102 110
7.3 92.7*
100 Alcohol Intake
Yes No Total
22 88 110
20 80*
100
* Option with the highest frequency amongst respondents
The mean total LUTS and ED scores were 15.81 ± 7.52 and 16.90 ± 6.45 respectively. Other graded LUTS scores and QoL scores are represented in table 3.
29
Table 3 LUTS, ED and Quality of life scores for patients (n = 110).
Range Mean ± SD
LUTS Score (Voiding phase)
0-19 7.6 ± 5.11
LUTS Score (Filling &
Storage phase)
1-15 8.12 ± 3.67
Total LUTS Score 2-33 15.81 ± 7.52
ED Score 8-25 16.90 ± 6.45
LUTS Quality of life score
1-6 4.05 ±1.07
ED Quality of life score 3-6 4.18 ± 1.22
The number of LUTS patients that had sexual intercourse within the preceding one month was 44 (40%) while the number of those that did not have sexual intercourse was 66 (60%).We did not assess the possible reasons for the greater number of patients that did not attempt sexual intercourse within the preceding one month. However, using ED scores to assess the LUTS patients that had sexual intercourse, 16 (36.4%) had normal sexual function (ED score >21), 8 (18.2%) had mild ED (ED score 17 to 21), 8 (18.2%) had mild to moderate ED (ED score 12 to 16), 12 (27.2%) had moderate ED (ED score 8 to 11) while none had severe ED (≤ 7). Thus a total of 28 (63.6%) LUTS patients who had attempted sexual intercourse had some form of ED without any severe ED (figure 5).
30
Figure 5: Distribution of ED among LUTS patients who had sex (n=44)
RELATIONSHIP BETWEEN SEVERITY OF ED AND LUTS
A linear regression between ED scores and LUTS scores indicated a significant relationship between ED scores and voiding phase, filling-storage phase, and total LUTS scores respectively (table 4, figures 6-8).
Table 4: Pearson’s bivariate correlation test between ED scores and LUTS scores ED Score vs. Regression Coefficient P-value
Voiding phase LUTS Score
0.388 0.009
Filling-storage phase LUTS Score
0.428 0.004
Total LUTS Score 0.445 0.002
n=0 n=12
n=8 n=8
n=16
0 5 10 15 20 25 30 35 40
NORMAL MILD ED MILD TO MODERATE
ED
MODERATE ED
SEVERE ED
INCIDENCE OF ED
FREQUENCY(%)
31
Figure 6: Scatter plot between voiding phase LUTS and ED (n=44)
32
Figure 7: Scatter plot between filling-storage phase LUTS and ED (n=44)
33
Figure 8: Scatter plot between total LUTS and ED (n=44)
This positive correlation thus shows that the higher the LUTS scores (voiding phase, filling-storage phase and total), the higher the ED scores. However Pearson’s chi-square analysis of severity of ED and graded LUTS score revealed no significant association between the severity of ED and that of voiding phase and filling-storage phase LUTS. Conversely, severity of ED was significantly related (p = 0.0001) to the severity of total LUTS score (Table 5).
34
Table 5: Relationship between the severity of ED and graded LUTS scores Severity of ED vs. Pearson’s Chi2 P-value
Graded voiding phase LUTS score
6.33 0.096
Graded filling-storage phase LUTS score
7.11 0.068
Graded Total LUTS score 26.15 0.0001
EFFECTS OF ED AND LUTS ON QoL:
The range and mean values of LUTS and ED QoL scores are as previously reported in table 3. One hundred (90.9%) of LUTS patients were worried about their LUTS while 10 (9.1%) were not worried. Among 44 (40%) of LUTS patients that had sexual intercourse, 22 (50%) were worried about their sexual function while same number of patients were not. Twenty-two of LUTS patients were worried about both LUTS and ED. Among these, 10 (45.5%) found LUTS more worrisome while 8 (36.3%) found ED more worrisome. In 4 (18.2%) of LUTS patients, both ED and LUTS were found worrisome (Table 6).
35
Table 6 Assessment of the quality of life of patients
Frequency Percentage Attempted Sex (n=110)
Yes No Total
44 66 110
40 60 100 Worried about LUTS (n=110)
Yes No Total
100 10 110
90.9 9.1 100 Worried about ED among sex
attempted group (n=44) Yes
No Total
22 22 44
50 50 100 Which is more worrisome (n=22)
ED LUTS Both Total
8 10 4 22
36.3 45.5 18.2 100
Pearson’s Chi-square analysis showed no significant relationship between severity of filling-storage phase and total LUTS scores and QoL of patients with LUTS. Conversely, QoL shows a significant relationship (P<0.05 and P<0.01) between severity of voiding phase LUTS and severity of ED (Table 7).
Table 7: Relationships of severity of LUTS and ED with the Quality of Life Pearson’s Chi2 P-value
Severity of voiding phase LUTS vs. QoL
8.36 0.015
Severity of filling-storage phase LUTS vs.
QoL
1.20 0.548
Severity of Total LUTS vs. QoL
5.48 0.242
Severity of ED vs. QoL 10.16 0.006
36
This indicates that the more severe the voiding phase LUTS or ED, the poorer the QoL and vice versa.
CO-MORBIDITIES AND OTHER CLINICAL FINDINGS
There was low incidence of co-morbidities and their family history among LUTS patients (Table 8).
Table 8: Prevalence of Co-morbidities in patients
Frequency Percentage Hypertension
Yes No Total
30 80 110
27.3 72.7*
100 Diabetes
Yes No Total
16 94 110
14.5 85.5*
100 Heart disease
Yes No Total
4 106 110
3.6 96.4*
100 Stroke
Yes No Total
4 106 110
3.6 96.4*
100 Previous surgeries
Yes No
No response Total
34 58 18 110
30.9 52.7*
16.4 100
* Option with the highest frequency amongst respondents.
37
CHAPTER FIVE DISCUSSION
DEMOGRAPHY
The peak age range of 71years to 75 years and mean age of 65.8 ± 7.95 years in this study supports the predominance of LUTS among the ageing population as reported by other studies2,91,92. Kupelian et al2 in a Boston community health survey reported peak age range 60 years to 69 years. He studied the prevalence of lower urinary tract symptom and effect on quality of life in a racially and ethnically diverse random sample. Elliott et al91 did a hospital based study to find the correlation between obstructive LUTS and ED.
They noted peak age range of 70 years to 80 years with mean age of 68.2 years.
Hoesl et al92 reported mean age of 63.4 ± 8.5 years. They studied ED prevalence, bothersomeness and diagnosis in patients consulting urologists for benign prostatic syndrome (PBS)
THE INCIDENCE OF ED
The incidence of ED in this study was 63.6%. This incidence is slightly higher than the finding by Berrada et al22. They worked on the prevalence of ED and its correlates among Moroccan men residing in Casablanca. The age range was 25years to 85 years. They reported ED incidence of 53.6%. Spector et al93 also reported a lower incidence of 53% among 109 United Kingdom men aged 16years to 65 years. They worked on the prevalence and perceived aetiology of male sexual problems in a non-clinical sample. This study was among older patients in whom ED incidence is expected to be higher. This study was also restricted to patients who had LUTS, a compounding issue for ED. Thus it is
expected that ED incidence would be higher among them.
38
This is corroborated by a similar hospital-based study done by Hoesl et al92 which noted a prevalence range of 58.2% to 72.2%. Shaeer et al14 conducted a study on the prevalence of ED and its correlates among men attending primary care clinics in 3 countries: Pakistan, Egypt and Nigeria. They noted prevalence of 63.6%, 57.4% and 80.8% in Egypt, Nigeria and Pakistan respectively. The figure for Nigeria is relatively low when compared to the finding in this study. However their study population was multicentric with a lower age limit (35years). They also used a modified questionnaire for assessment of ED and showed no clear scoring system for the grades of ED for comparison with this study. These may explain the differences between this study and theirs. In the work of Berrada et al22 on the prevalence of ED and its correlates among Moroccan men residing in Casablanca, they rated 37.5%, 15.0% and 1.1% as having mild, moderate and severe ED respectively. In this study, 18% had mild ED while 27% had moderate ED. No case of severe ED was recorded. This may be difficult to explain considering the methods of study. Berrada et al22 used a modified questionnaire on having and keeping one erection during sexual intercourse to assess ED. In this study, ED was assessed with having and keeping erections during sexual intercourse over the preceding one month without the use of sex enhancing drugs.
The ED classification scores used in their study was not reported. The mild to moderate ED (score 12 to 16) group was not included in their work unlike in this study. This may also have contributed to a higher value of mild and lower value of moderate ED noted in their study. However, the study populations in these studies should also be considered in explaining this difference. The mean ED score of 16.90 ± 6.45 in this study was slightly higher than 10.14 ± 7.77 reported by Elliott et al in a similar hospital based study. However, they did not aim to find out the total or graded incidence of ED in their study. This difference in mean ED score may be explained by their method of patient selection. They recruited patients from both BPH clinic and ED clinic among which, whom with
39
cancer of the prostate and those who had undergone surgery for BPH and ED were excluded from analysis.
CORRELATION BETWEEN SEVERITY OF ED AND LUTS
In this study, there was a strong positive relationship (r = 26.15, P = 0.0001) between severity of ED and severity of total LUTS score without adjustment for the age or co-morbidities. This agrees with several epidemiological studies1,8, 91. Sara et al1 worked on relationship between LUTS and ED in a Boston community based study and noted that LUTS worsened as prevalence and severity of ED also worsened. However, the P-values were not stated. They further evaluated the association of specific LUTS with ED and noted that nocturia was the only item individually associated with ED. Thus, this theoretically translates to only filling-storage phase LUTS being associated with ED. This is not in keeping with finding in this study and that of Elliott et al91. However, the possibility of erroneous association exists considering that other components of filling-storage phase LUTS had no association with ED in their study. In a multinational survey of the ageing male -7, Rosen et al8 working on LUTS and male sexual dysfunction noted that the ED scores decrease with worsening LUTS across the studied age groups. When they controlled for age, they noted that LUTS severity was the strongest predictor of ED.
Conversely, Elliott et al91 who worked on correlation between voiding phase LUTS and ED reported a correlation between ED and voiding LUTS (r = -0.20, P = 0.006), but not to total LUTS (r = 0.17, P = 0.023). This study noted no correlation with graded voiding phase LUTS (P-value 0.096, Pearson’s chi-square 6.33). This difference might be due to the study method. Elliott et al were more objective in further assessment of voiding phase LUTS by uroflometric study and ultrasound determinant of postvoid residual urine volume. This may have added higher positive values and tendency of significance compared with
40
this study where I depended only on subjectivity with tendency of underreporting.
EFFECT OF ED AND LUTS ON QoL
Studies have noted that LUTS either singly or in combination with ED have negative impact on the QoL of ageing men22,92. In this study, 90.9% of patients were worried about LUTS while 50% were worried about ED (among LUTS patients that attempted sex). QoL indicated a significant inverse relationship with severity of voiding phase LUTS and severity of ED. The more severe the voiding phase LUTS or ED, the poorer the QoL and vice versa.
Berrada et al22 noted a similar finding where he reported a significant inverse correlation of satisfaction with sex life (cited on a scale from 1 = extremely satisfied to 5 = extremely dissatisfied) with the severity of ED (P<0.0001). The satisfaction with sex life values increased from 2.7 to 4.3 in patients with mild ED and severe ED respectively. The reason for this similarity is not clear.
However, they did not correlate for LUTS. Hoesl et al 92 indicated that decreased sexual activity due to ED is a major concern for LUTS patients and has an impact on their QoL. They studied the ED prevalence, bothersomeness and diagnosis in patients consulting urologists for benign prostatic syndrome (BPS). They described BPS as LUTS due to BPH and reported average ED QoL score of 55.7 for patients with LUTS using the German version of the QoL Med Questionnaire that scores 0 to 100. They also noted that 44.1% of LUTS patients with ED (N=5446) had poor QoL, 18.8% had good QoL, 38.8% were indecisive while 1.2
% gave no answer. This was assessed using Cologne assessment of male erectile dysfunction questionnaire. Although the effect of LUTS on QoL of the patients was not assessed, their finding on effect of ED on QoL of LUTS patients is slightly lower compared to this study. This study reported mean ED QoL score of
41
4.18 ± 1.22 (using QoL scale 1 to 6 modified from IPSS QoL scale) while 50%
of LUTS patients who attempted sex were worried about their ED. However, QoL was not stratified in this study. The difference may be due to patient selection and study method. Hoesl et al92 quantified ED and its impact on QoL among clinically diagnosed ED patients presenting with BPH-related LUTS using two versions of dissimilar QoL questionnaires. These questionnaires were sent out to patients to fill without any intervention by the researcher. The level of education of these patients was also not reported. However, both studies used validated questionnaires, thus should have credible results.
42
CHAPTER SIX
CONCLUSION/RECOMMENDATION
Erectile dysfunction is prevalent in LUTS patients in our environment, most of whom are illiterates. Its severity worsens with worsening LUTS. Since LUTS is age-related with increasing incidence in the ageing population, a rise in overall incidence of ED is expected with the current drift in population dynamics towards the older population. Considering the negative impact ED and LUTS (especially voiding phase component) have on QoL of these patients, I recommend that:
1. The management of patients with LUTS should involve a thorough evaluation and treatment for ED. This calls for increased awareness of these conditions to both the doctor and the patient.
2. The treatment of LUTS should be rationalized while aiming to improve the patients’ overall QoL.
3. Further research to elucidate the causal basis for this relationship is also needed.
43
REFERENCES.
1. Sara TB, Carol LL, Jenny LD, and John BM: Relationship between lower urinary tract symptoms and erectile dysfunction. J Urol 2008; 179:250-255 2. Kupelian V, Wei JT, O’Leary MP, Kusek JW, Litman HJ et al: Prevalence
of lower urinary tract symptoms and effect on quality of life in a racially and ethnically diverse random sample: Boston Area Community Health (BACH) Survey. Arch Intern Med 2006; 166: 2381-2387.
3. Robertson C, Link CL, Onel E, Mazzetta C, Keech M et al: The impact of lower urinary tract symptoms and comorbidity on quality of life: The BACH and UrEpiK studies. Br J Urol Int 2007; 99(2): 347-354.
4. Kevin M: Lower urinary tract symptoms and sexual dysfunction:
epidemiology and patholophysiology. Br J Urol Int. 2006; 97(2): 23-28.
5. Frankel SJ, Donovan JL, Peters TI, Abrams P, Dabhoiwala NF et al:
Sexual dysfunction in men with lower urinary tract symptoms. J Clin Epidemiol 1998; 51(8): 677-685.
6. Macfarlane GJ, Botto H, Sagnier PP, Teillac P, Richard F et al: The relationship between sexual life and urinary condition in the French community. J Clin Epidemiol 1996; 49: 1171-1176.
7. Mario P, Alberto A, Enrico A, Geraldo F, and Miguel S: The prevalence of erectile dysfunction among Brazilian men screened for Prostate cancer. Br J Urol Int 2009; 104(8): 1130-1133.
8. Rosen R, Altwein J, Boyle P, Kirby R, Lukacs B et al: Lower urinary tract symptoms and male sexual dysfunction. The Multinational Survey of the Aging Male (MSAM-7). Eur Urol 2003; 44: 637-649.
9. Constabile RA, Steers WB. How we can best characterize the relationship between erectile dysfunction and benign prostatic hyperplasia? J Sex Med 2006; 3: 676-681.
44
10. Rhoden EL, Teloken C, Sogari PR, and Vargas Souto CA: The use of the Simplified International Index of Erectile Function (IIEF-5) as a diagnostic tool to study the prevalence of erectile dysfunction. J Sex Med 2002;
14(4): 245- 250.
11. NIH Consensus Development Panel on Impotence: Proceedings of a conference held December 7-9, 1992, Bethesda, MD. JAMA 1993; 270:
83-90.
12. Feldman HA, Goldstein I, Hatzichristou DG et al: Impotence and its medical and psychosocial correlates: result of the Massachusetts Male Ageing Study. J Urol 1994; 151: 54-61.
13. Nwofor AME, Yeboah ED, and Dogunro AS: Sildenafil Citrate (VIAGRA
TM ) in the treatment of Male Erectile Dysfunction. A 6 week Flexible Dose Evaluation of Efficacy and Safety. Nig J of Health and Biomed.Sc 2002; 1:
45-48.
14. Shaeer KZM, Osegbe DN, Siddiqui SH, Razzaque A, Glasser DB:
Prevalence of erectile dysfunction and its correlates among men attending primary care clinics in three countries: Pakistan, Egypt, and Nigeria. Int J Impot Res 2003; 15(1): 8-14.
15. Levinson IP, Khalaf IM, Shaeer KZM and Smart DO: Efficacy and Safety of Sildenafil Citrate (ViagraR) for treatment of erectile dysfunction in men in Egypt and South Africa. Int J Impot Res 2003; 15(1): 25-29.
16. Burneeti AL. Nitric Oxide in the penis: Physiology and Pathology. J Urol 1997; 157: 320-324.
17. Girman CJ, Jacobson SJ, Tsukomoto T et al: Health related quality of life associated with lower urinary tract symptoms in four countries. Urol 1998;
51: 428-436.
45
18. Guest JF, Das Gupta R: Health related quality of life in UK- based population of men with erectile dysfunction. Pharmacoeconomics 2002;
20: 109-117.
19. Alison MM, Eric BR, Edward G, Dale BG, and Elizabeth AP: A Prospective Study of Lower Urinary Tract Symptoms and Erectile Dysfunction. Urol 2008; 179: 2321-2326.
20. Roberts RO, Jacobsen SJ, Rhodes T, Girman CJ, Guess HA et al: Natural history of prostatism: impaired health states in men with lower urinary tract symptoms. J Urol 1997; 157: 1711-1717
21. Laumann EO, Paik A and Rosen RC: Sexual dysfunction in the United States: prevalence and predictors. JAMA 1999; 281(6): 537-544.
22. Berrada S, Kadril N, Mechakra-Tahiri S and Nejjari: Prevalence of erectile dysfunction and its correlates: a population-based study in Morocco. Int J Impot Res 2003; 15(1): 3-7.
23. Aytac IA, Mckinlay JB, Krane RJ: The likely worldwide increase in erectile dysfunction between 1995 and 2025 and some possible policy consequencies. BJU Int 1999; 84: 50-56.
24. Data on File. New York, NY: Pfizer Inc.
25. Mckinlay JB: The worldwide prevalence and epidemiology of erectile dysfunction. Int J Impot Res 2000; 12: 6.
26. United Nations World Population Prospectus 1996. United Nations Population Division; New York: Department of Public Information Publications Department, 1997.
27. Braun MH, Sommer F, Haupt G, Mathers MJ, Reifenrath B et al: Lower urinary tract symptoms and erectile dysfunction: co-morbidity or typical
“Ageing Male”symptoms? Result of the “Cologne Male Survey”. Eur Urol 2003; 44: 588-594.
46
28. Boyle P, Robertson C, Mazzetta C, Keech M, Hobbs R et al: The association between lower urinary tract symptoms and erectile dysfunction in four centres: the UrEpik study. Br J Urol Int 2003; 92: 719-725.
29. Blanker MH, Bohnen AM, Groeneveld FP, Bernsen RM, Prins A et al:
Correlation for erectile and ejaculatory dysfunction in older Dutch men: a community-based study. J Am Geriatr Soc 2001; 49: 436-442.
30. Constance GB, Murray AM, Ichiro K, Edward G, Dale B et al: A Prospective study of risk factors for erectile dysfunction Urol 2006; 176:
217-221.
31. Aytac IA, Araujo AB, Johannes CB, Kleinman KP, and McKinlay JB:
Socioeconomic factors and incidence of erectile dysfunction: findings of the longitudinal Massachusetts Male Aging Study. Soc Sci Med 2000; 51:
771-778.
32. Feldman HA, Johannes CB, Derby CA, Kleinman KP, Mohr BA et al:
Erectile dysfunction and coronary risk factors: prospective results from the Massachusetts Male Aging Study. Prev Med 2000; 30: 328-338.
33. Pinnock CB, Stapleton AM and Marshall VR: Erectile dysfunction in the community: a prevalence study. Med J Aust 1999; 177: 353-357.
34. Prins J, Blanker MH, Bohnen AM, Thomas S and Bosch JL: Prevalence of erectile dysfunction: a systematic review of population-based studies. Int J Impot Res 2002; 14(6): 422-432.
35. Jacobsen SJ, Girman CJ, and Lieber MM: Natural history of benign prostatic hyperplasia. Urol 2001; 58(1): 5-16.
36. Alfredo N, Edson DM, Masafumi S, Mohd Ismail BMT and Dale BG:
Epidemiology of erectile dysfunction in four countries: Cross-national study of the prevalence and Correlates of erectile dysfunction. Urol 2003;
61: 201-206.
47
37. Guess HA, Arrighi HM, Metter EJ, and Fozard JL: Cumulative prevalence of prostatism matches the autopsy prevalence of benign prostatic hyperplasia. Prostate 1990; 17: 241-246.
38. Chute CG, Panser LA, Girman CJ, Oesterling JE, Guess HA et al: The prevalence of prostatism: a population-based survey of urinary symptoms J Urol 1993; 150(1): 85-89.
39. Raymond CR: Assessment of sexual dysfunction in patients with benign prostatic hyperplasia. Br J Urol Int 2006; 97(2): 29-33.
40. Rosen RC, Cappelleri JC, Smith MD, Lipsky J, and Pena BM:
Development and evaluation of an abridged 5-item version of the International Index of Erectile Function (IIEF-5) as a diagnostic tool for erectile dysfunction. Int J Impot Res 1999; 11: 319-326.
41. Barry MJ, Fowler FJ.Jr, O’Leary MP, et al: The American Urological Association Symptom Index for benign prostatic hyperplasia. The Measurement Committee of the American Urological Association. J Urol 1992; 148: 1549-1557.
42. Rosen RC, Riley A, Wagner G, Osterioh IH, Kirkpatrick J et al: The International index of erectile function (IIEF): a multidimensional scale of assessment of erectile dysfunction. Urol 1997; 49: 822-830.
43. Moore KL: Clinical Oriented Anatomy 3rd ed, Lippincott Williams and Wilkins, Baltimore USA, 1992: 308-312.
44. Jordan GH: The Penis/Scrotum: In Graham SD Jr, Glenn JF, Keane TE et al (eds): Glenn’s Urologic Surgery 6th ed, Lippincott Williams and Wilkins, Philadelphia, USA, 2004: 531-532.
45. John FR. Anatomy of the urogenital tract. In: Hanno PM, Malkowicz SB, Wein AL (Editors): Clinical Manual of Urology; 3rd ed, McGraw-Hill, Medical Publishing Division, New York, 2001: 42-44.