Associations between sexual satisfaction and function and the severity of lower urinary tract symptoms among men in a rural sub-Saharan African community.
In high resource countries, the association of erectile dysfunction (ED) with the presence of lower urinary tract symptoms (LUTS) is well documented [1-3]. Individually, ED and LUTS are known to affect quality of life; both are common within individuals. This has led researchers to propose possible common metabolic pathways . Risk factors identified for men to develop ED/LUTS include obesity, hypertension, diabetes, and metabolic syndrome, and clinical care pathways now include questionnaires to assess sexual function in men with LUTS . However, in Africa direct measures of the prevalence and correlates of ED with LUTS are unknown.
Erectile dysfunction is a primary component of sexual dysfunction and a central marker in related research; defined as the inability to maintain an erection sufficient for satisfying sexual activity, ED prevalence is said to be underestimated in developing countries [5-6], and epidemiologic data and studies of sexuality in old age are considered relatively scarce in Africa [5,7]. In 2007, Ojewole noted that although ED affects many African men, "authentic figures on the incidence and/or prevalence of the disease are not available in African countries" ; while this situation is now changing in sub-Saharan Africa the number of reports available is still small [9-13], except from Nigeria [5-6,1418].
Generalizing prevalence data from high resource countries to African regions is no longer appropriate, especially for ED and LUTS, because, while many factors associated with ED are likely similar worldwide, their distribution and prevalence do differ across countries [4,14,19,20]. It is likely that important risk factors and comorbidities vary in Africa, including physiology, diet and metabolism. Also, that cultural practices and beliefs which cannot be divorced from sexuality are relevant [7,16,17,21]. In addition, food security is an important potential factor that to date has not been considered, regional diets differ markedly in Africa compared to North America, Europe and Asia, and the incidence of metabolic syndrome and obesity are very different [22-24].
The World Health Organization (WHO) and African practitioners have called for more direct measures of the incidence and burden of disease due to ED and LUTS [5,19,25], in order to rationalize the advances in investigation, prevention and treatment in Africa suggested by organizations such as the American Urological Association (AUA), European Urological Association (EUA) and International Continence Society (ICS) .
In this context, a unique opportunity was offered to collect such data, by adding to a larger study evaluating associations between the severity of obstructive LUTS and care seeking behavior in rural Africa, conducted as part of a Grand Challenges Canada project [26,27].
The objectives were to: (1) quantify the sexual function and satisfaction and severity of LUTS among men in a rural Ugandan setting; (2) examine how severity of LUTS is associated with sexual function and satisfaction, and; (3) examine effects of demographic factors on sexual function and satisfaction in the context of LUTS.
This was a cross-sectional study with two cohorts of men aged 55 years or older which was based on another parallel study. The collection of the data reported was part of a larger survey on the burden of bladder disease in rural Africa; this Grand Challenges Canada (GCC) project [26,27] provided a unique opportunity to evaluate in parallel the association of sexual function and the severity of LUTS.
Study Population: The GCC study included data from two populations to ensure a broad cross section of symptom severity. We hypothesized that a cohort living with their symptoms in the community would predominantly have mild or moderate symptoms while a cohort presenting to a clinic would have more severe symptoms as they were seeking treatment due to the extent of bother from LUTS. Because the design of the principal study required both community and clinic cohorts to capture a full spectrum of symptom severity, data on sexual health was obtained from the same two cohorts. This met our purpose of evaluating sexual symptoms in men with mild, moderate and severe LUTS, and enabled us to test the hypothesis that, as in studies reported from industrialized countries, increasing LUTS severity is associated with a greater degree of sexual dysfunction in Ugandan men.
This was obtained from the University of British Columbia and Mbarara University of Science and Technology.
This took place in the rural district of Sheema in South Western Uganda in 2015. The method for the principal study has been reported previously; this required recruitment of study participants as a stratified sample, with at least 50 men >55 years of age enrolled from each of 5 villages in the district into one of two cohorts, those living in the community and those seeking care at a community health clinic due to bother from LUTS . Subjects volunteered in response to calls broadcast during local radio programs and posters displayed at the health clinic.
The International Prostate Symptom Score (IPSS) was used to quantify participants' LUTS as mild (0-7), moderate (8-19) or severe (20-35) , and the Epstein Inventory (EI) to assess their sexual functioning . The EI was chosen as it included 4 elements of sexual function and no validated version of the International Index of Erectile Function (IIEF) existed in the local language Banyankole. Additionally, local investigators felt that the wording of the questions in the EI were culturally appropriate and suited to translation by the interviewers into Banyankole. The four EI elements specific to sexual function address (1) satisfaction with level of sexual activity or lack (scored from 0 [low] to 10 [high]), (2) frequency of sexual drive (scored from 1 [low] to 8 [high]), frequency of erections when sexually stimulated (scored 1 [low] to 6 [high]), and 4 change in sexual performance over the past year (scored 1 [poor] to 7 [best]) .
After providing informed consent, all recruits to both cohorts were interviewed individually and alone by trained health professionals who asked the questions from the IPSS, and from the EI. To ensure comprehension of the questions and optimal capture of individual's responses, both the IPSS and EI were administered in the local dialect (Banyankole). For accuracy, forward translation was completed by faculty at Mbarara University, and to ensure the meaning and intention of the questions was maintained, expert back translation was done by the health care professionals who were to conduct the interviews, who were experienced in the application of comparable questionnaires , and fluent in both English and Banyankole. Translation and use of the interview format also allowed equitable participation in the study regardless of a participant's fluency in English, and their ability to read or write.
We included each participant's age, marital status, number of children, total number in household, current employment status, sufficiency of food available to the household and highest level of education completed.
This was a descriptive study, so a formal inference-based power calculation was not undertaken; however, the resulting sample size was sufficiently large (more than 175 subjects each in community and clinic cohorts) to give 80% power detecting small-to-moderate effects sizes - p = <0.05. Bivariate analysis was done to compare the two cohorts with respect to demographic variables (chi-square tests of independence for categorical variables, and two-sample t-tests for measurement variables). Each EI sexual functioning item was analyzed to correspond to the three categorical levels of the IPSS. Mean scores across IPSS categories with respect to each sexual function item were compared using one-way analysis of variance. The association between IPSS categories and the categorical versions of each item was assessed with a chi-square test. For each item, means scores with respect to: cohort (community or clinic), availability of sufficient food, marital status, and education level attained were compared using two-sample t-tests and one-way analysis of variance. Pearson correlations examined the association of the measurement scale items with age, and number of people in the household. Statistical analysis was carried out with IBM (USA) SPSS, Version 24.
A total of 415 men participated; 238 men in the cohort who were living in the community and 177 in the cohort who had presented to the local clinic because of bother with symptoms of LUTS. One subject declined to answer questions 2-4 in the EI; calculations were done on the number of valid responses.
The demographics of the two cohorts are shown in Table 1. On average, clinic respondents were significantly older (67.5 +/- 12.9 vs 62.9 +/- 12 years), had lower levels of education (91.5% vs. 81.5% primary or less), and had slightly smaller families (5.2 +/-3.1 vs. 5.9 +/-3.1). The cohorts were not significantly different with respect to marital status, number of children, salaried employment, or self-reported availability of sufficient food.
Clinic respondents had statistically significantly lower mean scores for satisfaction with the level of their sexual activity (4.94 +/- 1.93 vs. 6.11 +/-3.27 p=<.001 score range 0 [low] - 10 [high]) and frequency of erections (3.32 vs. 4.10) (p= <.001 score range 1 [low] - 8 [high]). See Table 2a. Cohorts were marginally significantly different with respect to mean change in sexual performance (p= .048), but not with respect to mean frequency of sexual drive.
Worse IPSS scores (using a three-level categorical version of the IPSS) accompanied worse mean scores on each sexual function item. See Table 2b. Differences across the IPSS categories were strongly statistically significant (p= <.001). Those with mild LUTS (IPSS 0-7) had low mean scores for EI sexual function items 2-4. A companion analysis also showed strongly significant association (p= < .001) between the three-level categorical versions of the outcome measures and the IPSS categorical version; worse sexual function scores were seen for cases with worse IPSS scores.
The effect of demographic variables on mean sexual function scores was examined. See Table 3. Level of education showed significant differences; higher education was associated with higher scores (less dysfunction) on each of the four EI items. Age was negatively correlated with scores on all four items, but the correlations were weak, with the highest negative correlation at -0.32 occurring for the item on frequency of erections. Similarly, with respect to marital status, frequency of sexual drive and change in function over time were significantly higher for married men. Whether the household had sufficient food was not a significant predictor of response for any of the sexual function items. And number of people in the household was not significantly correlated with any of the four items. The other quality of life dimensions measured by the EI and their association with LUTS have been reported previously; the clinic and community cohorts differed. Health related quality of life (HRQL), bother from LUTS, interference with daily living and worry were greater (p<0.001) in the clinic cohort. 
The opportunity to collect these unique data came because of a larger study where two cohorts of men from a rural African community were evaluated for their LUTS. We now report that in the population of men in these cohorts - men 55 years or older in rural Uganda - declining sexual health co-exits with LUTS. It appears that sexual function is adversely affected in relation to the severity of their LUTS; however, this finding may be more suggestive of a significant prevalence of sexual dysfunction despite LUTS.
The inclusion of two cohorts was based on the hypothesis that this would provide a broad range of LUTS symptom severity, with those living with their symptoms predominantly having mild or moderate disease and those presenting to the clinic having moderate or severe disease as they were seeking treatment due to the extent of bother from LUTS. Our findings are consistent with our hypothesis.
The separate analysis of the cohort presenting at the clinic confirmed that sexual dysfunction increases with worsening LUTS and as men age; lower mean satisfaction with sexual activity and frequency of erection was reported in this cohort. The rationale of comparing men presenting to clinic to those in the community is also relevant in this geographic region as clinics are difficult to reach due to distance and lack of transportation. These factors may act as barriers to patients seeking care for both ED and LUTS.
Importantly, men with mild LUTS also reported dissatisfaction with elements of their sexual drive, erection frequency and/or performance; the clinical significance of this is that LUTS probably in and of itself negatively impacts sexual function in the majority of those affected. Men who reported concern about their LUTS also reported in negative terms about their sexual function; sexual function satisfaction and erection frequency were also negatively influenced by advancing age.
Higher education was associated with better scores (less dysfunction) on all 4 Epstein questions; scores for frequency of sexual drive and change in function over time were significantly higher for single respondents; but interestingly, as this was an African study, whether a household had sufficient food was not a significant predictor of response for any sexual function item.
We suggest the data we report are relevant because the association of sexual dysfunction and LUTS as comorbidities has not been reported previously in men living in sub-Saharan Africa. In addition, our data are direct measures of the prevalence and correlates of sexual dysfunction and LUTS for a cohort of Ugandan men, in contrast to most regional prevalence figures for African regions which are estimates based on extrapolations of symptom burden measured in other populations [14,30]. Furthermore, the association between sexual dysfunction and LUTS we report corresponds to evidence from epidemiological studies in North America and Europe [1-3].
WHO has called for more quantitative data from LMICs , and the relevance of region-specific data in Africa is increasing as advanced health care is planned and delivered [19,31]. Such care in the context of sexual dysfunction and LUTS is being called for by practitioners in sub-Saharan Africa [5,6,15], in addition to being advocated internationally, e.g. by the AUA, EUA and ICS . Our study now contributes such region-specific quantitative data on sexual dysfunction and LUTS.
Although we did not find that whether or not a household had sufficient food was a predictor of sexual dysfunction, we suggest that this variable has relevance in prevalence studies, particularly in Africa. This is because poverty, malnutrition and food insecurity are recognized to negatively impact social determinants of health, and adults who are food insecure are at an increased risk of developing chronic diseases. [34,35] While no prior research has explored an association of food security and the availability of adequate food with either ED or LUTS, we suggest that the issue of food security should still be included in future studies to either confirm or refute our findings, and further explore the potential association with increased risk of chronic disease. Food security varies globally; in Canada it is relevant that refugee populations and those living in poverty are particularly vulnerable.
Sexuality and related practices and beliefs were explored by Agunbiade amongst older Yoruba people where the impact of cultural practices and spiritual dimensions on sexual decline were emphasized , and by van de Geest in Ghana where waning 'strength' (equated by men with potency and penetration) was seen as central . Shaeer reported on the prevalence of erectile dysfunction and its correlates amongst men attending primary care in Nigeria; age-standardized prevalence estimates for any degree of ED were similar in Nigeria (57%) to those in Egypt (64%) but substantially lower to those in Pakistan (81%) . As in our study, age was a very strong correlate, as was marital status. While we found that single men reported higher levels of sexual dissatisfaction, Shaeer found that those separated, widowed or divorced were three times more likely to have moderate to severe ED than married men . As in the study we conducted, Claramonte studied a rural population in Uganda; but 204 of the 902 men enrolled were positive for HIV. The ED rate was 47.8% overall and 36.8% in those HIV negative; the influence of LUTS and diet were not explored  Mutagaywa reported the prevalence of ED and associated factors among diabetic men in Tanzania . ED severity was significantly correlated with increased age and significantly predicted by the presence of peripheral vascular disease and peripheral neuropathy; those with ED were more likely to suffer in other sexual domains, but no lifestyle component was associated. Said also reported data in diabetic men from Ethiopia , and Olugenga-bello noted an additional association with alcohol consumption and smoking in Nigeria .
Prior research related to LUTS in Africa has utilized the IPSS, or a visual version of components of the scale ; but data specific to sub-Saharan Africa remain limited; in 2012 Chokkalingam reported no prior population-based studies of BPH in Western Africa . Bajunirwe has estimated that the burden of LUTS in Uganda and sub-Saharan Africa as a whole is high , and Oliapade-Olaopa  reported that in Nigerian men LUTS severity is related to age.
While the association between ED and LUTS is established by epidemiological evidence from North America and Europe [1-3], when searching the literature linking the terms sexual dysfunction, ED and LUTS with Africa, the items found predominantly relate to studies of men of African origin living abroad. Reported differences in prevalence and etiology in these data raise the possibility of racial disparity [16,36], but future research is required to establish what factors if any may be involved.
Prior research on ED from sub-Saharan Africa [5-18] has predominantly relied on the International Index of Erectile Function (IIEF-5) . There is a validated version of the 5 item IIEF in Swahili  and forward translations into Tigregana  and into Kiswahili (15 item IIEF)  are reported. However, no validated translation exists for Banayankole. The Erection Hardness Score and Aging Male Symptoms Scale [9,33] have also been used in African populations. Other authors have used a single ED assessment question. Shaeer et al  reported validating the NIH Consensus Conference definition of ED 'the inability to attain and/or maintain penile erection sufficient for satisfactory sexual intercourse' in a study which included men from Nigeria. While this is an important question to validate, the broader content of the Epstein Inventory provides more information.
With the association of ED with LUTS now identified in Africa, and the prevalence of LUTS projected to increase as Africa's population ages , future studies on LUTS and associated ED are probable. We recognize that having validated translations of the commonly reported tools for evaluating sexual function and is desirable and will enable comparison with existing studies in the literature. A challenge in this context is that the number of African dialects is so large (there are 65 in Uganda alone). The practical reason for use of the EI in this study was the preference of local investigators regarding culturally appropriate language and ease of translation. The EI does capture data on sexual function and LUTS, and uses terminology and definitions approved by international agencies beyond Canada, such as the AUA, EUA and ICS.
We recognize limitations in what we report. The EI has no bona fide measure of ED, using instead surrogates such as frequency of erection, ability to obtain, and ability to maintain an erection sufficient for sexual activity. No history apart from the validated questionnaires or physical examination to assess respondents for underlying causes of sexual dysfunction or LUTS such as diabetes or hypertension were completed. Men in both the community and clinic cohorts came voluntarily for screening; hence generalizability of our results may be limited. This was also a community where economic status, employment and levels of educational attainment and literacy were low; however, this was likely a similar situation to that existing in many other parts of Africa. Because data collection came from interviews conducted using the local language, translation of the IPSS and EI questionnaires was required, followed by translation of the responses back into English, but the translated questions were checked by health professionals for accuracy and back translated to confirm that meaning and intention were maintained; the interviewers were health care providers with experience administering the IPSS and comparable instruments [26,27]. One subject declined to answer questions 2-4 in the EI questionnaire; however, complete data sets were obtained from 414/415 subjects. In a statistical context, this one missing case does not contribute any bias.
As estimates for the future global increase in the prevalence of both sexual dysfunction and LUTS are predicted to particularly affect Africa [30,37,39], clinicians need to be aware that LUTS and sexual dysfunction coexist, so as to inquire and educate patients appropriately and utilize treatment options available for both conditions. Further basic science investigation and applied research is also warranted to establish what the causal links are, and how the burden of these two conditions can be reduced in Africa.
Ugandan men over 55 years of age reported dissatisfaction with their level of sexual activity, frequency of sexual drive, ability to have erections and the change in their sexual performance over the past year that was statistically correlated with the severity of their LUTS. These data are the first from Africa to report similar findings to the evidence from North America and Europe that sexual dysfunction and lower urinary tract symptoms are strongly linked.
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Figures and Tables
Andrew J. Macnab (1,2); Lynn Stothers (2,3); Jonathan Berkowitz (4,5); Stacy Elliott (6); Francis Bajunirwe (7)
(1) Stellenbosch Institute for Advanced Study, Wallenberg Research Centre at Stellenbosch University, South Africa; (2) Department of Urologic Sciences, University of British Columbia, Vancouver, BC, Canada; (3) School of Population and Public Health Division of Global Health, University of British Columbia, Vancouver, BC, Canada and Principal Investigator International Collaboration on Repair Discover (ICORD); (4) Sauder School of Business, University of British Columbia, Vancouver, BC, Canada; (5) Department of Family Practice, University of British Columbia, Vancouver, BC, Canada; (6) BC Centre for Sexual Medicine, University of British Columbia, Vancouver, BC, Canada; (7) Department of Community Health, Mbarara University of Science and Technology, Mbarara, Uganda
Acknowledgments: Dr. Macnab received a competitive grant from Grand Challenges Canada Stars in Global Health (Award number 0382-01) to evaluate the use of novel non-invasive optical technology to screen for bladder problems impacting health outcomes in Uganda. The collection of the data reported was part of a larger survey on the burden of bladder disease; funds were used for ethical approval, translation/validation of survey tools, and data collection.
Table 1. Socio demographic variables of community and clinic cohort respondents Community Clinic Total (n=238) (n=177) (n=415) Age, mean (SD) 62.9 (12.0) 67.5 (12.9) 64.9 (12.3) Marital status Married 217 (91.2%) 161 (91.0%) 378 (91.1%) Divorced 3 (1.3%) 3 (1.7%) 6 (1.4%) /separated Widowed 14 (5.9%) 13 (7.3%) 27 (6.5%) Single 4 (1.7%) 0 (0.0%) 4 (1.0%) Number of children 7.3 (3.4) 7.8 (3.5) 7.5 (3.4) Total persons 5.9 (2.7) 5.2 (3.1) 5.6 (2.9) per household Salaried employment Yes 217 (91.2%) 165 (93.2%) 382 (92.0%) No 21 (8.8%) 12 (6.8%) 33 (8.0%) Household food sufficiency Yes 88 (37.0%) 78 (44.1%) 166 (40.0%) No 150 (63.0%) 99 (55.9%) 249 (60.0% Education Never attended 39 (16.4%) 59 (33.3%) 98 (23.6%) Primary 155 (65.1%) 103 (58.2%) 258 (62.2%) Secondary 27 (11.3%) 11 (6.2%) 38 (9.2%) Post-secondary 17 (7.1%) 4 (2.3%) 21 (5.1%) /tertiary p (*) Age, mean (SD) 0.001 (*) Marital status Married 0.33 (*[dagger]) Divorced /separated Widowed Single Number of children 0.13 (*) Total persons 0.016 (*) per household Salaried employment Yes 0.45 (**) No Household food sufficiency Yes 0.15 (**) No Education Never attended <0.001 (**) Primary Secondary Post-secondary /tertiary (*) Two-sample t-test. (**) Chi-square test. ([dagger]) Married vs. all others: p=0.94. Table 2. questionnaire results Q1: Activity satisfaction: How satisfied are you with the level of sexual activity or lack? Q2: Drive frequency: How frequently have you felt sexual drive? Q3: Erection frequency: How often are you able to have erections when sexually stimulated? Q4: Performance change: Over the past year how has sexual performance changed? 2A. Comparison of sexual function item means by cohort Community Clinic (n=238) (n=176) Mean (SD) Mean (SD) P (*) 95% CI for difference Q1: Activity 6.11 (3.27) 4.94 (3.28) <0.001 (0.53,1.81) satisfaction Score range 0-10 Q2: Drive frequency 4.26 (1.76) 4.41 (1.93) 0.41 (-0.52,0.21) Score range 1-8 Q3: Erection 4.10 (1.72) 3.32 (1.22) <0.001 (0.48,1.08) frequency Score range 1-6 Q4: Performance 2.93 (1.29) 3.23 (1.84) 0.048 (-0.61, -0.003) change Score range 1-7 2B. Comparison of sexual function item by International Prostate Symptom Score (IPSS) Mild Moderate Severe Total (0-7) (8-19) (20-35) (n=414) (n=164) (n=167) (n=83) Mean (SD) Mean Mean Mean (SD) (SD) (SD) Q1: Activity 7.34 (2.68) 4.72 (3.25) 4.02 (3.14) 5.62 (3.32) satisfaction Score range 0-10 Q2: Drive 4.88 (1.63) 4.05 (1.80) 3.80 (2.00) 4.33 (1.83) frequency Score range 1-8 Q3: Erection 4.59 (1.44) 3.40 (1.44) 2.88 (1.31) 3.77 (1.57) frequency Score 1-6 Q4: Performance 3.58 (1.21) 2.81 (1.54) 2.53 (1.86) 3.06 (1.55) change Score range 1-7 p (**) Q1: Activity <0.001 satisfaction Score range 0-10 Q2: Drive <0.001 frequency Score range 1-8 Q3: Erection <0.001 frequency Score 1-6 Q4: Performance <0.001 change Score range 1-7 (*) Two-sample t-test. (**) One-way ANOVA F-test. CI: confidence interval; SR: standard deviation. Table 3. Comparison of sexual function item means by demographics Does household have sufficient food? Sufficient Insufficient food (n=166) food (n=248) Mean (SD) Mean (SD) p (*) 95% CI for difference Q1: Activity 5.51 (3.36) 5.69 (3.30) 0.58 (-0.84, 0.47) satisfaction Q2: Drive frequency 4.22 (1.80) 4.40 (1.85) 0.34 (-0.54, 0.19) Q3: Erection 3.66 (1.58) 3.85 (1.57) 0.23 (-0.50, 0.12) frequency Q4: Performance 3.02 (1.59) 3.09 (1.53) 0.67 (-0.37, 0.24) change Marital status Married Unmarried (n=378) (n=36) Mean (SD) Mean (SD) p (*) 95% CI for difference Q1: Activity 5.57 (3.30) 6.11 (3.56) 0.35 (-1.68,0.60) satisfaction Q2: Drive 4.39 (1.76) 3.72 (2.40) 0.037 (0.04,1.29) frequency Q3: Erection 3.78 (1.56) 3.71 (1.79) 0.83 (-0.49,0.61) frequency Q4: Performance 3.01 (1.54) 3.63 (1.65) 0.023 (-1.16, -0.09) change Education level None Primary Secondary+ Total (n=98) (n=258) (n=58) (n=414) Mean Mean Mean (SD) Mean (SD) (SD) (SD) Q1: Activity 5.24 (3.49) 5.52 (3.33) 6.66 (2.81) 5.62 (3.32) satisfaction Q2: Drive 3.95 (1.82) 4.34 (1.87) 4.90 (1.51) 4.33 (1.83) frequency Q3: Erection 3.32 (1.54) 3.79 (1.57) 4.47 (1.42) 3.77 (1.57) frequency Q4: Performance 2.80 (1.60) 3.05 (1.56) 3.56 (1.35) 3.06 (1.55) change Education level p (**) Q1: Activity 0.028 satisfaction Q2: Drive 0.007 frequency Q3: Erection <0.001 frequency Q4: Performance 0.012 change (*) Two-sample t-test. (**) One-way ANOVA F-test. CI: confidence interval; SR: standard deviation.
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|Title Annotation:||Original Research|
|Author:||Macnab, Andrew J.; Stothers, Lynn; Berkowitz, Jonathan; Elliott, Stacy; Bajunirwe, Francis|
|Publication:||Canadian Urological Association Journal (CUAJ)|
|Date:||Jun 27, 2019|
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