Abstract
Socioeconomic status is a risk factor for poor disease prognosis. No studies of patients with ulcerative colitis (UC) have investigated the association between socioeconomic status and erectile dysfunction (ED), although UC is independently positively associated with ED. Therefore, the purpose of this survey to evaluate this issue in Japanese patients with UC. The study enrolled 165 patients with UC. Education status (low, middle, high) and household income (low, middle, high) were classified in three groups using self-administered surveys. The information regarding the Sexual Health Inventory for Men (SHIM) was obtained using self-administered questionnaires. The definition of mild to moderate or severe ED and severe ED was SHIM score <17 and SHIM score <8, respectively. The prevalence of mild to moderate or severe ED and severe ED was 64.9% and 47.9%, respectively. In crude analysis, household income was inversely associated with mild to moderate or severe ED and severe ED. After adjustment for age, current drinking, current smoking, exercise habit, body mass index, mucosal healing, and duration of UC, high household income was independently and inversely associated with mild to moderate or severe ED (adjusted odds ratio [OR] 0.23, 95% confidence interval [CI] [0.05, 0.93], p for trend = .038) and severe ED (adjusted OR 0.26, 95% CI [0.07, 0.85], p for trend = .024). In contrast, no association between education status and ED was found. In conclusion, household income was independently and inversely associated with ED in Japanese UC patients.
Keywords: ulcerative colitis, education, income, erectile dysfunction
Introduction
Erectile dysfunction (ED) is defined as the persistent or recurrent inability to achieve and/or maintain an erection sufficient for sexual intercourse (Hatzimouratidis et al., 2010). Ulcerative colitis (UC) is an inflammatory bowel disease (IBD) that causes inflammation and ulcers in the colon. The prevalence of UC is increasing worldwide, and the increase is prominent in Asian countries (Ng et al., 2017). Meta-analysis regarding sexual dysfunction and IBD shows a positive association between UC and ED (Wu et al., 2022).
Socioeconomic status is associated with the onset and prognosis of several chronic diseases. Socioeconomic status is recognized as a powerful predictor of health status. Several studies have shown the association between socioeconomic status and ED. Low socioeconomic status is associated with the onset of ED in Western countries (Aytaç et al., 2000; Selvin et al., 2007; Weber et al., 2013; Macdonald et al., 2023). Furthermore, the poor socioeconomic status is positively associated with prevalence of ED in U.S. population-based studies (Kupelian et al., 2008). On the other hand, in a Chinese study, no association between low income and ED was observed after adjustment, although low income was positively associated with ED in crude analysis (Zhang et al., 2017).
Similarly, the poor socioeconomic status is associated with the clinical outcomes in patients with UC (Kitahata et al., 2022; Nordenvall et al., 2021; Wardle et al., 2017). The close association between UC and ED was observed in some previous studies (Friedman et al., 2018; Kao et al., 2016; Wu et al., 2022). The reasons for the high prevalence of EDs in patients with UC remain unclear. In Japan, most medical costs for symptomatic UC are covered by medical insurance, regardless of household income. Insurance systems might mitigate the impact of low socioeconomic status on comorbidities in patients with UC. There is also little evidence on whether the insurance system weakens the association between socioeconomic status and ED in the UC. In addition, there have been no studies investigating the characteristics of ED patients in UC. In clinical practice, identifying the characteristics of ED patients might be useful for screening and preventing UC in the future. In addition, an international survey revealed that the prevalence of ED in Japan is higher than that in other countries (Rosen et al., 2003).
The aim of this survey is to evaluate the association between socioeconomic status and ED in Japanese UC patients.
Methods
Study Population
The present study employed a cross-sectional design utilizing baseline data from a prospective cohort study. The study subjects were 203 Japanese male patients diagnosed at the Department of Gastroenterology and Metabology, Ehime University Graduate School of Medicine, Japan. The study was conducted between 2015 and 2019. All participants provided written informed consent before enrollment and answered a self-administered questionnaire. The study protocol was developed and approved by Ehime University Ethics Committee (approval number 1505011) in accordance with the 1964 Declaration of Helsinki and subsequent ethical guidelines.
Measurements
Self-administered questionnaires were used to obtain information on smoking habits, alcohol consumption, regular exercise habits (at least once a week), education, and household income. Information on UC medication, disease severity, and duration of UC was also obtained from medical records. Body mass index (BMI) was calculated by dividing weight in kilograms by the square of height in meters. The definition of obesity was based on BMI being ≥25.
Definition of Mucosal Healing
Mucosal healing (MH) was defined as a Mayo Endoscopic Score (MES) category of 0 (Schroeder et al., 1987). Certified endoscopists assessed endoscopic activity by performing a complete colonoscopy and reporting endoscopic findings and key images. One endoscopist was responsible for MES and MH scoring at approximately the same time as this study. The endoscopist was blinded to other findings.
Assessment of ED
The Sexual Health Inventory for Men (SHIM) is a validated, shortened, five-question version of the 15-question International Index of Erectile Function (IIEF) questionnaire (Rosen et al., 1999). In the present study, the following outcomes were employed: (a) mild to moderate or severe ED: SHIM score <17 and (b) severe ED: SHIM score <8.
Statistical Analysis
The patients’ educational qualification and household income was categorized into each three groups: low, middle, and high. Low education corresponds to junior high school and high school, ≤12 years; middle education, junior college, vocational technical school, and 4-year college dropout, 13–15 years; and high education, college or graduate school, 16 years or more. Low income corresponds to earning ≤2,999,999 Japanese yen/year; middle income, 3,000,000–7,999,999 Japanese yen/year; and high income, ≥8,000,000 Japanese yen/year. Age was divided into tertiles as follows: (a) young age, <43 years; (b) middle age, 43–62 years; and (c) elder age, ≤63 years. Estimations of crude odds ratios (ORs) and their 95% confidence intervals (CIs) for ED in relation to education status and household income were performed using logistic regression analysis. Multiple logistic regression analyses were employed to adjust for potential confounding factors. These factors were selected a priori and included age, current drinking, current smoking, exercise habit, BMI, MH, and duration of UC. Statistical analyses of this survey were conducted using SAS software package version 9.4 (SAS Institute Inc., Cary, NC).
Results
Study Characteristics
The clinical characteristics of participants in this survey are presented in Table 1. After the exclusion of incomplete data, 81.2% of patients (165/203) were analyzed in this study. The mean age, prevalence of mild to moderate or severe ED, and severe ED was 52.1 years, 64.7% (107/165), and 47.9% (79/165), respectively. The proportion of participants with low education (≤12 years), middle education (13–15 years), and high education (≥16 years) was 53.9% (89/165), 13.9% (23/165), and 32.1% (53/165), respectively. The percentage of low income, middle income, and high income was 21.1% (35/165), 46.1% (76/165), and 32.7% (54/165), respectively.
Table 1.
Clinical Characteristics of 165 Study Participants
| Variables | n (%) |
|---|---|
| Age, years, mean ±SD | 52.1 ± 16.9 |
| Disease extent (pancolitis/left-sided/proctitis/others) | 75/41/77/5 |
| Duration of UC, year, mean ±SD | 7.7 ± 8.1 |
| BMI, mean ±SD | 23.24 ± 4.38 |
| Current smoking (%) | 16 (9.7) |
| Current drinking (%) | 77 (46.7) |
| Exercise habits (%) | 74 (44.9) |
| Medication | |
| 5-aminosalicylates (%) | 155 (93.9) |
| Prednisolone (%) | 35 (21.2) |
| Thiopurines | 24 (14.6) |
| TNF-α monoclonal antibody (%) | 6 (3.6) |
| Mayo endoscopic subscore, mean ±SD | 1.26 ± 0.91 |
| Complete mucosal healing (Mayo endoscopic subscore < 1) (%) | 40 (24.2) |
| Education, years | |
| Low (≤12 years) (%) | 89 (53.9) |
| Middle (12–16 years) (%) | 23 (13.9) |
| High (≥16 years) (%) | 53 (32.1) |
| Household income, Japanese yen/year | |
| Low income (≤2,999,999) (%) | 35 (21.1) |
| Middle income (3,000,000–7,999,999) (%) | 76 (46.1) |
| High income (≥8,000,000) (%) | 54 (32.7) |
| SHIM score, mean ±SD | 11.0 ± 8.3 |
| SHIM score <8 | 79 (47.9) |
| 8 ≤ SHIM score < 17 | 28 (17.0) |
| 17 ≤ SHIM score | 58 (35.2) |
| Severe erectile dysfunction (SHIM score <8) | 79 (47.9) |
| Mild to moderate or severe erectile dysfunction (SHIM score <17) | 107 (64.9) |
BMI, body mass index; UC, ulcerative colitis; SD, standard deviation; TNF, tumor necrosis factor; others: right-sided, segmental colitis, and postoperative patients (lack of any preoperative medical records for postoperative patients).
The Association Between Age and Socioeconomic Status
The association between age and socioeconomic status is summarized in Table 2. In the elderly age group, the percentages of individuals with low education and low household income were 73.7% (42/57) and 38.6% (22/27), respectively. The proportion of low education and low income increases with age.
Table 2.
Crude and Adjusted Odds Ratios and 95% Confidence Intervals for Education Status, Household Income, and ED in Relation to Aging
| Variable | Young age (n = 52) | Middle age (n = 56) | Elder age (n = 57) | p Value |
|---|---|---|---|---|
| Severe ED, n (%) | 16/52 (30.8) | 20/56 (35.7) | 43/57 (75.4) | .001 |
| Mild to moderate or severe ED, n (%) | 23/52 (44.2) | 33/56 (58.9) | 51/57 (89.5) | .001 |
| Education | ||||
| Low, n (%) | 23/52 (44.2) | 24/56 (42.9) | 42/57 (73.7) | |
| Middle, n (%) | 10/52 (19.2) | 10/56 (17.9) | 3/57 (5.3) | |
| High, n (%) | 19/52 (36.5) | 22/56 (39.3) | 12/57 (21.1) | .004 |
| Household income | ||||
| Low, n (%) | 5/52 (9.6) | 8/56 (14.3) | 22/57 (38.6) | |
| Middle, n (%) | 37/52 (71.2) | 39/56 (69.6) | 29/57 (50.9) | |
| High, n (%) | 10/52 (19.2) | 9/56 (16.1) | 6/57 (10.5) | .003 |
ED, erectile dysfunction.
The Association Between Socioeconomic Status and Life Style Habits
In Table 3, socioeconomic status and lifestyle habits were presented. Our analysis indicates that exercise habits show an increasing trend with rising income and education, but the differences were not statistically significant in this cohort. Only drinking habit was observed to increase with income status (p = .035).
Table 3.
Association Between Socioeconomic Status in Relation to Lifestyle Habits in This Cohort
| Variable | Exercise habits (n = 74) | Smoking (n = 16) | Drinking (n = 77) | Obesity (n = 41) |
|---|---|---|---|---|
| Education | ||||
| Low, n (%) | 34/89 (38.2) | 8/89 (9.0) | 40/89 (44.9) | 24/89 (27.0) |
| Middle, n (%) | 11/23 (47.8) | 2/23 (8.7) | 10/23 (43.5) | 8/23 (34.8) |
| High, n (%) | 29/53 (54.7) | 6/53 (11.3) | 27/53 (50.9) | 9/53 (17.0) |
| p Value | .152 | .891 | .745 | .197 |
| Household income | ||||
| Low, n (%) | 16/35 (45.7) | 4/35 (11.4) | 10/35 (28.6) | 7/35 (20.0) |
| Middle, n (%) | 44/105 (41.9) | 8/105 (7.6) | 56/105 (53.3) | 26/105 (24.8) |
| High, n (%) | 14/25 (56.0) | 4/25 (16.0) | 11/25 (44.0) | 8/25 (32.0) |
| p Value | .443 | .441 | .035 | .574 |
Association Between Socioeconomic Status and ED
The relationship between socioeconomic status and ED in this cohort is displayed in Table 4. In crude analysis, both middle and high income were inversely associated with mild to moderate or severe ED (middle income: crude OR 0.27, 95% CI [0.09, 0.70]; and high income: crude OR 0.15, 95% CI [0.05, 0.50]). After adjusting confounding factors, high income but not middle income was independently and inversely associated with mild to moderate or severe ED (adjusted OR 0.21, 95% CI [0.04, 0.88], p for trend = .036). Similar relationship between household income and severe ED was found in crude analysis (middle income: crude OR 0.31, 95% CI [0.13, 0.70], and high income: crude OR 0.19, 95% CI [0.06, 0.56]). Even after adjustment, only high income was independently and inversely associated with severe ED (adjusted OR 0.26, 95% CI [0.07, 0.85], p for trend = .024). On the other hand, in crude analysis, middle education was inversely associated with mild to moderate or severe ED and severe ED (middle education: crude OR 0.25, 95% CI [0.10, 0.65], and high income: crude OR 0.30, 95% CI [0.10, 0.80]). However, after adjustment for the confounding factor, education status was not associated with mild to moderate or severe ED and severe ED.
Table 4.
Crude and Adjusted Odds Ratios and 95% Confidence Intervals for Education Status and Household Income in Relation to ED
| Variable | Prevalence (%) | Crude OR (95% CI) | Adjusted OR (95% CI) |
|---|---|---|---|
| Mild to moderate or severe ED | |||
| Education | |||
| Low | 65/89 (73.0) | 1.00 | 1.00 |
| Middle | 10/23 (43.5) | 0.28 (0.11–0.73) | 0.41 (0.14–1.20) |
| High | 32/53 (60.4) | 0.56 (0.27–1.16) | 0.81 (0.35–1.88) |
| p for trend | .563 | ||
| Household income | |||
| Low | 30/35 (85.7) | 1.00 | 1.00 |
| Middle | 65/105 (61.9) | 0.27 (0.09–0.70) | 0.46 (0.13–1.38) |
| High | 12/35 (48.0) | 0.15 (0.04–0.50) | 0.23 (0.05–0.93) |
| p for trend | .038 | ||
| Severe ED | |||
| Education | |||
| Low | 48/89 (53.9) | 1.00 | 1.00 |
| Middle | 6/23 (26.1) | 0.30 (0.10–0.80) | 0.40 (0.12–1.17) |
| High | 25/53 (47.2) | 0.76 (0.38–1.51) | 0.95 (0.44–2.06) |
| p for trend | .812 | ||
| Household income | |||
| Low | 25/35 (71.4) | 1.00 | 1.00 |
| Middle | 46/105 (43.8) | 0.31 (0.13–0.70) | 0.47 (0.18–1.16) |
| High | 8/25 (32.0) | 0.19 (0.06–0.56) | 0.26 (0.07–0.85) |
| p for trend | .024 | ||
Adjusted for age, current drinking, current smoking, exercise habit, BMI, mucosal healing, and duration of ulcerative colitis. OR, odds ratio; CI, confidence interval.
Discussion
Household income but not education status was independently and inversely associated with mild to moderate or severe ED and severe ED in male patients with UC. This is the first study to demonstrate an inverse relationship between socioeconomic status and ED in patients with UC.
The association between socioeconomic status and ED was reported in Western population-bases studies. In two U.S. and an Australian population-based studies, low education was associated with the onset of ED (Aytaç et al., 2000; Selvin et al., 2007; Weber et al., 2013). In another U.S. study, low income was associated with the onset of ED (Macdonald et al., 2023). In a U.S. study of 2,301 men, socioeconomic status is significantly positively associated with the prevalence of ED (Kupelian et al., 2008). The results of this study are consistent with the findings in Western population-based studies.
On the other hand, only one Asian study investigates this issue. In a Chinese study of 5,210 men, low income is not independently associated with the prevalence of ED after adjustment for confounding factors, while the prevalence of ED is higher in lower income group (Zhang et al., 2017). This discrepancy is due to lifestyle including diet habit, age distribution, education, and income status of each country and can be partially explained by the healthcare system.
Few studies demonstrated the association between socioeconomic status and clinical outcomes in UC patients. According to a Canadian study, low socioeconomic status was associated with the mortality of UC (Nordenvall et al., 2021). In a Swedish retrospective study, neither education nor income was associated with restorative surgery in patients with UC (Wardle et al., 2017). In a Japanese study of patients with UC (Kitahata et al., 2022), a positive relationship between education status and MH was reported in only older but not younger UC patients. Notably, in Japan, most medical costs for symptomatic UC are covered by medical insurance, regardless of household income. While medical insurance might mitigate the impact of low socioeconomic status on comorbidities in Japan, the current study’s results suggest that Japan’s insurance systems may not fully mitigate the association between low income and ED in patients with UC. In general, education is closely associated with favorable health habits, as previously observed (Murakami et al., 2023). The data also suggest that higher education may serve as a protective factor against ED. In this cohort, no substantial association between education and ED was found. Aging is a well-known risk factor for ED, and in this cohort, higher education decreases with age. EDs may be more prevalent among the less educated, particularly among the elderly.
The mechanisms underlying this inverse relationship between household income and ED remain still unclear. High income might be protective for ED via high physical activity (Minami et al., 2018; Schultz et al., 2018), suitable nutrition (McMaughan et al., 2020; Nowroozi, 2018), low stress (Cohen et al., 2006), medication adherence (Goodhand et al., 2013), and access to healthcare (Andrulis, 1998). Further investigation is expected to clarify the unknown factors related to high income.
This study has several limitations. First, proof of a causal relationship between high income and ED is unclear given the cross-sectional study design. Second, the information on socioeconomic status was obtained using a no-validated questionnaire, any possible misclassification of nondiscriminatory exposure would introduce bias toward the null hypothesis. Third, employment status strongly affected socioeconomic status, but data on patients’ employment status are lacking. Fourth, this cohort might not be fully representative of all Japanese patients with UC. However, the mean age and the use rates of steroid and azathioprine in this cohort align with those reported in national surveys on UC in Japan (Matsuoka et al., 2021). Finally, countries differ in their education, income, and healthcare systems, which may make it difficult to generalize the findings of this study to other ethnic groups.
Conclusions
Household income but not education status was independently and inversely associated with ED in Japanese patients with UC. Further study regarding socioeconomic status and sexual dysfunction is warranted in patients with UC in the future.
Acknowledgments
The authors would like to thank Keitarou Kawasaki, Yuji Mizukami, Satoshi Imamine, Masamoto Torisu, Harumi Yano, Makoto Yano, Masato Murakami, Masumi Hino, and Tomo Kogama.
Footnotes
Authors’ Contributions: Conception and design: ET, SF, and YH; material preparation and data collection: ET, KT, KS, KT, YH, SY, TN, SS, NS, HM, KO, HT, YY, and YI; data analysis: SF; interpretation of data: ET, SF, TM, YH; first draft of the manuscript written by ET, SF, and OY; supervision: ET and YI. All authors read and approved the final manuscript.
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding: The author(s) received no financial support for the research, authorship, and/or publication of this article.
Ethical Considerations: The study protocol was developed in accordance with the 1964 Declaration of Helsinki and subsequent ethical guidelines and was approved by the ethics committee of Ehime University (approval no. 1505011). All participants provided written informed consent before enrollment.
Clinical Trial Registry: This study was registered in University hospital Medical Information Network (000051334).
ORCID iD: Shinya Furukawa 
https://orcid.org/0000-0002-0041-7688
Availability of Data: The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
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