Abstract
Objective
To investigate the relationship between metabolic syndrome (MetS) and lower urinary tract symptoms (LUTS) with functional and anatomic changes of the lower urinary tract with MRI.
Materials and Methods
The bladder and prostate of 95 subjects (56M, 39F) were segmented on T2-weighted pelvic MRI using Materialize Mimics 3D software. Bladder wall volume (BWV), post-void residual (PVR) and prostate volume (PV) were quantified from the 3D renderings. LUTS were quantified using validated questionnaires administered at the time of MRI. Wilcoxin rank sum, win ratio and chi-square tests were used to correlate symptom scores, BWV, PVR and PV in patients 1) without vs with MetS, 2) with mild (IPSS or UDI-6: 0–7) vs moderate-severe (IPSS: 8–35 or UDI-6: ≥8) and 3) normal vs enlarged prostates (>40cm3). Multivariate linear regression was used to determine predictors for BWV, PVR and PV.
Results
Men with MetS had increased BWV (66.8 vs 51.1cm3, p=0.003), higher PVR (69.1 vs 50.5cc, p=0.05) and increased PV (67.2 vs 40.1cm3, p=0.01). Women without and with MetS had similar BWV, PVR and LUTS (p=0.3–0.78). There was no difference in prevalence of MetS, BWV, PVR or PV in men or women with mild vs moderate-severe LUTS (p=0.26–0.97). Men with enlarged prostates were more likely to have MetS (p=0.003). There was no difference in BWV, PVR and LUTS for men with normal vs enlarged prostates (p=0.44–0.94). In men, BWV was highly correlated with MetS (p=0.005) on regression analysis.
Conclusion
MetS leads to detrusor hypertrophy and may contribute to impaired bladder function, likely related to the effect on the prostate.
Keywords: MRI, LUTS, benign prostate enlargement, BPE, bladder outlet obstruction
Introduction
Lower urinary tract symptoms (LUTS) is an umbrella term that encapsulates a number of bothersome symptoms which indicate dysfunction of the lower urinary tract in men and women. These symptoms range in severity from impaired quality of life to renal failure from chronic urinary retention. In affected men, LUTS are most often attributed to bladder outlet obstruction from benign prostatic hyperplasia (BPH) which is nearly universal among aging men. Prior studies support this paradigm by demonstrating an association between LUTS and anatomic changes of the lower urinary tract, such as bladder wall thickening and benign prostate enlargement (BPE) secondary to benign prostatic hyperplasia (BPH) (1–5).
Bothersome LUTS and BPH have been associated with metabolic syndrome (MetS), a cluster of medical conditions that contribute to chronic low-grade inflammation. In addition to increasing prostate volume, chronic inflammation of the prostate likely contributes to collagen deposition and prostate fibrosis leading to bladder outlet obstruction (6–17). MetS is diagnosed clinically when three or more of the following criteria coexist: waist circumference over 40 inches (men) or 35 inches (women), blood pressure over 130/85 mmHg, fasting triglyceride (TG) level over 150 mg/dl, fasting high-density lipoprotein (HDL) cholesterol level less than 40 mg/dl (men) or 50 mg/dl (women), and fasting blood sugar over 100 mg/dl.
Historically, anatomic changes of the lower urinary tract have been demonstrated with ultrasound (US) and computed tomography (CT). Both modalities have limitations that prevent either from providing reliable quantitative measurements of the lower urinary tract. US provides adequate soft tissue contrast to characterize the anterior bladder wall. Unfortunately, artifact from bowel gas and pelvic bones often obscures the remainder of the bladder and prostate. Transrectal US improves sonographic evaluation of the prostate but is invasive and poorly tolerated. Further, sonographic xwindows are narrow which precludes volumetric assessment of the bladder. CT has poor soft tissue contrast and the downside risk of radiation exposure (18–21).
Manual and semi-automated segmentation of pelvic magnetic resonance imaging (MRI) with 3D anatomical renderings provides a novel method for evaluating important parameters of the lower urinary tract (22–24). This methodology may allow for quantification of the changes in the lower urinary tract of patients with MetS. Therefore, the purpose of this study is to investigate the relationship between MetS and LUTS with functional and anatomic changes of the lower urinary tract using MRI.
Materials and Methods
Patient Population
This Health Insurance Portability and Accountability Act (HIPAA)-compliant, single center, prospective study was performed after informed consent was obtained. Patients scheduled for a pelvic MRI unrelated to the lower urinary tract at the University of Wisconsin-Madison were approached by a study coordinator. Clinical indications for pelvic MRIs included cancer staging (rectal, endometrial, cervical), characterization (ovarian cyst/lesion) and pain (hip, pelvis, SI join). All subjects who consented to participate completed a validated LUTS questionnaire administered at the time of MRI: the International Prostate Symptom Score (IPSS) for men or Urogenital Distress Inventory (UDI-6) for women. The IPSS includes 7 questions related to voiding symptoms. A score of 0–7 indicates mild symptoms, 8–19 moderate symptoms and 20–35 severe symptoms. The UDI-6 includes 6 questions related to stress incontinence and the impact on patient quality of life. UDI-6 scores range from 0–100 with higher scores attributed to increasing symptom distress.
Pelvic MRIs of 103 subjects [(63M, median age 64 years (IQR: 59–67)/median BMI 29 (IQR: 25.8–34.6) and 40F, median age 47.5 years (IQR: 40.5–65)/median BMI 26.9 (IQR: 22.8–35.3)] were analyzed. Clinical data were collected from the electronic medical record including body mass index, blood pressure, and fasting blood sugar, total cholesterol, and triglyceride levels.
MRI Analysis
Subjects were asked to void immediately prior to MRI. MRI was performed on a 3.0T (Discovery 750, GE Healthcare, Waukesha, WI) using a 32-channel surface coil (NeoCoil, Pewaukee, WI) or a 1.5T (Optima 450, GE Healthcare, Waukesha, WI) using an 8-channel cardiac array (NeoCoil, Pewaukee, WI). Axial or sagittal FSE T2-weighted acquisitions (TR 4119 ms; TE = 92.4 ms; matrix = 320 × 256; FOV = 260 × 234 mm2; slice thickness = 3 mm; true spatial resolution = 0.81 × 1.02 mm; flip angle = 90°; receiver bandwidth = 122.07±31.25 kHz). The acquired images, in DICOM (Digital Imaging and Communications in Medicine) format, were uploaded into Mimics (Materialize, Leuven, Belgium, 2016), version 21.0 to extract virtual anatomic 3D models (22). The bladder serosa, bladder lumen and prostate capsule (men) were individually segmented by a medical student and author (APT) in consensus with an experienced abdominal radiologist (SAW). After contouring the relevant organ on each MRI slice, a mask of the segmented anatomy was constructed. The mask was then converted into a 3D model using the “Calculate 3D from Mask” tool. This process was repeated separately for the 3D whole bladder, a second time for the 3D bladder lumen [postvoid residual (PVR)] and a third time for the 3D whole prostate [prostate volume (PV)]. The bladder wall was rendered as a 3D model by subtracting the 3D bladder lumen model from the 3D whole bladder model providing bladder wall volume (BWV) (Figure 1).
Figure 1.
A-C: Axial FSE T2-weighted MRI images of the bladder serosa (A), bladder lumen (B) and prostate capsule (C) were individually segmented and an anatomic mask constructed. D-F: The mask was converted into a 3-dimensional model. Bladder wall volume (D) was rendered by subtracting the bladder serosa from the bladder lumen. Postvoid residual (E) and prostate volume (F) rendered from the bladder lumen and prostate capsule segmentations, respectively.
Statistical analysis
Subjects were considered to have MetS when four diagnostic criteria were present, excluding waist circumference. Men and women with mild LUTS self-reported scores using standard rating scales of 0–7 (IPSS) and 0–10 (UDI-6). LUTS scores of 8+ (men) and 11+ (women) were categorized as moderate-severe. BPE was defined as prostate volume >40cm3 (5). Binary variables were summarized by N (%) and quantitative variables by median (IQR). Wilcoxin rank sum, win ratio and chi-square tests were used to compare LUTS scores, BWV, PVR and PV in patients 1) without vs with MetS, 2) mild vs moderate-severe LUTS and 3) normal sized prostates vs BPE (men). Multivariate linear regression was used to determine predictors for BWV, PVR and PV while controlling for sex, age, MetS, and BMI. Robust variance accounting for within-subject correlation between voiding and storage symptom scores was used to evaluate the V/S (voiding/storage) symptom ratio for men without and with MetS. Significance was set at p-values ≤ 0.05.
Results
Eight subjects were excluded due to incomplete bladder coverage, artifact/motion obscuring bladder/prostate or prior cystectomy/prostatectomy. The final study population consisted of 56M and 39F (n=95), with median ages of 64 years (IQR: 58.8–67) and 47 years (IQR: 39.5–65) respectively (Table 1).
Table 1:
Patient characteristics, lower urinary tract symptom scores and 3D MRI volumes
| Women (n=39) |
Men (n=56) |
|
|---|---|---|
| Age (years) | 47.5 (39.5–65) | 64 (58.8–67) |
| BMI | 26.9 (22.7–35.4) | 29.5 (25.8–34.8) |
| Metabolic Syndrome | ||
| Yes | 14 (36%) | 23 (41%) |
| No | 25 (64%) | 33 (59%) |
| Symptom Scores | ||
| UDI-6 (0–100) | 3 (1–7) | --- |
| IPSS (0–35) | --- | 6 (4–10) |
| Bladder wall volume (cm3) | 39.1 (33.9–57.8) | 54.9 (43.4–70.1) |
| Postvoid residual (mL) | 50.7 (24.2–100.1) | 58.5 (30.3–95.4) |
| Prostate volume (cm3) | --- | 45.6 (31.8–79.0) |
Values reported as median (interquartile range) or number (%).
Urogenital Distress Inventory (UDI-6)
International Prostate Symptom Score (IPSS)
Metabolic Syndrome
Men with MetS (n=23), compared to men without MetS (n=33), had a higher BWV [69.1 cm3 (IQR: 60.1–80.2) vs 51.1 cm3 (IQR: 40.3–60.3), p = 0.003], PVR [66.8 mL (IQR: 57.7–85.6) vs 50.5 mL (IQR: 27.6–91.5), p = 0.047], and PV [67.2 cm3 (IQR: 47.1–92.3) vs 40.1 cm3 (IQR: 29.9–55.6), p = 0.01]. Men without and with MetS had similar symptom scores on IPSS [10 (IQR: 4.5–12) vs 6 (IQRP 3–10), p = 0.278] (Table 2a). BWV correlated with MetS on multivariate linear regression (p=0.005, 95% CI: 5.17–28.29) (Table 3). The V/S (voiding/storage) symptom ratio for patients with and without MetS was similar [1.1 (95% CI: 0.87–1.4) vs 0.86 (95% CI: 0.64–1.1), p=0.19].
Table 2a:
Lower urinary tract symptom scores and 3D MRI volumes in men without and with metabolic syndrome (MetS).
| Non-MetS (n=39) |
MetS (n=23) |
p-value | |
|---|---|---|---|
| IPSS | 6 (3,10) | 10 (4.5,12) | 0.278 |
| Post void residual (cm3) | 50.5 (27.6,91.5) | 69.1 (60.1,80.2) | 0.047 |
| Bladder wall volume (cm3) | 51.1 (40.3,60.3) | 66.8 (57.7,85.6) | 0.003 |
| Prostate volume (cm3) | 40.1 (29.9,55.6) | 67.2 (47.1,92.3) | 0.011 |
International Prostate Symptom Score (IPSS)
Variables are summarized by median (IQR).
P-values are based on win ratio (IPSS) or Wilcoxon rank sum test (volume measurements).
Table 3:
Multivariate linear regression assessing predictors for bladder wall volume (BWV), post void residual (PVR) and prostate volume (PV).
| Coefficient | 95% Confidence interval | p-value | ||
|---|---|---|---|---|
| Bladder wall volume | ||||
| Age (years) | 0.15 | (−0.18, 0.48) | 0.370 | |
| BMI (kg/m2) | 0.34 | (−0.26, 0.94) | 0.267 | |
| MetS (Y vs N) (Women) | −6.95 | (−21.61, 7.71) | 0.353 | |
| MetS (Y vs N) (Men) | 16.73 | (5.17, 28.29) | 0.005 | |
| Postvoid residual | ||||
| Age | 0.29 | (−1.01, 1.59) | 0.665 | |
| BMI | 0.60 | (−1.73, 2.92) | 0.615 | |
| MetS (Men/Women) | 18.56 | (−19.64, 56.75) | 0.344 | |
| Prostate volume | ||||
| Age | −0.46 | (−1.51, 0.59) | 0.395 | |
| BMI | 1.10 | (−0.51, 2.72) | 0.188 | |
| MetS (Men/Women) | 16.52 | (−6.99, 40.03) | 0.175 |
Body Mass Index (BMI)
Metabolic Syndrome (MetS)
Women with MetS (n=14), compared to women without MetS (n=25), had similar BWV [40.5 cm3 (IQR: 33–48.5) vs 38.4 cm3 (IQR: 34–57.8), p = 0.784], PVR [40.5 mL (IQR: 32.2–97.6) vs 41.7 mL (IQR: 23–95.1), p = 0.392] and LUTS scores [3 (IQR: 2–7.8) vs 2.5 (IQR: 1–6), p = 0.303] (Table 2b) (Supplementary Figure 1). Neither BWV nor PVR correlated with MetS on multivariate linear regression (Table 3).
Table 2b:
Lower urinary tract symptom scores and 3D MRI volumes in women without and with metabolic syndrome (MetS).
| Non-MetS (n=26) |
MetS (n=14) |
p-value | |
|---|---|---|---|
| UDI-6 | 2.5 (1,6) | 3 (2,7.8) | 0.303 |
| Post void residual (cm3) | 41.7 (23,95.1) | 70.5 (32.2,97.6) | 0.392 |
| Bladder wall volume (cm3) | 38.4 (34,57.8) | 40.5 (33,48.5) | 0.784 |
Urogenital Distress Inventory-6 (UDI-6)
Variables are summarized by median (IQR).
P-values are based on win ratio (UDI-6) or Wilcoxon rank sum test (volume measurements).
Lower Urinary Tract Symptom Scores
Men with mild LUTS (n=26), compared to men with moderate-severe LUTS (n=30), had similar BWV [56.9 cm3 (IQR: 44.9–66.7) vs 53.9 cm3 (IQR: 41.5–82.1), p = 0.974], PVR [65.4 mL (IQR: 29.2–120.8) vs 52.5 mL (IQR: 30.5–69.8), p = 0.342] and PV [45.3 cm3 (IQR: 30.6–67.7) vs 52.2 cm3 (IQR: 35.5–93.9), p = 0.263]. The prevalence of MetS was similar for men with mild and moderate-severe LUTS [11/26 (42.3%) vs 12/30 (40%), p = 0.323].
Women with mild LUTS (n=30), compared to women with moderate-severe LUTS (n=9), had similar BWV [41.9 cm3 (IQR: 34.1–60.2) vs 37.3 cm3 (IQR: 32.3–39.1), p = 0.284] and PVR [63.2 mL (IQR: 24.0–101.5) vs 47.4 mL (IQR: 27.9–66.4), p = 0.756]. The prevalence of MetS was similar for women with mild and moderate-severe LUTS [10/30 (32.3%) vs 4/9 (44.4%), p = 0.781].
Prostate Size
Men with BPE (n=34), compared to men without BPE (n=22), had similar BWV [54.9 cm3 (IQR: 44.1–66.9) cm3 vs 56.9 cm3 (IQR: 45.5–75.1), p = 0.751], PVR [58.5 mL (IQR: 31.3–80.2) vs 63.3 mL (IQR: 25–107.2), p = 0.938] and LUTS scores [7 (IQR: 5–10) vs 6 (IQR: 2–14), p = 0.444]. The prevalence of MetS was higher in men with BPE [16/34 (47.1%) and 2/21 (9.5%), p = 0.013]. However, there was no correlation between prostate volume and MetS on multivariate linear regression (Table 3).
Discussion
In this single-center, prospective study, we quantified and compared anatomic and functional characteristics of the lower urinary tract with MRI and symptoms with validated questionnaires in men and women without and with metabolic syndrome (MetS). We found that men with MetS had increased bladder wall volume (BWV), elevated postvoid residual (PVR) and increased prostate volume (PV) compared to men without MetS. Further, men with benign prostate enlargement (BPE) (>40 cm3) were more likely to have MetS. However, only BWV correlated with MetS on regression analysis. MRI derived metrics (BWV and PVR) were similar for women without and with MetS. These data suggest that MetS leads to detrusor hypertrophy and may contribute to impaired bladder function likely related to the effect on the prostate.
Prior studies have demonstrated a strong association between MetS and increased PV. Hammarsten et al found that men with MetS had both increased PV and a faster annual rate of prostate growth (25–26). Our study echoes these findings – demonstrating that men with MetS had higher PV and men with BPE were also more likely to have MetS. Further, we found that men with MetS had higher BWV and PVR, both of which reflect anatomic and functional responses to bladder outlet obstruction. Despite these measured differences in bladder structure and function, symptom scores were similar between men with and without MetS. This may be explained by selection/recruitment bias and/or insufficient statistical power. Alternatively, these findings may be explained by a lag between anatomic and functional changes in the lower urinary tract and onset of symptoms from bladder outlet obstruction.
Prostatic inflammation and fibrosis are important contributors to bladder outlet obstruction independent of prostate volume. Cantiello et al reported that MetS was associated with increased periurethral inflammation and collagen and decreased elastin which collectively increase the opening pressure of the prostatic urethra and leads to remodeling of the bladder (5, 27–29). Our findings that BWV and not PV correlated with MetS suggests that prostate inflammation and fibrosis may be an important driver of outlet obstruction and bladder remodeling independent of prostate volume. In future studies, MRI will provide a powerful means to non-invasively quantify prostate stiffness, as a surrogate for fibrosis.
Several cohort and population studies have demonstrated a positive association between MetS and overall LUTS severity and a predilection for voiding symptoms indicative of bladder outlet obstruction. However, we report no difference between LUTS scores in either men or women with and without MetS. Despite similar symptom scores, we demonstrate that men with MetS had larger prostates, increased BWV, and elevated PVR. These anatomic changes reflect detrusor hypertrophy and impaired emptying secondary to urinary obstruction and are therefore concordant with prior studies showing voiding predominant symptoms in MetS patients. Further these bladder changes were absent in women with MetS, which supports the paradigm that MetS contributes to changes in the prostate that lead to outlet obstruction (BPE and fibrosis), detrusor hypertrophy and incomplete bladder emptying. The lack of a measured difference in symptom scores in our study may also be explained by study design. We recruited men and women who were undergoing pelvic MRI as opposed to patients with bothersome LUTS. This likely explains the lower average symptom scores in our study compared to prior studies. This difference may also be explained by lack of statistical power due to relatively small sample size.
MRI is a powerful tool to quantify clinically relevant anatomic and functional parameters of the lower urinary tract. Here and in prior work, we used a fast acquisition (~2 minute scan) to acquire axial or sagittal images of the bladder and prostate (22). Semi-automated, as described here, and emerging fully automated post-processing software strategies capable of quickly and accurately quantifying prostate and transition zone volume, regional changes in bladder wall thickness, bladder wall volume, and post-void residual provide a non-invasive means to collect actionable clinical information in near real time. Advanced MRI applications allow study of both anatomic and functional changes of the bladder and prostate that occur with ageing, disease states such as MetS, and in response to treatment. MR elastography of the prostate may enable quantification of prostate and periurethral stiffness, as a surrogate for fibrosis, and change in stiffness. MRI-based perfusion and diffusion measurements may enable quantification of the microvasculature of the bladder and location and extent of fibrosis in the prostate. Cine MRI of the bladder during voiding with strain imaging of the bladder wall may enable assessment of detrusor contractility.
Our study has several limitations. The prospective design was a study strength; however, many of the women that participated were young and did not have bothersome LUTS. This limited our power to detect MetS-related changes of the lower urinary tract in women. Further, the UDI-6 focus on incontinence may limit the applicability of this tool in our study. Abdominal circumference, obesity and visceral fat are associated with MetS and most strongly linked to BPE and lower urinary tract symptoms. This data was not available for our study; however, we were still able to demonstrate that the collective presence of the other clinical features of MetS contribute to BPE, detrusor hypertrophy and impaired bladder emptying. The prostate volume (>40cm3) used to define BPE in our study failed to stratify patients with detrusor hypertrophy (higher BWV) or impaired bladder emptying (higher PVR and LUTS scores) and may need to evolve. Future studies that correlate our findings with functional data from urodynamics and non-invasive uroflowemetry with prostate volume are needed. Finally, we used 2D MRI acquisitions with 3 mm slice thickness which may contribute to error on 3D volume renderings. A 3D isotropic MRI acquisition may provide more accurate volumetric data.
Conclusion
MetS leads to detrusor hypertrophy and may contribute to impaired bladder function likely related to the effect on the prostate. MRI is a powerful tool to quantify clinically relevant anatomic and functional parameters of the lower urinary tract.
Supplementary Material
Supplementary Figure 1 A-B: Axial FSE T2-weighted MRI of the pelvis in women without (A) and with (B) metabolic syndrome. Bladder wall volume and postvoid residual were similar regardless of metabolic syndrome. C-D: Sagittal FSE T2-weighted MRI of the pelvis in men without (C) and with (D) metabolic syndrome. Metabolic syndrome leads to detrusor hypertropy and may contribute to impaired bladder function likely related to the effect on the prostate.
Footnotes
Disclosures: None
References
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Supplementary Materials
Supplementary Figure 1 A-B: Axial FSE T2-weighted MRI of the pelvis in women without (A) and with (B) metabolic syndrome. Bladder wall volume and postvoid residual were similar regardless of metabolic syndrome. C-D: Sagittal FSE T2-weighted MRI of the pelvis in men without (C) and with (D) metabolic syndrome. Metabolic syndrome leads to detrusor hypertropy and may contribute to impaired bladder function likely related to the effect on the prostate.