Assessment of intrapelvic blood flow with the penile brachial index using a toe blood pressure cuff in Japanese patients with lower urinary tract symptoms :Keiichiro Hayashi, Haruaki Sasaki, Kohzo Fuji, Aya Hiramatsu, Motoki Yamagishi, Yuki Matsumoto, Eiji Matsubara, Katsuyuki Saito, Kimiyasu Ishikawa, Takashi Fukagai, Yoshio Ogawa, Urological Science

ORIGINAL ARTICLE
Year : 2020 | Volume : 31 | Issue : 4 | Page : 183--187

Assessment of intrapelvic blood flow with the penile brachial index using a toe blood pressure cuff in Japanese patients with lower urinary tract symptoms

Keiichiro Hayashi¹, Haruaki Sasaki², Kohzo Fuji¹, Aya Hiramatsu¹, Motoki Yamagishi², Yuki Matsumoto¹, Eiji Matsubara¹, Katsuyuki Saito¹, Kimiyasu Ishikawa³, Takashi Fukagai⁴, Yoshio Ogawa⁵,
¹ Department of Urology, Showa University Northern Yokohama Hospital, Yokohama, Japan
² Department of Urology, Showa University Fujigaoka Hospital, Yokohama, Japan
³ Department of Urology, Shinmidori General Hospital, Yokohama, Japan
⁴ Department of Urology, Showa University Koto Toyosu Hospital, Tokyo, Japan
⁵ Department of Urology, Showa University School of Medicine, Tokyo, Japan

Correspondence Address:
Keiichiro Hayashi
35-1 Chigasaki Chou, Tsuzuki-Ku, Yokohama, Kanagawa, 224-8503
Japan

Abstract

Purpose: We aim at investigating the relationship between lower urinary tract symptoms (LUTSs) and intrapelvic blood flow. Conventionally, intrapelvic blood flow is assessed using a Doppler blood flowmeter. In this study, the penile brachial pressure index (PBI), which is a simpler tool, was used. Materials and Methods: The participants of this study were 103 male outpatients with LUTS whose PBI was measured using the form pulse wave velocity/ankle-brachial index with a toe blood pressure cuff. Data including age, body mass index (BMI), penile blood pressure, PBI, complications (hypertension, dyslipidemia, and diabetes mellitus), International Prostate Symptom Score (IPSS), and Erection Hardness Score (EHS) were retrospectively examined. LUTS positivity was defined as an IPSS score ≥8 and LUTS negativity as an IPSS score <8. Results: The PBI and EHS scores were significantly higher in the LUTS-negative participants than in the LUTS-positive participants. Furthermore, a multivariate analysis showed a significant difference only in PBI. However, age, BMI, EHS, or previous history of complications did not significantly differ. Conclusion: PBI was found to be an independent factor of LUTS. Recent studies have shown that LUTS and erectile dysfunction are associated with lifestyle-related diseases, and that these conditions are caused due to impaired blood flow in the intrapelvic arteries due to arteriosclerosis. Therefore, LUTS should be treated as a vascular disease.

How to cite this article:
Hayashi K, Sasaki H, Fuji K, Hiramatsu A, Yamagishi M, Matsumoto Y, Matsubara E, Saito K, Ishikawa K, Fukagai T, Ogawa Y. Assessment of intrapelvic blood flow with the penile brachial index using a toe blood pressure cuff in Japanese patients with lower urinary tract symptoms.Urol Sci 2020;31:183-187

How to cite this URL:
Hayashi K, Sasaki H, Fuji K, Hiramatsu A, Yamagishi M, Matsumoto Y, Matsubara E, Saito K, Ishikawa K, Fukagai T, Ogawa Y. Assessment of intrapelvic blood flow with the penile brachial index using a toe blood pressure cuff in Japanese patients with lower urinary tract symptoms. Urol Sci [serial online] 2020 [cited 2023 Jun 1 ];31:183-187
Available from: https://www.e-urol-sci.com/text.asp?2020/31/4/183/249330

Full Text

Introduction

Lower urinary tract symptoms (LUTSs) associated with benign prostatic hyperplasia (BPH) are attributed not only to mechanical obstruction caused by urethral compression due to hyperplasia or growth of prostatic adenoma, but also to the presence of inflammation, changes in testosterone levels, and ischemia of the bladder and prostate. Moreover, erectile dysfunction (ED) is associated with impaired blood flow in the penile cavernous body. In this study, intrapelvic blood flow, which is an important factor in both disorders, was examined using the penile brachial index (PBI). PBI is the ratio of penile blood pressure (PBP) to brachial blood pressure, and this index decreases when penile blood flow is impaired.[1],[2] This study aims at investigating the relationship between LUTS and intrapelvic blood flow using this ratio.

Subjects and Methods

Ethics statements

This retrospective study was approved by the institutional review board of the participating hospital (approval number 30-11) and was initiated after providing information about the objectives to the patients and after obtaining a written informed consent.

Study participants

A total of 142 outpatients whose PBI was assessed at the Department of Urology, Yamanashi Red Cross Hospital, between September 2018 and October 2019; 103 of them, who were receiving outpatient treatment for BPH/LUTS and who provided consent to participate in this study, were included.

Exclusion criteria

The following patients were excluded from the study: those who had been or were treated for prostate or genitourinary cancer, those with a performance status of 3 or higher, and those who had difficulty in completing the questionnaires by themselves due to dementia or other conditions.

In patients with a prostate-specific antigen level of 4 ng/mL or higher, the presence of prostate cancer was ruled out by prostate biopsy or pelvic magnetic resonance imaging.

Intervention and data collection

Outcome measures

The PBI, the International Prostate Symptom Score (IPSS), and the Erection Hardness Score (EHS) were simultaneously measured. Generally, the LUTS is comprehensively assessed using a quality of life (QOL) index and the Overactive Bladder Symptom Score (OABSS), in addition to the IPSS. In this study, patients with IPSS ≥8 were included in the LUTS group and those with IPSS <7 in the non-LUTS group.

The study compared the age, body mass index (BMI), PBI, prostate volume, comorbidities (hypertension, dyslipidemia, and diabetes mellitus), and EHS between these two groups.

In addition, a multivariate analysis of variables with significant differences based on the univariate analysis was performed.

Age, PBI, prostate volume, EHS, and comorbidities were set as the outcome variables, and IPSS was set as the explanatory variable. The prostate size was evaluated with transabdominal ultrasonography.

Vascular endothelial function test

Form pulse wave velocity (PWV)/ankle-brachial index (ABI) (Fukuda Denshi Co. Ltd., Tokyo, Japan) was used in the assessment. ABI is defined as the ankle systolic blood pressure divided by the higher value of the right or left brachial systolic blood pressure. This tool is used to identify the presence or absence and severity of the clogging of arteries in the lower limbs. In patients with long-term diabetes mellitus and those on dialysis, severe medial artery calcification is frequently observed in the arteries in the ankles and the cranial side of the ankles. When ankle blood pressure is measured, compression of the artery by a manchette is insufficient, despite an increase in cuff pressure. Consequently, ankle blood pressure increases, and the ABI may elevate. However, medial artery calcification associated with this phenomenon rarely affects the toes. In such cases, the toe-brachial index (TBI) is evaluated instead of the ABI. Moreover, when a lesion is found in the periphery of the ankle, the ABI is difficult to measure accurately; thus, the TBI is used. In this study, the systolic blood pressure of the dorsal penile artery was assessed using a toe blood pressure cuff, which was wrapped around the root of the penis. Simultaneously, brachial arterial pressure was evaluated, and the PBI was calculated using the values obtained. The ABI/PWV machine used in this study was equipped with a changeover device, which can change the cuff mode from wrapping around the ankle to wrapping around the toe, thereby enabling easy measurement of TBI. This study determined PBI in patients with abdominal aortic aneurysm using this type of ABI/PWV machine, considering patients with digestive diseases as the controls, and compared the results with measurements obtained with a conventional Doppler blood flowmeter. The PBI values obtained by the two measurement methods showed a high correlation (correlation coefficient: 0.91 and 0.96, respectively),[3] indicating the usefulness of using a toe blood pressure cuff to determine PBI. [Figure 1] shows the assessment process. This test was performed after about 5 min of rest and was completed in about 10 min. Moreover, it is minimally invasive, and it is not influenced by diet or time of measurement. It can be performed independent of the technical skill of the examiner, yet it yields objective data.{Figure 1}

Statistical analysis

For statistical analysis, a Chi-square test was performed to analyze complications, and the Mann–Whitney U-test was carried out to examine the other variables. P < 5% was considered statistically significant. The JMP Pro14 (SAS Institute, Cary, NC, the USA) was used for all analyses.

Results

The characteristics of the patients are shown in [Table 1]. The mean values were as follows: age, 72.5 ± 7.35 years; height, 165.1 ± 5.55 cm; weight, 65.9 ± 9.02 kg; BMI, 24.1 ± 3.03 kg/m 2; waist circumference, 84.5 ± 7.13 cm; PBP, 113.8 ± 20.5 mmHg; PBI, 0.76 ± 0.12; prostate size, 35.1 ± 15.1 cc; IPSS, 11.3 ± 7.83; OABSS, 4.69 ± 2.89; EHS, 2.49 ± 1.06; and Sexual Health Inventory for Men (SHIM) score, 9.53 ± 8.10. In terms of complications, of the 103 patients, 77 (74.8%), 38 (36.9%), and 26 (25.2%) presented with hypertension, dyslipidemia, and diabetes mellitus, respectively.{Table 1}

The LUTS-positive and LUTS-negative groups statistically significantly differed in terms of PBI (P = 0.0318) and EHS (P = 0.0432). In contrast, no significant differences were observed in terms of age, BMI, penile systolic blood pressure, prostate size, or current complications. Furthermore, the multivariate analysis using logistic regression showed a statistically significant difference only in PBI (P = 0.0093) [Figure 2] and [Figure 3].{Figure 2}{Figure 3}

Discussion

Association of erectile dysfunction and lower urinary tract symptoms with vascular lesions

The common risk factors of ED and LUTS are vascular endothelial dysfunction and arteriosclerosis. Both disorders commonly coexist and are known to be correlated in terms of severity. In a study that examined 12,815 men aged 50–80 years in seven European countries, LUTS and ED were assessed using the IPSS and International Index Erectile Function (IIEF), respectively, and were adjusted for age and complications. The results showed that the severity of LUTS was correlated with that of ED, and that LUTS and ED were independent predictors.[4] In another study that analyzed data about complete medical checkups performed on 2084 patients in Japan, the odds ratio for severity based on age-adjusted scores on the 5-item version of the IIEF (IIEF-5) was 4.49 in patients with a moderate IPSS and 7.34 in those with a severe IPSS. The severity was dose dependent.[5] Both disorders are associated with sympathicotonia, ischemia of the pelvic vascular bed, attenuation of the nitrogen oxide–cyclic guanosine monophosphate system, and enhancement of the RhoA–Rho-associated coiled-coil-containing protein kinase signaling, which cause vascular endothelial hypofunction, enhanced smooth muscle contractility, decreased smooth muscle relaxation, and ischemia of the lower urinary tract. These conditions may cause histological damage and ultimately LUTS and ED. Both disorders impair the QOL.

In Japan, which has become a super-aging society, the prevalence of these disorders is expected to increase with the Westernization of the diet. Understanding of their pathology is important for urologists to extend the healthy life expectancy, defined as years of healthy and active life. The associations between arteriosclerosis and ED [6] and between arteriosclerosis and penile hardness [7] were previously reported in our studies that used PWV, a test that measures vascular wall stiffness.

Reasons for using penile blood pressure

To clinically assess vascular endothelial function, flow-mediated dilation (FMD) is used. FMD is the gold standard for noninvasive vascular endothelial function tests, which is utilized to assess the severity of early-stage arteriosclerosis.[8] However, to obtain reproducible results, the FMD test should be performed by a skilled examiner, and the vascular diameter, length of the upper arm, and other features of the body should be considered. In recent years, ABI has been used as a substitute for FMD in vascular endothelial function tests.[9]

Because the assessment of vascular endothelium using FMD is only intended for arteries in the upper arm or forearm, we believe that its results do not accurately reflect the vascular endothelial function around the lower urinary tract. To assess intrapelvic blood flow, color Doppler imaging, contrast-enhanced computed tomography scan, and angiography are carried out. However, color Doppler imaging is slightly difficult to perform and cannot rule out the possibility that the results might have been affected by the subjective views of the examiners. Examiners find other imaging modalities to be extremely invasive, and these modalities cannot be easily performed for screening. Thus, we measured the PBP. Unno et al.[10] have reported that PBP and PBP measurements based on Doppler blood flow measurements are highly correlated. Because several blood vessels distributed in the bladder, prostate, and urethra are branches of the internal iliac artery, the assessment of blood flow in the penile artery, which is an end branch of the internal iliac artery, can indirectly identify the state of intrapelvic blood flow. The PBP measured in our study may indicate blood pressure mainly in the dorsal penile artery; thus, the blood flow distribution in the lower urinary tract can be evaluated using PBP.

Limitations and strengths of the study

The study showed that the PBI was significantly lower in the LUTS-positive group than in the LUTS-negative group. Thus, the intrapelvic blood flow was decreased in the LUTS-positive group. Impaired blood flow in the lower urinary tract, including the bladder, is a cause of LUTS.[11] Because our study included several patients with hypertension, dyslipidemia, or diabetes mellitus, we assumed that a high number of patients had impaired blood flow. Thus, ischemia of the bladder and prostate might be associated with LUTS. However, PBP did not differ between the two groups, which might be attributed to the fact that PBP is greatly affected by the brachial systolic blood pressure. PBI, which is the ratio of PBP to brachial blood pressure, may accurately reflect intrapelvic blood flow. In our study, PBI was significantly lower in the LUTS-positive group than in the LUTS-negative group. This result indicated that impaired intrapelvic blood flow is associated with dysuria. Regarding the association between LUTS and vascular lesions, Matsui et al. have reported that worsening IPSS is significantly correlated with cardiovascular risk factors (FMD and nitroglycerine-induced vasodilation) and that moderate and severe LUTS were associated with the prevalence of coronary artery diseases. Moreover, LUTS may be a predictor of cardiovascular events.[12] Furthermore, in a systematic review, Gacci et al. have shown that the presence of moderate and severe LUTS was statistically significantly associated with the incidence of severe cardiovascular events (P < 0.001).[13]

In our study, the multivariate analysis revealed no significant difference in EHS, which may be attributed to the fact that blood pressure in the cavernous arteries that are mainly responsible for the erection is not assessed because PBP mainly indicates blood pressure in the dorsal penile artery, as previously described. Besides, our study used the EHS, instead of the IIEF-5 and SHIM, which are widely used for assessing erectile function, because the study included a high number of less sexually active patients aged 70 years or older, and we assumed that an accurate assessment of the sexual function would be difficult. In addition, EHS is a remarkably simple, clear, visually perceptive method of evaluation. It is feasible even in the evaluation of erectile function, which cannot be detected with the IIEF or IIEF-5.[14]

Recent studies that used the PBI have already been reported. Fukumoto et al.[15] have reported that ED patients with advanced arteriosclerosis present a low PBI and an advanced vascular disorder of the penis. Furthermore, Koyama et al.[16] have shown that in BPH patients who poorly respond to α1-blockers, the IPSS was significantly higher in those with PBP ≥110 mmHg than in those with PBP <110 mmHg. However, the present study has some limitations. This is a single-center, retrospective, cross-sectional study. Further large-scale clinical studies must be conducted to assess the association between LUTS/ED and intrapelvic blood flow.

Conclusion

Patients with poor response to LUTS treatment have low PBI. This result indicates that they might have concomitant impaired blood flow in the lower urinary tract. Thus, future prospective studies must be conducted to validate the results of the current study.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1	Britt DB, Kemmerer WT, Robison JR. Penile blood flow determination by mercury strain gauge plethysmography. Invest Urol 1971;8:673-8.
2	Engel G, Burnham ST, Caster MF. Penile blood pressure in the evaluation of erectile importance. Fertil Steri 1978;1978:687-790.
3	Unno N, Inuzuka K, Ishimaru KM, Sagara D, Konno H. Automated bedsides measurement of penile blood flow using pulse-volume-plethysmography. Surg Today 2006;36:257-61.
4	Rosen R, Altwein J, Boyle P, Kirby RS, Lukacs B, Meuleman E, et al. Lower urinary tract symptoms and male sexual dysfunction: The multinational survey of the aging male (MSAM-7). Eur Urol 2003;44:637-49.
5	Terai A, Ichioka K, Matsui Y, Yoshimura K. Association of lower urinary tract symptoms with erectile dysfunction in Japanese men. Urology 2004;64:132-6.
6	Hayashi K, Sasaki H, Yamamoto K, Sugawara S, Aoki K, Ota M. Vascular Evaluation in patients with ED. Jpn J Sex Med 2012;27:41-7.
7	Hayashi K, Sasaki H, Fukagai T, Kurokawa I, Sugishita H, Tanifuji S, et al. Association between vascular lesion and penile erection hardness in Japanese patients with erectile dysfunction. Urol Sci 2018;29:202-5.
8	Tomiyama H, Yamashina A, Arai T, Hirose K, Koji Y, Chikamori T, et al. The relationships of cardiovascular disease risk factors to flow-mediated dilation in Japanese subjects free of cardiovascular disease. Hypertens Res 2008;31:2019-25.
9	Kajikawa M, Maruhashi T, Iwamoto Y, Iwamoto A, Matsumoto T, Hidaka T, et al. Borderline ankle-brachial index value of 0.91-0.99 is associated with endothelial dysfunction. Circ J 2014;78:1740-5.
10	Unno N, Inuzuka K, Yamamoto N, Sagara D, Suzuki M, Konno H. Preservation of pelvic circulation with hypogastric artery bypass in endovascular repair of abdominal aortic aneurysm with bilateral iliac artery aneurysms. J Vasc Surg 2006;44:1170-5.
11	Yamaguchi O, Nomiya M, Andersson KE. Functional consequences of chronic bladder ischemia. Neurourol Urodyn 2014;33:54-8.
12	Matsui S, Kajikawa M, Maruhashi T, Iwamoto Y, Oda N, Kishimoto S, et al. Endothelial dysfunction, abnormal vascular structure and lower urinary tract symptoms in men and women. Int J Cardiol 2018;261:196-203.
13	Gacci M, Corona G, Sebastianelli A, Serni S, de Nunzio C, Maggi M, et al. Male lower urinary tract symptoms and cardiovascular events: A systematic review and meta-analysis. Eur Urol 2016;70:788-96.
14	Watanabe A, Imamura T, Morii A, Komiya A, Fuse H. The usefulness of Japanese version for erection hardness score. Jpn J Sex Med 2010;25:243-7.
15	Fukumoto K, Nagai A, Hara R, Fujii T, Miyaji Y. Tadalafil for male lower urinary tract symptoms improves endothelial function. Int J Urol 2017;24:206-10.
16	Koyama J, Kaiho Y, Kawasaki Y, Sato T, Fukushi T, Kyan A, et al. Penile blood pressure is useful to identify candidates for tadalafil treatment in patients with lower urinary tract symptoms. BJU Int 2019;123:124-9.