Penile arterial communications and severity of erectile dysfunction,evaluation by color Doppler ultrasound

Introduction

The National Health Institute (NHI) defines erectile dysfunction (ED) as the inability to achieve or maintain an erection for satisfactory sexual intercourse. ¹ ED is considered a public health problem. In the USA it has been reported that up to 40% of men in the fifth decade of life and up to 70% in the eighth decade of life have some degree of ED. ² The DENSA study conducted in northern South America, where patients from Venezuela, Colombia, and Ecuador were studied, found a prevalence of ED of 53% in men over 40 years. ³

The penis is perfused by two vascular systems: superficial perfusion, responsible for irrigating the skin and the foreskin, and deep perfusion that brings blood to the erectile tissues through the dorsal, bulbourethral and cavernous arteries, ⁴ irrigating the glans, the spongy body and the urethra, and the corpora cavernous, respectively. ⁵ The deep system has many variants; the cavernous arteries can be asymmetrical, bifurcated, multiple, with accessory or recurrent branches, or originate in the dorsal artery. Finally, the helicine arteries are branches of the cavernous arteries which perfuse the smooth muscle and the sinusoids of the cavernous bodies.^6,7

Most cases of ED have an organic origin, more commonly secondary to vascular diseases that decrease penile blood flow, but they can also be the result of neurological, hormonal, or psychological factors combined since the phenomenon of erection is very complex.^8,9 Nitric oxide (NO) has been described as the main neurotransmitter in this phenomenon, ¹⁰ however the penile erectile mechanism has not been completely defined. There is an understanding of the physiology of the erection of the penis based on neurophysiological experimentation that dates back more than 100 years when Eckhardt et al., ¹¹ reported that parasympathetic electrical stimulation of the sacrum plexus generated penile erection in dogs. ¹² Also according to animal studies, three phases of detumescence have been described. The first phase involves a transient increase in intracorporeal pressure, indicating the beginning of smooth muscle contraction against a closed venous system. The second phase shows a slow decrease in intracorporeal pressure, which suggests a slow reopening of the venous channels with the resumption of the basal level of arterial flow. The third phase shows a rapid decrease in pressure with a completely restored venous flow capacity.^13–15

Doppler ultrasound of the penis is a cost-effective tool for the evaluation of penile hemodynamics which, in turn, elucidates the patency of the arterial system and venous behavior during erection. ¹⁶ Maximum systolic velocity is a parameter commonly used to quantify arterial sufficiency and the resistance index, based on the end diastolic velocity, is used to detect veno-occlusive dysfunction. ¹⁷

An analytical observational study was conducted in order to assess the relationship between the communications of the cavernous arteries with the extracavernous arteries in patients complaining of ED.

Materials and methods

An observational, analytical, cross-sectional study was conducted which included 63 patients complaining of ED that had been referred from the urology and andrology services for a penile color Doppler study with a pharmacological test.

Patients with a history of traumatic penile injury, spinal cord injury, or who were not willing to participate in the study were excluded.

The International Index of Erectile Function Questionnaire (IIEF5) was performed to classify the severity of ED and to correlate it with the erection phase obtained on the Doppler ultrasound. In Phase 0, monophasic waves are evident having peak systolic velocities between 10–25 cm/s. In Phase 1, there is an increase in the peak systolic velocity higher than 35 cm/s and at the end diastolic velocity is over 8 cm/s, clinically, an increase in the size of the penis is seen without an increase in its rigidity. Phase 2 is characterized by a protodiastolic notch which is the result of an increase in pressure of the cavernous bodies. Clinically there is an increase in size and rigidity which is, however, not enough for sexual intercourse. During Phase 3 the diastolic flow disappears due to an intracavernous pressure that equals the blood pressure and, clinically, there is an increase in rigidity. In Phase 4 there is reverse flow in diastole, due to an intracavernous pressure that exceeds the blood pressure. Clinically the penis is at its maximum rigidity. Finally, Phase 5 is characterized by a decrease of the systolic peak with absence of diastolic flow and contraction of the bulbocavernous muscles. During detumescence, the diastolic flow returns.

For the purpose of the study; the patients showing phase 0, 1 and 2 were grouped in the ED group with total loss of erection (WTLE). The other group of patients among phases 3 and 4 were defined as the ED group without total loss of erection (WOTLE).

All patients were evaluated with a high frequency linear transducer of 7–12 MHz, using a Toshiba APLIO 400 device, operated by a senior radiologist with more than 20 years of experience performing ED tests. Doppler ultrasound observations were recorded continuously after the administration of an intracavernous dose of 20 micrograms of prostaglandin E1 up to 30 min from the beginning of the examination.

Most of the complications that can appear during or after the injection of PGE1 are minor, such as pain or burning; these symptoms are triggered by sudden distension of the tunica albuginea or by direct effects on the nerve fibers in the corpora cavernous. Some patients may persist with rigid erections for more than 4.5 h, with priapism and intense pain. To avoid this situation if, during a study, the patient ends up with a rigid erection, he is invited to wait for 90 min for a new assessment. If the patient is not able to ejaculate, other therapies should be considered, such as intracavernous etilefrine injection, up to blood aspiration from the corpora cavernous.

The variables of interest were exported for validation in the STATA program, obtaining means, medians, quartiles, and confidence intervals (CIs) for the numerical variables and proportions for the qualitative variables. For all hypotheses tested, 95% CIs were used, with a level of significance of p=0.05. The prevalence ratio was calculated as a measure of association.

The present study is classified as a risk-free research, because no additional intervention is proposed and has been approved by the ethics committee of the institution. Signing of informed consent by the study participants was required.

Results

Sixty-three patients between 22–83 years old with some degree of ED were analyzed (Figure 1). Of all the patients evaluated, nine (14.29%) presented complete pharmacological erection, 26 (41.27%) partial pharmacological erection, 23 (36.51%) tumescence of the corpora cavernosa and five (7.94%) absence of pharmacological erection. All sonographic hemodynamic findings were correlated with the clinical status of the patient groups; ED WOTLE with 35 patients (55.5%) and ED WTLE with 28 patients (44.5%).

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Figure 1.

Age distribution by year and grouping.

The prevalence of ED was higher in patients over 65 years (Figure 1). Twenty-seven patients (42.86%) had a prior history of arterial hypertension, 20 patients had been treated for dyslipidemia (31.75%). In 16 patients, benign prostatic hyperplasia was documented (25.4%), 12 patients were medicated for diabetes mellitus (19.5%), and eight patients had penile fibrous plaques (12.7%).

Regarding the severity of ED, we found an increased prevalence of ETP in patients with hypertension, prevalence ratio (PR) 2.06, 95% CI 1.16–3.64, and a p-value of 0.01. In diabetes mellitus, no statistically significant increase in the prevalence of ETP was found, p-value of 0.28. There was an increase in the prevalence of ED in patients with benign prostatic hyperplasia PR 1.63 95% CI 0.96–275, p=0.09.

Thirty-three patients (52.3%) were found to have arterial insufficiency on the doppler ultrasound with proximal obstruction of one or both cavernous arteries. Bilateral cavernosal artery occlusion was observed in 18 (54.5%), six (18%) had a proximal obstruction of the right cavernous artery and nine (27.2) had a proximal obstruction of the left cavernous artery. The prevalence of ED WTLE in patients with proximal obstruction of the left cavernous artery was increased by PR 2, 95% CI 1.24–3.24, p=0.005. Regarding venous leakage, 14 patients (34.9%) were found to have Doppler criteria for this diagnosis, with an increase in the prevalence of ED WTLE with PR 2.62, 95% CI 1.66–4.13, p=0.0001. In addition, in eight patients (12.69%) calcifications of the tunica albuginea were evident without being related to the severity of ED (Figures 2–4).

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Figure 2.

Color Doppler ultrasound of a patient complaining of erectile dysfunction. There are three helicine arteries coming from the cavernous artery and going through the tunica albuginea.

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Figure 3.

Color Doppler ultrasound showing a collateral flow coming from the bulbo-urethral artery through the tunica albuginea going to the cavernous artery.

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Figure 4.

Erectile dysfunction test of a patient with a history of pelvic trauma showing arterial outflow through a dorsal communicating artery with reversal of flow from the cavernous artery.

Of the 63 patients evaluated, 59 (93.6%) patients had some arterial communication; 40 patients (67.7%) showed an inflow artery connecting the dorsal artery of the penis to the cavernous artery. Conversely, two patients (5%) showed outflow coming from the right cavernous artery to the right dorsal artery and three patients showed outflow from the left cavernous artery to the left dorsal artery (7.5%). Of the 59 patients who were found to have arterial communications, seven patients (11.8%) had an artery with inflow communicating with the ventral artery of the penis to the cavernous arteries.

Inter-cavernous collateral communications were seen in 22 patients (37.2%). communications between helicine arteries and extracavernosal arteries (ACH) were present in 22 patients (37.2%) (Table 1), when these outflow communications of the helicine arteries were present there was an increase in the prevalence of ED WTLE, with a PR of 2.27, 95% CI 1.3–3.95, p=0.004.

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Table 1.

Arterial communications.

Variable	%
Total population	63 (100%)
Presence of some collateral	59 (93.6%)
Presence of AC-AD collateral with input flow	40 (67.7%)
AC-AD with output flow	5 (12.5%)
AC-AD with left 3 outflow	4 (7.5%)
AC-AD with right output flow	2 (5%)
Presence of collateral AC-AV	7 (11.8%)
AC-AV with outflow	6 (85.7%)
Presence of intercavernous collateral	22 (37.2%)
Presence of as helicins with output flow	22 (37.2%)

AC: cavernous artery; AD: dorsal penis artery; AV: ventral penile artery.

Venous leak was the variable most strongly associated to the severity of the erectile dysfunction (PR 4.77, 95% CI 2.92–7.80). Likewise, age over 65 years, arterial insufficiency, proximal obstruction of the cavernous artery, helicine collateral arteries passing through the tunica albuginea, BPH and arterial hypertension, were found to increase the prevalence of ED WTLE. Notably, patients with cavernosal-dorsal, cavernous-ventral and intercavernosal communications, showed an increase in the prevalence of ED WTLE of 2.4. For each outflow artery present the severity of ED increased, prevalence ratio of 1.33 (95% CI 1.13–1.56, p=0.001).

Discussion

Although communications between the cavernous arteries and the dorsal or ventral arteries of the penis, and intercavernous communications, are believed to be normal anatomical variants even though the function of these collateral arteries in the physiology of the erection is not yet clear, they might possibly represent a mechanism of natural adaptation to ischemia induced by chronic obstruction of the cavernous arteries and be part of the spectrum of severity in ED. Moreover, helicine arteries that show outflow through the albuginea have been detected in several patients with ED and the role of this is not clearly understood.^17–19

Electron microscopy has shown that the helicine arteries and their branches directly communicate the cavernous arteries to the cavernous sinusoids, being the source of the blood supply for the erection. ²⁰

The results of this study statistically support the hypothesis that other anatomical causes such as the presence of collateral arteries with outflow from the cavernous arteries, are associated with the severity of erectile dysfunction (Figure 3).

The failure of the veno-occlusive system has been proposed as an important etiology of ED based on the indirect sonographic finding of a persistent high end diastolic velocity (EDV) in the cavernous arteries during erection. ²¹ In accordance with other studies that have evidenced outflow through collateral arteries during erection, ²² our study found a significant relationship between the presence of such outflows and the severity of ED. Outflow of collateral arteries from the cavernous arteries seems to contribute to the low pressure of the cavernous bodies and represents a low impedance vascular reservoir that leads to high diastolic flow in the cavernous arteries, (guiding criterion in the diagnosis of venous leakage) contributing to the severity of ED. ²¹ This is why the evaluation of the arteriolar component of the penile circulation is becoming increasingly important to characterize erectile functioning.^17,23

During the color Doppler evaluation no venous channels are observed going through the albuginea of the corpora cavernosa to the extracavernous venous plexus. What is really evident is the presence of multiple arterial channels dependent on the helicine arteries that carry blood in a centrifugal pattern from the corpora cavernosa to the extracavernous vasculature, moreover these vessels show a change in the type of outflow from a purely arterial wave on the flaccid penis to a venous type wave, on the erect penis (Figure 4). Therefore, we hypothesize that venous leakage might actually be a phenomenon of flow from the corpora cavernosa through the arterial pathways of the helicine arteries to the venous plexus outside the albuginea.

The severity of ED is proportionally greater in individuals over 65 years having collateral flow to the cavernous arteries and arterial insufficiency or showing any outflow from the cavernous body to the extra cavernous circulation. The hemodynamic changes that accompany aging may be the most important factor associated with the deterioration of the age-related erectile process because erection is a hemodynamic event that involves an increase in cavernous arterial flow, relaxation of the cavernous smooth muscle, and occlusion of the outflow from the sinusoids. ²³

The role of the psychogenic sexual stimulus is a factor that could not be objectively evaluated. Studies need to be conducted aimed at evaluating whether the appearance of outflow communications of the helicine arteries from the cavernous arteries are evident when the psychogenic sexual stimulus decays, which will be in favor of a detumescence role for these outflow channels.

As a cross-sectional study, our findings provide statistical support for the association between collateral penile circulation and the different anatomical variants observed and the severity of the ED. However, due to the lack of statistical power of the sample, the possibility of a type II error is not ruled out, which is why studies with a more significant sample size are required.

The objective identification of arteries passing through the tunica albuginea, leading to outflow from the corpora cavernosa raises the possibility of new lines of treatment of ED.

Conclusion

ED is of multifactorial origin. Communications between the cavernous arteries and extracavernous arteries appear to be relevant in the genesis of ED. The helicine arteries participate in the erectile mechanism, however, their participation in the process of detumescence and erection maintenance has not been described. Therefore, we suggest that they are actually a fundamental factor in the veno-occlusive mechanism.

Supplemental Material