1 Introduction

The proposed classification for vasculogenic erectile dysfunction (ED) by Nomenclature Committee of the International Society of Impotence Research in 1998 is arteriogenic, cavernosal, and mixed. The previous term, `venogenic' does not mean a disease entity but a sign of venous leakage due to veno-occlusive dysfunction. Most corporal veno-occlusive dysfunctions are not of primary venous origin and are secondary to insufficient trabecular smooth muscle relaxation. This may result from a structural alteration of the cavernosal smooth muscles<sup>[1]</sup>, excessive adrenergic constrictor tone in an anxious individual<sup>[2]</sup> or damaged parasympathetic nerves. Anatomical abnormalities such as ectopic veins exiting the cavernous corpora or abnormal communications between the cavernosum and glans/spongiosum<sup>[3]</sup>, or weak tunica albuginea of the corpora cavernosa may also result in veno-occlusive dysfunction. Defects in endothelial cell function could result in depressed nitric oxide synthesis with subsequent reduction in smooth muscle relaxation and failure of the veno-occlusive mechanism<sup>[4]</sup>. The `cavernosal' ED means the veno-occlusive dysfunction due to a structural alteration of the trabecular smooth muscles or functional defects in endothelia of the cavernous sinusoidal space.  

Several tests are available for evaluating the penile vascular inflow and outflow tract, ranging from a simple pharmacological test to more invasive tests such as duplex ultrasonography, cavernosometry, and selective internal pudendal arteriography. These dynamic tests for functional and anatomical evaluation of ED needs complete relaxation of the cavernous smooth muscle with vasoactive drugs to exclude false abnormal results due to incomplete trabecular smooth muscle relaxation. In this respect, all possible efforts should be exerted to get the greatest erectile effect for an accurate dynamic test as possible. In a study of Hatzichristou et al^[5] in 123 impotent patients, 1, 2 and 3 doses of vasoactive agents were required to achieve hemodynamic relationships consistent with complete trabecular smooth muscle relaxation in 14%, 63%, and 14% of the patients, respectively. In 9% of the patients such hemodynamic relationships were unable to be reached, which means any dynamic test can not be perfect. Montorsi et al^[6] found erectile response after the genital plus audiovisual sexual stimulation session was significantly greater than that after re-dosing.

2 The first functional vascular test: Pharmaco-test

Intracavernous injection of vasoactive drugs to evaluate the erectile capacity has been widely used as the first functional vascular screening test. The usual agents are prostaglandin E1, papaverine, a mixture of papaverine and phentolamine, or a mixture of the three drugs. In a multicenter study comparing papaverine, a mixture of papaverine and phentolamine, and prostaglandin E1, prostaglandin E1 appeared as the most accurate diagnostic drug with an overall erection rate of 74% and with the lowest prolonged erection rate of only 0.1%^[7].

Initially, a positive erectile response, defined as a rigid erection, has been presumed to signify a normal vascular status, and neurologic or psychologic factors were considered as a predominant cause for ED. If only partial, short-lived, or no erectile response resulted, vasculogenic ED was presumed^[8]. In clinical practice, however, the interpretation of the pharmacotest appeared to be more complicated. To date, we know that a positive erectile response implies normal veno-occlusive function, but not necessarily normal arterial function^[9]. A positive erectile response merely reflects an intracavernous pressure equal to or greater than 80 mmHg.

Excessive adrenergic constrictor tone as a result of anxiety may result in a false negative erectile response. We measured the levels of catecholamine in penile blood during a pharmacotest to investigate whether the secretion of endogenous catecholamines was involved in response to intracavernous papaverine^[2]. The level of norepinephrine in penile blood during the pharmacotest was higher in patients with psychogenic ED than in healthy controls or patients with vasculogenic impotence. Moreover, in the psychogenic group, it appeared to be significantly higher in nonresponders than in responders.

To reduce the false negative response to pharmacotest, genital self-stimulation^[10], vibratory stimulation^[11], visual erotic stimulation^[12], or the application of a penoscrotal tourniquet^[13] has been used. Among them genital self-stimulation would be most simple and convenient, and familiar to almost all the patients. Donatucci and Lue^[10] instructed the patients, who did not achieve full rigidity 15 min after intracavernous injection, to perform genital self-stimulation for 5 min before reevaluation. Among 25 patients who did not show a good erection even after genital self-stimulation, 21 (84%) had moderate to severe venous leakage on subsequent cavernosometry and cavernosography. In our experiences, 84.2% of the moderate responders and 50% of the poor responders with psychogenic impotence showed good erections by the combined manual stimulation. The visual sexual stimulation is also a simple, practical, inexpensive, and useful method to enhance the erectile response. However, several factors, such as habituation to erotic movies, lack of interest in erotic movies or psychological factors may not work as an additional sexual stimulator^[14], or even might reinforce adrenergic constrictor tone.

3 Additional arterial evaluation

3.1 Duplex ultrasonography

The advantages of duplex ultrasonography for both the functional and anatomical evaluation of penile arterial blood flow make it an ideal screening imaging modality.

There is considerable controversy as to the most useful parameters to measure during Doppler ultrasound studies of the cavernosal artery and what constitutes normal values. Important diagnostic indicators include arterial diameter, peak systolic flow velocity, and blood flow acceleration.

3.1.1 Changes of artery diameter

The normal cavernosal artery diameter measures from less than 0.3 to 0.7 mm. The normal artery dilates to a diameter of approximately 1 mm in size. The greatest increase in arterial diameter during a pharmacologically induced erection is seen in the early (latent) phase of erection. Dilatation of the cavernosal artery of less than 75% is considered indicative of arterial disease^[15]. Other studies, however, have found poor correlation between percentage arterial dilatation and arteriographic evidence for arterial disease^[16]. In our study, there was wider variation in the percentage increase in diameter of the cavernosal arteries in cases with a normal appearance on selective internal pudendal arteriograms than in flow velocity and the absolute value of the diameter after intracavernous injection^[17]. The mean value of percentage increase in diameter (56.1%) was much lower than the generally accepted normal value. There was no significant correlation between the degree of arterial dilatation and peak systolic velocity.

3.1.2 Peak systolic velocity (PSV)

Review of the different parameters measured and indices produced from duplex ultrasonography revealed that cavernosal PSV is the most sensitive parameter in identifying patients with arterial insufficiency, although the results of some investigators were contradictory.

Lue and associates^[8,18], who introduced image-directed Doppler ultrasonography combined with pharmacological stimulation of erection in 1985, established that the PSV of the cavernosal artery should exceed 25 cm/s within 5 min following intracavernous injection of papaverine. In a study of normal volunteers, Meuleman et al^[19] found a wide range of PSV values of 19 cm to 120 cm per second. According to Wahl et al^[20], normal mean PSV ranged from 35-60 cm/s. A PSV of 25-35 cm/s indicates mild to moderate arterial insufficiency, while measurements of less than 25 cm/s correspond to severe arterial insufficiency. Generally speaking, however, a PSV of>30 cm/s is indicative of normal arterial function^[21,22].

The penile blood flow index was calculated as the percentage increase in the diameter of the right cavernosal artery plus the percentage increase in diameter of the left cavernosal artery added to the PSV values of both arteries. When these four parameters added together is less than 285, impotence is likely to be of arteriogenic origin. Lopez et al^[23] reported 97% sensitivity and 77% specificity in diagnosing arteriogenic impotence.

There are obvious pitfalls to ultrasonography in the evaluation of vasculogenic impotence. It is highly operator dependent and the arterial variability of the penis may affect interpretation. The correlation between Doppler ultrasound and pudendal arteriography was found in only 79% of patients with variant arterial anatomy^[15]. The blood flow is measured usually at the base of the penis where blood flow at the crural segment of the cavernosal arteries is greatest. However, blood flow through the cavernosal artery at the base of the penis may not represent the total blood flow to the corporal body if an anatomical variation is present. This could lead to an underestimation of blood flow to the corpora. In addition, measurement of cavernosal PSV may be affected by improper Doppler angle adjustment. Delayed timing of ultrasound measurements may also cause false positive studies after the administration of vasoactive agents. The flow velocity of cavernosal arteries is at its maximum in the early phase of erection. During the rigid phase of erection, blood flow and arterial diameter are significantly lower than in the earlier phases of erection. Therefore, any delay in localizing the arteries leads to a falsely low estimation of PSV. A small but significant number of patients will show a delayed but eventually normal arterial response to intracavernous injection^[24]. The examination should be extended for up to 30 min in order to detect these late responders. It is unclear whether the delayed arterial response represents a normal variant or a mild form of arteriogenic impotence. Many patients have a poor response to pharmacological agents alone due to sympathetic activity as a result of anxiety, embarrassment, or fear of injection^[2]. Manual self-stimulation^[10] or viewing erotic material^[12], or re-dosing of the vasoactive drugs^[5] could be a useful adjuvant in some patients.

Using arteriography as the gold standard, the sensitivity of Doppler ultrasonography varies from 53% to 100% and specificity varies from 44% to 100%^[15,25,26]. In comparing Doppler ultrasonography with nocturnal penile tumescence monitoring, both Shabsigh et al^[27] and Allen et al^[28] reported a good correlation between the two tests except in patients with neurogenic or psychogenic erectile dysfunction. In our study, the arterial dilatation and PSV, however, did not correlate with nocturnal penile erection.

3.1.3 Blood flow acceleration

Blood flow acceleration is calculated by dividing the PSV by the systolic rise time. The systolic rise time is the time from the start of the systolic curve to its maximum value. Proximal arterial disease would be expected to produce dampening of velocity waveforms with prolongation of systolic rise times. Mellinger et al^[29] reported that blood flow acceleration appeared to correlate well with the subjective quality of erections. Oates et al^[30] found that a systolic rise time of 110 ms or more gave a positive predictive value of 92% for arteriogenic impotence compared with selective pudendal arteriogram.

3.2 Cavernosal artery systolic occlusion pressure (CASOP)

CASOP is measured during dynamic infusion cavernosometry and cavernosography, thus, it is relatively invasive and not utilized as a single diagnostic tool. Intracavernosal pressure (ICP) is elevated above the cavernosal artery systolic pressure by infusion of heparinized saline. The infusion is terminated as the cavernosal artery pulsatile flow disappears. As the ICP diminishes, the pulsatile flow is reestablished. The CASOP is defined as the ICP at which the pulsatile flow is reestablished. Significant arterial insufficiency was defined as a pressure difference of more than 20-35 mmHg between a brachial artery systolic pressure and CASOP. Padma-Nathan^[31] reported that a pressure difference greater than 35 mmHg had a sensitivity of 77% and was significantly more sensitive than flow velocity of the cavernosal artery in predicting the presence of hemodynamically significant lesions at subsequent selective internal pudendal arteriography. Rhee et al^[32] reported that peak velocity flow significantly correlated with CASOP and, using a normal value of greater than 25 cm/s, resulted in a sensitivity and specificity of 95%. However, the author found wide variation in values of the pressure gradient in patients with a normal selective internal pudendal pharmaco-angiogram^[17]. There was no significant difference in the flow velocity and the diameter changes of the cavernosal arteries and the pressure difference between those with a normal appearance on SIPA and those where the cavernosal arteries were not visualized.

3.3 Selective internal pudendal arteriography (SIPA)

It is still assumed that angiography is the most reliable method of establishing the integrity of the cavernosal arteries. Penile arteriography is an anatomical rather than a functional study, and is necessary in any patient being considered for penile arterial reconstructive surgery.

The pudendal angiography, like Doppler ultrasonography, can be open to misinterpretation. Normal variants of penile arterial anatomy can easily be confused with arterial occlusion. The angiographer must be aware of the presence and significance of these normal variants and potential collateral pathways in order to avoid the misinterpretation of obstruction. Differentiation of the cavernosal from the dorsal artery is of clinical importance. These two vessels may sometimes be confused. The poor correlation between angiography and other less invasive tests may be accounted for by these factors. Therefore, high quality selective bilateral penile pharmaco-arteriography is mandatory.

Vasoconstriction frequently encountered in small and medium size arteries can be effectively overcome with direct intrapudendal arterial injections or intracavernous injection of vasoactive drugs. Angiography is invasive and may induce significant patient anxiety with increased sympathetic output leading to false arterial abnormalities. The timing of this procedure with respect to the injection of vasoactive drugs is critical and should occur during early tumescence when arterial dilatation is maximal. Angiography performed in a patient with venous leakage may yield false results due to the escape of vasoactive drugs from the corpora. Extremely anxious patients may not respond appropriately to a vasodilator, and additional sedation may be necessary to relieve some of the anxiety. Low-osmolar high concentration contrast agents are used routinely to reduce the discomfort of pudendal injections.

In our study, there was no significant difference in the results of functional evaluations of cavernosal artery, PSV and diameter changes on duplex scanning between the normal group and cases where the cavernosal arteries were not visualized on SIPA by a completely obstructed internal pudendal artery or common penile artery^[17]. This means the SIPA is an anatomical rather than a functional study.

3.4 Radionuclide imaging

Radioisotope erection penogram was obtained with ^99mTc-pertechnetate^[33] or ^99mTc-labeled RBC^[34] or washout methods using Xenon-133^[35] following intracavernous injection of vasoactive agents. A new dynamic radioisotope technique is based on the simultaneous quantification of the change of blood volume and venous outflow, using a combination of blood pool and washout studies^[36].

4 Additional evaluation of veno-occlusive function

4.1 Cavernosometry and cavernosography

The cavernosometry with cavernosography is recommended before venous surgery to confirm the diagnosis and to locate the site of venous leakage but could not be recommended only as a routine diagnostic tool. A sustained rigid erection lasting longer than 10 min on pharmacotest is indicative of normal veno-occlusive function and does not need further evaluation for venous leakage.

The diagnosis of veno-occlusive dysfunction remains a very controversial matter, mainly because of the lack of standardized diagnostic methods. Pump cavernosometry and gravity cavernosometry are the most commonly used methods for this purpose. However, normal parameters for each are different according to different authors and to patients selection criteria. Complete relaxation of the cavernous smooth muscle is a prerequisite like a duplex ultrasonography and penile arteriography. Wespes et al^[37] defined a flow to obtain erection between 30-40 mL/min and to maintain erection between 0-5 mL/min as normal parameters of pump pharmaco-cavernosometry. Meanwhile, Dickinson and Pryor^[38] stated that the possibility of veno-occlusive dysfunction could only be considered when maintenance flow is higher than 50 mL/min. Goldstein^[39] reported that a pressure decay greater than 40 mmHg for 30 s from 150 mmHg of ICP and a flow rate of more than 5 mL/min to maintain an intracavernous pressure of 90 to 100 mmHg are considered to be dynamic evidence of corporeal veno-occlusive dysfunction. Padma-Nathan^[31] found that this dynamic evaluation correlated with cavernosographic findings in 79% of cases.

Puech-Leao et al^[40] introduced gravity cavernosometry (GC) of which flow rate is determined by the pressure gradient between the infusion pressure (140 cmH₂O) and the ICP. They advocated that GC was less invasive, simple, inexpensive and reliable method. Krane et al^[41] reported direct correlation between equilibrium rigidity monitored with RigiScan at GC and equilibrium pressure of the pump cavernosometry and between volume infused over 20 min at the GC and pump cavernosometry to measure the pressure decay. We compared GC and pump cavernosometry with cavernosographic findings in 45 patients. A maintenance flow rate and pressure decay besides induction flow rate were supposed to be very valuable in the diagnosis of venous leakage. However, the standard deviation of maintenance flow rate was too wide. Therefore, our understanding is that GC and pressure decay of the pump cavernosometry are the most valuable and reliable methods for evaluation of veno-occlusive function.

4.2 Doppler ultrasonography

4.2.1 End diastolic velocity (EDV)

Doppler ultrasound has been successfully used to document veno-occlusive dysfunction in some patients. Some investigators have shown good correlation between EDV of the cavernosal arteries and the presence of venous leakage. In the normal erectile response, there should be little (<5 cm/s) if any detectable flow within the cavernosal arteries during the diastolic phase 15 to 20 min after intracavernous injection and self stimulation. Montorisi et al^[42] reported that persistently elevated (>10 cm/s) diastolic flow in the cavernosal arteries positively correlated with a diagnosis of veno-occlusive dysfunction obtained by cavernosometry in almost 80% of cases. Other investigators suggest that an end diastolic velocity of greater than 5 cm/s is diagnostic of veno-occlusive dysfunction^[16]. Chiou et al^[24] found a significant number of patients with EDV of 0 had only engorgement or partial erection and believed that it would be a mistake to conclude that patients have adequate veno-occlusive function based on EDV alone.

4.2.2 Resistance index (RI)

Because RI=(PSV-EDV)/PSV, the result depends on the EDV. RI has also been suggested to be of value in the diagnosis of venous leakage^[43]. Merckx^[44] found a good correlation between the results of image-directed Doppler ultrasonography and those of cavernosometry (93%), using clinical observation, a persistent diastolic flow, and the RI after 10 min as diagnostic criteria. Chiou et al^[24] advocated to interpret EDV and RI while considering the status of erection at the same time to avoid error.

4.3 Radionuclide investigation

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