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Published online before print January 25, 2008, 10.1148/radiol.2463070647
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(Radiology 2008;246:783-789.)
© RSNA, 2008

Experimental Studies

Benign Prostatic Hyperplasia: Transcatheter Arterial Embolization as Potential Treatment—Preliminary Study in Pigs1

Fei Sun, MD, Francisco M. Sánchez, DVM, PhD, Verónica Crisóstomo, DVM, PhD, Juan R. Lima, DVM, PhD, Laura Luis, DVM, PhD, Virginio García-Martínez, MD, PhD, Carmen López-Sánchez, PhD, Jesús Usón, DVM, PhD, and Manuel Maynar, MD, PhD

1 From the Minimally Invasive Surgery Centre Jesús Usón, Carretera N-521, km. 41.8, 10071 Cáceres, Spain. Received April 10, 2007; revision requested June 11; revision received June 15; final version accepted August 3. F.S. supported in part by grant 2PR03A013 from Plan Regional de Investigación, Consejería de Educación, Ciencia y Tecnología, Junta de Extremadura. J.U. supported in part by grant PDT05A027 from the Junta de Extremadura (Consejería de Infraestructuras y Desarrollo Tecnológico). Address correspondence to F.S. (e-mail: feisun{at}ccmi.es).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Purpose: To prospectively evaluate the technical feasibility and safety of transcatheter arterial embolization (TAE) of the prostate in healthy pigs.

Materials and Methods: The study was approved by the institutional ethics committee for animal research. Sixteen large white male pigs were randomly assigned to the embolization group (n = 8) or control group (n = 8). Selective angiography was performed in all animals after general anesthesia was induced. In the embolization group, microspheres 500–700 µm in diameter were used to occlude the prostatic branches. Three months later, the animals' sexual function while breeding with female pigs was subjectively evaluated by using a three-point scale. At necropsy, the prostates were removed for size measurement and histopathologic examination. Paired Student t and Wilcoxon rank sum tests were used for statistical analysis.

Results: TAE was technically successful in all animals, without associated complications. The mean prostate volume after embolization was significantly (P < .001) reduced compared with the mean prostate volume for the group control. No significant difference (P = .328) in sexual function was noted between the two groups. Histologic examination revealed that the microspheres had occluded the arterioles of the prostate, with disappearance of the nearby partially normal gland structure and atrophy of the residual gland tissue.

Conclusion: TAE of the prostate can induce shrinkage of the prostate without compromising the sexual desire and erectile function of animals. This finding suggests that TAE has potential as an alternative treatment for symptomatic benign prostatic hyperplasia in humans.

© RSNA, 2008


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Benign prostatic hyperplasia (BPH) is a common tumor in elderly men. More than 50% of men have microscopic evidence of BPH by the age of 60 years (1), and more than 40% of men older than this present with clinical manifestations of this tumor (2). In the year 2000, there were approximately 4.5 million physician office visits for the primary diagnosis of BPH in the United States, with a direct cost (excluding outpatient pharmaceutical expenses) of $1.1 billion (3). Treatments for BPH typically include medication and surgery. During the past decade, a number of minimally invasive treatment modalities—including transurethral microwave thermotherapy, interstitial laser thermoablation, transurethral needle ablation, and water-induced thermotherapy—have been introduced and have rapidly generated great interest among urologists. This indicates that minimally invasive therapies are a potential trend for the clinical management of BPH (4–7).

However, transcatheter arterial embolization (TAE) is rarely used as a minimally invasive technique. According to limited clinical reports, TAE has been used mainly to control massive hemorrhage after prostatectomy or prostate biopsy (8–12). Of interest is the case report of DeMeritt and colleagues (10): A patient with BPH who had severe gross hematuria and required blood transfusion underwent prostate embolization with polyvinyl alcohol particles. The patient stopped bleeding immediately after embolization. The prostate size had reduced to 52% and 62% of the initial size by 5- and 12-month follow-up, respectively; these results were beyond all expectations. The International Prostatic Symptom score immediately before embolization, 24, was decreased to 13 at 5 and 12 months after TAE. In addition, the patient reportedly experienced no change in sexual function after embolization. The results of this case (10) suggest that TAE might be an alternative treatment for symptomatic BPH. To our knowledge, no preliminary study of this subject involving animal experiments has been reported. Thus, the purpose of our study was to prospectively evaluate the technical feasibility and safety of TAE of the prostate in healthy pigs.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Animals
The experimental protocols were approved by the institutional ethics committee for animal research of the Minimally Invasive Surgery Centre Jesús Usón. Sixteen healthy large white male pigs with a mean body weight of 80 kg ± 5 (standard deviation) were used. All pigs were randomly assigned to the TAE group (n = 8) or the control group (n = 8). In the animals in the TAE group, selective angiography followed by embolization of the prostate was performed. Only selective angiography was performed in the animals in the control group. To evaluate the sexual function of the pigs after angiography and prostate embolization, 15 female pigs were used for mating.

Angiography and TAE
After receiving no food for 24 hours, each male pig was premedicated with 0.1 mg of diazepam per kilogram of body weight, 10 mg/kg ketamine, and 0.01 mg/kg atropine intramuscularly. Anesthesia was induced with 2 mg/kg propofol administered intravenously. After the pig was endotracheally intubated, it was connected to an anesthesia system (Ohmeda Excel 210 SE; Boc Group, Madison, Wis) and a mechanical ventilator (Ohmeda 7800; Boc Group). Anesthesia was maintained with 2.0%–2.5% halothane. The pigs were fixed supine on the operating table and given 0.15 mL of amoxicillin trihydrate plus potassium clavulanate (Synulox; Pfizer, New York, NY) per kilogram of body weight intramuscularly. The groin area and lower abdomen were shaved and draped in a sterile manner.

Femoral arterial access was gained percutaneously with a 5-F introducer sheath (Check-flo; William Cook Europe, Bjaeverskov, Denmark). After pelvic angiography (BV-300; Philips, Best, the Netherlands) was performed, a 5-F Cobra catheter (Radifocus Cobra Small; Terumo, Tokyo, Japan) was inserted into the aorta and the catheter tip was shaped into a Waltman loop from the contralateral external iliac artery. With road map guidance, selective catheterization to the internal iliac artery on both sides was achieved. Angiography was performed in the two arteries. The control group animals then recovered from anesthesia.

Selective embolization of the prostate was performed in the TAE group animals. After the systemic distribution of heparin by means of intravenous administration of 150 IU of heparin (Heparina ROVI 0.5%; ROVI SA, Madrid, Spain) per kilogram of body weight, a 3-F infusion catheter (MicroFerret-18; William Cook Europe) was inserted coaxially through the Cobra catheter and selectively placed in the prostatic branch of the inferior vesical artery. Superselective angiography was performed by manually injecting 1 mL of contrast medium to ensure that the tip of the microinfusion catheter was at the desired site. Microspheres (Embosphere; Biosphere Medical, Louvres, France) calibrated to 500–700 µm in diameter were used for embolization. Each vial of microspheres, containing 2.0 mL of microsphere particles, was diluted in a mixture of 20 mL of 50% iodinated contrast medium plus 50% normal saline solution. The mixture was slowly injected with fluoroscopic guidance. Embolization was immediately terminated when hemostasis was achieved without reflux of the mixture to undesired arteries. Follow-up angiography was performed. Embolization was then performed on the other side by using the same technique. All angiography and embolization procedures were performed by two interventionalists (F.S., V.C., 15 and 5 years experience, respectively). The animals were then allowed to recover from anesthesia and were sent to the animal care unit. After embolization, all animals were checked twice a day for 72 hours and then once daily for 1 week for possible complications associated with embolization.

Sexual Function Testing
To evaluate the chronic effects of TAE on sexual function, sexual function testing was performed in seven TAE group pigs and eight control group pigs 3 months after the procedures (F.S.). One TAE group pig was excluded from sexual function testing because of a severe infection that developed in one hind limb secondary to trauma in the second month after embolization. Accordingly, 15 prepubescent female pigs were used to evaluate the sexual function of the male pigs. To induce the onset of estrus, all female pigs were intramuscularly injected with one dose of pregnant mare serum gonadotropin plus human chorionic gonadotropin (PG 600; Intervet International, Boxmeer, the Netherlands). The female pigs were deemed to be in estrus when the vulva was reddened. Once estrus was exhibited, each female pig was randomly allocated to mate with one male pig. The sexual behavior of each male pig was subjectively rated on a scale of 0–3: A score of 0 was assigned when the pig did not exhibit sexual behavior; a score of 1, when the pig attempted to mount the partner; a score of 2, when the pig had an erect penis when it mounted the partner; and a score of 3, when the pig accomplished intromission and ejaculation.

Prostate Size Measurement and Histopathologic Examination
After being premedicated, all animals were sacrificed by means of intravenous injection of potassium chloride solution. Necropsy and gross pathologic examination were immediately performed. The prostate was removed, and the volume of the prostate was measured in a measuring cylinder partially filled with 10% buffered formalin solution (F.S.). Formalin-fixed specimens were processed by means of paraffin embedding. After transverse 5-mm-thick sections were prepared, standard hematoxylin-eosin staining was performed. Microscopic examinations were conducted by two pathologists (V.G., C.L., 25 and 15 years experience, respectively), with focus on the occluded arteriole and the biologic reactions of the gland tissue.

Statistical Analyses
Statistical software (SPSS, version 11; SPSS, Chicago, Ill) was used to perform statistical analyses. Prostate volumes in the embolization and control groups were compared and tested for significant differences by using the Student t test for paired samples. Sexual function scores were compared between the two groups by using the Wilcoxon rank sum test. P < .05 was considered to indicate a significant difference.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Angiography and Embolization
For all procedures, selective catheterization and angiography of the internal iliac artery were successfully performed on both sides by using a 5-F angiographic catheter. The angiograms showed that the prostate received its blood supply from the bilateral fine prostatic branches (Fig 1). Superselective catheterization to the bilateral prostatic branches and subsequent embolization were performed with a 3-F microinfusion catheter in all animals in the embolization group (Fig 2). In each animal, approximately one-fourth to one-third of the microsphere vial (5–7 mL of the mixture of embolic agents) was used to achieve embolization on both sides.


Figure 1
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  		Figure 1: Selective posteroanterior-view angiogram of left internal iliac artery shows bilateral visceral arteries due to vascular anastomosis. Note the inferior vesical artery (arrow) and its prostatic branches (arrowheads).

 

Figure 2
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  		Figure 2: Superselective posteroanterior-view angiogram obtained by using microcatheter before embolization shows the prostatic branches.

 
Postprocedural Observation
No acute urinary retention, sign of peritonitis, skin or muscle ischemic necrosis in the perianal region or the buttock, or hind limb lameness was noted during the first-week veterinary observation after the procedures.

Sexual Function Testing
When the 15 male pigs—seven embolization group animals and eight control group animals—were evaluated for sexual behavior with use of subjective scoring, Wilcoxon rank sum testing revealed no significant difference in sexual function between the two groups (P = .328) (Table 1).


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  		Table 1. Sexual Function Test Scores

 
Histopathologic Examination
At necropsy, the urinary bladder, ureters and deferent ducts on both sides, urethra, sigmoid colon, and rectum appeared to be normal in all animals. The prostates of the embolization group animals were pale and deformed in shape compared with those of the control animals. The mean volumes of the prostate were 3.9 mL ± 1.3 (standard deviation) and 7.3 mL ± 2.3 for the embolization group and control group animals, respectively. Results of the Student t test for paired samples suggest that the prostate volume in the embolization group animals was significantly decreased (P < .001) compared with that in the control group animals (Table 2).


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  		Table 2. Prostate Volumes for Pigs in Embolization and Control Groups

 
Microscopic examination revealed that the microsphere particles had occluded the arterioles of the prostate in the embolization group pigs. The walls of the occluded arterioles were thickened and showed leukocytic infiltration. The partially normal gland structure near the occluded arterioles disappeared and was replaced by fibrotic tissue, while most of the residual gland tissue appeared to be atrophied (Fig 3).


Figure 3
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  		Figure 3: Photomicrograph of histologic section shows a microsphere particle occluding the arteriole of the prostate (E), disappearance of the nearby normal gland structure, and atrophy of the residual gland tissue. (Hematoxylin-eosin stain; original magnification, x32.)

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
It is generally believed that lower urinary tract symptoms (LUTS) in patients with BPH are a result of static and dynamic pathologic components (13). The static component is related to the enlarged prostate with hyperplasia of the glandular epithelium and stroma, which directly leads to bladder outlet obstruction due to mass effect. Although the pathogenesis of BPH is still poorly understood, circulating androgens and intraprostatic androgen metabolism have been suggested as major mechanisms. Free plasma testosterone enters the prostatic cell, where 5{alpha}-reductase converts at least 90% of the testosterone to dihydrotestosterone (DHT). DHT binds to the androgen receptor and then induces alterations in DNA, leading to metabolic effects on protein synthesis and prostate growth (13,14). This mechanism represents a cornerstone of the use of 5{alpha}-reductase inhibitors, such as finasteride, in the treatment of BPH.

The dynamic pathologic component of BPH-related LUTS is related to the prostatic smooth muscle tone or the degree of smooth muscle contraction within the prostate. The prostate receives innervations from the sympathetic and parasympathetic nerve systems. An increase in neuromuscular tone in the prostate may lead to a reduced urinary flow rate and thus worsened symptoms associated with BPH. Previous studies have revealed that {alpha}1-adrenergic receptors predominate in the prostatic stroma, prostatic capsule, and bladder neck and mediate the tone of the smooth muscle (15,16). These findings are the basis for the use of {alpha}1-adrenoceptor blockers, such as tamsulosin, in the management of symptomatic BPH.

With a primary purpose of relieving the clinical symptoms of BPH, TAE is also focused on the two pathologic components. The primary goal of TAE in the treatment of BPH is to reduce the volume of the enlarged prostate. TAE has been widely used for treatment of symptomatic uterine fibroids with satisfactory clinical outcomes (17,18). A well-accepted underlying mechanism of TAE is the ischemia or hypoxia that it induces in tumors, with resultant apoptosis, necrosis, sclerosis, and subsequent shrinkage. Since clinical responses to TAE vary greatly, depending on the tumor's tolerance of or sensitivity to hypoxia, the biologic reactions of prostatic tissue to hypoxia are critical to the potential application of TAE. Results of previous studies (19–21) involving castrated rat models suggest that the loss of the bulk of the prostate tissue due to apoptosis is driven by hypoxia that occurs as a result of the loss of prostatic blood flow. In these studies, 45% and 92% reductions in prostatic blood flow were observed during the first 24 hours and 7 days after castration, respectively, and 86% of the rat prostate gland cells were lost owing to the induction of prostatic cell apoptosis within the first week (19–21).

However, the sensitivity of the prostate to ischemia is rarely reported for large animals. In a preliminary study, the prostates of all four examined dogs were noted to have shrunk remarkably after the ligation of both inferior vesical arteries (22). In our study, the prostate volume for animals in the embolization group was found to be significantly reduced 3 months after TAE compared with the prostate volume for animals in the control group. Histologic examination revealed that the partially normal gland tissue near the occluded arterioles disappeared, with fibrotic tissue formation seen in its place. These findings further support the assumption that the prostate is sensitive to hypoxia and TAE may effectively reduce the prostate volume.

Despite the lack of evidence of the effectiveness of TAE in experimental animals with BPH, the case report by DeMeritt and colleagues (10) indicates that TAE can successfully induce shrinkage of the enlarged prostate and thus relieve the clinical symptoms of patients with BPH. A more recent clinical report on TAE in the management of symptomatic BPH published in the non–English-language literature (22) describes the findings in 12 patients aged 61–82 years who underwent TAE with 150–250-µm polyvinyl alcohol particles and gelatin sponge particles: When the baseline clinical data before embolization were compared with those at 6-month follow-up, the mean International Prostatic Symptom score had decreased from 24.2 to 4.8 and the mean prostate volume had decreased from 127 to 90 mL, with a mean reduction of 29%.

In addition, prostate embolization may greatly decrease the amount of free plasma testosterone that enters prostate cells such that less DHT is converted from the plasma testosterone in the prostate. This, in turn, results in less protein synthesis and the secondary inhibition of prostate growth. This process might be a potential rationale for performing TAE therapy. Furthermore, given that hypoxia or ischemia may induce prostate cell death and necrosis, it is reasonable to expect a decreased number of some receptors, such as {alpha}1-adrenergic receptors, in the affected prostate tissue to some extent after embolization. As a result, the neuromuscular tone might decrease and the severity of clinical symptoms associated with the dynamic pathologic component of BPH might decrease. Although the assumption of induced apoptosis and decreased number of {alpha}-receptors after transurethral microwave thermotherapy and transurethral fine needle ablation has been proved (23–25), the loss of {alpha}1-adrenergic receptors in the prostate after TAE and the related benefits remain to be addressed in future studies.

Several severe complications associated with internal iliac artery embolization to control pelvic hemorrhage have been documented in the literature. These complications include skin necrosis, muscle necrosis, bladder wall necrosis, and paresis due to ischemic neurologic damage (26–29). Most such complications were reported early in the 1970s to 1980s. In the procedures associated with these complications, an angiographic catheter rather than a microcatheter with a coaxial system was used. Because the relatively large size of the angiographic catheter limits further superselective catheterization to the fine visceral branches, embolic agents may occlude muscle vessels—directly or indirectly by means of reflux—and thus potentially lead to skin and muscle necrosis or infarction of the spinal cord or major nerves (26,28,29). When the embolic agents extensively occlude the umbilical artery, inferior vesical artery, and obturator artery that maintain the blood supply to the normal bladder wall, bladder wall necrosis may occur (27). In contrast, with use of a coaxial system, the microcatheter can be readily inserted into small visceral vessels, such as the prostatic branches from the inferior vesical artery described in our study. Accordingly, embolic agents injected with the microcatheter can selectively block the blood supply to the prostate without untoward embolization of the muscle branches or associated complications. The fact that none of the described complications was observed in our study supports the technical safety of prostate embolization performed by using a microcatheter and a coaxial system.

It is worth noting that bladder catheterization was not performed before TAE in our study and no acute urinary retention was encountered after embolization in any case. This indicates that TAE performed for management of BPH might not necessitate postoperative bladder catheterization in future clinical practice. In contrast, with conventional surgery and most minimally invasive therapies, an indwelling catheter is generally maintained for days to weeks (30). These described advantages of TAE may facilitate greatly shortened hospital stays.

Sexuality is an important component of quality of life. Although sexual function decreases with age, survey results have revealed that sexual activity is common in the majority of men older than 50 years and that approximately 65% of men are still sexually active at the age of 70 years (31,32). Studies have revealed that LUTS and sexual dysfunctions such as erectile dysfunction (ED) and abnormal ejaculation are strongly linked and that the presence and severity of LUTS are independent risk factors for sexual dysfunction in older men (32–34). Accordingly, optimal management of BPH in patients is aimed at both effective relief of LUTS and reduced sexual dysfunction.

Transurethral resection of the prostate (TURP) remains the most effective therapy for relief of BPH-related LUTS. However, the reported median frequencies of ED and ejaculation dysfunction after TURP are 10% and 65%, respectively, compared with a 2% frequency of both conditions in sham-controlled conditions (30). Open surgery (suprapubic or retropubic prostatectomy), another conventional surgery indicated for large obstructive prostates, is reportedly associated with a 3%–5% risk of ED and a 61%–93% risk of retrograde ejaculation (30,35).

Transurethral microwave thermotherapy, transurethral needle ablation, and interstitial laser thermoablation are common minimally invasive therapies for symptomatic BPH. It is generally believed that the ED associated with these therapies is minimal, with ejaculation dysfunction being the major sexual side effect. In a prospective clinical study (36), ejaculation loss or severely decreased ejaculate volume was reported in 48.6%, 28.1%, 21.6%, and 24.3% of cases of treatment with TURP, interstitial laser coagulation, transurethral microwave thermotherapy, and transurethral needle ablation, respectively.

Compared with the described therapies, TAE as an alternative treatment may have less of a negative effect on sexual function. Previous study results suggest that decreased libido and ED might be related to reduced DHT levels and that the serum DHT concentration may be lowered by 60%–80% after administration of 5{alpha}-reductase inhibitors such as finasteride (37,38). ED, especially that associated with TURP, has also been attributed to cavernous nerve damage. Neurovascular bundles extend posteriorly and laterally to the prostate at a few millimeters from the prostatic capsule and terminate in the cavernous nerves. Thus, thermal nerve damage or direct injury to the neurovascular bundles due to capsular perforation during TURP may lead to postoperative ED (39). In our study, analysis of the pigs' subjective scores for sexual behavior revealed that neither libido nor erectile function was compromised after TAE, whereas the prostate volume was significantly decreased. These findings can be explained by the facts that TAE does not affect the serum DHT concentration and that with superselective catheterization, the TAE is focused on the therapeutic target without damage to the neurovascular bundles.

Retrograde ejaculation is a common concern and is frequently experienced by patients after TURP and other minimally invasive therapies. With these procedures, the normal bladder neck mechanism that contracts to allow antegrade ejaculation is surgically damaged. As a result, the bladder neck is fixed in a static open position and semen flows backward into the bladder during ejaculation (40). Although it seems reasonable that TAE could relieve the clinical symptoms of BPH while preserving the normal bladder neck mechanism, we did not address the issue of retrograde ejaculation in our study. The other major limitation of our study was the lack of an animal model of BPH, mimicking this abnormality in human patients, in which to evaluate the technical effectiveness and safety of TAE.

Practical applications: The results of our animal experiments suggest that TAE is a potential alternative treatment for symptomatic BPH. TAE of the prostate can be safely performed in pigs by using a microcatheter with a coaxial system. After embolization, the prostate volume was significantly decreased without a compromise in the animals' sexual desire or erectile function.


   ADVANCES IN KNOWLEDGE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 


   IMPLICATION FOR PATIENT CARE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
References
 


   FOOTNOTES
 

Abbreviations: BPH = benign prostatic hyperplasia • DHT = dihydrotestosterone • ED = erectile dysfunction • LUTS = lower urinary tract symptoms • TAE = transcatheter arterial embolization • TURP = transurethral resection of the prostate

Guarantor of integrity of entire study, F.S.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, F.S.; experimental studies, all authors; and manuscript editing, F.S., M.M.

Authors stated no financial relationship to disclose.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 

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M. A. Mauro
Can Hyperplastic Prostate Follow Uterine Fibroids and Be Managed with Transcatheter Arterial Embolization?
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