Monitoring brain activation changes in the early postoperative period after radical prostatectomy using fMRI

Highlights

• We evaluated the fMRI response in patients prior to and after RRP.

• Regions previously identified in healthy volunteers could be seen in the patients.

• We noted lower peak activation, probably attributed to age-related changes.

• Postoperative changes in the activation level could be demonstrated.

• Disturbances of the afferent and efferent innervation may result in those changes.

Abstract

Urinary incontinence is a major concern following radical prostatectomy. The etiology is multifactorial involving intrinsic sphincter deficiency and/or detrusor hyperactivity and/or decreased bladder compliance. Recent studies employing functional imaging methodology nicely demonstrated the reference regions of the micturition circuit. Based on these landmarks this work complements this field of research by studying patients with bladder dysfunction. Our aim was to evaluate, whether iatrogenic impairment of the pelvic floor muscles after retropubic radical prostatectomy (RRP) causes detectable changes in fMRI in the early postoperative period.

fMRI was performed at 3 T in 22 patients before and after RRP with urge to void due to a filled bladder. In a non-voiding model they were instructed to contract or to relax the pelvic floor muscles repetitively.

As previously reported in healthy men, contraction and relaxation of pelvic floor muscles induced strong activations in the brainstem and more rostral areas in our group of patients before and after RRP. In general, all of them had stronger activations during contraction than during relaxation in all regions before and after the operation. Even though there was no difference in the activation level when relaxing the pelvic floor before and after the operation, we found stronger activation during contraction when comparing the preoperative with the postoperative level in some of the regions.

The results suggest that the same cortical and subcortical networks can be demonstrated for micturition control in patients with prostate cancer as in healthy subjects. However, impaired pelvic floor muscle function after RRP seems to induce different activation intensities.

Introduction

Urinary incontinence is a major concern following radical prostatectomy. Continence rates described in the literature vary around 90% (Kundu et al., 2004, Rassweiler et al., 2003). The etiology is multifactorial. Intrinsic sphincter deficiency and/or detrusor hyperactivity and/or decreased bladder compliance may play a role (Porena et al., 2007).

In recent years functional imaging studies such as functional magnetic resonance imaging (fMRI) (Di Gangi Herms et al., 2006, Griffiths et al., 2005, Kuhtz-Buschbeck et al., 2005, Seseke et al., 2006, Seseke et al., 2008, Zhang et al., 2005) and positron emission tomography (PET) (Athwal et al., 2001, Blok et al., 1997b, Kitta et al., 2006, Matsuura et al., 2002, Nour et al., 2000) succeeded in demonstrating the core regions of the micturition circuit. The midbrain periaqueductal gray (PAG) and the pontine micturition center (PMC) as central structures and the modulating supratentorial regions known from animal and clinical studies could be visualized. Based on these landmarks patients with bladder dysfunction were studied. Griffiths et al. (2007) showed that urge-incontinence results in increased activation of the anterior cingulate gyrus. Tadic et al. (2010) demonstrated that in urge-incontinent women the strongest correlation with the severity of the symptoms can be found in regions which are usually deactivated. They concluded that the deactivated areas suppress the voiding reflex and that less deactivation leads to more severe incontinence.

There are no studies concerning iatrogenic injuries of the continence mechanism. Our aim was to evaluate whether it is possible to parallel our findings concerning the known regions of the micturition circuit from our study in healthy young males (Seseke et al., 2008) in elderly patients, despite the fact that increasing age leads to decrease in BOLD (blood oxygenation level dependent) responses (Griffiths et al., 2007, Griffiths et al., 2009). Additionally, we evaluated whether compromising the continence mechanism after retropubic radical prostatectomy (RRP) will influence the activation level or sites using fMRI in an early postoperative stage. Will the surgical alteration lead to an increase of the activation level as a result of the compensation of the weakened continence system? The results of the present study could serve as a basis to further evaluate, whether early postoperative interventions like medical treatment have an impact on cortical and subcortical activation patterns. The evaluation of the early postoperative period might be especially interesting, as the internal urethral sphincter is damaged during the RRP, causing incontinence. And even if the external sphincter is well preserved during surgery, some patients nevertheless have problems with their continence.