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Urodynamics, Neurourology and Pelvic Floor Dysfunctions

Gianfranco Lamberti
Donatella Giraudo
Stefania Musco Editors

Suprapontine
Lesions and
Neurogenic Pelvic
Dysfunctions
Assessment, Treatment and
Rehabilitation
Urodynamics, Neurourology and Pelvic
Floor Dysfunctions

Series Editor
Marco Soligo
Obstetrics and Gynecology Department
Buzzi Hospital - University of Milan
Milan, Italy
The aim of the book series is to highlight new knowledge on physiopathology,
diagnosis and treatment in the fields of pelvic floor dysfunctions, incontinence and
neurourology for specialists (urologists, gynecologists, neurologists, pediatricians,
physiatrists), nurses, physiotherapists and institutions such as universities and
hospitals.

More information about this series at http://www.springer.com/series/13503

Gianfranco Lamberti • Donatella Giraudo
Stefania Musco
Editors

Suprapontine Lesions
and Neurogenic Pelvic
Dysfunctions
Assessment, Treatment
and Rehabilitation
Editors
Gianfranco Lamberti Donatella Giraudo
Neurorehabilitation Unit and Pelvic Floor Urology Department
Dysfunction Rehabilitation Center San Raffaele Hospital
SS Trinità Hospital Milano
Cuneo Italy
Italy

Stefania Musco
Department of Neurourology
Careggi University Hospital
Florence
Italy

ISSN 2510-4047     ISSN 2510-4055 (electronic)

Urodynamics, Neurourology and Pelvic Floor Dysfunctions
ISBN 978-3-030-29774-9    ISBN 978-3-030-29775-6 (eBook)
https://doi.org/10.1007/978-3-030-29775-6

© Springer Nature Switzerland AG 2020

This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of
the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation,
broadcasting, reproduction on microfilms or in any other physical way, and transmission or information
storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology
now known or hereafter developed.
The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication
does not imply, even in the absence of a specific statement, that such names are exempt from the relevant
protective laws and regulations and therefore free for general use.
The publisher, the authors, and the editors are safe to assume that the advice and information in this book
are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the
editors give a warranty, express or implied, with respect to the material contained herein or for any errors
or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims
in published maps and institutional affiliations.

This Springer imprint is published by the registered company Springer Nature Switzerland AG
The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland
Foreword

Since 2015, Springer has published five volumes on functional pelvic floor hot top-
ics under the auspices of the Italian Society of Urodynamics (SIUD). Our volumes
always try to portray at best functional aspects in different clinical settings: oncol-
ogy, male urology, genital prolapse, paediatrics, giving original and innovative per-
spectives in different backgrounds in an eclectic way.
The present volume fulfils our mission, looking at neurogenic pelvic floor dys-
functions from an original and, at the present time, still poorly investigated point of
view: the suprapontine lesions. Since recent years, neurourologists have been focus-
ing mainly on spinal cord lesions, developing high-level expertise in their under-
standing and management. More recently, also driven by the changing epidemiology
of neurological disorders with an impact on pelvic floor functions, suprapontine
lesions are increasingly becoming a matter of study. This book will offer an in-depth
look on this topic from a multidisciplinary and multi-professional perspective, wid-
ening the scenario of potentially interested readers, spanning from neurourologists
and clinicians devoted to urodynamics, to those operating in stroke units, including
all the rehabilitation professional figures who will find an updated understanding of
the set of problems many of their patients are involved with. The international fac-
ulty further guarantees an appealing experience with this book.
In the major interest of our patients, we do hope this volume will pique your
interest.

Prof. Marco Soligo

Adjunct Professor in Urogynecology - University of Milan
President of the Italian Society of Urodynamics (SIUD)
Milan, Italy

v
Preface

If we wanted to choose an area of rehabilitation, the field in which we can find the
most multicultural and interprofessional evolution, this could be indeed the rehabili-
tation of perineal and pelvic dysfunctions. Despite that, few are known about the
role of pelvic rehabilitation in some specific neurological populations who poten-
tially benefit on that. The purpose of this book is to provide a general introduction
to the knowledge of pelvic disorders in people affected by suprapontine lesion. The
book is addressed to professionals who are dealing with these types of illnesses for
the first time as well as to those who are already experts and want to extend their
knowledge and interests in this field.
The book takes its cue from the literature and gives more in-depth insights on the
diagnosis and treatment of neurogenic urinary and bowel dysfunctions considering
also the evolution of the functional imaging techniques in the last decades which has
helped us to better understand the physiopathological differences and peculiarities
of this subtype of neurological patients having suprapontine lesions and secondary
pelvic dysfunctions. The interdisciplinary and multidisciplinary fields of actions
involving doctors and health professionals (often with profoundly different back-
grounds) are often still uncharted, but surely, it should tend towards an increasingly
holistic view, in which overall components cannot be dissociable from the context.
Furthermore, the relationships and networks between damage, brain function, blad-
der and intestinal behaviour are still poorly understood. Thus, the management of
pelvic floor dysfunctions in such complex patients is a harder challenge to face
compared to non-neurological or even in spinal cord-injured patients.
We hope that this book can open up ways of communication among different
professionals by making this topic more accessible, often inexplicably confined
(concerning the epidemiological impact and quality of life), to few specialized
centres.
In order to make the material more friendly, we have tried to easily explain the
various subtopics to be understandable even by professionals who are not specialists
in neurourology. We hope we have succeeded in giving a reasonably exhaustive
view of this area of its extensive and complex investigations and treatments, in such
a way as to involve professionals of other specialties (e.g. rehabilitation, internal
medicine, neurology) who often are involved in these pathologies.
After a general introduction on the neurophysiopathology of suprapontine
lesions, the book is divided into chapters, each one concerning a specific subtopic

vii
viii Preface

including the diagnosis and treatment of the various pelvic dysfunctions among the
different types of neurological suprapontine lesions. The influence of the clinical
experience in the daily management of these problems is evident in the development
and writing of the authors’ contributions.
The main epidemiological aspects, always in relation to the patient with a supra-
pontine lesion, clinical evaluation of the perineum and the main reflexes, functional
imaging of the central nervous system, urodynamic investigation and chronic pelvic
pain are then taken into consideration. Particular attention has been paid to the reha-
bilitative aspects of bowel dysfunctions, often neglected in these neurological sub-
populations compared to spinal cord injury patients. Again, also, two interesting but
still poorly addressed arguments have been taken into account, namely, pelvic floor
muscle training and sexual dysfunctions. The various chapters necessary for educa-
tional purposes are actually to be understood as inseparable moments of a unitary
and continuous process.
The writing of this book would not have been possible without the tolerance and
goodwill of many of our colleagues to whom we extend our gratitude. Finally, we
are very grateful to our many patients who, despite the personal tragedy of brain
damage, have made the development of our observations possible.

Milano, Italy Donatella Giraudo

Florence, Italy  Stefania Musco
Piacenza, Italy  Gianfranco Lamberti
Contents

1 The Bladder, the Rectum and the Sphincters: Neural Pathways

and Peripheral Control������������������������������������������������������������������������������   1
Gianfranco Lamberti and Antonella Biroli
2 Reflex Testing and Pelvic Examination���������������������������������������������������� 23
Donatella Giraudo and Francesco Verderosa
3 Investigation of the Central Nervous System in Neurogenic Pelvic
Dysfunctions by Imaging�������������������������������������������������������������������������� 35
Achim Herms and Alida M. R. Di Gangi Herms
4 Urodynamic Patterns and Prevalence of N-LUTDs
in Suprapontine Lesions���������������������������������������������������������������������������� 45
Eugenia Fragalà
5 Suprapontine Lesions and Neurogenic Pelvic Dysfunctions������������������ 53
Julien Renard, Eugenia Fragalà, Gianfranco Lamberti,
Federica Petraglia, Francesco Verderosa, Anna Cassio,
and Giovanni Panariello
6 Management of the Central Nervous System Chronic
Pelvic Pain�������������������������������������������������������������������������������������������������� 61
Marilena Gubbiotti and Antonella Giannantoni
7 Management of Bowel Dysfunction in Patients with Central
Nervous System Diseases �������������������������������������������������������������������������� 71
Gabriele Bazzocchi, Mimosa Balloni, Erica Poletti, Roberta Manara,
Paola Mongardi, Marica Vicchi, Eugenia Fragalà, Elena Demertzis,
Antonella Manzan, and Humberto Cerrel Bazo
8 Management of the Suprapontine Neurogenic Lower Urinary
Tract Dysfunction�������������������������������������������������������������������������������������� 81
Gaetano De Rienzo, Gianfranco Lamberti, Luisa De Palma,
Donatella Giraudo, Elena Bertolucci, Giuseppina Gibertini,
Caterina Gruosso, and Roberta Robol

ix
x Contents

9 Pelvic Floor Muscle Training and Neurogenic Overactive Bladder

in Stroke and Multiple Sclerosis �������������������������������������������������������������� 93
Kari Bø
10 Sexual Dysfunction in Suprapontine Lesions������������������������������������������ 107
David B. Vodušek
The Bladder, the Rectum
and the Sphincters: Neural Pathways 1
and Peripheral Control

Gianfranco Lamberti and Antonella Biroli

1.1 Introduction

Despite the fundamental contribution given by functional imaging in recent years, to

date, the relationships between the different pathways in coordinating the alternation
between the bladder-filling phase and the emptying phase have not yet been clarified
nor, above all, which area should be considered as the “final decision maker” for
activating micturition. The periaqueductal grey (PAG) and the pontine micturition
centre (PMC) (Fig. 1.1), under physiological conditions with mutual influence, under
the voluntary control of the prefrontal cortex (PFC) (Fig. 1.2), control the function.
These three areas, in turn influenced by various afferents, coordinate the synchroni-
sation between recruitment and inhibition of smooth and striated muscles [1–6]
which regulate the behaviour of the bladder (the system’s reservoir), the bladder neck
and the urethra. The neural control is peripherally guaranteed by the parasympathetic
sacral nerve (pelvic nerves), by the sympathetic thoracic lumbar nerve (hypogastric
nerves) and by the sacral somatic nerve [pudendal nerve] [7, 8].
The importance of bladder control in controlling the homeostasis of the organism
is guaranteed by the regular emptying of the bladder itself, which must be both safe
and appropriate.
Processing the sensation of the bladder filling up is a cognitive element for main-
taining equilibrium [9–11] which must determine finalised behaviours and conse-
quent coherent motor activities [12].
The progression of the feeling of fullness begins with nerve signals whose fre-
quency, intensity and unpleasantness increase proportionally to the bladder filling,

G. Lamberti (*)
Neurorehabilitation Unit and Pelvic Floor Dysfunction Rehabilitation Center,
SS Trinità Hospital, Cuneo, Italy
A. Biroli
Neurological and Autonomic Dysfunction Rehabilitation Unit,
S.G. Bosco Hospital, Turin, Italy

© Springer Nature Switzerland AG 2020 1

G. Lamberti et al. (eds.), Suprapontine Lesions and Neurogenic Pelvic
Dysfunctions, Urodynamics, Neurourology and Pelvic Floor Dysfunctions,
https://doi.org/10.1007/978-3-030-29775-6_1
2 G. Lamberti and A. Biroli

Fig. 1.1 Cerebral and

brainstem nuclei and
pathways related to
micturition and defecation. CC FNX
Abbreviations: CC Corpus
callosum, FNX Fornix, HY
Hypothalamus, DLF DLF
Fasciculus longitudinalis HY PAG
dorsalis, PAG
Periaqueductal grey, PBN INF
Parabrachial nucleus, SOL 1
Nucleus solitarius. PBN
1 = Pontine micturition 2
centre (PMC).
2 = Kölliker-Fuse nucleus.
3 = Pontine continence 3
SOL
centre (PCC)

Fig. 1.2 Hippocampus,

amygdala, subregions of
prefrontal cortex and
dorsal anterior cingulate Dorsal anterior
cortex, cerebral areas cingulate cortex
associated with the control
of the temporal and spatial Amygdala
appropriateness of social
continence Ventromedial
prefrontal
cortex
Hippocampus
Orbitofrontal Dorsolateral
prefrontal prefrontal
cortex cortex

until the individual is obliged to urinate: the fullness cannot be maintained indefi-
nitely and at some point the bladder must be emptied.

1.2 The Bladder Function

The filling and the emptying phase:

Urodynamic tests record the perception of the fullness level: the “first filling
sensation” in healthy subjects (a sensation that is often not precisely perceptible,
which often one does not pay attention to) occurs at about 40% of the total capacity
of the detrusor; the International Continence Society (ICS) defines the “first desire
to urinate as the sensation during a flow cystometry, which would lead the patient to
urinate at the first opportune moment, although with the possibility of postponing
further the emptying” [13] and usually refers to approximately 60% of the total
1 The Bladder, the Rectum and the Sphincters: Neural Pathways and Peripheral… 3

Fig. 1.3 Bladder filling,

desire to void and
behaviour

300 - 500 cc
Strong desire

Volume voided
Bladder filling
Achievement
First desire
Orientation
First sensation
Initiation
100 cc

detrusor capacity. The “strong desire” to urinate is defined by ICS as “the persistent
urge to urinate without the fear of the urine escaping” [13] (Fig. 1.3). These three
conditions should be considered normal; the appearance of a “sudden and impelling
desire to empty” (urgency) can instead be considered as a symptom of overactive
bladder syndrome. People who report urinary urgency should, in any case, be con-
sidered in a non-physiological condition concerning the bladder function.
Under normal conditions, continence control allows the accumulation of urine,
preventing emptying until the filling is complete.
The emptying phase only lasts for a short period of the complete behavioural
cycle: considering how long the micturition can last and that it can be done six
or seven times a day, the time dedicated to emptying does not exceed 1% of the
total time [14].
Finally, the emptying occurs only if appropriate and the main criteria are social
(adequate place and adequate time) and behavioural appropriateness (an adequate
situation in order to avoid any embarrassment concerning the gesture) [15]. It is
known that an attentional shift can influence the perception of the bladder-filling
status, similarly to what occurs with the perception of pain, while a state of anxiety
can increase the level of the desire to urinate, which only confirms how many psy-
chological conditions may, in fact, alter the state of perception of the fullness of the
bladder [14].

1.2.1 Spinal Cord Afferents

The afferent pathways reach the lower urinary tract through the pelvic, hypogastric
nerves and the pudendal nerve stem [5, 14, 16, 17]: they are activated by the bladder
distension and inhibit the detrusor parasympathetic system. Thanks to modern
4 G. Lamberti and A. Biroli

impregnation techniques it is possible to map first-level axons, coming from the

peripheral areas, directed towards the lumbosacral posterior root ganglia (dorsal
root ganglion, DRG) and to the terminations in the spinal cord, in order to then
interpret their hypothetical role. The neurons from the detrusor wall project to the
lumbar (T11–L2) and sacral (S2–S4) tracts and are responsible for controlling spi-
nal reflex activity and for transmitting the perception of the need to urinate through
the ascending pathways to the encephalic regions.
In men, it is possible to identify a dense nervous network (“sensory web”) [4]
widespread in the basal urothelial layer of the bladder [18–20] with some nerve end-
ings projecting as far as the urothelium [21–23]; hence the medullary afferents are
represented by two different types of fibres: myelinated fibres “A-δ” and small non-­
myelinated “C” fibres [24–28] (Fig. 1.4).
The lower threshold fibres (“A-δ”) are myelinated (while non-myelinated
fibres—“C” fibres—have higher thresholds) [4] and in most cases are sensi-
tive to mechanical stimulation and respond to the bladder filling with a varying

PGC

1
3
5
ILC
7

IMG Sympathetic T10-L2

HN

PG

PGC

1
PN DRG 3
B 5
ILC
Ad
7

PG

Parasympathetic S2-S4
EUS Somatic S2-S4
PN

Fig. 1.4 Neural control of the lower urinary tract. Abbreviations: PG Pelvic ganglion, IMG
Inferomesenteric ganglion, HN Hypogastric nerve, PN Pelvic nerve, DRG Dorsal root ganglion,
PGC Posterior grey commissure, ILC Intermedio-lateral column: 1, 3, 5, 7 = Rexed laminae I, III,
V, VII. Dotted line = Afferent pathways. Full line = Efferent pathways
1 The Bladder, the Rectum and the Sphincters: Neural Pathways and Peripheral… 5

volume sensitivity threshold, from normal filling to extreme distension. Both

passive distension and active contraction activate fibres with larger diameters to
convey information related to bladder filling in physiological conditions [16].
The fibres with smaller diameters can normally be called “silent”, since they
do not operate with bladder distension alone, except with large volumes; also
found in the intestine, they are instead able to convey information from intra-
luminal stimuli of a chemoceptive nature such as saline hypertonicity or that
of a thermal nature [29, 30] sensitising themselves in pathological conditions
(neuropathic or inflammatory ones) and determining the sensation of urgency
or visceral pain.
In addition to the intrinsic characteristics of the detrusor smooth muscle, the fill-
ing phase is made possible by the inhibition of the parasympathetic efferent path-
ways [3] and by the sympathetic system with the activation of the sphincter function
[31, 32]. Bladder adaptation allows an intra-bladder pressure with low values with
a volume below the threshold of the desire to urinate.
The afferent bladder fibres project to the posterior horn of the sacral cord [33–37].
These neurons possess two interesting characteristics: they project directly to the
PAG and the Rexed laminae V, VII and X [38, 39], regions containing parasympa-
thetic interneurons and parasympathetic dendrites [38, 39].
This “direct” connection with the PAG [35, 40] (and not with the PMC) is typical
of human, cat and dog and would allow control of the bladder filling without its
perception (the latter guaranteed by the thalamus). Only reaching a certain filling
level would determine the passage of information between the PAG and the PMC
(and therefore its awareness) and the potential choice of voiding [37].
The intraspinal neurons identified as involved in spinal segmental reflexes
[41–47] with excitatory and inhibitory synaptic connections [48–51] are located in
the Rexed laminae I, V and VII and the posterior grey commissure [52–58] (Fig. 1.4).
The afferent pathways of the pelvic area originating from the urethra, the ure-
thral sphincter and the neuromuscular pelvic spindles present an essentially over-
lapping pattern of endings [59] and this arrangement presumably coordinates the
pelvic floor muscles (PFM) and the sphincteric function during micturition and
defecation [60].
The overlap between the dendritic afferents from the detrusor and the urethra on
the posterior horns and on the posterior grey commissure indicates that these regions
are the most important routes for receiving information from the peripheral area:
these are probably essential sites for the visceral-somatic integration which may
represent a fundamental element in coordinating the detrusor function and the
sphincter activity, which in fact have a similar dendritic pattern [33]. In summary,
during the entire filling phase, the sensation of the detrusor being full is conveyed,
thanks to first-order neurons, by the pelvic and hypogastric nerves [5, 16] while the
hypogastric nerves and the pudendal nerve convey the sensory information from the
neck of the bladder and the urethra [4].
Some spinal interneurons connect with the bladder afferents [52, 54, 55], trans-
mitting signals through the ascending sensory pathway and reaching, after a partial
decussation [35], mainly the gracile nucleus (which conveys the nociceptive
6 G. Lamberti and A. Biroli

sensitivity to the thalamus and the cortex), the PMC and the PAG [10], that is in turn
connected with numerous other brain areas [61–63] through third-order neurons
[63, 64]. There is a second ascending pathway to the gracile nucleus from the pelvic
organs and subsequently to the thalamus for transmitting nociceptive impulses [65].

1.2.2 Spinal Cord Efferents

The sympathetic preganglionic system is located medially and laterally in the lum-
bar spinal cord segments, the external urethral sphincter motor neurons in Onuf’s
nucleus and the parasympathetic preganglionic neurons in the sacral cord
segments.
The preganglionic cholinergic efferent neurons reach the pelvic plexus ganglia
and the detrusor wall. The axons originate from the sacral parasympathetic nucleus
from S2 to S4, and have synaptic connections with the pelvic ganglia as well as with
the small ganglia on the detrusor wall which release acetylcholine. Nicotinic recep-
tors mediate postsynaptic activation: postganglionic axons run for a short distance
in the pelvic nerves and have terminations in the detrusor wall where they release
acetylcholine which induces the contraction of the smooth muscle fibres. Muscarinic
receptors mediate this postganglionic stimulation; there are two subtypes of musca-
rinic receptors, M2 and M3, in the detrusor: although M2 receptors are more numer-
ous, subtype M3 is specific for the contractions of the detrusor [66, 67].
During the filling phase, the whole set of active afferents and efferents, under
physiological conditions, allows continence to be maintained, thanks to the pres-
ence of urethral reflexes known as a whole as “guarding reflex” [4, 10, 14, 68–70].
In the pelvic-hypogastric component of the “guarding reflex”, the parasympathetic
innervation of the detrusor is inhibited while at the same time the smooth (internal
urethral sphincter, through the hypogastric nerve) and striated components (external
urethral sphincter, through the pudendal nerve) are active. The pelvic-pudendal
component of the reflex, similarly active, under normal conditions, in the occasion
of increases in intra-abdominal pressure (cough, laughter and physical activity),
through the action of glutamatergic pathways and N-methyl-d-aspartate receptors
(NMDA) with the release of acetylcholine, is responsible for the anticipatory con-
traction of the external urethral sphincter.
Unlike what occurs in animals, where the sympathetic lumbar nerve contributes
mainly to inhibiting the detrusor’s smooth muscle and to contracting the bladder
neck [71, 72], in man there could be a control exercised specifically during the fill-
ing phase by the activation of the dorsal portion of the anterior cingulate cortex
(dACC) (Fig. 1.2) and of the surrounding sensory-motor areas, together with the
action of the supplementary motor area, which is active when PFM and urethral
striated sphincter contract [73–77].
Similar control is exercised from an area at the dorsal-lateral pontine tegmentum,
known as “pontine continence centre” (PCC) (Fig. 1.1), which facilitates the reflex
activity of the sphincters [7, 10, 64, 78–88]. This area would receive signals directly
from Onuf’s nucleus and its stimulation, activated via the spinal reflex pathway by
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