The Spastic Forms of Cerebral Palsy Adriano Ferrari • Giovanni Cioni

The Spastic Forms of Cerebral Palsy A Guide to the Assessment of Adaptive Functions

Forewords by Alain Berthoz Pietro Pfanner Adriano Ferrari Child Rehabilitation Unit S. Maria Nuova Hospital Department of Neuroscience University of Modena and Reggio Emilia Reggio Emilia, Italy

Giovanni Cioni Department of Developmental Neuroscience Stella Maris Scientific Institute Division of Child Neurology and Psychiatry University of Pisa Pisa, Italy

This is a revised, enlarged and completely updated version of the Italian Edition published under the title “Le forme spastiche della paralisi cerebrale infantile. Guida all’esplorazione delle funzioni adattive” edited by A. Ferrari, G. Cioni © Springer-Verlag Italia 2005 All rights reserved

Translation: Maurizio Boni and Vincent Corsentino, Italy

ISBN 978-88-470-1477-0 e-ISBN 978-88-470-1478-7

DOI 10.1007/978-88-470-1478-7

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Springer-Verlag Italia S.r.l, Via Decembrio 28, I-20137 Milan, Italy Springer is part of Springer Science+Business Media (www.springer.com) Foreword

by A. Berthoz

The publication of this volume, edited by Adriano Ferrari and Giovanni Cioni, is a major event for several reasons. Most importantly, it concerns an area of child pathology that has yet to be fully explored. In this context, the authors’ efforts to compile their observations as well as those of other clinicians and to elaborate their theories have resulted in an essen- tial step in the field of cerebral palsy (CP). The originality of the book is its very clear focus, while at the same time the authors have encouraged the book’s contributors to express their ideas and personal opinions. This leads sometimes to redundancy, but this is precisely one of the benefits of the book because the same problems are then exposed from different points of views. The reader is thus spared the normative attempts of many other pathology books, in which the complex- ity of a given disease is hidden by the authors’ or editors’ desire to impose a rigid taxono- my or epidemiology. The chapters in the book offer a lively, up to date discussion about the mechanisms of CP as well as the possible approaches to the child with CP. This will be fruitful to the reader, whether he or she is involved in practical training and rehabilitation or in clinical prac- tice. Furthermore, the book is a rich source of information for designers of rehabilitation equipments, basic research scientists, and those who are interested in the social consequences of this pathology (education, transportation, etc.). A special feature of this book is that, in accordance with the originality of the Stella Maris Institute and its departments of Child Neurology and Psychiatry, it also includes chapters in which the psychiatric and psychosocial dimensions of CP are discussed. This book is of interest not only because of the diversity of its approaches to CP, but also because it contains a number of extremely new ideas concerning the mechanisms of this condition. For instance, the possible involvement of top-down, cognitive, and perceptive factors in so-called motor deficits is extensively discussed. This is crucial because too often motor pathology is attributed only to low-level or muscular deficits. However, as frequently stated in the book, an understanding the relationship between cognitive, perceptive, and bottom-up sensory-motor factors still requires extensive research. The consequences of this and related research will be important for the design of new rehabilitation methods; but they will also lead to “remediation” procedures, i.e., activities

v vi Foreword by A Berthoz that allow the brain to discover and put into action as-yet-unexploited resources, alterna- tive sensory-motor strategies, and new combinations of the elements of the motor reper- toire – the brain is, after all, a clever and creative machine. This will also require that each individual with CP is given free rein to find his or her way to recuperation, or to a substi- tution of function. The wide range of knowledge offered in this book will enable readers to consider the problem of “generalization”. Today we see a rapidly developing market of training devices some of which are deceiving as the CP patient’s capacities improve on the machine, but the improvements are not transferred to the many unexpected situations of daily life. We owe the authors of this book our gratitude for inviting us to join in their efforts to better the life of so many bright and promising children.

Paris, September 2009 Alain Berthoz Professor at the College de France Member French Academy of Sciences Associate member of American Academy of Arts and Sciences and Royal Belgium and Bulgarian Academies of Medicine Foreword

by P. Pfanner

It is with great pleasure that I present this book devoted to cerebral palsy, in which Adri- ano Ferrari and Giovanni Cioni have collected from their experiences and reflections the results of over a decade of productive collaboration in this field. Its layout and contents mirror the expertise and background of the authors and their co- workers, and their original scientific approach. Besides being a university professor in Child Neuropsychiatry, Giovanni Cioni is the director of the clinical department of an Italian scientific biomedical research institute, dedicated to child neurology, psychiatry, and rehabilitation, in which the research and clinical aspects of neurological and psychiatric disorders in childhood are treated. Adriano Ferrari is the founder and director of an important specialized hospital center operating on a national level, that carries out multifaceted and innovative child rehabilitation program. Progress in the rehabilitation field, a recent science that still needs to construct a frame- work in order to consolidate knowledge and experience, has to appropriately develop from the collaboration between clinics and rehabilitation, between purely neurobiological aspects of functioning and orthopedic ones of the locomotor apparatus, namely anatomy and pathology. However it must go further to also include important psychological aspects related to the motivation of the motor act and its emotional components, both of which in- evitably play a crucial role in learning under pathological conditions. In my opinion, the great medical and scientific contribution of Giovanni Cioni and Adriano Ferrari, expressed in this book, lies in their ability to integrate all these aspects in theoretical models and clinical procedures on cerebral palsy. A look through the table of contents of this book will confirm my statements. The first part summarizes the history of cerebral palsy and describes how the understanding of this pathology has been modified over the years up to its present interpretation, which states palsy is a disorder that involves not only strictly motor functions, but also perceptual, cognitive, and emotional ones. This part also points out the recent contribution of neuroimag- ing, especially ultrasound and magnetic resonance, in visualizing and identifying brain le- sions that cause cerebral palsy. Imaging, but also and especially careful observations of neonate’s and young infant’s movements, enables us to make diagnoses and prognoses

vii viii Foreword by P. Pfanner starting from the first weeks of life, thus doing away with the ancient concept of the silent period. The second, more extensive part of this book analyzes the adaptive functions of cerebral palsy patients, offering an extremely complete and integrated examination of the clinical aspects of these special children. This is followed by a section dealing with the classification of spastic forms of cerebral palsy. Here, the taxonomic proposal, which the authors have been working on for several years, is presented in an analytic format enhanced with designs and diagrams taken from the files of the Motion Analysis Laboratory in Pisa. This classification proposal is innovative because it utilizes not only kinematic, but also multiple parameters in order to classify the various forms of cerebral palsy, and because it also gives suitable indications for prognosis and treatment. As with all proposals, also in this book, it is the intention of the authors to submit their model to the contributions and criticisms of the readers. The book also comes with an interactive DVD on the different forms of cerebral palsy, prepared by the physiotherapists of Reggio Emilia and Pisa. It is particularly useful because it also contains exercises to assess learning. This book therefore is full of the information and ideas of Giovanni Cioni and Adriano Ferrari and their co-workers, who have collaborated in drafting several chapters. Howev- er, as indicated by the authors themselves in their introduction, this is not a textbook in the classical sense, that is to say a comprehensive review of the literature and state of the art of the studied topic. The book instead reflects on the cultural and methodological approach and the original and very often provocative interpretation by the authors and their collaborators. It presents working hypotheses that in part must be confirmed through further research of evidence and verified by other groups, and one of the purposes of this text is to stimulate and promote additional useful and necessary scientific contributions. I welcome and agree with the choice of the authors to search for the neurophysiopatho- logical connection in every aspect of cerebral palsy, to more than merely present their quantitative data and clinical series collected over many years of work. Springer has superbly edited and printed this work, praiseworthy of this well-known publishing house. I would like to express once again my warmest congratulations to the authors. I am cer- tain this book will be a great success among doctors, child neuropsychiatrists and physiatrists, therapists, and students specializing in these related fields.

Pisa, September 2009 Pietro Pfanner Former Professor of Child Neurology and Psychiatry University of Pisa Preface

This book is the result of studies and reflections on cerebral palsy (CP) in children that the authors and their collaborators (medical doctors and therapists) from the Pisa and Reggio Emilia specialised centers have carried out in recent years. It addresses the main topics associated with the evaluation of adaptive functions in the spastic forms of CP (accepted definition and its modifications over the most recent decades, new taxonomic orientations, etiopathogenesis, semiotics, and the so-called associated impairments: visual, cognitive and behavioral). The main goal of this book is not to relate or update the state of art of these topics, but to offer readily accessible information on the explored themes in order to encourage con- siderations and comparisons with the readers’ experiences. The topics are treated from a pathophysiological point of view that guides the authors’ interpretations of the nature of the disease (functional diagnosis), the problems correlated with prognosis (such as the hypothesis of its natural history) and with rehabilitation (such as modification of the architecture of functions in adaptive terms). The text comes with a DVD of clinical cases which are subdivided according to classification criteria elaborated by the authors. These cases enhance the teaching usefulness of this book for people already working in this field (medical doctors, child neuropsychiatrists and physiatrists, rehabilitation therapists), for university students of physical and occupational therapy, and for resi- dents in rehabilitation medicine, child neurology, and orthopedics. The reader, student, or professional interested in CP will find innovative ideas, proposals, remarks, and correla- tions resulting from the collective expertise of our two groups, to which the reader can compare his own personal ideas. For this reason, the book maintains the structure of personal notes, like a travel journal, offering the authors’ interpretations and reflections, while referring to other scientific publications for detailed analyses of related clinical cases and comparisons with the viewpoints of other specialists. In this sense, every chapter represents an autonomous unit that can be studied separately. The statements presented in each chapter are frequently full of repercussions and, we hope, this will lead the reader to further reflections, comparisons, and, obviously, doubts and disagreements based on his own experiences. Also for this reason some concepts and references to the scientific literature and to primary authors are quoted in several chapters, as a common basis for specific topics.

ix x Preface

The publication of this book would not have been possible without the effort and contribution of all the colleagues, medical doctors and therapists, of our specialised centres, and the collaboration of children and their parents. We would like to thank everyone for their cooperation.

Reggio Emilia and Pisa, September 2009 Adriano Ferrari Giovanni Cioni Contents

PART I Nature of the Defect

1 Cerebral Palsy Detection: from John Little to the Present ...... 3 Giovanni Cioni, Paola B. Paolicelli

Historical Models for the Classification of Cerebral Palsy ...... 8 Traditional Clinical Syndromes ...... 9 Limitations of Traditional Classifications and Perspectives ...... 11 Conclusions ...... 13 References ...... 14

2 Guide to the Interpretation of Cerebral Palsy ...... 17 Adriano Ferrari, Silvia Alboresi

Definition of Cerebral Palsy ...... 17 Palsy: from a Neurological to a Rehabilitative Diagnosis ...... 18 Cerebral ...... 24 Child CP ...... 25 References ...... 27

PART II Function Analysis

3 Functional Diagnosis in Infants and in Very Young Children: Early Predictive Signs ...... 31 Giovanni Cioni, Andrea Guzzetta, Vittorio Belmonti

Introduction ...... 31 Techniques for the Clinical Assessment of the Neonatal Nervous System . . . . . 32 Neonatal Neurological Examination: a Novel Approach ...... 34 Conclusions ...... 48 References ...... 50

xi xii Contents

4 Motor Defects ...... 53 Adriano Ferrari

First Level: Motor Modules ...... 54 Second Level: Praxias ...... 60 Third Level: Actions ...... 63 References ...... 70

5 Perceptive Defects ...... 73 Adriano Ferrari

Action Organizes Perception ...... 73 Perception Leads Action ...... 74 First Level: Sensations ...... 76 Second Level: Perceptions ...... 80 Third Level: Representations ...... 93 References ...... 96

6 Praxic Organization Disorders ...... 99 Simonetta Muzzini, Federico Posteraro, Roberta Leonetti

Definition of Developmental Dyspraxia and Pathogenetic Hypotheses ...... 99 Dyspraxia and Infantile Cerebral Palsy ...... 101 Motor Control Models ...... 102 Neurophysiological Basis of Action ...... 104 Clinical Hypotheses ...... 106 Assessment: a Clinical Proposal ...... 108 Assessment: an Experimental Methodology ...... 110 Recommendations ...... 112 References ...... 113

7 Visual and Oculomotor Disorders ...... 115 Andrea Guzzetta, Francesca Tinelli, Ada Bancale, Giovanni Cioni

Introduction ...... 115 Diagnostic Tools ...... 116 Complex Visuoperceptive Disorders and Correlation between Visual Abnormalities and Other Aspects of Development ...... 132 Main Neuropsychological Tests for the Support of Visuoperceptive Disorders . 135 Test for the Evaluation of Visuoperceptive Abilities ...... 136 Cerebral Visual Impairment and Mental/Motor Development ...... 138 References ...... 139 Contents xiii

8 Neuropsychological Evaluation ...... 143 Daniela Brizzolara, Paola Brovedani, Giovanni Ferretti

Introduction ...... 143 Disorders and Factors Associated with CP Influencing Psychological Outcome . 143 Cognitive Evaluation in the First Years of Life ...... 146 Neuropsychological Approach to Spastic Diplegia ...... 153 The Neuropsychological Approach to Forms of Infant Hemiplegia ...... 159 Neuropsychological Assessment of Hemiplegia ...... 169 Cognitive Evaluation of Pre-school Age and School Age Children with Tetraplegic and Dyskinetic Forms ...... 170 Conclusions ...... 172 References ...... 172

9 Emotional, Behavioral and Social Disorders in Children and Adolescents with Cerebral Palsy ...... 181 Gabriele Masi, Paola Brovedani

Introduction ...... 181 Brain Disorders and Psychopathology ...... 182 Psychopathology of Cerebral Palsy: Epidemiologic Studies ...... 184 Psychopathology of Cerebral Palsy: Clinical Studies ...... 185 Peer Relationships in Hemiplegic Children ...... 187 Cerebral Palsy, Balance Disorders and Anxiety Disorders ...... 188 Treatments ...... 189 Conclusions ...... 190 References ...... 190

10 Observing Interactions ...... 193 Sandra Maestro

The Child ...... 194 The Family ...... 196 The Caregiving Team ...... 197 Conclusions ...... 199 References ...... 199

PART III Classification of Spastic Syndromes and Clinical Forms

11 Critical Aspects of Classifications ...... 203 Adriano Ferrari

Motor Perspective ...... 206 Dyspraxia ...... 207 xiv Contents

Motor Learning ...... 209 Perceptive Perspective ...... 212 Intentionality Perspective ...... 215 References ...... 216

12 Kinematic Classification ...... 219 Adriano Ferrari

A New Proposal ...... 229 Conclusions ...... 235 References ...... 238

13 Tetraplegic Forms ...... 241 Adriano Ferrari, Manuela Lodesani, Simonetta Muzzini, Rosa Pascale, Silvia Sassi

Postural Analysis ...... 241 Posture Organization Disorders ...... 246 Main Forms of Tetraplegia ...... 249 References ...... 272

14 Dysperceptive Forms ...... 273 Silvia Alboresi, Vittorio Belmonti, Alberto Ferrari, Adriano Ferrari

Introduction ...... 273 Clinical Features of Perceptual Disturbances in Diplegias (Semiotics) ...... 274 How to Detect Clinical Signs of Perceptual Disorders ...... 280 Some Hypotheses on the Nature of Perceptual Disorders ...... 282 Clinical Aspects of Perceptual Disorders ...... 285 1. The Falling Child ...... 285 2. The Stand-Up Child ...... 288 References ...... 290

15 Forms of Diplegia ...... 293 Adriano Ferrari, Manuela Lodesani, Silvia Perazza, Silvia Sassi

Controlling Central Pattern Generators ...... 294 Reducing Speed ...... 294 Four Limb Coordination ...... 294 Stabilization and Achieving Proximal Fixation ...... 295 Modules and Praxes ...... 295 Sensations and Perceptions ...... 295 Upper Cortical Functions ...... 296 Manipulation ...... 296 Contents xv

Muscular Retractions and Articular Deformities ...... 296 Clinical Forms of Diplegia ...... 297 Validation of the Proposed Classification of Diplegia ...... 300 Main Aspect of Each Form of Proposed Classification of Diplegia ...... 305 References ...... 328

16 Forms of Hemiplegia ...... 331 Giovanni Cioni, Giuseppina Sgandurra, Simonetta Muzzini, Paola B. Paolicelli, Adriano Ferrari

Definition and Prevalence ...... 331 (RE) - Organization of the Sensory-Motor System ...... 334 Clinical Signs of Hemiplegia ...... 339 Classification of Manipulation ...... 343 Main Features of the Four Clinical Forms of Hemiplegia ...... 346 References ...... 353

Subject Index ...... 357 List of Contributors

Silvia Alboresi Giovanni Cioni Child Rehabilitation Unit Department of Developmental S. Maria Nuova Hospital Neuroscience Reggio Emilia Stella Maris Scientific Institute Division of Child Neurology and Ada Bancale Psychiatry Department of Developmental University of Pisa Neuroscience Pisa Stella Maris Scientific Institute Pisa Adriano Ferrari Child Rehabilitation Unit Vittorio Belmonti S. Maria Nuova Hospital Department of Developmental Department of Neuroscience Neuroscience University of Modena and Reggio Emilia Stella Maris Scientific Institute Reggio Emilia Pisa Alberto Ferrari Daniela Brizzolara Department of Electronics, Department of Developmental Computer Sciences and Systems Neuroscience Engineering Faculty Stella Maris Scientific Institute University of Bologna Division of Child Neurology and Bologna Psychiatry University of Pisa Giovanni Ferretti Pisa Department of Developmental Neuroscience Paola Brovedani Stella Maris Scientific Institute Department of Developmental Pisa Neuroscience Stella Maris Scientific Institute Pisa xvii xviii List of Contributors

Andrea Guzzetta Rosita Pascale Department of Developmental Department of Developmental Neuroscience Neuroscience Stella Maris Scientific Institute Stella Maris Scientific Institute Pisa Pisa

Roberta Leonetti Silvia Perazza Child Neuropsychiatry Unit Department of Developmental Local Health Service Neuroscience Carpi (Modena) Stella Maris Scientific Institute Pisa Manuela Lodesani Child Rehabilitation Unit Federico Posteraro S. Maria Nuova Hospital Neurological Rehabilitation and Reggio Emilia Severe Acquired Brain Lesion Unit Auxilium Vitae Sandra Maestro Volterra (Pisa) Department of Developmental Neuroscience Silvia Sassi Stella Maris Scientific Institute Child Rehabilitation Unit Pisa S. Maria Nuova Hospital Reggio Emilia Gabriele Masi Department of Developmental Giuseppina Sgandurra Neuroscience Department of Developmental Stella Maris Scientific Institute Neuroscience Pisa Stella Maris Scientific Institute S. Anna School of Advanced Studies Simonetta Muzzini Pisa Child Rehabilitation Unit S. Maria Nuova Hospital Francesca Tinelli Reggio Emilia Department of Developmental Neuroscience Paola B. Paolicelli Stella Maris Scientific Institute Department of Developmental Pisa Neuroscience Stella Maris Scientific Institute Pisa List of Contributors xix

DVD by

Giulia Borelli Annarosa Maoret Child Neuropsychiatry Unit Child Rehabilitation Unit Local Health Service S. Maria Nuova Hospital Scandiano (Reggio Emilia) Reggio Emilia

Michele Coluccini Antonella Ovi Department of Developmental Child Rehabilitataion Unit Neuroscience S. Maria Nuova Hospital Stella Maris Scientific Institute Reggio Emilia Pisa Maddalena Romei Maria Rita Conti Child Rehabilitation Unit School of Physiotherapy S. Maria Nuova Hospital Medical Faculty Reggio Emilia University of Modena and Reggio Emilia Reggio Emilia Angelika Schneider Child Rehabilitation Unit Franca Duchini S. Maria Nuova Hospital Department of Developmental Reggio Emilia Neuroscience Stella Maris Scientific Institute Elisa Sicola Pisa Department of Developmental Neuroscience Maria Cristina Filippi Stella Maris Scientific Institute Child Rehabilitation Unit Pisa S. Maria Nuova Hospital Reggio Emilia