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Home , Ataxic cerebral palsy, Cerebral palsy, Diplegia, Hemiparesis, Moro reflex, Neurology

Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

Review Article

Arch. Dis. Childh., 1966, 41, 337. The of

T. T. S. INGRAM* From the Department of Child Life and Health, University of Edinburgh

Cerebral palsy is an inclusive term used to The fact that the clinical findings in cerebral palsy describe a number of chronic non-progressive dis- do change, especially in young , means that orders of motor function, which occur in young the same sequential clinical studies used in child children as a result of ofthe . Excluded patients with degenerative or transient disorders of by this definition are transient disorders of motor the central must be employed in function, such as those that may occur in encephali- those who suffer from cerebral palsy. Cerebral tis or ; disorders such as , in palsy is part of child neurology (Meyers, 1958; which the disturbance of motor function is predomi- Ingram, 1966). nantly due to disease of the ; and degenerative conditions, including progressive de- Principles and Methods of Diagnosis myelinations. The clinician faced with the problem of the The of the brain which cause cerebral diagnosis of a of the in palsy are by definition non-progressive, but must be a mature adult thinks in terms of the nature of the thought of as giving rise to a clinical picture that disease process, its localization, its extent, and its

changes. As the child's nervous system develops likely progress. He considers what effects the copyright. the clinical findings he manifests will change too lesion is likely to have on the individual in terms of (Crothers and Paine, 1959). the further dissolution or recovery of function. The effects of of the hemispheres differ The neurologist who deals with the child has to be not only according to their nature, their situation, aware of the fact that, in the early months particu- and their extent, as they do in the adult, but also larly, quite extensive abnormalities of the hemi- according to the age at which they were sustained spheres may not be manifest by changes in the and the neurological maturation of the child at the behaviour of the child. In the first 6 to 8 weeks of time he is examined (Byers, 1941; Ingram, 1964a, b). life, for example, even anencephalic babies may http://adc.bmj.com/ It is because the child's nervous system, damaged or behave relatively normally if they survive (Peiper, undamaged, is still developing and the child is 1964). It is for this reason that it is so rash to acquiring new motor, linguistic, adaptive, and social predict that a baby who appears to have made a good skills that the methods of diagnosis used by the recovery from apparent birth by the age of a paediatric neurologist have to differ from those few weeks will later be normal. Much is still to be employed with adult patients. They must take leamt about the prognostic significance ofabnormal- account of the fact that, whereas an acquired lesion ities of behaviour in the newbom period (Prechtl in the brain of an adult may be expected to produce and Beintema, 1964). on September 26, 2021 by guest. Protected loss of acquired skills, a similar lesion in the brain of The first manifestations of hemisphere lesions in a young child may or may not delay the attainment the infant may be that he is late in reaching some of of a particular milestone of development. For the milestones of motor, linguistic, adaptive, and example, it is unreasonable to expect a child of 6 social behaviour. Developmental diagnosis-the months to be rendered dysphasic as a result of an ages at which the has reached particular mile- extensive fronto-temporal lesion in the dominant stones of development-is thus of great importance hemisphere. Dysphasia implies loss of the ability (Gesell and Amatruda, 1941; Thomas and Saint to use language, and the child aged 6 months has not Anne Dargassies, 1952). yet acquired language. In such a case there may or Developmental diagnosis may be applied both to may not be subsequent retardation of speech the whole child and to his various parts. It is development (Ingram and Barn, 1961). important to know when children could first sit up, with or without support, say their first intelligible * Address: 17 Hatton Place, Edinburgh 9. words, feed themselves, and play successfully with 337 Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

338 T. T. S. Ingram NORMAL CHILDREN Feet-Hands Test 2-4 5-7 8-10 11-13 14-16 y 0/0 y y V V 100- -~~~~~~~ 75.

50

25

Supination marked slight Pronation or ambiguous No ass. movement (b) FIG. la and b.-The 'feet-hands test' of the Fogs. (a) The left upper limb, which in this patient is less mature neuro-

logically, shows more associated involuntary movement when copyright. the child is asked to walk with hisfeet inverted. (b) Chart to show proportion of normal children at different ages (a) displaying supination, or other involuntary movement of hand, with this test. children of the same age; but a consideration of the stood with support may often allow a prediction to function of various parts of the body may also be be made about the likely age at which independent rewarding. It may be found, for example, that a will be achieved (Bobath and Bobath, 1962). http://adc.bmj.com/ child can reach accurately using the pincer grasp Most ofthe information about the child's develop- between the thumb and forefinger with the right ment must necessarily be obtained by questioning hand but not with the left, and that he cannot release parents about the ages at which their children the grasp voluntarily in the left hand, though he has reached particular milestones, and additional in- been able to do this from the age of 8 months in the formation can be obtained from baby books, old right. In such a situation the motor function of the photographs, or from hospital and clinical notes left hand can be regarded as being immature and its made in earlier years. motor function slow in developing. Similarly, a While a strange environment often inhibits on September 26, 2021 by guest. Protected normal development of manipulative function in the the child's behaviour at the time of a first interview, upper limbs may be in striking contrast to retarded it is usually possible to obtain a fairly clear idea of development of locomotion, and might suggest that the level of motor maturation that the child has functional development of the lower limbs had been reached, and what level of motor maturation has retarded to a greater extent than that of the upper been reached by a particular limb. The assessment limbs. This is the situation in diplegic cerebral of motor maturation is becoming increasingly palsy or in infantile . precise as standardized tests are developed (Berges As well as giving a great deal of information about and Lezine, 1965; Fog and Fog, 1963; D. H. Stott, the nature, extent, and severity of neurological 1965, personal communication). (Fig. la and b.) impairment in cerebral palsy, developmental diagno- The assessment of motor maturation is reached sis is also useful prognostically. For example, an both positively and negatively: positively by noting assessment of the ages at which a child has first sat the motor achievements of the child, for example up with support, then without support, crawled, and his ability to reach for objects, sit without support, Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

The Neurology of Cerebral Palsy 339 crawl, and stand with support; negatively by considering the extent to which behaviour patterns characteristic of the young infant have been inhibited by the development of higher nervous centres. Thus the paediatrician is interested to find out whether the stepping, Moro, lip, and grasp persist or have disappeared. In the past 30 years, largely because of the interest shown by Peiper (1964), Thomas, Chesni, and Saint Anne Dargassies (1960), Prechtl and Beintema (1964), Bobath and Bobath (1956), Oppe and Paine (1966), and other authors, a systematic study of infantile reflexes in normal children and in patients who suffer from a variety of disorders of the central nervous system has taken place, and a much more accurate grading of maturation on the basis of the persistence and inhibition of these reflexes has become possible (Fig. 2). Some reflexes tend to be much more easily elicited in one type of cerebral palsy than in another, and for this reason they will FIG. 2.--.Abnormal 'parachute' reaction in a child be discussed in more detail when the various types from mild cerebral palsy. When tiltedforwards the upper are considered (Paine, Brazelton, Donovan, Dror- limbs should flex, extend at the elbows and wrists, and the hands open-as if to protect the head from hitting the baugh, Hubbell, and Sears, 1964). ground. History Taking and Examination original disease process would not necessarily be

Since paediatricians and neurologists began to inferred from the later neuropathological findings. copyright. take a serious interest in cerebral palsy (Crothers and Classification on the basis of neuropathological Paine, 1959; Hansen, 1960; Denhoff and Holden, findings was therefore likely to be unrewarding. 1951), more has been learnt about the predisposing Since the clinical history and examination could and precipitating causes of cerebral palsy, and this not reliably identify disease processes responsible for influences the type of questions to be asked in taking cerebral palsy in the majority of cases, classification the history. is no longer practically on the basis of the presumed cause of the condition, confined to what happened in the perinatal period; as had been suggested (Sachs and Hausman, 1926), a more detailed family history is taken as to the was also impractical. More recent work has http://adc.bmj.com/ reproductive history ofthe mother, and ofher sisters, supported Freud's conclusions, for it is shown how mother, and aunts (Ingram and Russell, 1961; difficult it may be to distinguish on clinical grounds Ingram, 1964b; Drillien, Ingram, and Russell, 1964). (and even after radiological and other investigations) The history is usually taken from the mother, when cerebral palsy has been the result of develop- though it is helpful if she can be supported by either mental malformations of the brain and when it has her husband, her mother, or her mother-in-law been caused by perinatal injury (Minkowski, 1955; during the course of history taking. The order of Courville, 1953, 1954; Norman, 1963). The need history taking and examination matters less than the for caution in attributing 'a cause' to the brain on September 26, 2021 by guest. Protected order in which it is recorded. It is a great help if damage in these patients has been further emphasized histories and examinations are routinely written out by the demonstration that there appear to be in the same sequence; not only does this lessen the predisposing factors, probably genetically determin- risk of important items being omitted but it facili- ed, which make some individuals susceptible to tates ease of reference later on. cerebral palsy as a result of perinatal injury to the brain (Drillien, Ingram, and Russell, 1962). Classification of Cerebral Palsy Freud hoped that as methods of clinical investiga- The work of (1897) marked a tion improved precise diagnosis of disease entities significant advance in the study of cerebral palsy and within the group of patients who suffered from particularly in the definition of clinical syndromes cerebral palsy would become increasingly possible. and their classification. He pointed out that His hopes have been fulfilled to some extent; for cerebral palsy was the end result of a number of example, there is a known association between different disease processes, and that the nature of the maternal rubella occurring during the first two or Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

340 T. T. S. Ingram 'diplegias' comprised generalized rigidity-or Little's disease-in which there was more or less symmetrical of voluntary movement, more severe in the lower limbs than in the upper, accom- panied by or rigidity in the lower limbs, and dwarfing. The difference between paraplegic rigidity and generalized rigidity was one of degree and extent rather than of kind. Bilateral hemiplegia was the name given to bilateral paresis of the limbs which might be symmetrical or asymmetrical and which affected the upper limbs more severely than the lower limbs. Patients with bilateral hemiplegia almost invariably had involvement of the bulbar musculature and a high proportion were severely microcephalic, mentally retarded, and epileptic. Patients with generalized or double were those in whom involuntary movements and inappropriate changes of in the course of voluntary movement were the major . Freud fore- saw that patients with generalized chorea and double athetosis might be better placed in the major FIG. 3.-Pigmentation and enamel defects, best seen on the category separate from cerebral , and he lateral incisors, in a child suffering from as a result of kernikterus at an estimated 8 months' gestational speculated as to the need for a category of 'congenit- age. al ', of which a few case reports had appeared. He felt, however, that these might still be atypical copyright. three months of gestation and rubella retinopathy types of progressive spinal cerebellar disease to and occurring in the foetus. The which attention had recently been attracted by finding of the characteristic retinal pigmentation of Friedreich (1863, 1876), and Freud (1891, 1893, rubella retinopathy in an affected patient makes the 1897). Within 10 years of the publication of retrospective diagnosis of rubella embryopathy Freud's major paper, Batten (1903, 1905, 1907) had virtually certain (Stark, 1966). Similarly the find- established the existence of a condition of non- ing of rhesus incompatibility between mother and progressive congenital ataxia, attributable usually to patient, with a history suggestive of kernikterus and developmental malformations or perinatal injury of http://adc.bmj.com/ clinical findings of congenital with the and its connexions. defective upward movement of the eyes, high-tone As interest in the of cerebral palsy deafness, and enamel defects of the teeth (Fig. 3), developed other classifications evolved. In particu- allows a diagnosis to be made of dyskinetic cerebral lar, classification by neurological syndromes tended palsy attributable to rhesus incompatibility to be replaced, especially in the United States, by (Crothers, 1921; Byers, 1942; Evans and Polani, classification according to the state ofmuscle tone and

1950; Forrester and Miller, 1955; Plum, 1965). The the presence or absence of incoordination and on September 26, 2021 by guest. Protected clinical picture of more or less symmetrical paresis involuntary movement in the limbs. Thus Phelps of the limbs, more marked in the lower limbs than in (1941, 1943, 1948) recognized 5 major categories the upper, and usually associated with rigidity or of cerebral palsy with, (1) spasticity, (2) athetosis, spasticity, which is found in a high proportion of (3) rigidity, (4) , (5) ataxia. babies of small birth weight, is also characteristic, This classification has been influential, and many though it is much more difficult to identify the others are based to a large extent upon it (Perlstein, 'cause' in this example (Drillien, 1964; Russell, 1952; Minear, 1956; Little Club, 1959). The 1960a). objections to classification primarily on the basis of Freud classified patients on the basis of clinical changes in muscle tone are that muscle tone in findings. He distinguished between unilateral individual patients varies greatly according to cerebral palsy or hemiplegia, in which paresis usually emotional state, environmental temperature, alert- accompanied by spasticity might be complicated by ness, and particularly posture. Young babies who the presence of involuntary movement, and bilateral suffer from a bilateral cerebral palsy more severe in cerebral palsy. The bilateral cerebral palsies or the lower limbs than the upper ('diplegia' or 'Little's Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

The Neurology of Cerebral Palsy 341

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FIG. 4A, B, C.-Characteristic postures in a child with mixed cerebral palsy, dyskinesia copyright. predomninatintg in the upper limbs, and diplegic paresis in the lower. (A) and (B) demonstrate the effect of head extension and flexion on the position of the limbs when the child lies supi.ne. (C) shows the child placed in the erect position; an inzcrease in alti-travitv hypertonus cauises scissorinzn and extensioni of the lower limlbs. positions, and it has been suggested that in the future it may be possible to define clinical categories disease') are often hypotonic when lying in the prone in terms of 'patternological diagnosis' rather than in position, but show generalized rigidity when placed terms of classical neurological syndromes (Milani- in the erect position. A more serious objection is Comparetti, 1965) (Fig. 4). http://adc.bmj.com/ that classification primarily on the basis of altera- The classification used in Edinburgh, and which tions of muscle tone takes no account of the chang- will be used in this article, is shown in Table I. ing clinical picture which is observed as patients This derives from that of Freud, but the term mature. Thus patients who suffer from diplegia diplegia is reserved for patients with more or less are frequently hypotonic in the first months of life, symmetrical paresis of the limbs, affecting the lower then show variable muscle tone according to changes limbs more severely than the upper; and bilateral in position, and finally reach a stage in which hemiplegia, ataxia, and dyskinesia become major on September 26, 2021 by guest. Protected rigidity and spasticity predominate. Because of categories. Patients are further classified according these drawbacks, classification on the basis of to the stage of the evolution of their cerebral palsy, neurological syndromes has returned to favour and the extent and severity of motor involvement in increasingly in recent years, though some clinicians the limbs. A category for mixed and other types of have adopted compromises between classification on cerebral palsy is provided, but most of those who the basis of mucle tone and of neurological syn- cannot be classified in the major categories are dromes (Perlstein, 1952; Balf and Ingram, 1955; either too young for accurate diagnosis to be Minear, 1956; Crothers and Paine, 1959). possible, or have combinations of dyskinesia and Increasing attention has been paid to reflex diplegia or hemiplegia and ataxia (Ingram, 1964a). changes in posture which occur in different types of cerebral palsy (Bobath and Bobath, 1962). Characteristic positions of the limbs and trunk have Hemiplegia been described in children with cerebral palsy Hemiplegia is of congenital origin in approximately either at rest, or when they are placed in particular two-thirds of young children with this condition in Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

342 T. T. S. Ingram TABLE I Classification of Cerebral Palsy

Neurological Diagnosis Extent Hemiplegia .Right or left Bilateral hemiplegia Diplegia (hypotonic; dystonic; rigid; or ) .Paraplegic; triplegic; tetraplegic Ataxic diplegia (hypotonic; or spastic). . Paraplegic; triplegic; tetraplegic Ataxia ..Predominantly unilateral; or bilateral Dyskinesia (dystonic; choreoid; athetoid; tension; or with tremor) .. Monoplegic; hemiplegic; triplegic; or tetraplegic Other forms of cerebral palsy including mixed forms. most series (Hood and Perlstein, 1955; Perlstein and Kovacs, 1963; Bax and Mitchell, 1962; A. Holzel, Hood, 1954; Eastman and DeLeon, 1955; Eastman, 1966, personal communication; Smith, 1954). A Kohl, Maisel, and Kavaler, 1962; Crothers and less common cause is thrombosis of the internal Paine, 1959; Mitchell, 1961a). Though develop- carotid artery, which may occur in cyanotic congeni- mental malformation of the brain, particularly tal heart disease, or following trauma to the carotid hypoplasia or even agenesis of a hemisphere, may be artery, usually after a penetrating injury has affected responsible for a minority of cases of congenital the artery in the tonsillar fossa (Braudo, 1956; Till hemiplegia, the majority appear to be the result of and Hoare, 1962; Goldstein and Burgess, 1958; sustained in the perinatal period. Brandt, 1962). Commonly there are multiple abnormalities of late Patients who suffer from congenital hemiplegia , labour, delivery, and the neonatal show poverty ofmovement in the affected limbs (and period, so that it is often difficult to assess the extent commonly the face) without spasticity for a period copyright. to which the condition is the result of in of two to three months. When the child is about pregnancy, trauma during labour or delivery, or 3 months the mother may observe that the infant is brain damage from neonatal apnoea. More are moving the affected upper limb much less than the immature by birth weight and more are post-mature contralateral one, and in particular that the paretic by dates than expected, and there is an excess of hand is not opened as the other one is. It is only babies with birth weights above 3,850 g. (81 lb.) about this age that true spasticity is apparent on (Eastman et al., 1962; Ingram, 1964b). examination (Byers, 1941).

In about one-third of hemiplegic children the The appearance of acquired hemiplegia is usually http://adc.bmj.com/ cause is disease or trauma affecting the brain after preceded by a , and it is usually after the birth, usually in the first 3 years of life and most seizure, which may be unilateral or bilateral, that the commonly in the first year. Acquired hemiplegia affected limbs are noted to be abnormal. Paresis is may result from cerebral or sinus maximal immediately after the seizure; there is thrombosis complicating middle ear disease, or poverty of movement and flaccidity in the arm, leg, respiratory tract , or dehydrating condi- and face following the brain injury and then a gradual tions such as gastro-enteritis (Byers and Hass, 1933; return of some voluntary movement. The return Mitchell, 1952). Para-infectious , is characteristically first in the proximal parts of the on September 26, 2021 by guest. Protected for example those complicating , chicken- limbs and spreads gradually, distally. The order in pox, and other infections and which may also which movements return is very similar to the order follow vaccination or immunization against diph- in which they are acquired in normal infants. theria, , whooping cough, or typhoid, are Spasticity appears only after 2 or 3 weeks and other major causes of acquired hemiplegia (Sandifer, noticeably increases in severity in the ensuing 6 to 8 1962; Miller and Stanton, 1954; Miller, Stanton, weeks. During this time the affected upper limb and Gibbons, 1956). Other causes are encephalo- takes up the characteristic posture of adduction, pathies of unknown origin (Lyon, Dodge, and flexion, and internal rotation of the shoulder, Adams, 1961) or those that occur with lead poison- semiflexion at the wrist, and pronation of the fore- ing, with overwhelming infections, or with meningi- arm with flexion at the wrists and fingers over the tis, particularly pneumococcal, influenzal, or tuber- adducted thumb. The lower limb tends to be culous (Todd and Neville, 1964; Wood, 1964; semiflexed and adducted, and internally rotated at Nyhan and Richardson, 1963; Hutchison and the hip, semiflexed at the knee, and the foot is Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

The Neurology of Cerebral Palsy 343 plantar flexed. There is often either associated Sensory loss of 'cortical type' may be demonstrat- varus or valgus deformity ofthe foot (Mitchell, 1962; ed in between one-quarter and one-half of patients Wuillamier, 1882; Glenting, 1963; Twitchell, 1951, who suffer from hemiplegia. Patients show im- 1957, 1958). pairment of kinaesthetic and two-point discrimina- The extent of recovery and the time it takes to tion, and often some loss of of positional occur vary greatly in acquired hemiplegia, and it is change in the limbs, though the appreciation of light more difficult to predict the degree offunction which touch, pin prick, and temperature is usually normal. will eventually be achieved (Bax, 1962). Similarly Sensory loss of this type tends to occur more in congenital hemiplegia, voluntary movements are commonly in patients with acquired hemiplegia acquired later in the hemiplegic hand than in the than in those with congenital hemiplegia. It is normal hand, but it is difficult to predict with any associated with homonymous defects of the homo- reliability those movements that are likely to be lateral in a significant proportion of cases acquired and those that are unlikely to be acquired (Tizard, Paine, and Crothers, 1954; Mitchell, 1961b; before the child is about 1 year of age. Bax, 1962). In mildly affected patients the voluntary move- Vasomotor disturbances also occur in a high ments which are absent are those that are the last to proportion of patients. Commonly the affected be acquired in the course of normal child develop- limbs are colder than the normal limbs and they ment, for example, abduction of the thumb and full become relatively much colder when exposed to low supination of the forearm. In more severe cases, temperature, so that distal cyanosis, sometimes movements which the normal child acquires earlier accompanied by oedema, may occur. The motor may be lost, e.g. the ability to extend the fingers of the hand in some patients may be voluntarily. In very severely affected patients much increased in cold weather, a fact to which there may be virtually no use of the paretic hand. little attention has been paid (Ingram, 1964a). From the functional point of view it is convenient to Dwarfing of the limbs also occurs, more severely grade severity as follows: in patients with marked paresis than in those in

Mildly affected, those who use the hemiplegic whom the paresis is mild, but not necessarily copyright. hand independently. proportional to the severity of motor involvement Moderately severely affected, those who use the (Brissaud, 1896; Holt, 1965) (see Fig. 8.) paretic hand as an assistant to the other. The extent to which the child uses the affected Severely affected, those who make virtually no hand depends not only upon the degree of motor use of the hemiplegic hand. involvement and the extent to which sensation is Though the major abnormality in hemiplegia is impaired, but also upon whether higher level loss of voluntary movement patterns, mobility is disturbances of function are present. The same further impaired by the fact that the limbs are neglect of the hemiplegic limbs is found in some http://adc.bmj.com/ spastic. Spasticity is manifest in increased resist- adult patients with parietal lobe lesions, and there is ance to passive movement, the clasp knife phenom- evidence that may be very disturbed. ena, increased stretch reflexes, and increased biceps, Gross neglect of the affected limbs and dyspraxia triceps, supinator, knee-, and ankle-jerks on the occur more frequently in acquired hemiplegia than affected side. The plantar response on the affected in congenital hemiplegia and are important causes of side is almost always extensor. A high proportion disablement (Critchley, 1953; Denny-Brown and of patients with hemiplegia show associated disabili- Chambers, 1958; Russell, 1960b; Ingram, Jameson, ties. Athetosis, a slow writhing movement of the Errington, and Mitchell, 1964; Albitreccia, 1958). on September 26, 2021 by guest. Protected distal parts of the limb, most commonly the hand, Mental retardation, of various types, occurs in more than 60% of cases, much more often speech disorders, specific learning difficulties, and than is seen in adults after cerebrovascular accidents. behaviour abnormalities occur in a high proportion It is best seen when the child tries to reach with the of patients with hemiplegia and will be discussed affected hand, when involuntary abduction and later. extension of the digits and the wrist may be seen. Choreoid movements occur less frequently and Bilateral Hemiplegia almost exclusively in patients in whom hemiplegia Bilateral hemiplegia is the term given to tetra- is acquired (Gowers, 1876). Recent studies of paresis which affects the upper limbs more severely athetosis have suggested that it may be explained in than the lower. It amounts to more than the terms of lack of inhibition of competing grasp and summation of two hemiplegias, since the bulbar avoiding reflexes (Twitchell, 1958; Rushworth and musculature which is spared in hemiplegia is Denny-Brown, 1959; Denny-Brown, 1960). invariably more or less severely affected. The great Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

344 T. T. S. Ingram plegia is similar to that found in hemiplegia. Usually the severity of involvement is asymmetrical. As in hemiplegia, sensory impairment, vasomotor changes, and dwarfing of the limbs occur. Involvement of the bulbar musculature leads to feeding difficulties in early infancy, often with nasal escape and choking, sometimes with complicating inhalation of food materials. Later in infancy from the mouth is a prominent feature, and the few children who subsequently develop speech show gross (Ingram and Barn, 1961). The degree of mental defect is commonly severe. As a result behaviour development is retarded, and few patients outgrow the neonatal stage so far as motor achievements and reflexes are concerned. The lip reflex is commonly brisk and when swallow- ing is stimulated it is characteristically of the neonatal type with tongue protrusion preceding the (Fig. 5). The , reflex stepping, and the tonic neck reflexes may also easily be obtained (Zappella, 1964; Thomas and Saint Anne Dargassies, 1952; Bobath, 1954; Peiper, 1964). Diplegia Diplegia is nearly always congenital in origin, and FIG. 5.-The neonatal type of lip reflex with tongue at least one-third to one-half of patients in regional copyright. protrusion preceding swallowing in a microcephalic child suffering from bilateral hemiplegia. surveys are found to have been prematurely born (Hansen, 1960; Mitchell, 1961b). Although ab- normalities of pregnancy, labour, and delivery are majority of patients are severely mentally retarded. reported in about two-thirds of patients born at Most are also epileptic and the commonest type of term and in 85% of patients born prematurely as epilepsy which young patients show is myoclonic judged by weight, yet the importance of perinatal jerks (infantile ). Patients with bilateral injury has probably been overstressed in the past. hemiplegia amount to no more than 4 to 5 ° of Mothers of children who suffer from diplegia tend http://adc.bmj.com/ children with cerebral palsy, but the condition is an to be less fertile than other women in the community, important one because of the severity of the physical and there is a high reproductive casualty rate and mental handicaps (Yannet, 1949; Ingram, amongst other conceptions through abortion, still- 1955a). birth, neonatal death, and postnatal death. In Developmental malformations of the brain are addition, a higher proportion than expected of usually responsible for congenital bilateral hemiple- surviving children are mentally retarded, and have gia. A veriety of abnormalities has been described epileptic , or other diseases of the central including , hydroanencephaly, true nervous system (Drillien et al., 1962, 1964). These on September 26, 2021 by guest. Protected , and schizencephalies (Monakov, studies suggest that Freud's (1897) speculations 1901, 1926; Minkowski, 1955; Yakovlev and about there being predisposition to suffer from Wadsworth, 1946). These malformations occur diplegia and other abnormalities of the nervous more commonly in girls than in boys and are system in the offspring of some mothers may have frequently associated with developmental abnormal- been well founded. Diplegia occurs more common- ities of the spine, cardiovascular, alimentary, and ly in than in singleton births (Russell, 1961). genito-urinary systems. Patients who suffer from diplegia are retarded in Bilateral hemiplegia is usually of congenital motor development, and they are relatively more origin. Acquired bilateral hemiplegia after birth is retarded in locomotor development than in manipu- caused by meningitis, acute encephalopathies, and lative skill, because the neurological involvement in head trauma, and occasionally follows carbon diplegia is greater in the lower limbs than in the monoxide poisoning or cardiac arrest. upper. The motor deficit in the limbs in bilateral hemi- The extent to which linguistic, adaptive, and Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

The Neurology of Cerebral Palsy 345 social development is retarded depends more upon extend suddenly, the lower limbs flex, adduct, and the degree of any mental subnormality than upon internally rotate at the hips, extend at the knees, and the severity and extent of motor involvement. The plantar flex at the ankles, so that scissoring occurs. majority of diplegics are mentally subnormal and The back is extended and the upper limbs either show proportionate slowness in reaching milestones assume positions similar to those found in hemi- in these spheres of development (Crothers and plegia, or are adducted, flexed, and internally rotated Paine, 1959; Dunsdon, 1952; Bice and Cruickshank, at the shoulder, extended at the elbow, pronated at 1955). The mean intelligence is in the region of 70. the forearms, flexed at the wrists, and the fingers are More patients with are severely mentally flexed over the adducted thumbs. These postures retarded than are those with . The can readily be interpreted in terms ofthe uninhibited physical findings in diplegia change in a predictable action of neck, labyrinthine, and contralateral way as the child matures, and various stages in the extensor reflexes described by Sherrington (1906, development of the full clinical picture of diplegia 1947), Magnus (1926), Peiper (1964), Bobath and may be defined. These stages merge into each Bobath (1950, 1956). In this stage the asymmetrical other and are not clearly seen in mildly affected neck reflexes may be shown to be far brisker than patients, particularly those in whom only the lower they should be, the Moro reflex often persists, the limbs are affected. But in severely and moderately stepping reflex is usually still present, and the grasp severely affected tetraplegics the stages are easier to reflexes in the hands and feet are likely to be far too identify (Ingram, 1955b). easily elicited (Fig. 6). At rest, with the head flexed In the first hours or days after delivery a high and with the child in the prone position, muscle tone proportion of the babies show behaviour such as is is usually below normal rather than above, but the commonly considered to be caused by perinatal tendon jerks, especially in the lower limbs, are injury to the brain. The child may be unduly increased. lethargic and sleepy, difficult to feed, and limp, or The dystonic stage of diplegia is succeeded by the overexcitable, hypertonic, and jittery, or he may rigid/spastic stage. Gradually the response of the

have (Craig, 1938; Prechtl, 1960; child being placed in the erect position becomes less copyright. Prechtl and Dijkstra, 1960). Once these abnormal- abrupt. is not only apparent when the ities of behaviour in the immediate postnatal period child is placed in the erect position, but is apparent have disappeared, patients with diplegia tend to go also when he is prone, though it is even more through a latent period during which their behaviour increased when he is placed upright. Initially the is not sufficiently abnormal to make parents consult hypertonia is of rigid type and the lower limbs tend their doctors. On examination in this phase (which to be extended at the knees and plantar flexed at the probably lasts between 6 and 12 weeks in moderately ankles, as in the attacks of stiffening which were severely affected tetraplegic patients) the clinician earlier characteristic of the dystonic stage (Fig. 7). http://adc.bmj.com/ will find a rather lethargic baby who tends to lie in In the spastic phase of the rigid/spastic stage, the semiflexed posture, characteristic of the young flexor hypertonus is gradually superimposed upon newborn, and shows marked poverty of spontaneous the underlying rigidity, and the biceps, triceps, movement, especially of the lower limbs. When supinator, knee, and ankle jerks are grossly held in the erect position he cannot support his head increased, and stretch reflexes are easily elicited by and feels floppy or hypotonic. Reflexes character- sudden muscle stretching. The position assumed istic of the newborn period are abnormally easy to when erect tends to be similar to that found in elicit, particularly the Moro reflex, stepping reflex, bilateral hemiplegia, except that in diplegia the on September 26, 2021 by guest. Protected and tonic neck reflexes-further indications of the positions are more extreme in the lower limbs than immaturity of motor development. in the upper (Fig. 8). This hypotonic stage is gradually succeeded by a A few severely affected patients never reach the 'dystonic' stage in which there is involuntary mass stage of achieving rigid/ but movement and generalized alteration of body tone remain in the dystonic stage. A very small minority when the child's position is changed. The child of still more severely affected children live for some stiffens when held erect or when the head is years in the hypotonic stage. The majority, how- extended or when pressure is put on the soles of the ever, reach the rigid/spastic stage in which there is feet. Mothers commonly notice this stiffening persistent hypertonus of the limbs in the resting when they handle the child, usually at about the time stage, which is exacerbated to a greater or lesser he is beginning to have some head control in the degree by changes of posture. To some extent the erect position. When the child is abruptly placed outlook for patients suffering from diplegia may be in an erect position, or when his head is allowed to predicted from a study of their early course. Those Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

346 T. T. S. Ingram copyright. http://adc.bmj.com/ on September 26, 2021 by guest. Protected

FIG. 6.-A child with diplegia, aged 11 months. (A) Brisk asymmetrical neck reflex. (B) Moro reflex. (C) Stepping reflex. (D) Grasp reflex. Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

The Neurology of Cerebral Palsy 347

(a)

tU) 'G. 8a and b.-Diplegia, flexor hypertonus gradually ereases in the rigid/spastic stage. Postures in the sup- rted sitting and supported standing positions in a later stage of rigid/ than is shown in Fig. 7.

FIG. 7.-Dippegia, a characteristic posture in the early Ataxic Cerebral Palsy rigid/spastic stage. Ataxic cerebral palsy is more often unrecognized

who rapidly go through the stages of and than any other type of cerebral palsy, though recent copyright. and then progress through the predomi- regional surveys have suggested that 5-10% of cases nantly extensor phase or rigid/spastic stage of of cerebral palsy are suffering from ataxia (Skatvedt, diplegia have a relatively good prognosis. Patients 1958; Woods, 1957; Andersen, 1954). The majori- who are hypotonic for a prolonged period, dystonic ty of cases are congenital in origin and result from for a period of years, and then only gradually merge malformations of the cerebellum and its connexions into the rigid extensor phase of the rigid/spastic (Norman, 1963). Acquired ataxic cerebral palsy stage, have a less good prognosis. Patients who are may be caused by meningitis, by septic, acute, still in the dystonic stage by the age of 3 rarely walk disseminated, and toxic encephalopathies, and by http://adc.bmj.com/ unsupported in later childhood. trauma. The major disability in diplegia, as in hemiplegia, It is convenient to distinguish between ataxic is loss of voluntary movement patterns, but there children who also develop spasticity in the lower are other causes of impaired motor function. limbs as they grow older and those who remain Associated movements of athetoid type similar to hypotonic (Table II, Ingram, 1963). those found in hemiplegia occur in a minority of In the majority of cases of children with ataxic patients. In many patients dystonic movements diplegia or ataxia the birth was normal, but even in persist into the rigid/spastic phase. Choreoid the neonatal period many of the children were noted on September 26, 2021 by guest. Protected movements are rare. tend to occur to be lethargic, relatively immobile, and floppy when especially in the equinus positions. Impairment of picked up. Indeed, congenital ataxic cerebral palsy vasomotor control in the lower limbs occurs in the is one of the more frequent and important causes of majority of cases of diplegia. Chilblains are the 'floppy baby syndrome' (Schutt, 1963; Brandt, additional complications especially in the winter 1950; Tizard, 1964). There is retardation of motor months. development. The babies are slow to hold up their There is some degree of dwarfing of the pelvis and heads, to sit without support (Fig. 9), and, as noted lower limbs in practically all diplegics, and this is by Schutt (1963), 'the more erect the posture usually roughly proportional to the severity of the becomes the longer the delay in attaining the paresis. The complications of mental defect, subsequent stage of locomotion'. The mean age epilepsy, speech disorders, and abnormalities of the for walking in his patients was 34 months. He noted eyes, particularly which occurs so the great fear of standing or walking unsupported frequently in diplegia, will be discussed later. that many children had, even when they could walk Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

348 T. T. S. Ingram TABLE II Comparison of Findings in Children with Ataxic Diplegia and Ataxia

Ataxic Diplegia Ataxia . .Less broad-based; on the toes Very broad-based; flat-footed Muscle tone Spastic, especially in lower limbs Hypotonic Tendon jerks . . . Always exaggerated especially in lower limbs Usually sluggish Plantar responses t. Usually ;; Later contractures Frequent Never Epilepsy . . . Quite frequent Infrequent quite confidently with a little support. As noted in disabilities in dyskinesia, are of various types. By Table II patients with only ataxia tend to have a dystonia is understood a slow writhing movement of broad-based, flat-footed gait (Fig. 10), whereas in the proximal part of the limbs and trunk, which those with ataxic diplegia this gait is modified by the commonly results in the affected part of the body diplegia so that they tend to walk on their toes and assuming a position like that found in . on a less broad base (Fig. 11). Athetosis is a slow writhing movement which affects Hypotonia is maximal in the neonatal period, the the distal part of the limbs and is most evident in the muscle tone gradually increasing with age, though fingers and wrists in the upper limbs. It is best never reaching normal. The limbs show , seen when patients reach for an object, for instead incoordination of voluntary movement, dysdiado- of grasping it with accurate finger flexion and chokinesis, , and titubation which opposition of the thumb and index finger, an may be apparent even in the sitting position. involuntary writhing movement occurs which It is unusual to find either or a positive consists of extension and abduction of the digits and Romberg sign in congenital ataxia or ataxic diplegia. extension of the wrists. Choreoid movements are The extent to which linguistic, adaptive, and social rapid movements of the proximal parts of the limbs

behaviour is retarded in development depends more which involve agonists and antagonists. Like copyright. upon the degree of the mental subnormality which is dystonic movements they usually tend to use commonly present than upon the ataxic cerebral positions similar to those found in opisthotonus. palsy itself. Ataxic diplegia is the form of cerebral By tremor is understood a recurring involuntary palsy most often associated with . movement which usually has a rhythm. Tremor is classically seen in Parkinson's disease in the adult Dyskinesia but is less common than dystonic, choreoid, and The involuntary movements and involuntary athethoid movements in cerebral palsy affecting changes in muscle tone, which are the major motor children. By tension is understood the sudden http://adc.bmj.com/ on September 26, 2021 by guest. Protected

(a) (b) FIG. 9.-(a) Inability of a child aged 14 months with ataxia to sit without support. The excessive 'balancing' movements of the upper limbs are well shown. (b) The same child standing supported. Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

The Neurology of Cerebral Palsy 349

ta) to) FIG. lla and b.-Tendency to rise on to the toes when walking in ataxic diplegia. The gait is broad-based FIG. 10.-Characteristic broad-based, flat-footed because the diplegic component is not marked.

gait in severe ataxia. copyright. unwanted involuntary increase of tone in agonists with most if not all everyday activities and cannot and antagonists, which stiffens the operating limb feed, dress, or toilet themselves. This classification and often other parts of the body. It may seem is similar to that suggested by Mitchell (1961a). paradoxical to include it under the heading of Dyskinesia is almost always the result of perinatal 'involuntary movements', yet, by arresting voluntary injury to the brain, from causes such as perinatal movement, 'tension' disturbs the hypoxia, or hyperbilirubinaemia leading to kernik-

voluntary patterns http://adc.bmj.com/ of movement in much the same way as dystonia, terus, so that in a high proportion of cases there is a choreoid movements, or athetosis. history of abnormal behaviour in the neonatal Patients who suffer from dyskinesia commonly period (de Lange, 1924). After the acute symptoms show two or more types of involuntary movement, and signs of '' or kernikterus have and it is important that these should be recorded and resolved, these patients pass through a latent stage in their distribution noted when the patient is describ- which their behaviour does not appear to be grossly ed. In a high proportion of patients who suffer abnormal, though a rather high proportion have from dyskinesia, involuntary movements and tension feeding difficulties (more than two-thirds give a on September 26, 2021 by guest. Protected affect all four limbs, the bulbar musculature, and history of regurgitation, difficulty in swallowing, or the trunk (Phelps, 1943; Carlson, 1942; Evans and in the early months of infancy). A few, Polani, 1950). The severity of dyskinesia has to be particularly those who have suffered from kernikter- judged by the extent to which patients are handi- us, have alterations of rhythm which parents capped in everyday activities. Mildly affected often have good cause to remember even years later. patients are those who are leading virtually normal On examination at this stage oflatent or hypotonic lives, though they may have difficulty in some tasks dyskinesia, the most striking findings are the general requiring high manipulative skills, such as dealing retardation of the neuromuscular development, the with small buttons or shoe laces, and in writing. poverty ofmovement, and the generalized hypotonia. Patients with moderately severe dyskinesia are those Reflexes which are normally present only in the who require help with more everyday activities and newborn baby persist, and even at the age of 3 or 4 require attendance. Severely affected patients are months may be elicited with ease (Fig. 12). The those who are chair- or bed-ridden and require help stepping reflex and Moro reflex are commonly very Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

350 T. T. S. Ingram

(a) FIG. 12.-(a) The asymmetrical neck reflex in a baby suffering from early dyskinetic cerebral palsy following kernikterus. The staring downcast eyes are characteristic. (b) The lip reflex in the same baby. FIG. 13.-'Overflow' of involuntary movement affecting easy to elicit, but it is the persistence and dominance both upper limbs and face when she tries to stand without of the asymmetrical neck reflex which is most support. characteristic of dyskinetic cerebral palsy. In especially if he is placed in the erect position or his kernikteric patients the inability to look upwards is head is allowed to extend suddenly as when he is manifest at an early age, and even in the absence of the and being bathed. The positions of trunk copyright. other signs suggestive of cerebral palsy should put limbs which are assumed during this stage are thus the clinician on his guard and make him suspect very similar to those found in diplegic children brain damage (Evans and Polani, 1950; Greenwald during their 'dystonic stage'. As in diplegia, the and Messer, 1927; Plum, 1965). duration of the dystonic stage or stage of mass The duration of the latent or hypotonic stage is movements is variable. Severely affected patients very variable and in severely affected babies it may may never outgrow it, but in the majority it will last persist for a year or more. The hypotonic stage is for only a few weeks and then gradually merge into

succeeded by a stage in which involuntary movement a stage in which involuntary movements become http://adc.bmj.com/ of the trunk and limbs occurs when the baby progressively more limited in their extent and attempts voluntary movements and when it is distribution, and occur rather less readily. handled. There is a tendency to mass involuntary It is in this stage of dyskinesia in which discrete movement. This may appear gradually so that the involuntary movements are apparent, that the parents can hardly date its onset, or it may come on various types of involuntary movement can be suddenly, very often in the presence of a febrile ill- recognized, and the distribution in which they occur ness. In this stage of mass involuntary movement, may be perceived. Thus instead of showing a which does not occur in all patients who suffer from position equivalent to generalized opisthotonus on September 26, 2021 by guest. Protected dyskinesia, there is a tendency for head retraction, whenever he attempts to move, the child who enters back arching, and opisthotonus. For example, a the stage of more discrete involuntary movements baby aged 5 or 6 months may try to reach for an will show some tendency to extensor hypertonus and object, and as he does so he involuntarily stiffens and show back arching. But it is only the upper limb shows hyperextension of the neck and trunk, that he is trying to move that will assume the full adduction, internal rotation and flexion of the opisthotonic posture. The amount of overflow of shoulders, extension of the elbows, pronation of the involuntary movement from one part of the body to forearms, semiflexion of the wrists, and flexion of the other during this stage is variable. Those the fingers over the adducted thumbs. The lower patients with severe choreoid movements and limbs adduct and internally rotate at the hip, extend dystonia show a tendency to 'overflow', so that any at the knee, and the feet plantar flex. There is attempted movement of a hand will be accompanied scissoring of the lower limbs. The same type of by involuntary movements not only in the other mass movement occurs when the child is handled, hand but in the face, trunk, and lower limbs (Fig. 13). Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

The Neurology of Cerebral Palsy 351 As in diplegia, various infantile reflexes persist in of vision and , and specific educational and patients with dyskinesia. The stepping reflex is behavioural abnormalities, that the majority cannot often completely uninhibited and uncontrolled, and take their place in normal society (Crothers and may appear as 'cycling movements' of the legs, Paine, 1959; Henderson, 1961; Ingram, 1964a). especially in the erect position in severely affected patients. The asymmetrical tonic neck reflexes Intellectual impairment. The majority of (Fig. 14) may be so marked that the child cannot patients with cerebral palsy are of subnormal turn her head without completely disorganizing her intelligence (Dunsdon, 1952; Floyer, 1955; Illing- whole balance, as her limbs involuntarily alter worth, 1958; Cockburn, 1961). In most series position, and the Moro reflex may also be elicited by approximately one-third of patients are found to be a wide variety of slight movements on fairly quiet of average or superior intelligence and the remainder sound stimuli. are mentally subnormal. In a recent study in Edinburgh it was found that approximately 22% of patients had IQs of less than 55, and 24°o had IQs between 70 and 84. Children with bilateral hemi- plegia, or diplegia with tetraplegic involvement, were less intelligent than those with hemiplegia, diplegia with only paraplegic involvement, or dyskinesia. Within the individual categories of cerebral palsy, children with extensive or severe physical defects tended to be less intelligent than those whose limb FIG. 14.-The asymmetrical neck reflex in an older child involvement was less marked. suffering from dyskinesia. Difficulties in learning to read and write occur frequently in patients with cerebral palsy. Those with retarded speech development are likely to have

At absolute rest in the prone position with head difficulties in breaking down words correctly into copyright. flexed, the patients with dyskinesia are usually their component sounds when trying to write them, hypotonic, though as noted by Plum (1965) a and in synthesizing the parts they have correctly proportion, particularly those who have suffered read and sounded when reading. Others, particu- from perinatal hypoxia, show some spasticity. In larly those with ataxia, are likely to have great dyskinesia, however, more than in any other type of difficulties in recognizing, orienting, and placing in cerebral palsy, it is by prolonged observation of the order patterns such as letter shapes, and in repro- child in everyday activities such as walking, talking, ducing them. These difficulties, which mav be dressing, and undressing, feeding, or attempting to termed 'visuo-spatial', have been increasingly http://adc.bmj.com/ play that the clinician diagnoses the nature of his recognized by teachers of cerebral palsied children illness and assesses its distribution. (Taylor, 1959; Berko, 1954; Lord, 1937; Nelson, Fewer patients who suffer from dyskinesia are 1962; Nielsen, 1962; Prechtl, 1962; Wedell, 1960; seriously mentally subnormal than are patients who Ingram, 1960). suffer from other types of cerebral palsy. Fewer have epilepsy. On the other hand, a relatively high Speech defects. The percentages of children proportion have high tone or even nearly total considered to suffer from defective speech in . Because of the combination of different series will vary according to the criteria of on September 26, 2021 by guest. Protected involuntary movements of the lips, tongue, and defective speech adopted by the workers concerned. palate, and hearing loss, a high proportion have When moderate intelligibility is required, about severe speech defects, the more damaging since 50% of patients in regional surveys have significant these patients tend to be intelligent (Asher, 1952; speech defects (Ingram, 1955a; Hansen, 1960). Fisch, 1955; Crothers and Paine, 1959). Contrary to many published opinions, true dysphasia is rare in these children (Guttmann, 1942). True Associated Disabilities in Patients Who dysphasia may occur in children who suffer from Suffer from Cerebral Palsy injury to the dominant hemisphere after the age of If the motor deficit in cerebral palsy were the only about 3 years, but if the injury is sustained much causes of handicap, a high proportion of patients before this then the effect on speech is likely to be would be leading almost normal lives. It is because either to retard subsequent development or to of the associated disabilities, in particular intellec- produce a mixed picture of loss of acquired speech tual impairment, epilepsy, speech defects, disorders and slowness of development. Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

352 T. T. S5. Ingram In a series of patients studied in Edinburgh it was dysarthria. The consistency with which word found that the commonest disorder of speech in sounds are either omitted or substituted is less hemiplegic children was simple retardation of speech constant in the dysarthria which complicates ataxic development. The acquisition of speech sounds, cerebral palsy than it is in diplegia. Dysrhythmia words, and phrases was slowed. The next most and associated abnormalities of intonation and stress frequent type of abnormality was speech dysrhyth- which are very difficult to analyse occur in a high mia. Specific language disability occurred in proportion of ataxic children. approximately 12% of hemiplegic patients. The characteristic facile talkativeness of many The most important cause of speech abnormality hydrocephalics is well known. Their readiness to in diplegic patients was retarded speech develop- speak may give a false impression of intelligence, ment, and the retardation of speech development which is only dispelled when the content of what tended to be proportional to the degree of mental they say is analysed and found to consist of 'parrot- handicap and to the extent of the paresis. Dysarth- tings' of adult speech and repetitive jargon (Ingram ria was commoner amongst diplegic than amongst and Naughton, 1962). hemiplegic children; it occurred more often in Only a small proportion of dyskinetic children tetraplegia than in or paraplegia; it was speak normally. The majority have complex speech invariably accompanied by impairment of voluntary defects due to a number of different causes. In the movements of the lips, tongue, or palate, and in same Edinburgh series 78% of 67 children who most of the severely affected patients aU three suffered from dyskinesia were found to have speech organs were involved. A high proportion of defects or virtual absence of speech due to multiple children with severe dysarthria or no speech causes. Only in 22% were the disorders thought to development had a history of feeding difficulty or be entirely the result of dysarthria, retardation of drooling in infancy. Many of these were found to speech development, or dysrhythmia. Retardation have lip and sucking reflexes that were remarkably of speech development attributable to mental easy to elicit. subnormality was a less important cause than in

There is a characteristic form of dysarthria in other categories of cerebral palsy, but retardation of copyright. diplegic children, which consists of slowing of speech due to impairment ofhearing was much more utterances and monotony of intonation and stress frequent than in the other categories. patterns. There is often slight or moderate nasal escape because of palatal paresis, and hypernasality Behaviour abnormalities. Since Strauss and results. Speech sounds are laboured and vowels Lehtinen (1947) described patterns of behaviour are better used than consonants. Dysarthria which they considered were directly attributable to occurred as the only abnormality of speech in about the effects of brain damage, there has been increas-

20% of the diplegic patients and in association with ing interest in the behaviour abnormalities that are http://adc.bmj.com/ other speech disorders in a further 24% (Ingram and found in cerebral palsy. Michell (1963) has Barn, 1961). described hyperkinesis, short attention span, and Most children with ataxic cerebral palsy have distractibility, lability of mood, antisocial behaviour defective speech. As with other forms of cerebral manifest as lying, stealing, truancy, offences of palsy, the commonest disorder is simple retardation cruelty, difficulties in abstract thought, and attacks of speech development. This may occur alone, but of extreme anxiety with panic, as characteristic of is commoner in association with dysarthria and other the brain-damaged child. It is, however, difficult to abnormalities including dysrhythmia of a character- assign abnormalities of behaviour such as these to on September 26, 2021 by guest. Protected istic type. The retardation of speech development either 'organic' causes or to the consequential tends to be proportional to the degree of mental 'psychological stresses' (Bice, 1952; Wortis and impairment, but a few patients who suffer from Cooper, 1957; Kelman, 1964; Ingram, 1963) ataxia show severity of retarded speech development (Table III). which is quite disproportionate to their mental Distractibility and short attention span are as often subnormality. Thus children who appear to be of as not secondary manifestations of mental defect, average intelligence so far as their general behaviour but the syndrome of hyperkinetic behaviour which development is concerned may have little or no occurs in a proportion of children who have suffered speech even at the age of 5 or 6 years. from localized hemisphere damage affecting one or The characteristic scanning speech found in adult both temporal lobes is characteristic. They show patients with ataxia is also found in children with an intense preoccupation with their immediate ataxic cerebral palsy, and in addition incoordination surroundings, marked restlessness, and an almost of tongue, lip, and palatal movements results in compulsive desire to explore everything in the Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

The Neurology of Cerebral Palsy 353 TABLE III Relationship of Various Clinical Syndromes (excluding Cerebral Palsy, Epilepsy, and Mental Defect) to Organic Brain Abnormality

Defined Clinical Syndrome with Defined Clinical Syndromes with Symptoms in Which Brain Abnormality Constant Evidence of Brain Inconstant Evidence of Brain May be an Inconstant Direct or Abnormality Abnormality Indirect Contributory Cause Examples Examples Examples Choreiform syndrome Specific retardation of speech Distractability development Minor cerebral palsy Variability of behaviour Specific developmental and Hyperkinetic behaviour syndrome dysgraphia Impulsiveness Specific 'clumsiness' Irritability Anxiety Emotional immaturity vicinity by touching it or putting it to the mouth. ataxic diplegia than in those with diplegia or Often there is an almost complete lack of insight or dyskinesia. Myoclonic attacks (infantile spasms) consideration for other people, and an inability to occur most commonly in children with severe accept the least frustration, so that any checking of mental defect, especially if their brain anomalies are activities may result in the child attacking whoever attributable to severe developmental malformations. tries to stop him from gratifying his momentary True petit mal is relatively rare in cerebral palsy, whim. A similar type of behaviour may be pro- though it is often diagnosed (Woods, 1957; Skatvedt, duced in monkeys by making discrete lesions in one 1958). or other temporal lobe in the region of the hypo- A much higher percentage of patients who have

campus (Kliiver and Bucy, 1939; Ounsted, 1955; clinical seizures have abnormal EEGs than do those copyright. Ingram, 1956). It is characteristic of this syndrome without seizures (Perlstein, Gibbs and Gibbs, 1955; that the administration of phenobarbitone to Woods, 1965; Gibbs, Gibbs, Perlstein, and Rich, patients exacerbates it, while administration of anti- 1963). The latter authors noted that there was a high epileptic drugs such as primidome or sulthiame may correlation between the presence of multiple focuses alleviate it. As affected patients grow older their of spike activity and educability. Their extensive hyperactivity diminishes. Overactive behaviour of study on 2,124 cases of cerebral palsy suggests that the type described by Ounsted is most commonly the value of the EEG in cerebral palsy has not yet found amongst cerebral palsy patients who suffer been fully appreciated. http://adc.bmj.com/ from acquired hemiplegia and ataxic diplegia. Seizures in patients with cerebral palsy are difficult to control, and in particular focal seizures in Epilepsy. In most regional studies of cerebral hemiplegia seem to be resistant to treatment with palsy epilepsy has been present in 20-50% of anti-epileptic drugs (Crothers and Paine, 1959; patients, though the reported incidence of recurrent Fukuyama, Arima, Nagahata, and Okada, 1963), as seizures has varied considerably (Asher and Schonell, are also myoclonic seizures (Jeavons and Bower, 1950; Perlstein and Hood, 1954; Perlstein, Gibbs, 1964; Pederson, 1964; Gastaut, Poirer, Payan, and Gibbs, 1953; Skatvedt, 1958; Hansen, 1960). Salamon, Toga, and Vigouroux, 1960). on September 26, 2021 by guest. Protected In a recent study, 23 of 57 children suffering from hemiplegia and followed for an average of 4 - 5 years Visual disorders. Visual acuity is difficult to had epilepsy: poor control of seizures was associated test in young children, and it is only recently that with lower intelligence and lower speech and attempts to test vision in children under 1 year have behaviour levels than were found in seizure-free proved reliable (Sheridan, 1965). This may patients (Jabbour and Lundervold, 1963). account for the fact that the incidence of visual The commonest form of seizure encountered in disorders reported in different series of patients cerebral palsy is grand mal, and this is most fre- varies so greatly. The most comprehensive study quently found in those with hemiplegia, bilateral is that of Douglas, who studied 168 patients in the hemiplegia, and diplegia. Children with ataxic survey conducted in Dundee by Henderson (1961), cerebral palsy and dyskinesia less often have grand though even his series is selected, so that the mal seizures. Focal seizures occur more commonly conclusions that can be drawn from it must be in those with hemiplegia, bilateral hemiplegia, and limited. Douglas found that 35% of the patients Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

354 T. T. S. Ingram suffered from strabismus, 13°% from nystagmus, 4% cord-the so-called y system. Efferent impulses from colobomata, 10% from optic atrophy, and 1 % from higher nervous centres acting through the y from congenital cataract. system cause changes in the length of muscle If this survey had been carried out a few years spindles, and hence increase or decrease the afferent earlier, cases of retrolental fibroplasia would no discharges to the spinal cord. The y system appears doubt also have been found, particularly in pre- to operate as a closed-loop servo-mechanism control- maturely born patients who suffered from diplegia ling the length and tension of muscle, both in (Ingram and Kerr, 1954). voluntary movement and the involuntary activity of Visual field defects are practically confined to muscles, which serves to maintain posture (Fig. 15). patients with hemiplegia, bilateral hemiplegia, and ataxic diplegia, and are found in 10-25% of cases. MOTONEURONE MUSCLE They are difficult to diagnose before the patients can F~~~F~~~aiu s~xtafua co-operate fully, particularly since good compensa- ^ _8t vLoad tion can be achieved by the age of 2 or 3, even in Centres b LY ~~Muscle Spindle those with complete hemianopia. Further studies of eye movements in the newborn FIG. 15.-Simplified diagram of the a and y pathways for and of strabismus in cerebral palsy have recently controlling (from Matthews, 1964). been presented by Douglas (1963), Smith (1963), and Griffiths and Smith (1963). It is apparent that A continual state of equilibrium between load and strabismus is a frequent and important muscle length and tension can be envisaged- of cerebral palsy, but it is debatable how far paresis muscle activity being reflexly stimulated through of ocular is responsible. tendon endings and muscle spindles, whenever the load stretches a muscle beyond certain limits. Hearing impairment. Fisch (1957) found that Thus the activity of the y system can set the level at 259/ of patients with cerebral palsy who attended which the operates. In states in school had some hearing impairment. In Dundee

which the y system is uninhibited the stretch reflex copyright. 23% of 70 co-operative cerebral-palsied patients is active; when the clinician moves a muscle in this without severe mental impairment were found to be state passively he is likely to consider it to be hyper- hard of hearing (Mowat, 1961). In contrast, 5% tonic or rigid or spastic. Whereas if the y system of cerebral-palsied children were found by Mac- is relatively inactive he will appreciate that resistance Gregor, Pirrie, and Shaddick (1957), to suffer from to passive movement is less than he had expected, hearing impairment, 7% by Woods (1957), and 8% and will consider the muscle to be 'hypotonic'. It by Ingram (1955a). These varied figures may well appears that the effect of local anaesthetic and of be attributable to different techniques of assessment alcohol in reducing rigidity and spasticity in http://adc.bmj.com/ as well as to the selection of cases. experimental animals is a result of a relatively All appear to agree, however, that hearing loss specific action ofthese substances on y endings occurs more frequently in those with dyskinesia (Walshe, 1923, 1924; Matthews and Rushworth, than it does in other forms of cerebral palsy, and that 1957; Rushworth, 1959, 1960, 1962). children with bilateral hemiplegia and severe It is tempting to speculate about the role of the y diplegia more often suffer from hearing loss than do system in altering muscle tone in children with those with ataxia and hemiplegia (Ingram, 1964a). cerebral palsy. Infiltrations of alcohol into nerves, motor points, and other parts of muscles have been on September 26, 2021 by guest. Protected Recent Studies of Changes of Muscle Tone in carried out in children with spasticity attributable to Cerebral Palsy cerebral lesions. The success of the procedures has It is not proposed to discuss the underlying varied greatly, but when successful they have of cerebral palsy, but recent work resulted in a marked reduction of muscle hypertonia on the origin of muscular hypertonus and its (Sachs and Hausman, 1926) and of the stretch reflex. abolition by the injection of local anaesthetics and This finding not only suggests a new approach to the alcohol into nerves and nerve endings must be treatment of spasticity and palsy, but mentioned. provides promising avenues for future research, Resting muscle tone is changed by many influ- which may lead to better understanding of disorders ences, such as the age of the child, his alertness, his of muscle tone and more rational treatment of many emotional state, and his temperature. Tone is patients with cerebral palsy (Tardieu, Tardieu, influenced by these factors through the muscle Hariga, Gagnard, and Velin, 1964; Tardieu and spindles and their neural connexions with the spinal Hariga, 1964). Arch Dis Child: first published as 10.1136/adc.41.218.337 on 1 August 1966. Downloaded from

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