A METHOD FOR NEUROLOGIC EVALUATION WITHIN THE FIRSTYEAROF LIFE i

CLAUDINE AMIEL-TISON

TABLE OF CONTENTS

GENERAL

CONSIDERATIONS

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Long-Term Fellow-up Studies, Aims and Results, Improving Outlook . . . . . . . Minimal Brain Dysfunction at School Age: Progressive Dilution of Perinatal Causes by Deleterious Environmental Factors . . . . . . . . . Transient Neurologie Abnormalities within the First Year: The Clue to Late Outcome . . . . . . . . . . . Neurologic Evaluation within the First Year of Age: A Logical Conclusion to a Continuous Evaluation of Intensive C a r e . . . . . . . . . . . The Choice of A Technique for Neurologic Evaluation Within the First Year of Life . . . . . . . . . Selectiofl of the Population at Risk . . . . . . DESCRIPTION OF THE M E T H O D

Technical Notes .

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Norm~I Evolution during the First Year and the Most Common Patterns of Abnormalities . Order of ImPortance and GrOuping of Anomalies: Provisiofial SYnthesis at E n d of-First Y e a r . Comparison of Data Obtained by Neurologic Evaluation and Data O b t a i n e d b y Developmental Scales . . . Interpretation o f Data According to 'the Probable Responsibility for the Perinatal Insult . . . . . . Interobserver Reliability . . . . . . . . . . APPENDIX

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is Associate Professor at the University of Paris and heads the neonatal intensive care unit of the Port-Royal Maternity Hospital. Doctor Amiel-Tison received her M.D. degree f r 0 m t h e University of Paris, where she also took her clinical residency in pediatrics. After a one-year fellowship at the Babies' Hospital of Ccrlumbia University, she joined the Department of Neurology at Port-Royal Hosp~at and completed her training in respiratory physiology at Stanford University. H e r research and clinical interests a r e i n the field of perinatal brain damage and its late consequences.

CONSIDERATIONS [ FOLLOW-UP STUDIES, AII~iS AND RESULTS, OUTLOOK

iICIANS AND PEDIATRICIANS have always been in evaluating the late outcome of the newborns they for. The link between perinatal insult and late handiitablished long ago. Although neurologists and psyay argue about the relative importance of this link, itseff is irrefutable; there is a "continuity of repromalty.,,1, 2 lrly days of neonatal intensive care, tl~e main concern a increase in survival rate would be followed by an inmber of handicapped Children. This anxiety has been xcept for a few survivors after massive intraventricular e followed by hydrocephaly, the incidence of cerebral rinatal origin has decreased significantly. 3. 4 ecent reports of follow-up studies clearly show that the of brain damage in high-risk newborns is decreasing dy with the progressive improvement in intensive care. groups have been studied: newborns with idiopathic r distress syndrome treated with artificial ventilalfants with low birth weight, n-2~ fetal hypotrophy gestational age),22.2~ children who had received intrainsfusions,23 infants of diabetic mothers 24 and unfavortric circumstances.25-~0 ~udies have been invaluable in allowing optimistic stateut the efficiency of pre- and postnatal care. However, of follow-up study is no longer satisfactory and the !gy itseli is subject to criticism.

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The first criticism is of tim tests used. To detect brain damage of moderate severity, the neurologic evaluation must become more accurate. However, developmental scales such as the Bayley scale31 or the Brunet-Lezine scale,~2 for example, very often have been the only test given in these studies. This means that only severe cases of motor handicap have been taken into account. The second criticism is the delay of about seven years considered necessary before reaching an individual prognosis with developmental,scales. The rapid advances in pre- and postnatal care are such that waitirig for school age before coming to any conclusion is unacceptable. Finally, the questions must be asked: Are obstetricians and pediatricians interested in individual prognosis and what is the meaning of individual late outcome? Jane MacFarlane, a pioneer of theBerkeley study, once concluded with humor and philosophy that "what is interesting with human beings is how uhpredictable" they are." ~fhis means t h a t adult achievement is something different from neuromotor integrity or adaptation at school age. Although it may be impossible to predict outcome in any individual case, it is worthwhile to evaluate the results of various modes of ~herapy statistically in newborn intensive care units. MINIMAL BRAIN DYSFUNCTION AT SCHOOL AGE: PROGRESSIVE DILUTION OF PERINATAL CAUSES BY DELETERIOUS ENVIRONMENTAL FACTORS

Several studies on national or regional scales have gathered a remarkable amount of information on the role of environmental factors and have contributed to increasing disillusionment over these endless long-term studies ~on late outcome. The two most extensive of these projects are the British Per[natal Mortality Survey and the Collaborative Perinatal Study of the National Institute of Neurologica1 Diseases and Stroke. They analyze for each nation the respective roles of multiple deleterious factors in the perinatal period on subsequent wellbeing and adaptation. Davie and ass0ciates 33 demonstrated in children 7 years of age a very clear relation between perinatal factors such as prematurity or intrauterine growth retardation and percent 0f secluelae. However, the role of social class and birth order on "educational backwardness," for instance, at 7 years of age appear much more deleterious. This superb follow-up, still going on,~4 is of importance f o r the organization of special education in t h e high-risk population. But this data was not Of m u c h h e l p in separating handicaps dependent on per[natal lesions and handicaps linked to unfavorable environment in childhood. Neligan ~5 reached the same conclusions in the birth, family, 4

and development study in Newcastle upon Tyne. This methodologic difficulty also has been discussed 36 when analyzing the signs of minimal brain dysfunction in children from 3 to 10 years of age. Environmental factors have played such a role at this age that it becomes impossible to separate neurologic and behavioral difficulties. ]'RANSIENT NEUROLOGIC ABNORMALITIES ~VITHIN THE FIRST YEAR: THE CLUE TO LATE OUTCOI~IE

Mild or even transitory abaormalities observed during the first year of life probably are:the best Clues to distinguish~between per/natal insult and minimal brain dysfunction at school age: this is the working hypothesis to be tested. Transitory tonu.s abnormalities have been recognized for many years and recently have been reconsidered,v. 37, as Drillien3~ has named these transitory abnormalities "transient dystonia associated with low birth weight." She suggests t h a t among infants with birth weights of 1.500 gm or less, a lower percentage of these children with abnormalities during the first year will have a normal developmental quotient than a group who had exhibited no abnormal signs, 39% agffinst 78%, respectively. This means that the group of infants having had these transitory abnormalities will be a high-risk group for school age. Among children of school age with "minimal brain dysfunction," those having had transitory neurologic abnormalities prob9fl)ly suffered brain damage; psychogenic or environmental dysfunction is additive to this abnormal substratum. For semanti c reasons, I shall not Call this syndrome of transi(,nt abnormal neurologic signs in the firs~ y e a r "dystonia~" as proposed by Drillien, but I shall use t h e descriptive denomination. DescriSed in infants with low birth weight, this syndrome can be detected as well in full-term newborns after perinatal distress; it does not seem specificto any maturational stage, even though it is more frequent in premature newborns. NEUROLOCIC EVALUATION WITHIN THE FIRST YEAR OF AGE: A LOGICAL CONCLUSION TO A CONTINUOUS EVALUATION OF INTENSIVE CARE

Obstetricians want to judge their methods of pre- and intrapartum care, and pediatricians want to compare new methods of respiratory care with older ones. Because iatrogenesis is sometimes added to new advances in therapy, a rapid answer is an imperative necessity. Thus, evaluation at 1 y e a r of age seems to be perhaps the only reasonable way to determine the incidence of lesions of perinatal

origin continuously. Moreover, since it is impossible to keep track of minimal lesions until school age, there is nothing wrong with a longer period of observation. Therefore the assumption suggested by Drillien's results could give the best compromise: mild or transient neurologic abnormalities during the first year of age will be followed in a high percent of cases by intellectual and behavioral handicaps at school age, all these anomalies being successive expressions of moderate brain damage of perinatal origin. The neurologist or other physician in charge of follow-up studies will not focus"on individual prognosis but on evaluation of perinatal care. He will be able at the end of the first year, to classify survivors in three groups: (1) normal during the first year; (2) clear handicaps, motor or mental, or both; and (3) normal after transient abnormalities during the first year. With this classification, a given obstetric or neonatal unitwill be able to compare its results year after year, observing not only decreasing numbers of severely handicapped children but the number of transient abnormalities as well. With widespread acceptance, the method would allow comparisons with other departments. The proposed link between transient neurologic abnormalities during the first year of life and minimal brain dysfunction at school age remains to be demonstrated in seven years. This working hypothesis tends to place an emphasis on lesions, with transient abnormalities being the clue to mild late sequelae. THE CHOICE OF A TECHNIQUE FOR NEUROLOGIC EVALUATION ~VITHIN THE FIRST YEAR OF LIFE

Several methods for the neurologic evaluation of the newborn and infant have been described in various texts. 39-4s The tendency of the school of Andre Thomas is to rely on a meticulous study of passive t o n e , active tone, primary reactions, and postural reactions. Severalstudies in the last 15 years with this method have accumulated a g r e a t deal of data, allowing an earlier and more accurate diagnosisof brain damage. 44-4s Other groups oriented toward early l~inesitherapy have developed a completely different approach. They evaluate the motor function, and determine what amount of stimulative help is necessary to obtain a given motor response. The aim of this "kinesiologic" approach is therapeutic; there is no attempt at anatomical or etiologic diagnosis, 47-~~ Although this type of dynamic evaluation appears overly complex, the evaluation of postural reactivity of the central nervous system may be added to the classic neurologic evaluatiofi, and has a good predictive value on motor function in lower limbs, s~ 6

This very abundance and variety of methods, however, can be somewhat discouraging--so discouraging t h a t the .absence of neurologic items is a fairly constant phenomenon in most of the follow-up studies reported during the past 20 years. Most of the results are based exclusively on developmental scales; the good standardization and quantification of such scales probably being the reason for this general attitude. Because Of t h e possibility of quantification and after experience with his work, I had decided that a method derived from Andre Thomas probably would be the most logical and practical one for neonatalogists, allowing a precise detection of transitory as well as permanent abnormalities. This assessment would be strictly neurologic and would not duplicate the mental and motor scales of infant development. Mter the first few weeks of corrected age, the developmental ~r should be performed monthly in addition to the examination described here. Evaluation of muscle tone is a fundamental part of this examination and includes study of the resting posture, passive tone and active tone. Spontaneous posture is appreciated by inspection of the infant while he lies undisturbed. Passive tone is evaluated by applying certain movements to the infant while he remains passive and at rest. The resistance of an extremity to these manipulations ~ measured by recording the angle formed by the passive movement. The maneuvers must be performed slowly and gently, just to the point of being uncomfortable. Active tone is Studied with the infant moving spontaneously in 9"esponse to a given stimulus. Only a few items are observed here, ia order not to duplicate the development sc.ales. However, for a few maneuvers it is more 9 to ~tudy the anomalies in performance than to consider a t which age the acquisition is piesent. This is. especially important for head control 5xand.sitting and standing positions. T e s t i n g head control during a-given 9movement-of t h e trunk must be performed by the examiner with the correct speed--n0t .too slowly, n o t too quickly; this proper speed can be determined after a bit of experience. The choice of items is based p a r r y on information from the literature and partly on my own clinical experience at the PortRgyal Maternity Hospital. T h e technique chosen and the possible responses have been analyzed for each item. The order in which they appear corresponds to a logical procedure for a physical examination. To express the results o f e a c h successive t e s t a n d permit a. statistical analysis, there is a form to fill out. The limits of normal for each response are defined graphically. Each result may be designated simply as normal or abnormal, according to the normal pattern foreach trimester.

The first examination for a premature takes place approximately at the time Of expected term, after his acute problems have had time to resolve and he has begun to feed and gain weight. The nutritional and respiratory status of both premature and full-term newborns must be sufficiently stable for the examination to be reliable and reproducible. Therefore, if the initial testing is performed at 38-42 weeks (corrected age for prematures) for all infants, interpretation of the results then is not depenclent on the maturationa! stage of thebrain. Later on, a monthly examination will be performed until the end of the first year. The corrected age will be used for premature newborns all during the first year of life, by subtracting the missing weeks of gestation from the age up to the day of the evaluation. Each number, from 1 to 12, designates the month of corrected age. To take an example, a 33-week premature will have a correction factor of 7 weeks. The first examination (no. 1) will take place at about the time of expected term, or when the infant is 7 weeks old. The second examination at 11-12 weeks of life, will thus take place at a "corrected age" of 4-5 weeks. At that time, in the second month of postterm life, the infant will be given examination no. 2. Every neurologist defines a list of optimal conditions for neurologic evaluation to be valid; state of alertness, of exteroceptive and interoceptive stimulation are examples. This is imperative for research and standardization; however, one must admit that all these conditions rarely are fulfilled during the whole examination in an outp~itient clinic. For this, defining the state of alertness for each item with'the five :different stages of Beintema,43 for example, is unrealistic in the usual ~conditions of practice. I t is w h y I have chosen a rough evaluation of alertness during the whole test. SELECTION OF T H E P O P U L A T I O N A T RISK

Full-term infants and infants with a low birth weight must be clearly separated when selecting a high-risk population.

Full-term Newborns.--Selection is based on neurologic abnormalities during the neonatal period; these can be divided into three degrees of severity, whose symptoms vary in type and duration.S2-~4 1. The most severe degree is status epilepticus, which usually begins some hours after resuscitation and is confirmed by an inactive or paroxysmal interictal EEG tracing. 5s Neonatal death 8

occurs in approximately 50% of the cases. Cerebral necrosis is observed at autopsy. 56. 57 If the infant survives, severe neurologic findings still are present. 2. In moderate degrees of fetal asphyxia, neurologic abnormalities are observed in many cases during the first few hours but have a tendency to increase later on in the first few days of life. Several types of syndromes are observed--alteration of consciousness, of tone and of reflexes, w h i c h are grouped roughly into two categories:-hypotonia, lethargy and hyporeactivity, or hypertonia and hyper~eactivity. Experimental data allows us fo assume that cerebral edema (brain swelling) is the main lesion. 57 :Survival is the rule. Moderate neurologic abnormalities, including abnormalities of tone, reflexes a n d consciousness, persist on discharge. 3. In mild degree, neurologic abnormalities at birth usually are hypertonia and ir.ritability, v~hich disappear in a few days. N o cellular lesions are likely. 57 The child is normal at the end of the first week. In conclusion, a neurologic evaluation of every newborn following birth is necessary, regardless of the Apgar score. In a few cases, there is no sign of fetal distress during labor, and the Apgar score is above 7; however, neurologic abnormalities are observed, probably, as a secondary problem to hea d compressi0n, with: local hemodynamic disturbances. 54' 5s. 59 Althoug h a correlation was demonstrated long ago between brain ~damage and the Apsar score, 25 neurologi.c abnormalities are a bette~r index than abnormal circumstances. 5~

Low Birth Weight.--In the g r o u p s with low birth weight (2,500 gm), neurologic abnormalities fotmd'during the neonatal period are of much lessdiagn0stic and p~ognostic va!ue than for the full:term infant. Except for massive intraventricular hemorrhage, which is quite spectacular Clinically, or for hydrocephalus, which often complicates this type 0f hemorrhage, there'! s n o re, liable clue to a brain lesi0ri. Leiikbmalacias are clinically silent in the neonatal period; ~1 nevertheless, they :aide:probably: the most common lesions 62, G~ending in cerebral palsy: Finally, for infants with low birth weighi, n eonata.1 :events known to b e unfavorable are better indices t h a n are 'neurologic abnormalities. This symptomatologic weakness probably~is related to immatur, ity, or to chronic distress in fetal intrauterirle growth rate, Therefore, the decision to follow an infant as a high-risk problem cannot reasonably be based only on neonatal neurologic signs. In: fants with low birth weight have to be :selected for follow:up studies according to their high-risk history and gestational and neonatal events. 6~ 9

DESCRIPTION OF THE METHOD

TECHNICAL NOTES For each item chosen, the way to elicit the reaction is indicated. The different patterns of response are analyzed and described as normal or abnormal. On the f o r m (see Appendix), the normal developmental pattern is shown graphically: Thus, each response must be compared to the normal c~evelopmental stage. By comparisonwiththe pattern considered normal for each trimester, the result is immediately "interpreted," and the interpretation also appears on .the form.

Head Circumference.--The head circumference is measured and then plotted on a growth curve. ~s Serial measurements are necessary for interpretation, particularly in cases of borderline microcephaly or suspicion of hydrocephalus. Anterior Fontanelle.--The Size of the anterior fontanelle is extremely variable, increases with gestational age from 28 to 40 weeks and is much larger in infants that are small for their gesrational age. ss Sutures.--During the neonatal period, the width of the sutures is interpreted according to which suture is considered. The sagittal and parieto-occipital sutures often are 4 or 5 mm wide or more, a findingwith no significance, 4- or 5-mm separations may also be observed in the portions of the metopic and coronal sutures that are close to the anterior fontanelle. However, separation of the squamous sutur~ (parietotemporal) of more than 2 mm must be considered as a reliable sign of hydrocephalus. When hydrocephalus is suspected, several o t h e r signs h a v e t o be checkeddaily and interpreted as a whole, including the squamous suture-and increase of head circumference. Usual Pattern for Wakefulness and Sleep.--This is asked of the mother and interpreted roughly according to age, and in the absence of a nutritional problem. "Normal" is an approximate evaluation based on quantity and quality of sleep in 24 hours, according to age. Note particularly three abnormal situations belonging to different stages of development. The first two will be recorded on the "agitated, too much crying" line; the third will be recorded on the "lethargic, no crying" line. 1. The infant sleeps for very short periods-in the daytime and is very agitated and crying when awake. The state of quiet alertness is never obtainable. Anxiety and discomfort seem a permanent status. This pattern is observed mostly in the first months of life. 2. The infant is quiet in the daytime but falling asleep at night 10

is a long and difficult process, with a very prolonged state of drowsiness precedingsleep. This pattern is 6bserved mostly during the third and fourth trimesters. 3. T h e infant sleeps for excessively long periods and too much per 24 hours. He is lethargic and difficult or impossible to awaken fully, or remains awake only for very short periods.

State of Alertness During the Test.--The examination should be done when the infant is as wide awake as possible, since ff he is sleepy, muscle tone becomes much more relaxed and the primary reactions become slow or absent. Following a feeding, the infant usually is sleepy and just before a feeding he is often agitated, so t h a t the best tirne is about 1 hour before a feeding. T h e ~tate of quiet alertness is essential to obtain most of the responses. Excessive external stimulations such as noise and light must be avoided. Stimulations from the gastrointestinal tract also can interfere in an unavoidable and Unmeasurable way. Estimation of the alertness during the test is to be noted on the form. If too many response s are judged unsatisfactory because of sleepiness or crying, t h e test should be repeated at a more favorable time. Quality o[ the Cry.--Note if the cry is normal, high pitched, weak, monotonous, moaning, discontinuous, or other, resulting in cyanosis or vasomotor anomalies, difficult to elicit. Sucking Behavior.--Note if the sucking is normal, with a good .~ucking-swallowing coordination; if only partial bottle feeding i~ possible or completely impossible, making garage indispensable; if choking has been observed repeatedly. Convulsions during the Preceding Month.~Generalized convulsion, focal convulsion, febrile convulsions, infantile spasms (salaam seizures). Hypertonia o[ the Levator Muscles o[ Upper EyeIids.~When ~hese muscles are hypertonic; the resulting lid retraction makes the upper sclerae visible (Fig 1). In contrast to the se~ting-sun sign, the pupil is entirely visible. The globe itself is.in normal position, whereas iri the setting-sun sign it is lowered in the orbit. It is important to distinguish these two conditions. One is not a mild form of the other. This hypertonia of the lid retractors is usually n o t an isolated finding, amt general hyperexcitability is often associated.

Setting-Sun Sign.~The downward rotation of the globes with the pupils partially covered by the lower eyelids and the sclerae ~isible above the pupils, is called the setting-sun sign. It may be Constant, at rest, or elicited in the course of the clinical examination. 11

Fig 1.--Hypertonia of the levator muscles of the upper eYelids. Lid retraction makes the upper sclerae visible.

.Marked Strabismus.mConvergent or divergent, uni- or bilateral.

Sustained Nystagmus.--Pendular nystagmus is observed when there is ~mperfect visual fixation of central or peripheral origin. When the eyes are directed straight forward, the movements arc at equal speed. Note if nystagmus is sustained. Pursuit of:Light.--The infant must be awake and quiet. The frequently observed Synergy between sucking and opening of the eyes m a y facilitate the observation in: the first month. I t is easier to test visual pursuit with a source of light than with an object in the neonatal period. The soarce of light m a y be a small flashlight or a window with moderately bright ligh t. T h e infant turns his head toward the source of light. Then, when the infant's b o d y is turned to either side, his eyes continue to fix on the light. Acoustic Blink Reflex.--The acoustic blink reflex is elicited by using a handclap a b o u t 30 cm to the side of the infant's ear. The response is positive if the eyes close or the lids blink. Asymmetric Tonic Neck Reflex (Spontaneous or Postural).-When lying on his back with his head turned to one side, the infant tends to extend the arm and leg o n the side of the body toward which the face is turned and to flex the arm and leg of the opposite side (Fig 2). The reflex is considered as present even if the posture involves only upper limbs or only lower limbs. Note if present at the beginning of the examination or later on.

Abnormal Hypertonia in Neck Extensors.--At any maturational stage, when the infant is lying supine in the resting posi12

Fig 2.--Asymmetrictonic neck reflex, postural. Posture in upper and lower tirnbs depen-ds on lateral rotation of the head.

tion, the neck is normally flat, the muscles are relaxed and there is no free space between the spine and the bed. If there is permanent hypertonia of the neck extensors at rest, the infant is unable to lie flat when supine and one notes a free .~pace between the neck and the bed. As a result;the resting position often is the lateral decubitus, with ~he head extended (Figs 3 and 4). The condition is considered present if there is free space when the head is maintained in'the midline. It is important to note that interpretation of this sign may be difficult in a premature with a" prominent occiput. The results in this Case should be considered together with that of repeated ventral flexion of the neck. The mother usually is a good observer of this symptom and may confirm that a lateral decubitus position with the head extended is very common.

Opisthotonos.--Permanent hypertonia of the extensor muscles of the spine is called opisthotonos. This hypert0nia causes the back to remain in a permanently arched position. The infant is unable to lie flat when supine, and the resting position is in lateral decubitus position with the head extended. This position is more marked than in the preceding condition. Permanent Closure of the Hands.---The newborn's hands usually are closed. However, when the infant is sleeping or very quiet, the hands open and close spontaneously. Later on, the hands are open most of the time. Note if hands are always dosed (abnormal after 2 months); if the thumb is across the palm in a clenched hand (abnormal at any time). 13

normal resting poslt~n

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Fig 3.--Abnormal hypertonia in neck extensors. A, posture in case of abnormal hypertonia in neck extensors. Note the free space and the tendency to lateral decubitus. B, testing of neck flexors in case of abnormal hypertonia in neck extensors. 8'traightening of the head is impossible. O, testing of neck extensors in case of abnormal hypertonia in these muscles. The head is not hanging on the chest atstarting position. (From Amiei-Tison, C.: Neurologic Evaluation of the Neonate, in Gluck, L. [ed.]: Modern Perinatal Medicine. Copyright 9 1974 by Year Book Medical Publishers, Inc., Chicago. Used by permission.)

Asymmetry o[ Posture in Limbs.--With the head carefully maintained in the axis of the trunk, check if the posture is about identical in both upper lim~s and in both lower limbs. A permanent difference i n posture might indicate a n asymmetry in passive tone which will be confirmed later in the examination by specific maneuvers. Theposture is in flexion in all four limbs in a full-term infant. But, since the breech position during the last months of gestation modifies the'postur e in the legs so much for several weeks, this pattern will not be considered here; only asymmetry will be noted. Facial Paralysis.--This condition reveals itself most clearly when the infant:Cries, for the affected side of the face is flat and motionless, the mouth is drawn to the opposite side, and the eye remains open and the lids on the normal side are closed, Spontaneous Motor Activity.raThe speed, intensity and amount of movement are observed when the infant i.4 lying supine on the examination table. This examination is necessarily subjective and involves comparing the quantity and quality of the spontaneous movements of the patient to those of normal in14

Fig 4.--Abnormal.hypertonia in neckextensors. In the resting position the .",~ad is extended and rotated laterally.

fants. Only a very rough evaluation is possible, so only the obvious deviations from normal will he note~. The findings are recorded as follows: poor, if low speed, low intensity, few movements; normal~ i f medium speed, medium intensity, moderate number Of movements; excessive, if high speed, very intensive and excessive movements; asymmetric, if spontaneous movements are rare or absent in one limb When compared to the opposite side.

Abnormal Movements.--Incessant tremor (high frequency, low amplitude): the tremor frequently is observed during the first days of life in normal full-term newborns and is increased by hunger and crying. It is most easily noted-in the extremities and mandible. Considered present if incessant and observed when the infant is not crying or being handled. Burst of clonic movements (low frequency, high amplitude): a few clonic movements are commonly observed during elicitation of the Moro response in newborn infants. They also are frequent with spontaneous motor activity during the first hours of life. Considered present if very marked and sustained. 15

Other abnormal movements: incessant chewing movements; abnormal movements of the arms, the infant often extending the elbows with pronation at the wrist. Dyskinetic Movements of the Limbs.--This is more Stiffening than movement and can be defined as transitory contraction of a group of muscles, occurring spontaneously or provoked by examinati0n, and lasting for a few seconds (extension and pronation in u p p e r limb, extension of the lower limb, including the

foot).

AdductorsJAngle.~With the infant lying supine, both legs are extended and gently pulled laterally as far as possible. The angle formed by the two legs is the adductors angle. Evaluate the angle and compare with the zone of normality for the age. Note if obvious a s ~ e t r y , more limited fight or more limited left. NOTE: for all the passive tone-maneuvers described, maintain the head carefully in the midposition to avoid errors linked with the asymmetric tonic neck reflex. Heel-to-Ear.--With the infant lying flat, lift the legs as far as possible in am attempt to reach the ear with the feet. Observe the amplitude Of t h e a r c traversed by the legs, taking care not to lift the pelws from the table. An asymmetry may be detected if there is more resistance felt on one side than the other. Here, the examiner should be Sure that the pressure he applies is equal on both sides. Estimate the angle and compare with the normal zone for the age: It is important to bear in mind that when flexor tone is very strong, the popliteal angle is not completely o p e n d u r i n g this maneuver. The angle to b~ measured is not the one formed between the table and the thigh, b u t rather the one formed bet~veen the table and the infant's heels. 9

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PopliteaI Angle.--Maintaining the pelvis flat on the table, flex t h e t h l g h at the hip to achieve a knee-chest position. Holding the thigh in the knee-chest position, lift the lower segment of the leg and observe the angle formed with the thigh, which is the popliteal angle. Estimate the angle and compare with the normal zone for the age. An asymmetry is easier to detect than with the heelto-ear maneuver. Seemingly small differences of 10-20 degrees are quite significant. NOTE: in the preceding threemaneuvers, if a surprising hypotenia is observed in the lower limbs in the first months of life, check if compl_ete breech was the type of delivery. If so, don't take this hypotonia into account if it is an isolated abnormality. Dorsiflexion Angle of the Foot.raThe foot is dorsifle=ed on the leg, pressure being applied by t h e examiner's thumb on the sole of the foot, the other fingers maintaining the leg and the heel. The 16

angle formed by the dorsum of the foot and the anterior aspect of the leg is the dorsiflexion angle. This movement should be carfled out twice, first slowly and then quickly; the rapid movemeht elicits the stretch reflex with the angle formed. T h e result is abnormal if asymmetric and if there is more than a 10-degree difference between the slow and rapid movements, which indicates an abnormally strong stretch reflex. NOTE: 1. In the neonatal period, the angle itself depends on the gestati0nal age at the time of birth and ranges from 50 to 60 degrees in very premature newborns to nearly zero in full-term newborns. 2. This measurement, s h o u l d b e made with the leggin extension at the knees, testing the whole triceps surae muscle..If tested in flexion at t h e knee, the gast.rocnemius muscles are excluded and only the extensibility in t h e soleus muscle is tested.

Scar[ Sign.--Scarf sign means that the arm encircles the neck like a scarf. Sustain the infant in a semireclining position using the palm of the hand as a support; then take the infant's hand and try to pull the a r m across his Chest toward the opposite shoulder, continuing as far posteriorly as possible. Observe t h e position assumed by the elbow in relationto t h e umbilicus. Three positions are described; it is a rough evaluation: (1) elbow does not reach midline; (2) elbow passes mldline; (3) very ample movement, the arm encircles the neck. NOTE: the next five items will be tested only if asymmetry has been observed in the maneuvers just described. Flapping of the Foot.--The foot is flapped at the ankle and the amplitude of the m o v e m e n t imparted is noted. An inequality of response between the two feet is the only find!ng to look for, as a confirmation when a hemisyndrome is suspected. Square Window.--The hand is flexed on t h e forearm, as much as possible.: The angle formed b e t w e e n the palm and ventral aspect of the forearm is measured. An inequality of angle between the two sides is the only finding to look for. Flapping of the Hand.--The hand is flapped at the wrist and the amplitude of the movement imparted is noted. Note any striking asymmetry. Lateral Rotation o! the Head.--Turn the head toward each shoulder, evaluating the resistance of t h e C0ntralateral muscles. The amplitude of the movement is roughly symmetrical. Note any striking asymmetry. Repeated Ventral Flexion of the Head.--After flexlngthe neck several times, the resistance felt by the examiner normally remains about the same. "Results are considered abnormal if the 17

resistance increases with repetition, in which/case it usually reaches a maximal level after four or five trials and the head remains in hyperextension (Fig 5).

Ventral Flexion of the Trunk.--Grasp the flexed legs and pelvis and push them toward the head, achieving an incurvation of the trunk, Normally, t h e range of passive flexion of the trunk is g r e a t e r than extension..However, the amplitude is frequently limited because, of the volume of t h e abdomen. The response is recorded as exaggerated if the amplitude Of the movement allows the knees to be brought very Close :to the chin and impossible if no flexion at all is achieved. Extension of t]~e Trunk.--With the baby on his side, one hand maintains the lumbar spine and the other pulls both legs backwards. T h e amplitude of this movement is normally Very limited (close to zero). The response is noted as exaggerated if a real dorsal curve is achieved and if ~ncurvation is greater than t h a t produced in flexion. Lateral Flexion of the Trunk.--This is tested only if an asymmetry bet~veen right and left has been detected. With the i n f a n t lying supine, his right flank is maintained by one hand. His legs are then pulled to the right as far as possible, in an attempt to achieve an incurvation of the trunk. This is repeated on the left Fig 5.--Repeated ventral flexion of the head. When there is abnormal hypertonia in neck extensors the resistance increases with repetitive movement.

18

Fig 6.--Permanent hypertonia in neck extensors. Permanent hypertonia of neck extensors maintains the hyperextension of the head.

side. This movement, depending on the: tonicity of contralateral muscles, normally is limited. The response is noted as exaggerated, if a real incurvation is achieved or as asymmetric if so.

Straightening with Neck Flexors.--With the infant lying supine, grasp the shoulders a n d p u l l him slowly to the sitting position, observing the position of the head in relation to the:trunk. Before the full vertical position is reached, the flexor muscles are s t i m u l a t e d t o raise-the head. By full term~ the exten~6r a n d flexor tone are nearly balanced and the head will be maintained momentarily in the axis of the trunk. The result is considered abnormal if: (1) the head, pendulous at first, is pulled passively, passes the vertical midline and i m mediately drops forward, or is difficult to elicit, is brisk, o r is impossible to repeat; (2) permanent hypertonia of neck extensors maintains the head backward (Fig 6); however, a powerful contraction is see'r/in flexor muscles. The predominance of extensors often keeps the head from falling downward with gravity a t the end of the maneuver (see Fig 3). When eliciting the reaction, the observer must be sitting down, in order to face the child. If he is standing up and the child 19

Fig 7.--Pitfall in head control observation. With the observer standing, apparent hyperextension of the neck is due to the child's attention to the examiner.

becomes very interested in the observer's face, misinterpretation may result (Fig 7). Neck Extensors.--With the infantsitting and leaning forward, and the head hanging dowr, on the chest, while holding the shoulders move the trunk slowly backward and observethe react i o n of the head.:Bef0re the vertical p6siti0n i s reached , the extensor muscles are stimulated t o raise the head. T h e result is abnormal if: ( I ) ' t h e head, pendulou~ a t first, is pulled passively, passes the vertical midline a n d drops backward, Or the response is difficult to elicit, is brisk, or is notrepro-ducibl~; (2)" the head, unable to hang on the chest.a.t the beginning of the movement, is maintained strongly by the extensors and passes backward too quickly in such a way t h a t the reaction appears "too go~d" (see Fig 3). Head Erect and Steady.--Observe if the child, maintained in the sitting posit~ion holds his head.erect and steady for at least 15 seconds. This is bbserved at the same timeas the straightening reactionswith flexors and extensors, and is indicated b y a n arrow above the month during which it first occurs. If permanent hypertonia in neck extensors is still present by the third or fourth month, .the head .may be held steady for a long time but not in a normal position in the axis of the trunk: 20

In this instance, the constantly predominating extensors are maintaining the head backward, which the infant often corrects by keeping the trunk leaning slightly forward. Pulls to Sitting Position.--With the child lying on his back, the observer offers his thumbs and allows the infant to pull himself to a sitting position. Present when t h e infant actively :~chieves the sitting position. Sits Alone.--Place the child in a sitting position on the table, with his legs in semiflexion and spread at an angle of about 50 ,legrees. Observe if the child sits momentarily or for 30 seconds or more without support. Two different responses may be observed in cases in which the sitting position cannot be maintained even momentarily. 1. Axis is completely hypotonic, leaning forward on the knees. This usuallyoCCurs when global hypotonia is present. 2. Axis is very rigid, falling l~ackv~ard (Fig 8), This usually occurs when passive tone in the lower limbs remains abnormally strong. This situation makes it impossible for the child to open his legs because of the limitation of abduction, the knees remain high because of the limitation of popliteal and heel-to-ear angles. To suppress this difficulty, it is helpful to t e s t the sitting position at the edge of the examination table. Then, if the active tone f~f the axis is satisfactory, the sitting position is present. If not, the axis keeps falling backward. Global Straightening.--In the newborn period, stand the child up with the examiner's hand in his axillae while supporting his rhest anteriorly. Head and neck are supported during this maneuver by examiner'shand. First, observe tl~e:straightening reaction of the legs.Then ob.~erv6 that t.he-trunk muscles contract and t h a t the infant,supports some of his ownweigh t. For an older infant, support:the trunk with b o t h hands and judge if there is a positive Supp0rting reaction, with or .without crossing of the:legs. A: specialpattern may be observed around 7 to 8 months, with a rapid succession of flexion arid extension, as if the child would be ready to jump. Fig 8.~Beg!nning of sitting, position: A, normal pattern around 5 months. B, =-bnormal p'attern with the trunk falling backward.

21

Automatic Walking.--The infant is held b y the trunk as above, and tilted slightly forward. Automatic walking is produced on contact of the feet With a solid surface. The reactionis considered present if a few steps occur. Compare with developmental scale. Palmar Grasp.--The examiner's index fingers are inserted into the hands of the infant from the ulnar side and pressed gently against the palmar surface. Palmar stimulation produces a flexion of the fingers onto the stimulating object. Note if response is pre'sent and compare with developmental scale. Response to Traction.--When palmar grasp is achieved, if the infant's hands are drawn flexor muscles of the arm, the bed. This response to Note if response is present

upward, the response spreads to the so ttiat the infant can be lifted from traction is dependent on active tone. and compare with development scale.

Moro Reflex.--The infant is lifted a few centimeters off the bed by holding both hands and is released suddenly. Observe first abduction of the arms at the shoulder and extension of the forearms at the elbow. Then, adduction of the arms a t the shoulder (embrace~ and flexion of the forearms at the elbow. Complete opening of the hands occurs during the first part. Crying is consistently provoked. An extension may be observed in lower limbs, b u t n o t c o n s t a n t ! y . The complete response includes abduction of the arms, opening of the hands and crying. An incomplete response (often "observed before disappearance of the reflex) associates crying and opening of t h e hands. Note if complete, incomplete, absent, asymmetric o r w i t h very low threshold. Bfirsts of clonic movements usually are observed when there is a very low threshold. AsymmetricTonic Neck Reflex (Evoked).--Brisk passive rotation of the head causes a modification of tone'in the limbs. The child is tested in the dorsal decubitus position. The arm and leg on the side toward which the head is turned become extended, the arm and leg on the other side become more flexed. A full extension of the limbs is rarely seen. T h e reaction is more visible in upper limbs. TO be considered present, the reaction is a rapid and clear-cut change of limb position, easy to elicit several times in a row. Biceps Reflex.--With the infant in the supine position, the elbow is held in a semiflexed position. T h e examiner places his index finger on the biceps tendon, holding the forearm with the thumb and other fingers and taps his index finger with the opposite index finger or third finger. The response is a contraction of the biceps muscle with flexion of the forearm on the arm. The 22

result may be absent or it may be exaggerated (abrupt contraction of large amplitude).

Ankle CIonus.--With the lower limb flexed at the hip and knee, a rapid but gentle dorsiflexion of the ankle is achieved (should be done with limb relaxed and the infant quiet). Ankle clonus consists of a series of rhythmic alternate flexions and extensions of the foot at the ankle. Persistent clonus over 10 is abnormal. Knee-Jerk.-,With the infant in the supine position, the knee is held in a semiflexed position. The reflex is elicited with the index finger Or third finger; a sharp blow on the patella[.tendon is followed by a contraction of the muscle. The response may be absent or exaggerated (abrupt contraction of large amplitude). Landau Reflex.--When the child is held in ventral suspension , the head, spine, and legs extend. If the examiner flexes the head passiyely, the whole body will flex. The reaction is considered present when both components are elicited: first, spontaneous extension, then provoked flexion. Lateral Propping Reaction.--When the child in the sitting 13osition is pushed to one side, the arms extend to the appropriate position as if to protect him from falling. This response cannot be elicited before a stable sitting position is achieved. The result is deafly asymmetric .if there is spastic hemiplegia. Parachute Reaction.--The reflex is elicited by holding the child in ventral suspension and making a sudden flinging motion down toward the examination table. The arms extend as if to protect him from falling. The response is deafly asymmetric if there is spastic hemiplegia. NOTE: postural reaction such as lateral propping and parachute normally are perfect and reproducible at 8 and 9 months, iespectively, although they m a y be observed earlier in many infafits. Thus their absence is interpreted as abfi0rmal only after S or 9 months.

INTERPRETATION NORMAL EVOLUTION. DURING THE FIRST YEAR AND THE ~IOST COMMON PATTERNS OF ABNORMALITIES

Rough guidelines are necessary to interpret the results Of the aeurologic examination according to the age of the child (corrected age for prematures), The main difficulty in making up the form has been the definition of what is normal tone at a given age and to set limits that are wide enough to avoid false impressions of abnormality. All 23

the measurements proposed are angle me.asurements and normal limits have been defined rather widely-for each developmental stage. In longitudinal studies, Stamback and Ajuriaguerra44 have shown a large variability in the pattern of evolution of tone during the first two years. Some infants reach the maximum of extensibil.ity between 7 and 10 months, others bet~veen 15 and 18 months only. The authors also demonstrated that these large individual differences do not modify the age at which the sitting position is acquired. However, it 'modifies the age at which the standing position is acquired, the function being delayed in the children who demonstrated an early maximum hyperextensibility. The same remark on wide individual variations is true for spontaneous motor activity. For both tone and activity, individual or familial differences have to be taken into account , and consequently thezone of normality has to be wide enough. The range of normality with the Specific techniques proposed here has not been standardized as yet; however, these figures are generally accepted to define the approximate border of normal development during the first year. Some particular cases will be discussed later on. The normal development is summarized here, and the most common patterns of abnormalities described for each trimester. Severe brain damage such as hydrocephaly, microcephaly, hypotonia and tetraplegia may be suspected or confirmed at any stage.

First Trimester.--Normally, during the first trimester, the hypertonia in t h e four limb flexors remains about the same; the opening of the hands, which is the first step in the preparation for prehension, becomes permanent. Much better active tone allows motor acqu!sitions such as head control. Most of the primary reactions cannot be elicited at 3 months. The asymmetric tonic neck reflex, grasping, and automatic walking disappear di/iring the second or third month; t h e Moro response is often elicited later but is weak and incomplete. (However, the time of disappearance of these reflexes is so variable that no conclusion can be drawn about their persistence until at least 4 months of age.) As there is a wide range of normality, usually no firm conclusion can be drawn from neurologic evaluation until the fourth month. Developmental scales based on behavior and sociability are a better index at this stage. The most common pattern of abnormality is the association of hypertonia of neck extensors and hyperexcitability (manifested mostly by insufficient sleep and tremulati0ns). Another common pattern is hypotonia, hyperactivity and lethargy. Second trimester.--Normally, passive tone decreases dramatically during the second trimester. This evolution already has 24

Fig 9.--Sitting position at 5 months. The legs are extended and in abduction; _~!'.'.ing position is maintained for a few seconds with the help of the arms with a ~;;,ward inclination of the trunk.

begun during the third month in the upper limbs and later reaches the lower limbs, which now lie in extension at rest and ~lre capable of much more abduction. Conversly, the active tone increases regularly in the n e c k .and trunk, allowing very important postural acquisitions. It is no longer possible to elicit primary reflexes. Beginning of sitting position al~pears at this Stage, and global straightening in standing position is no longer possible (Figs 9 arid 10). During the second trimester, abnormalities may be observed in a very characteristic pattern in the10wer limbs, hypertonia persists in flexor muscles, all the-anglesremaihing almost unt'hanged. Head control and ability to sit, the two important postural acquisitions depending on active tone in neck and trunk, are delayed. Hypertonia in the flexor muscles of the legs increases the difficulty in sitting; the child is n o t able to lean forward on his .'emiopen legs; because of the very limited popliteal angle, the knees remain very high and the t r u n k tends to fall backward (see Fig 8). At the same time, global straightening in the standing position is still very strong. Therefore, a very abnormal pattern is realized: a 5- or 6-month old child is ableto stand and not to sit. Frequently, primary reflexes are still easy to elicit. Irritability 25

Fig 10.--Slanding posilion at 5 months. Global straightening has disappeared, the upright position is no longer possible.

is striking, with poor sleep, tremor, or bursts of clonic m o v e ments; the psychological acquisitions are delayed as well. However, during this second trimester there is no reliable way to separate the patients whose signs will regress from those who will have a fully developed spastic diplegia a few months later. I t is during this second trimester, too, that spastic heraiplegia usually is diagnosed, e v e n though it is of perinatal origin. In these cases, frank symptoms become striking between 4 and 6 months, at first in the upper limb: poor voluntary motility, no prehension, hypertonia, exaggeration Of biceps reflex. The s a m e sort of signs appear a little later in the lower limb. Why is there often a silent period during the first trimester? In some cases 26

possibly because the comparative measurements of passive tone have not been done carefully enough. In some cases, a hemisyndromc was documented, b u t it is the hyperLonlc side which progressively appears as the abnormal one, when hyperrettexia and poor prehension become obvious. (However, the evolution of most of the hemisyndromes observed at the neonatal period is toward a slow diminution of this isolated asymmetry in passive tone and is without known significance.) But it seems probable, too, that the clinical signs of spastic hemiplegia begin to appear x~th a given stage of development first in the upper limb then in the lower limb. As with many other developmental neurologic abnormalities, there remains a latent period between cerebral insult and clinical expression.

Third Trimester.mNormally, development continues in the same manner, with progressively decreasing flexor tone and increasing extensor tone, preparing for upright posture. Equilibration reactions appear, as well as important mental and visual acquisitions. It is only during the tbSrd trimester that two groups wiU be separated clearly. In one group, all abnormalities observed d u r i n g the first two trimesters will disappear abruptly. Those infants for whom the diagnosis of spastic diplegia was considered as possible between 5 and 8 9 are catching u p i n a very spectacular way around ,~ months: the flexor tone in the lower limbs decreases rapidly to normal, and sitting.position is acquired; at the same time, signs of irritability disappear rapidly,, and mental acquisitions are seen. Therefore, it is only around 9 months that this syndrome earlbe designated as transitory. At. the end of t h e first year, no distinction is possible between the group 0f children who have been normal all along and the so-called transient.groups. This group s h o u l d b e f611owedcarefully in the-ensuing years to pick~ut other expressions of minimal brail~ damage, including febrile seizures. This transitory s y n d r o m e i s much more frequent than definitive spastic diplegia. Spastic hemiplegia may also disappear almost completely at this stage. Mild or transitory cases are more frequently seen now than definitive cases. In the other group, the diagnosis of clear-cut cerebral palsy will be confirmed. Spastic diplegia occurs nearly exclusively in prematures. I t is a spastic paraplegia, with upper limbs either normal or, more often, with some awkwardness and athetold movements, and hypotonia of the neck and trunk. Thus.spasti: city develops its full expression with increasing extensor tone during the third trimester and, a.t least in mild cases, cannot be diagnosed with certainty before this time. 27

Fourth Trimester.--Normally, as development goes on, standing position is achieved, the child is ready o r nearly ready to walk. Fine prehension is acquired. It is usually only at this stage that the abnormal posture and movements of athetosis and chorea become apparent in a previously hypotonic child with delayed acquisitions. ORDER OF IMPORTANCE AND GROUPING OF ANOMALIES: PROVISIONAL SYI~ITHESIS AT END OF FIRST YEAR

At the moment, a" classification based on the most typical patterns according to each stage of development is advisable as a provisional synthesis for each child. This classification does not take into account isolated anomalies of uncertain significance. At the end of the first year, the infants of an intensive care unit will be classified as follows: 1. Normal child at all successive stages of development during the first year. 2. Transitory anomalies, with normalization at the end of the first year: (a) First trimester: irritability, global hypertonia or hypertenia In neck extensors; lethargy, global hypotonia. Normalization is observed around 3 months. (b) Second and third trimesters: irritability, persisting flexor tone in lower limbs, poor active tone in neck and trunk, hyperreflexivity. Normalization is observed around 9 months, or there may be transitory spastic hemiplegia. 3. Signs o[ definitive brain damage, severe brain damage such as hydrocephaly, microcephaly, hypotonia, tetraplegia, or seizure disorder may be suspected or confirmed at any stage. Spastic hemiplegia or diplegia are diagnosed by 9 months. Severe global hyp0tonia might be classified as specific neurologic or muscular disorders, during the first y e a r of life. It is not possible now, and probably w i l l n o t be possible even after standardization, to take into account scaitere~d ~n0malies of tone. An anomaly found only at one examination probablY will have to be interpreted as an incorrect maneuver. An isolated anomaly found at several successive examinations may be interpreted as Subnormal or atypical development but not as a pathologic pattern. It is important to.consider the normal range as a rough guideline; tone evolution is a continuous process which, for didactic reasons, has been indicated in a discontinuous way for each 3month period. The longitudinal pattern obtained b y m o n t h l y examination is more important for interpretation than scattered anomalies. For all these reasons and because the component items have very different values, I consider unwise any attempt to derive a score. 28

COMPARISON OF D A T A OBTAINED ]BY NEUROLOGIC EVALUATION AND D A T A OBTAINED BY DEVELOPI~IENTAL SCALES

This type of correlation has to be studied carefully in the coming years. M o s t commonly in cases with transitory abnormalities, the same p a t t e r n is observed by psychological examination with abnormalities until 9 months a n d then a very rapid catching up. There is occasionally:a complete discrepancy between the two types of data: e.g., t h e child who does n o t have any tone or reflex abnormalities t h r o u g h a u t the first year; however, he h a s poor developmental acquisitions, and the development~l~tuotient is rather low at 1 year of age. Thus, t h e psychological data add a fourth group to the above classification, with children normal on neurologic grounds b u t not on psychological grounds. INTERPRETATION OF DATA ACCORDING TO THE PROBABLE

RESPONSIBILITY FOR THE I~ERINATALINSULT Isolated anomalies raise questions which cannot be solved by clinical examination alone. Standardization is needed but will not solve the problem because of the very wide range of normalcy in tone evolution, in disappearance of primary reflexesand in appearance of postural reactions. Keeping in mind the aim of this type of evaluation within the first year, the main concern of perinatalogists is to separateas much as possible signs resulting from per]natal insults from those resulting from other causes. One example, demonstrative and fairly common, is represented by global hypotenia. CASE l.--Elsa B. was the 4,050-gin full-term product of a nol'mal pregnancy and difficult midforceps delivery. She had several neurologie abnormalities during the first week of life, including abnormal cry with cyanosis, hypertonia of theextensor muscles of the neck and global hypotonia; By the end of the first week all abnormaiitie-s,-exceldthypotonia, had disappeared. She remained normal in all other respects, but the hypotouia persisted. Head control was acquired at 4 months. At 6 months passive tone was still in the abnormal range: abductors, 160 degrees; heel-to-ear, 140 degrees; pop: liteal, 180 degrees; scarf sign, position 3, exaggerated dorsal and ventral extension of the trunk. Questioning of the mother about the family revealed that one maternal uncle, 60 years of age, was still able to put his feet behind h~s neck. Thus separating normal and. abnormal and computing results, the child will be in the abnormal group, w i t h global hypotonia. But separating perinatal insult from other causes, one might assume t h a t this child belongs in the " o t h e r " groups, a s her 29

s y m p t o m s are m o r e likely familial t h a n related to h e r mild perinatal obstetric t r a u m a . A n o t h e r example will d e m o n s t r a t e t h a t s i m p l y falling in the range of n o r m a l c y for passive t o n e m e a s u r e m e n t s is sometimes n o t enough, considering t h e l o n g i t u d i n a l p a t t e r n a t the e n d of the first year. CAS~. 2.--David P. was the second twin born at 38 weeks' gestation to a primigravida mother. Birth weightwas 2,470 gin; length,o44 cm; head circumfei'ence, 35.5 era. Delivery was breech but without difficulty. Apgar scores, 8 at 1 minute and 10 at 5 minutes. Two weeks before delivery the mother had fallen down a flight of stairs onto her abdomen. At birth, the infant had signs of a right subdural hemorrhage with an asymmetric, bulging fontanelle, widely separated sutures, (old) retinal hemorrhage and hypertonia of the neck extensors. However, his state of consciousness was normal and he sucked well; reflexes were normal. A bilateral subdural puncture was performed and 35 ml Of serosanguinous fluid was removed from the right side. There was no fluid on the left and the following day there was no reaccumulation on the right. The child did well but some abnormal neurologic signs persisted. At 7 months, although passive tone was normal, there were dystonic attacks, exaggerated spontaneous motor activity, poor active tone in the trunk and opisthotonic posturing. Postural acquisitions were still delayed during the eighth month, with sitting position at the 5-month stage of leaning forward. At the latest examination, at 10 months of age, the child is fairly normal in regard to passive tone, sitting and standing positions and postural reflexes (Fig 11). R e c o n s i d e r i n g passive tone items, there a r e s o m e striking facts: 1. T h e p a t t e r n of evolution t o w a r d h y p o t o n i a in the lower limbs was n o t a s m o o t h One b u t t h e r e was an a b r u p t c h a n g e between 8 a n d 10 m o n t h s . 2. For the f i r s t 8 m o n t h s , t h e angles were q u i t e different f r o m t h o s e observed in the o t h e r twin, a perfectly n o r m a l girl~ b u t s u d d e n l y c a m e within the same r a n g e as t h a t of the sister between 8 a n d 10 m o n t h s ~ T h e n , for each m a n e u v e r , a l t h o u g h the resulting angle a l w a y s Fig 11.--Case 2, David P. Pattern of evolution toward hypotonia in lower limbs. Angles are in normal limits, but an abrupt change is observed between 8 and 10 months. Age, in months, is given at the bottom of each column. ADDUCTOR

100 I 0 0

110 13C

150

}tEEL TO EAR

100 100

110 110

140

100 100

10 120

170

"t'~OPLIT~'AL 1

30

2

3

4

5

5

7

8

9

10

iI

127

may have been within normal values for a given month, the patiern of evolution of passive tone at the end of the year was not a smooth and regular one: a relative hypertonia in lower limbs abruptly vanished around 9 months. Other anomalies present in tl~e second and third trimester disappeared at the same time; a t l0 months the child was very comparable to the other t w i n . He has to be classified in the group of transitory anomalies, even for passive tone in lower limbs. This case is of particular interest because of the precisely known etiology, prenatal trauma having been responsible for subdural hemorrhage , with an important blood loss and ifltracranial hypertension, both repaired 2 weeks later, just after birth. In concluding, at each Step of a follow-up study, the exact aim has to be kept in mind. In a "kinesiologic approach," both'cases must be treated. Separating "normal" passive .tone from "abnormal" passive tone in the lower limbs, case 1 is abnormal , case 2 is normal. Trying to evaluate the etiology, case I is a case of familial benign hypotonia, case 2 is a case of brain damage of traumatic origin. INTEROBSERVER ~ELIABILITY

Clinical objectivity is difficult to maintain. One is easi]y..influenced by the obstetric history and by the findings of the last preceding examination. Being aware of that, it is possible to a k~rge extent to decrease these two factors of subjectivity. First, it is advisable not to l o o k a t the neonatal chart before the neuro-i lo~c evaluation. Second, it is advisable not to look at the results of previous evaluations. In any case, it is more convenient to have an aide write the results on the form, which prevents influence of the preceding findings on the examiner. As far hs.quantification is concerned, there certainly are several imanswered questions. T h e evaluation of primary reflexes o r 0ostural reactions is the easiest part of t h e examination. Appre-. clarion 0f'acti~e--tb-ne-in the first months of life is the most difficult part, both for elicitation of response in the neck muscles and for the appreciation of the response itself, normal or abnormal. This is acquired by experience. Regarding passive tone, angle measurements carry with them an apparent accuracy but in fact remain an estimate. The range of normalcy being very wide, a slight variation from one to another observer is acceptable; what is more important is to elicit the pattern of evolution of tone for a give~ child. I have tried to evaluate interobserver reliability, indepefidently examining 30 infants with two observers. The correlations are ,'xcellent for scarf sign, dorsiflexion angle of the foot and popliteal angle, b u t poorer for heel-to-ear and adductor angle (Figs 12 31

SCARF SIGN A

27

DORSIFLEXION ANGLE OF THE FOOT

B

II 8

5 I

_1

/-+/y,'/

~ ,

907o POPLITEAL ANGLE C

~

80% HEEL TO EAR D

IO

7

5

3 "

I '

o

12

3

'/

I o

~.

o

o

5

'/3% I

A-%)

I

~1 66%

Fig 12.--Passive ton~: interobserver reliability. Thirty infants were tested independently by two observers. The correlations are acceptable for scarf sign (A), dorsiflexion angle of the foot'(B) and popliteal angle (C), but are poorer for heel-to-ear angle (D).

and 13, A}. To separate t h e m a n e u v e r i t s e l f from evaluation'of angle, we repeated the s t u d y with a single examiner and several members of the staff evaluating the angle, in this way, the possible variation of strength exerted b y different observers in doing the maneuver is eliminated and only the angle evaluation is tested. The correlations are much better, especially for the adductor 32

AADDUCTORANGLE

ADDUCTOR ANGLE

B (one performer) 2O \\\-, x~xx xxxx x~xx

,x,\-~ xxxx

6 5 ~

6 5 9

# I~

50%

j o

84

6

li

Cb (b ,

90% Fig 13.--Adductor angle: interobserver reliability. A, thirty infants were tested ~dependently by two observers; the correlation is poor. B, there was only one :.~ster but several observers. Only the angle evaluation was tested and the cor~-Iation is much better.

'angle (see Fig 13, B) showing.clearly that the difficulty is in the maneuver itself and not in the evaluation of the angle. As a result I feel it is unnecessary to use a protractor or other measuring device.These studies have been performed in m y outpatient clinic where high-risk infants are not specially selected but mixed with low-risk infants as" well. This is considered in m y group as very important for several reasons: from a teaching point of view, it is aecessary not to select handicapped children from normal ones hut to show at random what normal development is and whaiL is deviation from normal. From the mother's point of view, this absence of segregation of supposedly handicapped "children decreases her anxiety. She knows her child is being evaluated in a 9specialized department, but she also meets mothers of low-risk infants. The child is followed b.y the neonatal staff with_whom she was acquainted in the intensive, care unit and all medical problems are considered at the same time as the neurologic evaluation. Some of the mothers might become anxious-during the first visit by the filling out of the form. A trained examiner, however, is very able to speak with her while examining the child, and while somebody-else writes the resets. I n this way the mother relaxes rapidly and does not think any more about this 33

type of examination. In this fairly quiet atmosphere, our inter. observer reliability study has been perfectly well accepted. ACKNOWLEDGMENT I wish to acknowledge and t h a n k Diane Abuelo and Rowenl l{orob]{in for their expert corrections. The pictures are from Do, lo1' I{orobkin. The drawings are from Annette Tison.

34

NEUROLOGIC

EVALUATION

-

AMIEL-TISON

B.ECORD FOIl},[ F C ~ MONTHLY EXA},[L~ATIOH WITHIN THE F H I S T Y E A R

NAME

SEX

D A T E OF BIRTH GE STATIONAL A G E

[----7 V/BE KS

CCB.P.ECTION F A C T O ~ 40--G.A.- I [IATE AGE

CORBZCTED AGE

I WEEKS EXAMINATION NUMBER

TESTED B Y

35

IIEAD C I R C U M F E R E N C E

( see .growth eur~'es ) .I

2

3

4

5

6

7

8

9

I0

II

12

11

12

percen

ANTERIOR FONTANELLE Normal Tense Depressed

SUTURES lqormal Sep~.r~tvd O', erlapping

USUAL PATTE~'4 FOR WAKEFULNESS AND S L E E P " Normal Agitated, too much c r y i n g Lethargic, no c r y i n g

ESTIMATION OF ALERTNESS DURING TItE T E S T Satisfac~nry

Constantly agitated

b

Lethargic

CRY Normal High-pitched Weak Monotonous

I ;% I

O~herl

1

36

2

3

4

5

- 6

7

8

9

10

:~ CKD;G BEItAVIOUTi I

2

3

4

5

6

'I 9

8

9

lO

11

12

Norm~l

partl~ bottle-feeding No bottle-feedlng

|m

Choking 9~ N Y U L S I O N S D U R L ~ G ' H I E P R E C E D L N G M O N T t t

Absent Gener~ized }oc~d Febrile L-Jz~tilespasms - ~ ;'ERTONIA O F E L E V A T O R S

PALPEBRAE

SUPERIOIRI

9~ .rTL~G-SUH S I G N

Absent Present '.:.;~ RK~ D STRABISMUS Absent Present

[I I t I [ [~ l lilt [Ili liliIlil[

:STAL-NED N Y S T A G M U S Absent CPr esen t

]l.ll-]lJl11'll.t

','P.SUIT O F L I G H T

Present Absent

I I Jf~j I i I I.I J-ll -

~COUSTIC BLIIqKREFLEX Present Absent

[ 1] I:~ 1 13 141 -5

~ 6

7

8

9

10

'11

12

37

A S Y M M E T R I C TONIC IqECK P . . E F L E X ( P C ~ T U R A L ) Normal pattern

+

~'~l~r-a~-I-e--- : : : ~ s e n [ - ~ * - = - - - : - - - - i - ~ _ - ~

Present 1

2

I

II

11|11

"

3

4

~

"

5

6

7

8

~

" "

"

10

11

p E R M A N E N T HYPERTONICITY O F N E C K E X T E N S O R S

+P r e+s e n t

OpISTHOTON06 Absent Present

IttllIlllllIl llllIIllilt!J :

C O N S T A N T CLC~U'B.E OF T H E H A N D S Normal pattern

tolerabl~[-'~('--'-----:----=nC-~::-~=--:-no ! ........no-.,

Absent

{ T

Present Thumb across t h e

I m

Iy palm ASYM~KETRY O F P O S T U R E O F L I ~ 3 S

Abnormal limb

indicate :

FACIAL PARALYSIS

right

leit

~

Abseot

II

P*esent

I } I I I 11

111

II I l l

Ill

.111"1

I1

SPONTANEOUS MOTOR ACTIVITY.

|1

Low

.

. .

:W

|1

High

il

Asymmetric Abnormal limb

.".

indicate : 1

3B

-. "

H!

Medium = Normal

2

3

4

5

6

7 .

8

9

10

11

12

.~BNOP.MAL M O V E I ~ N T S

I

2

3

4

5

6

7

8

9

10

11

12

I

Absent L~ce s ~ n t t r e m o r

:

:

Civnir m o v e m e n t s (~.her

9~YSKKNETIC MOVEMENTS O F TIFF.. LI~U3S Absent PreSent AVnOrmal~mb

II

I I,lt Ill,l-Ill

~ DDUCTOI~ ANGLE 40~ to 80~

70~ to 110~

I00 ~ to 140~

130~ to 150r

Normal pattern

.~-,gle R ~. L t.iraited E.~ggerated ~,tore limited right M.Jre limited left

HEEL TO EAR

Normal pattern

[.Exaggerated

'Angle Left

Limited

l

[Exaggerated 2

3-

4

5

6

7

8

9

39

I)OPLITEALANGLE 80~

~ 90~

~

110~ to 160~ 150~

~

_Y

Norm~l p~.ftern

Angle Right ILirnlted LEx,'Lggerated 1"

2

3

4

5

6

7

B

9

10 11 12

I

t

angle Left ]Limited

.I

LExagger~ted

DOKSIFLEXION.~N'GLEOF THE FOOT Normal pattern

'

60~ 70o~

50~ 70~

60~ 70~

60~ 70~

I 'Angle (slow) Angle (rapid) Hight ..$1vw.,~.C~o 70o Di/ferenee L"rapid- s low"~l.0~ m

tangle (slow) |Angle (rapid) LefL I"S low""~60~ 700 IDilference -

J

L"rapid-slow"> I 0~

A~Y,fME~Y Rio~t,,e~t I'] I

40

] I ] I I,, I ] I,I 2

3

4

5

6

7

8

9

10

]7 11

12

~d?~RF SIGN

Normal pattern

Position rt~ght

[Limited LExaggerated .

Left

Position Limited

LEx~ggerated Y~LMETI'tY B i g h t / l e f t

III!

2

3

II4

5

l 6l t 7l [8 l l9

10

II

12

I

THE NEXT FOUR I T E ~ WILL BE TESTED ONLY IF ASYMMETRY HAS BEEN OD~c::FtVED BY TIlE MASOEUVRES DESCFt~ED ABOVE. ' APPI~G OF THE FOOT

M~

l

I

I

I

I

I

I

~t AP.E WINDOW

,~lo~mallo. righ~l I t I I i [ I I I I I i '~,e~,erle.|. 1 l I i I, I I I 1 I I LAPPING OF THE HAND

More.mplelo** k 1 I l

i I I

~.TERAL NOTATION OF TIFf. HEAD More limited

,

, ..... d~ri~h, I II I I III li It More limited ,o.~*d~,e~* I 1 I 2 I 3 I 4 I 5 I 6 ! 7 t 8 { 9 I 10 i 1! I 12 i

41

R E P E A T E D V E N T R A L FLEX]ON O F THE t[EAD

::::v~, ....

1

J ll 2

3

4

5

6

I III 7

8

9

10

11

II 12

VENTRAL FLEXION O F T HE TRUNK Normal

(slight)

Exaggerated Impossible

DORSAL EX'TENSION O F THE TRUNK

:::=:::~~

II I I I I

I~

LATERAL FLEX]ON OF THE TRUNK (tested only i.f an a s y m m e t r y R / L a l r e a d y detected) Normal

[

Exaggerated More limited t o w a r d s right More limited towards lelt

STRAIGIITENING WITIt NECK FLEXORS Normal No active m o v e m e n t tlypertonicitT of extensors

!

!

STRAIGIITENING WITIt NECK EXTENSORS Normal No active m o v e m e n t "'Too good" 1

~Indicate ~when

42

2

3

4

fi

6

7

head e r e c t a~d steady m o r e than 15 second~.

8

9

10

11

12

PULLS TO SITTLNG POSITION 1

Normal pattern

2

3

4

5

6

7

~sent ---j! ~,soo~

[r

8

9

10

11

12

It - present

~l

Absent 51T~ ALONE MOMENTARILY Normal pattern

[

"absent

][ inconstant]~

present

-}I

A

Absent ~|TS ALONE 30 SECONDS OR MORE Normal pattern ['.

absent

II inconstant 1~

present

]I

I .~]'RAIGHT~NI~G WITtt LOWER LI2,I.BS AND TRUNK (supporting reaction)

{'Labsent. ---i ilPossiblenot Present

~l~resens"l Normal pattern

inca~~st-!

~ustalned

Present Absent I.'~terp retation Crossing

AUTOMATIC WALKING Normal pa.ttern

P.resent~ 1

--absent......absent! st_

".]

Present Absent Interpretation 1

I2

3

4

5

6

7

8

9

10

11

12

43

10

PAL~tAR GRASP

~re- inconst- ._~-~absent--:--- absent ............... sent ant

Normal pattern Present Absent

Interpretation Asymmetry R/L I

RESPONSE

5

4

2

6

"/

8

9

10

11

12

TO TRACTION

l pre-linconst ..... absent ...... absent 2_

Normal pattern

I

sent I ant Present Absent Interpretation Asymmetry R/L

MORO

R E F L ~--X

~-i~e~en!~---~ in.... t-.._-..... absent-L~-.-ant

Normal pattern

absent ....

Complete Incomplete Absent Interpretation Asymmetry R/L Clonic torts. J, low thrcsh. Abnormal limb in the last 3 manoeuvres ASYM'METRIC

TONIC NECK

Normal pattern

REFLEX

~

left

( evoked )

'"~toI e i:a~ e . ~ [ E - ~ b s en~-:~ [ ~-~--.-~_.-~:-- - : - [ - -. ab se n t ---~L|

1

44

] right

[

2

3

4

5

6

7

8

9

l0

II

12

:CEPS R E F L E X

1

2

3

4

5

6

7

8

9

I0

11

12

Normal ' '.. c.~,t I Abscnt

[ Exaggerated

'.~h

Normal |Absent I LExaggerated

9, FY MM~ETRY R / L

I I I I III

! j ./.

}'11

".dLE CLONUS Absent Present

right

Present

left

; '-EE JERK

Normal !{..:h~ IAbsent [Exagge rated

'Normal ; t-'I

Absent LExaggerated

, :YMMETRy R/L

I I I 2I I3i 4

5

II 6

7

II8

9

I10 III

i..l 12

45

LANDAU REFLEX Normal p~tttern

1

2

3

4

5

6

7

8

9

11

10

--~se~t-- ~ t~%i-7~t'y_____Ir o~ --~I~-~ . . . ... . .

12

__

prbsen"~'Kf~--,

Present Absent

Interpretation

L A T E R A L PROPPLNG REACTION Normal pattern

9=: ~bse~t ------- absent L'..'2. inconSt-ant~

Present Absent

__i

:L" present?

I

Interpretation Asymmetry PARACHUTE Normal pattern

Present Absent

1

2

3

:-- abseht

~_

4

5

6

7

8

9

10

11

12

[ ~tbseni.'q:~_~--Ciinconst-%- pr-esenT'2 ant ,

.

L~terpretati0n Asymmetry Abnormal llmb in the last 2 manoeuvres

46

~bl

F'~

left

REFERENCES !.ilienfield, A. M., and Pasamanick, B.: T h e association of m a t e r n a l :rod fetal factors with the development of cerebral palsy and epilepsy, Am. J. Obstet. Gynecol. 70:93, 1955. Gr,~ham, F. K., Ernhard, C: B., Thurston, D., and Craft, M.: Development Three Years after Perinatal Anoxia and Other Potentially Dam,~12ing NezL,born Experiences, Psychol. Monogr. 76, whole 522, 1962. Prod'horn, L. S., Calame, A., and Steinhauer, J.: The Outcome of LowBirth Weight In[ants of Less than 1.500 g, in TILe Third European .~,[cetin~ of Perinatal Medicine (Bern: Hans Huber, 1973). llagberg, B., Hagberg, G., and Olow, I.: T h e changing panorama of rerebral palsy in Sweden 1954--1970, Acla Paediatr. Scand. 64:187, 1975. ,.)uterbridge, E. W., and Stern, L.: DevelopmentaI follow-up of artificially ventilated infants with neonatal respiratory failure (abstract), l)ediatr. Res. 6:412, 1972. .~tahlman, M., Hedwall, G., Dolanski, E., et al.: A six-year follow-up ~,( clinical hyaline membrane disease, Pediatr, Clin. N o r t h Am. 20:433, 1973. :'ukier, F., Amiel-Tison, C., and Minkowski, A.: I R D S infants treated 9,ith artificial ventilation: Neurological and intellectual sequellae at 2 to 5 years of age, Grit. Care Med. 2:265, 1974. .h)hnson, J. D., Malachowski, N. C., Grobstein, R., et at.: Prognosis of ..hildren surviving with the aid of mechanical ventilation in the new!,~,rn period, J. Pediatr. 84:272, 1974. [[arrod, J. R., L'Heureux, P., ~,Vangensteen, O. D., and Hunt, C. E.: l.,mg-term follow-up of severe respiratory distress syndrome treated with IPPB, J. Pediatr. 84:277, 1974. Visch, R. 0., Bilek, M. K., Miller, L. D., et al.: Physical and mental ~ta(us at 4 years of age of survivors of the respiratory distress syndrome, 9I. Pcdiatr. 86:497, 1975. 9l:mus.Kukusska, A., and Lis, S.: Developmental peculiarities of pre,mturely born children with birth weight below 1250 g, Dev. Med. ( "hiid Neurol. 8:285, 1966. l)rillien, C. M.: T h e incidence of mental and physical handicaps in -rhool age children of very low birth weight, Pediatrics B9:238, 1967. XlcDonald, A.: Children o[ Very Low Birth tVeighl, M.E.I.U. Research \fnnograph, no. 1,'Spastics Society (London: William Heinemann, l.qG7). tbiwlirigs, G., Reynolds, E. O. R., Stewart, A., et al.: Changing progrmsi.~ for infants of very low birth weight, Lancet 1:516, 1971. Wright, F. H., BIough, R. R., Chamberlin, A., el al.: A controlled followup study of small prematures born from 1952 through 1956, Am. J. Dis. r :hild. 124:506, 1972. l.ubchenco, L. O., Delivoria-Papadopoulos, M., Butterfield, L. J., et al.: Re.lationships of handicaps to nursery routines, J. Pediatr. 80:501, 1972. I.ubchehco, L. O., Delivoria-Papadopoulos, M., Butterfield, L., el al.: i.