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Update of the Amiel-Tison Neurologic

Assessment for the Term Neonate or at 40


Weeks Corrected Age
Claudine Amiel-Tison, MD

Amiel-Tison neurologic assessment at term has re- the follow-up clinic, not clinical findings. This failure is a
cently been updated for clinical application. Experi- shame, particularly at a time when clinical neurology in
ence in this field, in addition to a better understanding the neonate has such a promising future, as expressed by
of pathophysiologic characteristics of the immature Volpe, “Perhaps of greatest importance is the realization
brain, has taught us that an increased precision in that careful clinico-anatomic correlations are only begin-
assessing central nervous system function in the neo- ning to be made in neonatal neurology, especially since the
nate is compatible with a simplification of the clinical advent of high-resolution brain imaging techniques. Fur-
instrument. The complete procedure takes approxi- ther significant insight into the impact of cerebral injury
mately 5 minutes. A simple 0, 1, and 2 scoring system on the neonatal neurological examination is expected to be
is proposed. Because this coding system is not quanti- gained from such correlations” [1].
tative, any computation of quotient or total score is Because brain damage in the neonate is mainly located
inappropriate. Rather, a final synthesis based on clus- in cerebral hemispheres, the best predictive value should
ters of signs and symptoms is advisable. A distinct final be found in responses depending on the upper control
synthesis is proposed for term newborn infants in the system and not in responses depending mainly on brain-
first week of life and for preterm neonates at approx- stem activity. The cerebral maturation around term is such
imately 40 weeks of age corrected. Clinical profiles that the upper hemispheric structures can be clinically
emerging from repeated assessments in the term new- explored, within the first days of life in a term newborn or
born and early clinical findings indicating a brain at approximately 40 weeks corrected age in a premature
damage of prenatal origin are described. Interrater newborn.
reliability has been proved to be more than satisfac- The Amiel-Tison neurologic assessment at term is an
tory. Such an assessment is useful for any newborn attempt to answer this challenge by (1) substantially
infant in maternity wards or for any preterm infant increasing clinical accuracy in assessing central nervous
approximately 40 weeks of age, with or without abnor- system function in the neonate by using a simple scoring
mal imaging findings. © 2002 by Elsevier Science Inc. system; (2) focusing on the most meaningful items,
All rights reserved. eliminating those that appear redundant; (3) promoting a
clinical synthesis at term, for term and preterm infants, not
Amiel-Tison C. Update of the Amiel-Tison Neurological
defined as the sum of individual scores but as a gradation
assessment for the term neonate or at 40 weeks corrected
system based on clusters of signs and symptoms.
age. Pediatr Neurol 2002;27:196-212.

Trends in Clinical Methodology Since the Early


1960s
Introduction
The French Methodology: Conceptual Background
Examining neonatal intensive care unit discharge sum-
maries the clinicians’ devaluation is observed all over the Initial Description and Later Simplification. Largely
world. Abnormal ultrasound findings provide the key to influenced by his background in adult neurology, André-

From the Department of Pediatrics; Port-Royal; Paris V School of Communications should be addressed to:
Medicine; Paris, France. Dr. Amiel-Tison; Port-Royal-Baudelocque; 123 Bd de Port-Royal;
75679 Paris Cedex 14, France.
Received January 2, 2002; accepted April 30, 2002.

196 PEDIATRIC NEUROLOGY Vol. 27 No. 3 © 2002 by Elsevier Science Inc. All rights reserved.
PII S0887-8994(02)00436-8 ● 0887-8994/02/$—see front matter
Table 1. Incidence of central nervous system dysfunction of severe and moderate grades in term infants during an 18-year period (1973-
1990) in the Port-Royal-Baudelocque Maternity Hospital

Neurologic Signs and Symptoms*


Maternity Years Term Live Severe Moderate
Hospital Studied Births (n) n Per 1000 n Per 1000

Port-Royal [32] 1973-75 1785 2 1.1 17 9.5‡


Port-Royal [33] 1976-78 5825 5 0.9 8 1.4‡
Baudelocque† 1979-80 2880 2 0.7 —
Baudelocque [16] 1981-82 2364 0 0 1 0.4
1983-84 3170 2 0.6 2 0.6
Baudelocque [14] 1985-86 3883 1 0.3 3 0.8
1987-88 4232 1 0.2 4 0.9
1989-90 3913 3 0.7 5 1.3

* Gradation based on signs and symptoms observed within the first week of life (after exclusion of central nervous system malformations, genetic
factors, infection).

Unpublished data.

The difference between the values in the first two rows is statistically significant; P ⬍ 0.001.

Thomas in Paris [2] was fascinated by brainstem activity, severity is proposed at the end of the first week, with the
which is so conspicuous in the term newborn infant following three grades:
because of the immaturity of the upper control system at
1. Mild: abnormalities of tone and excitability but no
this stage of maturation. He defined passive and active
central nervous system depression and no seizure.
tone and considered tone changes to be valuable clinical
signs. As a young neonatalogist, I had the opportunity in 2. Moderate: abnormalities of tone with signs of central
the early 1960s to observe his disciple, Saint-Anne Dar- nervous system depression (poor interaction, hypoac-
gassies, assessing neonates in Port-Royal-Baudelocque tivity, hyporeflexia) and up to two isolated seizures.
Hospital in Paris. At the time, she was accumulating data 3. Severe: repeated seizures (lasting more than 30 min-
on the pattern of neurologic maturation from 28 to 40 utes) associated with overt central nervous system
weeks gestation [3]. Since then my goal has been to depression from lethargy to coma.
integrate neurologic assessment into daily practice, which
The only methodologic change to this gradation system
meant devising a simplified methodology.
use was introduced in early 1980s. The use of the bull’s
One significant step has been to reach a better under-
eye to test the fix-and-track function [8] has helped to
standing regarding what we are assessing clinically. Much
establish a more accurate limit between moderate grade
help concerning the construct validity of such an assess-
ment came from Sarnat [4] when he reviewed anatomic (cluster of signs indicating central nervous system depres-
and physiologic correlates of early neurologic develop- sion) and mild grade (cluster indicating no central nervous
ment. As a consequence of these clinicophysiologic cor- system depression) [9].
relates, the modifications proposed in the clinical assess- This three-level gradation system has been routinely
ment may be summarized as follows: more emphasis on used since that time in two referral maternity hospitals in
signs that depend on upper structures integrity, such as Paris to monitor safe obstetric management in term preg-
passive and active tone in the axis, alertness tested by nancies [10-15]. Certain trends have been observed over a
visual fixation and pursuit, and cranial signs linked to the period of 18 years. The incidence of newborns presenting
volume increase of cerebral hemispheres at the expense of moderate or severe cerebral dysfunction is presented in
signs depending on brainstem function, such as primary Table 1. The rate of severe grade was remarkably low and
reflexes and passive tone in limb flexor muscles. Then, stable with one per thousand or less. In moderate grade the
easy guidelines have been provided to understand matu- incidence has significantly decreased from 9.5/1000 in
rational steps in motor control from fetal life to infancy 1973-1975 to 1.4/1000 in 1976-1978 (P ⬍ 0.001), reach-
and to interpret signs and symptoms. Most pediatricians ing an almost similar incidence as that for severe grade.
were at last able to develop the self-confidence to practice This decrease could be explained by several changes in
a meaningful neurologic assessment [5,6] instead of con- these delivery rooms in the mid-1970s, which consists of
sidering this approach as exceedingly sophisticated, time- the constant in-house presence of a senior obstetrician,
consuming, and unreliable. systematic use of fetal heart rate monitoring, and the
Gradation Based on Clusters of Signs Observed in the presence of a pediatrician in the delivery room. This
Term Neonate. A gradation system based on a combina- gradation system has later been used in cases of cesarean
tion of individual signs and symptoms has been used in section to determine the morbidity rate [12,16].
our institution since 1969, describing three degrees of Scoring System for Individual Items. To attain more
central nervous system dysfunction [7]. An estimate of the precision with a wider repertoire of possible responses for

Amiel-Tison: Neurologic Assessment at Term 197


each item, a description of the severity of signs and value is even more consensually acknowledged in the
symptoms has been achieved and then transferred on a literature (i.e., a normal neurologic assessment around
three-point scale. After the first attempt described above term is reassuring).
other systems were devised, such as a research instrument
for birth asphyxia [17] and for the assessment of older Comparison of Data
infants [18,19]. The assessment presented here for term
and preterm infants around due dates is an attempt to Comparison of obstetric management between institu-
progress in a 0, 1, 2 scoring system that is simple enough tions or nations requires an agreement on the gradation
to be used in daily practice. Despite the alphanumeric system, as discussed by Levene [34]. Sarnat and Sarnat
character of the scale (0, 1, 2), any computation of quotient [35] were the first to devise a method that described the
or total score is inappropriate. One benefit of this scoring progression of symptoms in asphyxiated term infants.
system is to be in accordance with the assessment pro- Subsequently a number of methods based on the same
posed for follow-up in the first 6 years of life [19]. scheme has been described, including the method de-
scribed by Levene et al. [36].
Other Clinical Methods Differences are mainly caused by the requirement for
perfect alertness in mild grade or by accepting mild central
In the 1960s, André-Thomas was not the only pioneer in nervous system depression for the first 48 hours as
newborn neurology. Peiper in Leipzig, Germany, [20] and compatible with mild grade. Researchers agree that to
Prechtl in Groningen, The Netherlands [21] both devel- define the limit between optimal central nervous system
oped other types of assessments derived from their own function and mild degree of central nervous system dys-
scientific background—pediatrics for Peiper and ethology function is the only real difficulty. Moreover, in the early
for Prechtl. During the same time period, psychiatrists stages of extra-uterine adaptation, it is difficult to separate
were studying the behavior of neonates. Wolff, in North the transient effects of cardiorespiratory and metabolic
America, carefully studied visual pursuit and attention problems from the specific expression of brain damage.
[22], and, subsequently, the organization of sucking [23]. Repeated assessments provide the only good way of
Since then and with the impetus given by the work of resolving the difficulty posed by the fluctuation of the
Brazelton [24,25], behavioral observations became part of clinical signs soon after birth. The definition of moderate
the neurologic assessment. As analyzed by Scott [26], the and severe degree is similar in various systems, therefore
distinction between neonatal neurologic and behavioral allowing meaningful comparisons concerning obstetric
assessments appears unclear, and the content of the assess- care (see the discussion of comparison of their predictive
ment instruments overlaps to a great extent. In more recent value above).
years, technical apparatus for artificial ventilation and
monitoring of vital functions has made access to the Criteria for the Selection of the Appropriate Method
neonate in the acute stage even more difficult. These
circumstances explain the more recent emphasis given by Based on these facts, what are the criteria for choosing
Prechtl and followers to the observations of spontaneous one method or another? Different schemes of reference
movements [27-29]. have been proposed in various parts of the world and have
spread. Currently there is no consensus on the theoretical
Diversity in Approaches: Consensus on Predictive model for neonatal assessment. Purpose and feasibility
Validity remain the two essential criteria. The context of applica-
tion is also important to consider.
Levene et al. [30] analyzed the predictive validity of the In research, the choice depends mainly on the goal of
neonatal assessment for adverse outcome based on five the study. When looking for identification of brain dam-
different studies using the following grading systems: (1) age, for instance, one of the “mainly neurologic” methods
no infant with mild grade developed significant neurode- would be appropriate. When looking for early adaptive
velopmental handicap; (2) 15-27 % of infants with mod- skills, one of the “mainly behavioral” methods is more
erate grade had a poor outcome; (3) in four of the five appropriate. Because of the characteristics of each avail-
studies, 75% of infants with severe grade manifested a able test (purpose, format, standardization, type of scoring,
poor outcome. These results are in agreement with our time to administer), one test will be preferable to others.
own data that have been pooled from several personal In routine assessment, feasibility is essential, partly
follow-up studies and using the gradation system de- because of the time necessary to perform the assessment.
scribed above [7,31-33]. A poor outcome was observed in Certainly, rapidity is not a goal in itself, but it must be
20-30% of infants with moderate grade and in 50-70% of considered for practical and economic reasons. A basic
infants with severe grade. One can concur with Levene screening test based on optimal versus nonoptimal re-
[34] that, despite slight variations in defining the grades of sponses, administered in approximately 4 minutes has
encephalopathy, there is a remarkable consensus when been demonstrated to be satisfactory in maternity wards
predicting adverse outcome. A good negative predictive [6].

198 PEDIATRIC NEUROLOGY Vol. 27 No. 3


Personal preferences also have an influence. Some 0 ⫽ a typical result, within the normal range.
clinicians like to observe spontaneous activity without 1 ⫽ a moderately abnormal result.
interfering, which is the ethologic approach developed by 2 ⫽ a very abnormal result.
Prechtl. Others like to manipulate the newborn infant to
One usually is confident in assigning a score of 0 or a
establish a contact with his/her hands, to feel the tone at score of 2. However, there is sometimes uncertainty when
rest, and to evoke activity in a given situation, which is assigning a score of 1, the latter indicating an abnormal
more akin to the French approach. result of moderate degree.
For certain items, scoring is considered inappropriate,
and the examiner will circle an “X” to indicate examina-
Revised Version of the Amiel-Tison Neurologic tion results. No conclusions should be made regarding the
Assessment at Term normal or abnormal nature of results.
Data Recording. Page I of the form includes four
Scoring and Recording columns that allow for recordings of repeated assessments.
In fact, four assessments are generally enough to cover the
General Remarks. The record form presented here as
neonatal period, except in a few severe conditions. Data on
an Appendix is aimed to replace the form previously used
fetal growth and perinatal events are summarized on page
[10,12]. Because no new items have been added to
II of the form. The result for each item is recorded on
preceding descriptions, the technical definitions may be pages III-VI. The assessment covers cranial characteris-
found in various didactic texts [5,15,19,37]. tics, alertness, behavior and spontaneous activity, passive
Corrected age is used for children born before 37 weeks tone in limbs and axis, active tone, and primary reflexes.
gestation. To obtain corrected age, postnatal weeks are Imaging, electrophysiologic data, and any additional in-
added to weeks of gestation. For example, when a child formation are summarized on page VII.
born at 36 weeks gestation is assessed 4 weeks after birth,
his/her corrected age is 40 weeks (i.e., around due dates).
No specific order is required. The assessment usually Final Synthesis
proceeds from observation to manipulation. More activity
is demanded from the infant as the examination For the term newborn within the first week of life, the
progresses. When a poor response to a procedure is final synthesis is found on page VIII. When every item is
obtained, the procedure should be repeated and the best assigned a score of 0, it can be concluded that central
response taken as the right one. nervous system function is optimal. Most often one
A neurologic examination should ideally take place assessment on day 1 or 2 is enough. A second assessment
may be necessary within the first 48 hours if the alertness
when the infant is quiet but alert, spontaneously awake
does not appear perfect at the time of the first assessment,
after a 2-hour sleep after feeding. For one reason or
preventing any valid interpretation of the infant’s perfor-
another, however, it is usually impossible to choose such
mance.
a favorable time and a clinician is faced with stimulating
When a score of 1 or 2 is assigned to some items in the
a sleeping baby or quieting a disturbed one, hoping to
first days of life of a term newborn, the assessment will be
obtain a few minutes of quiet alertness.
repeated on the following days. The type of clustered
Finally, it is important to stress one common pitfall in
abnormalities observed within the first week of life is the
interpreting findings, as a result of deformations (in utero basis of the gradation change into mild, moderate, and
by restriction of space at the end of pregnancy or postna- severe, as mentioned above. Moreover the clinical profile
tally acquired in the neonatal intensive care unit). As an will be identified based on repeated examinations. Finally,
example, when preventive positioning has been neglected the presence or absence of morphologic signs that could
in sick and preterm infants, postural arching will often be indicate a prenatal origin when observed since birth should
present and wrongly interpreted as a severe neurologic be recorded.
sign [38]. Moreover, this acquired posture will not allow For the preterm infant around 40 weeks corrected, the
the passage forward of the head in the raise-to-sit maneu- final synthesis is found on page IX. The preterm infant
ver. After a few weeks of physical therapy, if posture and should be assessed as close as possible to 40 weeks. The
active responses are back to normal, this condition re- infant may be assessed in the post-intensive care unit,
quires a peripheral explanation. If it does not, brain ready or not for discharge, or asked to come to the
damage is very likely present. Therefore, correction of follow-up clinic if already at home at this age. In this case,
fetal deformations and prevention of postnatally acquired any time between 37 and 42 weeks may be acceptable
muscle shortening and deformations are important issues because of practical contingencies. The central nervous
to obtain accurate results when assessing central nervous system function may be judged optimal when every
system function. individual item is coded 0. When a score of 1 is assigned
Scoring system. The scoring system for each item is as on some or most of the items, an impairment of minor to
follows: moderate degree is considered. When some or most of the

Amiel-Tison: Neurologic Assessment at Term 199


Table 2. Distribution of 100 term neonates according to nonoptimal outcome, corroborated other studies. A recent
optimality or nonoptimality of central nervous system function at
birth (assessed separately by the pediatrician and by the midwife review of psychometric properties of nine standardized
[39]) neurologic assessments [40] indicated that stability of the
scores over the first weeks of life is generally poor. One
Pediatrician Midwife can agree with this review that the infant himself changes
Neurologic Final Final
assessment n Outcome n Outcome
rapidly so that variable results do not mean that the clinical
instrument is not reliable; it simply confirms the tradi-
Optimal findings 97 97 tional warning to young pediatricians: “Never trust a
First assessment 86 71 newborn!” The need for repeated assessments is well
Second assessment 11 26
Nonoptimal findings 3 3 recognized.

items are coded with 2, severe impairment should be Clinical Profiles and Etiologic Orientation
considered. Some difficulties in interpretation because of
extraneurologic problems are not rare in very low– birth- The following two statements are generally accepted in
weight infants and should be mentioned in the synthesis. neonatal neurology: (1) the nonspecific character of early
In the same line, in utero growth retardation and maternal neurologic signs whether the cause is related to a hypoxic-
diabetes may modify the initial pattern of maturation at ischemic event or to any other adverse factors, and; (2) the
birth and should be taken into account in the interpretation absence of free interval in cases of hypoxic-ischemic
of the infant’s performance. encephalopathy (i.e., signs are present from birth). When a
For any neonate with neurologic findings the most free interval is actually present, experience indicates that
probable etiology will be recorded on page X, as well as the etiology is to be found in a genetic disease or brain
the guidelines for the neurodevelopmental surveillance. malformation, not in hypoxic-ischemic encephalopathy
[41]. These two statements are used in any litigation to
Interrater Reliability accept or refute birth asphyxia as the possible cause of an
encephalopathy. Neurologic signs have to be present from
Between March and December 1998, a convenient birth, but they are not specific of birth asphyxia.
sample of 100 low-risk term newborn infants was tested at Identification of the clinical profile becomes essential
Port-Royal Maternity Hospital, Paris, France [39]. A for interpretation. When the profile is identified as dy-
double-blind design was used to test the interrater reliabil- namic (evolving), cranial signs of intracranial hyperten-
ity. One rater was the pediatrician in charge, and the other sion and autonomic nervous system disturbances are often
was a midwife in her last year of training. She previously present. This evolving profile is typical of a recent insult,
was taught the theoretical basis for this examination (3 most often occurring intrapartum. When central nervous
hours) and was then trained by technical demonstration system depression remains stable within the first weeks,
and personal practice under supervision (10 hours within a with nearly no variation in the clinical picture, the profile
2-week period). The mean duration for this assessment identified as static indicates that the insult occurred several
was approximately 4 minutes, ranging from 2 to 8 min- weeks or months earlier, the birth occurring after the phase
utes. At the time of this study, the three-level scoring of stabilization that took place in utero.
system was not yet available. Therefore, the dichotomous In such cases, when present from birth, morphologic
approach, optimal or nonoptimal, was used [6]. Reliability signs, such as a high-arched palate, a nonreducible adduc-
was calculated on this final score using Kappa coefficient tion of thumbs in a tightly clenched fist, and cranial
as recommended for categorical data. sutures ridges, indicate prenatal brain damage [41,42].
The results are presented Table 2. Although the same These signs are not specific for any etiology, although
three infants were found to have moderate signs at the first early identification may be the only way to exclude
examination by both raters, a total of 26 infants needed to intrapartum birth asphyxia as the cause of brain damage. If
be reassessed to confirm their normality in the first week these signs are not identified soon after birth, but only
of life. Eleven of these infants were the same for both later, their presence will be of no value in dating the insult
raters, whereas the other 15 needed to be reassessed only as prenatal (just as adductus thumb and cranial ridges may
by the midwife mainly because of her difficulty in obtain- develop a few weeks after any severe brain damage at
ing a good fix-and-track at the first assessment, demon- birth).
strating the importance of training. All of these observations are obviously of the utmost
Interrater reliability was good with a Kappa of 0.57 for importance in cases of litigation. If an adequate neurologic
the first examination and of 1 for the second examination. assessment was offered to every term neonate, debates on
Meanwhile, the instability of results over time for up to the role of birth asphyxia among other causes of cerebral
25% of the cohort, even though the method could not palsy, such as the recent one published in the British
allow the calculation of test-retest reliability coefficient Medical Journal [43,44], would be less passionate and
because of repetition of assessment only on infants with more consistent.

200 PEDIATRIC NEUROLOGY Vol. 27 No. 3


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