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ELSEVIER

Prospective Follow-up of Primitive Reflex


Profiles in High-Risk Infants: Clues to an
Early Diagnosis of Cerebral Palsy
D i m i t r i o s I. Z a f e i r i o u , M D , P h D , l o a n n i s G . T s i k o u l a s , M D , P h D , a n d
George M. Kremenopoulos, MD, PhD*

To clarify reflex profiles in the first year of life in of infants less than 1 year old [1]. Posture and/or muscle
connection with categories of neurologic abnormality, tone disturbances during the first 12 months of life in
eight primitive reflexes (i.e., the palmar grasp reflex, high-risk infants are not always prognostic of the later
the plantar grasp reflex, the Galant response, the diagnosis; some of these infants are normally developed,
asymmetric tonic neck reflex, the suprapubic extensor while others have various types of cerebral palsy (CP) or
reflex, the crossed extensor reflex, the Rossolimo re- developmental retardation (DR) without motor distur-
flex, and the heel reflex) were prospectively examined bance [2-4]. In such patients, examination of primitive
in 204 high-risk infants, of whom 58 developed cere- reflexes could contribute toward a more accurate and
bral palsy, 22 had developmental retardation, and 124 timely diagnosis, as well as toward a differential diagnosis
were normal at follow-up examination at 2 years of among neurologic abnormalities [5-7]. In our study, we
age. The change in the retention time of reflex activity examined the primitive reflex profiles of 204 high-risk
for each of these reflexes was characteristic for each infants to clarify their importance in early diagnosis and
category or type of neurologic abnormality: retention differential diagnosis of categories or types of neurologic
of palmar grasp reflex, suprapubic extensor reflex, abnormalities.
crossed extensor reflex, Rossolimo reflex, and heel re-
flex in spastic cerebral palsy, as well as retention of Patients and Methods
plantar grasp reflex, Galant reflex, and asymmetric All patients were referred to the Department of Developmental Med-
tonic neck reflex in athetoid cerebral palsy and some- icine of the Ist Pediatric Clinic, Aristotle University of Thessaloniki,
during the first month of life. The study period ranged from January 1993
what weaker retention of these reflexes in developmen-
to March 1995. Two hundred four high-risk infants had a complete
tal retardation (statistical significance P < .001 com- neurodevelopmental examination, including examination of primitive re-
pared with normally developed patients). These char- flexes, at age 1, 3, 5, 7, 9, and 11 months, as well as a later follow-up
acteristic changes imply that a presumptive diagnosis examination at age 2 years. At 2 years of age the patients were divided
can be made in neurologically high-risk infants by ex- into three categories according to neurologic diagnosis: patients with CP,
patients with DR without motor disturbance, and normally developed
amination of the primitive reflexes, which are of spe-
patients.
cific significance among the other neurologic criteria CP was defined as a nonprogressive disorder of posture and gait due
within the first year of life. to a lesion of the immature brain [8]. Clinically, a classification system
according to Ingram [9] and Bax [8], modified by Vojta [6], was used.
Zafeiriou DI, Tsikoulas IG, Kremenopoulos GM. Pro- According to this classification, spastic diplegia was diagnosed if spas-
spective follow-up of primitive reflex profiles in high-risk ticity in the lower limbs was greater than in the upper limbs: spastic
hemiplegia, if spasticity of the extremities was seen on only one side; and
infants: Clues to an early diagnosis of cerebral palsy. Pe-
spastic tetraplegia, if spasticity was more pronounced in the upper than
diatr Neurol 1995; 13:148-152. lower limbs, or at least of the same degree. Athetoid CP was defined as
the presence of athetoid movements with defective regulation of the
muscle tone shifting from hypotonia to normal. A diagnosis of ataxic CP
was made when ataxia was the only prominent symptom, without pyra-
Introduction midal or extrapyramidal tract signs.
The CP group comprised 58 patients: 49 patients with a spastic CP (24
The evaluation of posture, muscle tone, and primitive with spastic diplegia, 12 with spastic hemiplegia, and 13 with spastic
reflexes is an integral part of the neurologic examination tetraplegia), 7 patients with athetoid CP, and 2 patients with ataxic CP.

From the 1st Pediatric Clinic and *Department of Neonatology; Communications should be addressed to:
Aristotle University of Thessaloniki; Thessaloniki, Greece. Dr. Zafeiriou; Egnatia Street 106; 54622 Thessaloniki, Greece.
Received April 20, 1995; accepted July 5, 1995.

148 PEDIATRIC NEUROLOGY Vol. 13 No. 2 1995 by Elsevier Science Inc. 0887-8994/95/$9.50
SSDI 0887-8994(95)00143-4
Table 1. Eliciting the primitive reflexes*

Reflex Position Method Reaction

Palmar grasp Supine Placing the index finger in the palm of the infant Flexion of fingers--fist making
Plantar grasp Supine Pressing a thumb against the sole just behind the Flexion of toes
toes in the foot
Galant Prone Scratching the skin of the infant's back from the Incurvation of the trunk, with the concavity on the
shoulder downwards, 2-3 cm lateral to the stimulated side
spinous processes
Asymmetric tonic neck Supine Rotation of the infant's head to one side for 15 s Extension of the extremities on the chin side and
reflex flexion of those on the occipital side
Suprapubic extensor Supine Pressing the skin over the pubic bone with the Reflex extension of both lower extremities, with
fingers adduction and internal rotation into talipes
equinus
Crossed extensor Supine Passive total flexion of one lower extremity Extension of the other lower limb with adduction
and internal rotation into talipes equinus
Rossolimo Supine Light tapping of the 2nd-4th toes at their plantar Tonic flexion of the toes at the 1st
surface metacarpophalangeal joint
Heel Supine Tapping on the heel with a hammer, with the hip Rapid reflex extension of the lower extremity in
and knee joint flexed, and the ankle joint in a question
neutral position

* Based on data from References 6 and 11.

The CP patients were further classified as of prenatal, perinatal, or un- authors (DIZ), with the patient lying quietly on the examination bed in
known etiology according to Hagberg [10]. In 25 (43.1%) patients CP the waking state. Each reflex was obtained 3 or 4 times for evaluation of
was considered to be of prenatal etiology and in 21 (36.2%) patients of the response, and the reaction was classified as positive only in those
perinatal etiology; in the remaining 12 (20.7%) patients no clear etiology cases where the mean of the positive responses was >0.5 of all trials.
for the CP could be found. The results were statistically analyzed by means of chi-square analysis
DR was diagnosed as a developmental quotient (DQ) <75 in Griffiths and Fisher's Exact Test to evaluate the differences in reflex reactivity
Mental Developmental Scale at the age of 15 months. This group con- between normally developed patients and those with various neurologic
sisted of 22 patients, 3 of whom had Down syndrome, 1 had congenital abnormalities at each age of examination.
hydrocephalus, 3 had intraventricular hemorrhage (2 grade II and 1
grade Ill), 3 had neonatal convulsions, and 12 had no clear etiology. Results
The ratio of preterm to term infants was 32/26, 4/18, and 54/70 in the
CP group, the DR group, and the normal group, respectively. For pre- The palmar grasp reflex (Table 2) was preserved in the
term infants, the age at the time of each neurodevelopmental examination
majority of normal infants until age 5 months, after which
was expressed as the corrected age according to the expected birth date.
The primitive reflexes examined in our study were the palmar grasp it began to disappear. Most spastic patients exhibited full
reflex, the plantar grasp reflex, the Galant reflex, the asymmetric tonic activity of the reflex until age 11 months (statistical sig-
neck reflex (ATNR), the suprapubic extensor reflex, the crossed extensor nificance P < .001 compared with normal infants). The
reflex, the Rossolimo reflex, and the heel reflex. Their selection from reflex profile in athetoid, ataxic, and DR patients was not
among other neurologic signs or criteria was made because the judge-
different from normal.
ment of their reactions is simple and their clinical significance has been
suggested in the literature [6,7,11 ]. The manner of eliciting each of these The plantar grasp response (Table 2) exhibited nearly
primitive reflexes and the expected reactions are shown in Table 1. full activity until 7 months of age in the normal infants,
All neurodevelopmental examinations were performed by one of the while it could be elicited in only 1/5 of the patients at age

Table 2. Retention time of palmar grasp reflex and plantar grasp reflex

Examination Spastic CP Athetoid CP Ataxic CP DR Normal


age (n) (n) (n) (n) (n)
(mos) PaR PrR PaR PrR PaR PrR PaR PrR PaR PrR

1 49 49 7 7 2 2 22 22 119 124
3 49 37* 6 7 2 2 22 22 119 121
5 48 28* 6 7 2 2 21 22 119 117
7 44* 20* 4 7 1 2 9 20 24 93
9 41" 15" 1 7 1 1 5 14" 8 70
11 41" 9* 1 7* -- 1 4 12" 5 25

* Statistical significance: P < .001 compared with normal patients.

Abbreviations:
CP = Cerebral palsy n = Number of patients with positive reflex PrR = Plantar grasp reflex
DR = Developmental retardation PaR = Palmar grasp reflex

Zafeiriou et al: Prospective Follow-up of Primitive Reflex 149


Table 3. Retention time of Galant reflex and asymmetric tonic neck reflex

Examination Spastic CP Athetoid CP Ataxic CP DR Normal


age (n) (n) (n) (n) (n)
(mos) GR ATNR GR ATNR GR ATNR GR ATNR GR ATNR

1 49 49 7 7 2 2 22 22 124 124
3 44 45* 7 6 2 2 18 18 102 58
5 39* 39* 7* 6* l I 17" 16' 10 11
7 34* 39* 7* 6* -- -- 14' 10" 8 --
9 24* 33* 7* 5* -- -- 5* 4* 5 -
11 8* 28* 7* 5* -- -- 4* 2 4 --

* Statistical significance: P < .001 compared with normal patients.

Abbreviations:
A T N R = A s y m m e t r i c tonic neck reflex DR = Developmental retardation n : N u m b e r of patients with positive reflex
CP = Cerebral palsy GR = Galant reflex

11 months. In patients with athetoid CP, the response was patients with ataxic CP, ATNR disappeared by age 7
strongly retained until age 11 months (P < .001), while in months, while children with DR manifested prolonged re-
spastic patients, there was a gradual decrease of reflex tention of the above reflex, which was statistically signif-
reactivity from 3 to 11 months of age (P < .001). DR icant from 3 to 9 months of age (P < .001).
infants displayed a longer retention of the reflex compared Similarities in the reflex profiles of all patient groups
to normal patients, which was statistically significant at were observed for the following primitive reflexes: supra-
the age of 9 months and beyond. pubic extensor reflex, crossed extensor reflex, Rossolimo
In most of the normal infants, the Galant reflex (Table reflex, and heel reflex (Tables 4, 5). In patients with nor-
3) started to disappear at age 3 months and was completely mal development, these primitive reflexes were strongly
gone by age 9 months. In all athetoid CP patients, Galant retained until the first month of age and then rapidly de-
reflex remained positive until age 11 months (P < .001 creased, disappearing by age 5 months. In infants with
compared to normal infants />5 months old), while in spastic CP, these reflexes were retained much longer than
spastic CP patients the Galant reflex disappeared more in normal infants, to 11 months of age (statistical signif-
slowly than in normal patients, remaining positive in icance, P < .001). Infants with athetoid CP, ataxic CP,
about 2/5 of them at age 9 months. Infants with DR also and DR displayed reflex profiles similar to those of normal
manifested a prolonged retention of Galant reflex which infants.
was statistically significant from age 5 months (P < . 001). The above results are summarized in Table 6. There are
In about half of the normal infants, ATNR (Table 3), clear differences in the reflex activity of the palmar grasp
started to disappear at age 5 months, with total disappear- reflex, suprapubic extensor reflex, crossed extensor re-
ance by age 7 months. In spastic or athetoid infants, flex, Rossolimo reflex, and heel reflex between infants
ATNR was retained for a longer period than in normal with spastic and athetoid CP. The 2 patients with ataxic
infants, the difference in reflex reactivity being statisti- CP manifested no differences in the retention time of these
cally significant (P < .001) at age 3 months for the spastic primitive reflexes compared with normal patients; how-
group and at age 7 months for the athetoid group. In the 2 ever, their number is too small to allow any statistical

Table 4. Retention time of suprapubic extensor reflex and crossed extensor reflex

Examination Spastic CP Athetoid CP Ataxic CP DR Normal


age (n) (n) (n) (n) (n)
(mos) SER CER SER CER SER CER SER CER SER CER

1 49 49 7 7 2 2 22 19 124 105
3 45* 48* 3 2 1 -- 6 5 102 19
5 43* 44* 1 -- -- -- 3 2 10 3
7 41" 41' . . . . 1 -- 8 ---
9 41" 41" . . . . 1 -- 5 --
11 40* 39* . . . . 1 -- 4 --

* Statistical significance: P < .001 compared with normal patients.

Abbreviations:
CER = Crossed extensor reflex DR = Developmental retardation SER = Suprapubic extensor reflex
CP = Cerebral palsy n = N u m b e r of patients with positive reflex

150 PEDIATRIC NEUROLOGY Vol. 13 No. 2


Table 5. Retention tirae of Rossolimo reflex and heel reflex

Examination Spastic CP Athetoid CP Ataxic CP DR Normal


age (n) (n) (n) (n) (n)
(mos) RR HR RR HR RR FIR RR HR RR FIR

1 48 45 7 7 2 2 20 22 102 115
3 46* 42* 1 2 -- 1 4 7 15 25
5 45* 40* -- 1 -- -- -- 5 -- 11
7 45* 39* . . . . . 2 -- 3
9 45* 39* . . . . . . . .
11 45* 38* . . . . . . . .

* Statistical significance:P < .001 compared with normal patients.

Abbreviations:
CP = Cerebralpalsy HR = Heel reflex RR = Rossolimoreflex
DR = Developmentalretardation n = Numberof patients with positive reflex

conclusions. DR patients demonstrated the same tendency months; and a negative plantar grasp reflex after 3 months.
as athetoid patients for retention of plantar grasp reflex, These findings indicate a poor prognosis; on the basis of
Galant reflex, and ATNR, although this tendency was these primitive reflexes, neurologically abnormal children
stronger in the athetoid group. could be in part diagnosed earlier (after 3 months of age).
Examination of these eight primitive reflexes (Table 6)
Discussion can clearly distinguish between spastic and athetoid CP.
The diagnosis of ataxic CP, as well as the distinction
In the present prospective study, we analyzed the prim-
between athetoid CP and DR, is not possible with exam-
itive reflex profiles in high-risk infants referred for neu-
ination of the primitive reflexes alone. The combination of
rodevelopmental examination in the Department of Devel-
posture, muscle tone, and primitive reflex examination
opmental Medicine during the first year of life. Our results
can help in such presumptive diagnoses [ 13,14].
concerning the reflex profiles for normal infants are con-
The neurodevelopmental evaluation of an infant should
sistent with other studies which used the same method of
therefore be comprehensive, including observation of pos-
eliciting reflexes [6,11,12], thus indicating the validity of
ture, voluntary and involuntary movements, muscle tone,
the method used. From our results, we have concluded
primitive reflexes, as well as other responses and signs.
that early diagnostic clues as to whether a high-risk infant
The neurologic status of an infant cannot be judged on the
will become normal or abnormal at the age of 2 years is
basis of a single criterion, because there exists no criterion
the presence of the suprapubic extensor reflex, the crossed
that predicts the prognosis in all cases [15]. On the other
extensor reflex, the Rossolimo reflex, and the heel reflex
hand, the examiner should critically review the practical
after 3 months; a positive Galant reflex and ATNR reflex
significance of each procedure, so as to more easily reach
after 5 months; a positive palmar grasp reflex after 7
an early diagnosis. Our study indicates that examination of
the eight primitive reflexes beginning at age 3 months is a
Table 6. Retention of reflex activity in infants with
neurologic abnormalities useful diagnostic tool for early diagnosis of CP.

Spastic Athetoid Ataxic References


Reflex CP CP CP DR
[1] MenkesJH. Neurologicalexaminationof the child and infant.
Palmar grasp + 0 0 0 In: Menkes JH, ed. Textbook of child neurology. 4th ed. Philadelphia:
Plantar grasp - ++ 0 + Lea & Febiger, 1990:12-16.
Galant + ++ 0 + [2] Piper MC, Mazer B, Silver KM, Ramsay M. Resolution of
Asymmetric tonic neck neurologicalsymptomsin high-riskinfants during the first two years of
reflex + ++ 0 + life. Dev Med Child Neurol 1988;30:26-35.
Suprapubic extensor + 0 0 0 [3] Burns YR, O'Callaghan M, Tudehope DI. Early identification
Crossed extensor + 0 0 0 of cerebral palsy in high risk infants. Aust Paediatr J 1989;25:215-9.
Rossolimo + 0 0 0 [4] PeBenito R, Santello MD, Faxas TA, Ferretti C, Fisch CB.
Heel + 0 0 0
Residual developmentaldisabilities in children with transient hyperto-
nicity in infancy. Pediatr Neurol 1989;5:154-60.
Abbreviations:
CP = Cerebralpalsy [5] Capute AJ. Identifyingcerebral palsy in infancy through study
DR = Developmentalretardation of primitivereflex profiles. Pediatr Ann 1979;8:34-42.
+ + = Markedlyretained reflexes [6] Vojta V. Die cerebralen Bewegungstoerungenim Kindesalter.
+ = Slightly retained reflexes 4. Auflage. Stuttgart: FerdinandEnke Vedag, 1988.
0 = Unchangedreflexes [7] Futagi Y, Tagawa T, Otani K. Primitive reflex profiles in in-
- = Decreased reflexes fants: Differences based on categories of neurological abnormalities.
Brain Dev 1992;14:294-8.

Zafeiriou et al: Prospective Follow-upof PrimitiveReflex 151


[8] Bax CO. Terminology and classification of cerebral palsy. Dev JP, Sears EM. Evolution of postural reflexes in normal infants and in the
Med Child Neurol 1964;6:295-7. presence of chronic brain syndromes. Neurology 1964;4:1036-48.
[9] hlgram "ITS. Paediatric aspects of cerebral palsy. Edinburgh: E [13] Soiomons G, Holden RH, Denhoff E. The changing picture of
& S Livingstone, 1964. cerebral dysfunction in early childhood. J Pediatr 1963;63:113-20.
[10] Hagberg B, Hagberg G, Olow I, yon Wendt L. The changing [14] Taudorf K, Hansen FJ, Melchior JC. Spontaneous remission of
panorama of cerebral palsy in Sweden, V. The birth year period 1979- cerebral palsy. Neuropediatrics 1986;17:19-22.
1982. Acta Paediatr Scand 1989;78:283-90. [15] Miller G. The cerebral palsies. In: Miller G, Ramer JC, eds.
[11] Towen B. Neurological development in infancy. Philadelphia: Static encephalopathies of infancy and childhood. New York: Raven
JB Lippincott, 1976. Press, 1992:11-26.
[12] Paine RS, Brazelton TB, Donovan DE, Drorbaugh JE, Hubbell

152 PEDIATRIC NEUROLOGY Vol. 13 No. 2

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