Terapia neurohabilitatoria

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Neuroscience Letters 611 (2016) 59–67

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Neuroscience Letters

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Research paper

Longitudinal study of children with perinatal brain damage in whomearly neurohabilitation was applied: Preliminary report

Thalía Harmony∗, Jesús Barrera-Reséndiz, María Elena Juárez-Colín,Cristina Carrillo-Prado, M. del Consuelo Pedraza-Aguilar, Aurora Asprón Ramírez,Manuel Hinojosa-Rodríguez, Thalía Fernández, Josefina Ricardo-Garcell

Unidad de Investigación en Neurodesarrollo,Departamento de Neurobiología Conductual y Cognitiva, Instituto de Neurobiología, UniversidadNacional

Autónoma de México, Campus Juriquilla, Mexico

h i g h l i g h t s

• It is a longitudinal study of perinatal brain damaged children.• Katona’s neurohabilitation procedure was used as treatment.• 89% of preterm ≤34 weeks treated had normal neurodevelopment.• Only 20% of non-treated preterm ≤34 weeks had normal neurodevelopment.• Application of neurohabilitation to perinatal brain damaged infants is recommended.

a r t i c l e i n f o

Article history:

Received 31 March 2015

Received in revised form

26 September 2015

Accepted 10 November 2015Available online 17 November 2015

Keywords:

Perinatal brain damage

Prenatal risk factors

Neurohabilitation

Preterm encephalopathy

Hypoxic ischemic encephalopathy

MRI

a b s t r a c t

Objective: The neurohabilitation treatment has been shown to be a successful method for decreasing the

sequelae of perinatal brain damage (PBD) in Hungarian population. The goal of this pilot trial was to

introduce this procedure by describing the results of its application in infants with PBD as demonstrated

by clinical, developmental and MRI studies. As this procedure has proved to be useful, according the

declaration of Helsinki, no control clinical trial was permitted.Participants: Infants younger than 2 months of corrected age (CA) with prenatal and/or perinatal risk fac-

tors for brain damage. Two groups were considered. One group was treated using the “neurohabilitation”

method (n=20), and the other was not treated (n=13) because treatment was voluntarily discontinued

after the initial evaluation. Evaluations were carried out prior to 2 months of CA and at 6–8 years of age.

All children showed abnormal clinical and MRI characteristics in the first study.

Results: The treated group had a higher percentage (90%) of children with normal outcome than did the

non-treated group (38%; OR = 2.37, CI 95% = 1.2–4.7; p< 0.005). In this latter group, only one out of five

(20%) children born at or before 34 weeks of gestational age hada normal outcome. In contrast, eight out

of nine treated preterm infants had normal outcomes (8/9 =89%, OR = 4.45, CI 95% = 0.7–26; p= 0.017).

Conclusions: This pilot trial confirms previous studies suggesting that Neurohabilitation decreases the

neurological and cognitive sequelae of preterm and at-term infants with PBD.

© 2015 Elsevier Ireland Ltd. All rights reserved.

1. Introduction

Despite advances in medicine and significant improvements in

the survival of preterm infants over the last 10–20 years, the inci-

dence of births at risk for brain damage has not diminished; in

∗ Corresponding author at: Instituto de Neurobiología, UNAM Campus Juriquilla,

Querétaro 76230, México. Tel.: +52 442 1926101x113.

E-mail address: [email protected] (T. Harmony).

fact, some evidence suggests that disability rates have increased

[1]. Data in the literature also showed that even preterm children

who survive without apparent motor disability, have a substantial

reduction in the mean intelligence quotient (IQ) and an increased

incidence of cognitive and educational difficulties [2–5].

A revision of the literature related to early interventions pro-

grams to study high risk premature infants has shown that when

applied to severe low weight preterm babies’ scores [6] or infants

with brain lesions [7] did not show any improvement on neurode-

velopment. Neurodevelopmental treatment (NDT) is the method

http://dx.doi.org/10.1016/j.neulet.2015.11.013

0304-3940/© 2015 Elsevier Ireland Ltd. All rightsreserved.

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60 T. Harmony et al. / Neuroscience Letters 611(2016) 59–67

most frequently used for intervention in children with a develop-

mental disorder [8]. NDT is generally applied later in life, when

there are symptoms and signs of brain injury, therefore as a reha-

bilitation procedure. The same happened with Vojta’s method. On

the other hand, the effectiveness of the NDT approach and other

pediatric therapies is currently an issue generating considerable

professional debate [9]. None of five studies that evaluated NDT

effects demonstrateda statisticallysignificanteffect of intervention

in motor development [9–13]. In a report comparing NDT vs. Vojta

methods for the earlytreatment of cerebral palsy, Vojta’s procedure

showed to normalize more infants than NDT method [14].

Although decreasing the number of births at risk for brain

damage should be the priority to decrease theneurologicaland cog-

nitive sequelae, the early diagnosis and treatment of brain damage

in newborns at risk may also decrease these sequelae. This is the

goal of the therapy known as “neurohabilitation”, as proposed by

Ferenc Katona [15–18] to differentiate this process from rehabilita-

tion. The maindifference between the two is thatneurohabilitatory

treatment should begin before the lesion sequelae have beenestab-

lished, during the first 3–4 months after birth, to try to reduce or

abolish the neurological sequelae that may result from perinatal

brain damage. The results of the application of this therapy to 2189

infants of less than 6 months old with suspected perinatal brain

damage showed, at 18 months of corrected age (CA), that 46% hada normal outcome, 32% improved relative to their initial symp-

toms, and22% hadno change or their symptoms hadbecome worse

[15,16]. These results were obtained in Hungary where this tech-

nique has been applied for more than 30 years; however, it is not

well known in other countries. The results obtained in Hungary led

us to evaluate this procedure in our group of patients in Mexico. To

our knowledge, this is the first report describing the longitudinal

results obtained in the application of neurohabilitation to infants

with perinatal brain damage demonstrated by magnetic resonance

images (MRI) as well as by clinical and psychological evaluations.

2. Patients and methods

The Ethics Committee of the Instituto de Neurobiología of

the Universidad Nacional Autónoma de México approved this

study, which also complies with the Ethical Principles for Medi-

cal Research Involving Human Subjects established by the Helsinki

Declaration. Informed written parental consent for participation in

this study was obtained for all subjects.

2.1. Patients

Inclusion criteria: infants during the first 2 months of corrected

age (CA) with prenatal and/or perinatal history of risk factors for

brain damage. These risk factors are described in Tables 1 and 2 f or

each patient. After the infants were discharged from the hospital

where they were born, their parents were invited to participate ina special project of the Unit for Neurodevelopmental Research at

the National Autonomous University of Mexico in Querétaro. This

Unit currently has a data base with 1138 subjects from 0 to 8 years

old.

Two groups of children were considered: the treated and the

non-treated groups. To build a non-treated group who did not

undergo treatment but who had initiated the protocol with all the

indicated studies, we looked for children between 6 and 8 years

old that voluntarily discontinued the treatment after one month.

We used these criteria for ethical reasons. If it had been shown that

the neurohabilitation procedure is useful to improve development

even in the case of infants with severe brain lesions [15–18], it is

against the Helsinki declaration to leave infants without the treat-

ment in order to have a control trial. The parents of 13 children

agreed to return to the unit for re-evaluation. They comprised the

non-treated group, and they did not have any type of treatment. In

thisgroup theclinical observationswere onlydone before 2 months

of corrected age (CA) and at 6-8 years old.

Then, from a pool of 1138 treated children from our data base,

20 were pseudo-randomly selected [19] f rom those who had fol-

lowed the treatment and all the evaluations and who were similar

to the non-treated group in terms of age, gender, weight at birth,

Apgar, risk factors and diagnosis. These 20 children formed the

treated group. Exclusioncriteria were: infants older than 2 months

of CA,presenceof geneticfactorsassociatedwith brain damage,car-

diovascular pathology, brain malformations and/or chromosomal

aberrations.

2.2. Evaluations

The initial evaluations were performed in the two groups and

they included:

(a) Clinical pediatric and neuropediatric examinations [20], (b)

Bayley scales [21] (c) Magnetic resonance imaging (MRI) using 1.0

T Philips equipment, and (d) Katona’s evaluations [17,18,22]. These

evaluations were repeated accordingto a time schedule only in the

treated group. Neuropediatric evaluations were done each month

during the first year, each 3 months during the second year, andeach 6 months after 3 years old. Bayley’s evaluationsand MRIs were

done each 4 monthsduring the first year and each 6 monthsduring

the second and third year. In the fourth year WIPPSI scales were

used and applied each 6 months and later on, WISC was applied

each year. After the fourth year, MRIs were obtained each year

if there was some abnormal finding. When the children reached

6–8 years of age, the following evaluations were performed: (a)

neuropediatric examination, (b) clinical psychological evaluations

and performance in the WISC-IV test [23], (c) clinical language

evaluations [24], and (d) MRI evaluations. At these ages MRI was

performed using a 3.0 T GE scanner. If in the first 3 examinations

the child showed normal results, or a borderline IQ, then her/his

outcome was considered “normal”. The abnormal outcomes were

classified as neurological when the last neuropediatric examina-tionshowed abnormalfindings, andas cognitive sequelae whenthe

clinical psychological evaluation and/or IQ values were abnormal

and/or language delays were observed.

2.3. Katona’s procedure (see Ref. [25], data in brief)

Katona’s methodology is both diagnostic and therapeutic.

Katona’s assessment is performed with some of the maneuvers

used in the therapy itself, where it has to take into account several

evaluation parameters such as: muscle tone (passive and active);

hemi bodies symmetry along the maneuver performance; atten-

tion, eye tracking and auditory monitoring; neurological signs

of alarm (thumb in fist, scissor gait, strabismus, irritability, axial

hyperextension, among others).Katona based the neurohabilitation procedure on the “ele-

mentary neuromotor patterns”. These early integrated complex

movements are chains of processes in which the neck, trunk and

extremities perform complex and continual movements in cer-

tain repetitive patterns. These motor patterns are characterized

by a high degree of organization, persistence and stereotypy and

can be divided in two groups: (1) complex chains of movements

directed to verticalization of the body and(2) complex movements

directed to locomotion [17,18,25]. Thesemovements are controlled

by the developing subcortical structures and can be activated by

determined positions of the head and the body that triggers the

activation of the vestibular nuclei andtheir projections to thespinal

cord, the reticular formation, thalamus, cerebellum, basal ganglia

[26]. Nearly all these tracts project to the motor cortex [27]. At the


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T. Harmony et al. / Neuroscience Letters 611 (2016) 59–67 63

Fig. 1. Main maneuversfor verticalization. (1)Lift trunk with hand drive.(1a) Doublelift trunk with hand drive.(2) From lying to sitting. (3)Lift thetrunkwith back andhip

support. (3a) Lift trunk with back support. (4) Sitting in the air. (5)Front protection to support thighs and chest.(6) Lateral and anterior protections.

Table 3

MRI Initial findings.

Diagnosis Control Treated OR CI(95%) P

N % N %

Diffuse white matter damage 6 46 12 60 1.75 0.427–7.171 0.436

Increased LV volumes 5 38 4 20 2.50 0.522–11.955 0.251

Decreased CC volume 4 31 4 20 1.77 0.355–8.881 0.483

Cerebral atrophy 0 0 2 10

Table 4A

Outcome of the patients with ≤34 weeks of GA.

Group Normal outcome Abnormal outcome Total

Control≤34 weeks 1 4 5

Treated≤34 weeks 8 1 9

OR= 4.45, CI 95% =0.7–26; effect size= 0.68, CI 95% =0.1–0.9; p= 0.017.

same time, movements generate activation of different receptors,

which send afferent impulses. This constant feedback helps in the

organization of motor control.

A therapeutic program consists of training of a series of neu-

romotor patterns each day for a certain time. The generation of these movements repeated several times produce brain engrams

that improve motor development [28]. At the initiation of the

treatment, specialized therapistsconducted theKatona evaluations

to obtain a diagnosis and to program the exercises that parents

should learn to apply to their infants at home during the first

month of therapy. The therapy was intensive and specific for each

infant.

The differentpositions to generate the specific neuromotor pat-

terns are described in Refs. [22] and [25]. Figs. 1–5 show the

different maneuvers described in Ref. [25].

During the first 3 months, parents should go daily with the

therapist in order to learn how to stimulate the infant under the

supervision of the therapist. The therapy consists in the elaboration

of the individual program, a session consists in the repetition, 4–8

Table 4B

Outcome of the patients with >34 weeks of GA.

Group Normal outcome Abnormal outcome Total

Control > 34 weeks 4 4 8

Treated > 34 weeks 10 1 11

OR= 4.45, CI 95%= 0.1–22; effect size= 0.4, CI 95%= −0.07 to 0.7; p= 0.28.

times, of 6–9 sensoromotor patterns such as lift trunk with hand

drive [25]. One sessionhas a duration of 45min and sessions should

be repeated 3 or 5 times daily. Parents learn how to correctly per-

form the exercises since they are going to treat the infant at home.

Therapy must be integrated to the infant’s schedule and dividedinto periods according to patterns of sleeping and wakefulness as

well as feeding and nursing schedules.

Eachmonth,the infant was examinedevaluating not onlymotor

performance but also visual and auditory attention and the ages at

which the infant mastered various developmental milestones.

2.4. Statistics

Almost all comparisons between groups were performed using

Chi-square statistics. Odds ratio (OR) and 95% confidence intervals

(CI) were calculated for proportions. Effect size and 95% CI were

calculated following Cummings [29] software. The Student’s t -test

was used to compare WISC values between groups. As it is known

that the outcome of preterm infants with equal or less GA than


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64 T. Harmony et al. / Neuroscience Letters 611(2016) 59–67

Fig. 2. Maneuversto changeposture.(7) Rolling over ona blanket. (8)Rolled over with head support. (9)Halfroll over. (10) Sitting to four pointssupport.(11) From kneeling

to standing.

Fig. 3. Maneuvers to creeping. (12) Elementary horizontal creeping. (13) Elementary creeping downward on slide. (14) Elementary creeping upwardon a slide. (15) Shiftingsupport in knees (kneeling creeping).

34 weeks (GA≤34) is worst than the outcome of infants with GA

greater than 34 weeks (GA> 34), comparisons between treated and

non-treated groups were also done separately for infants GA≤34

and GA> 34 weeks.

3. Results

Tables 1 and 2 describe the characteristics of the treated and

non-treated groups. No significant differences between groups

were observed in the initial findings and diagnosis. All children

showed abnormal findings in the first clinical and MRI examina-

tions, indicating brain damage (see Table 3).

In terms of outcomes, the treated group had a significantly

higher percentage of children with normal neurodevelopment

(18/20) compared to the non-treated group (5/13= 38%; Odds

ratio=2.37, CI 95%= 1.2–4.7; effect size= 0.5, CI 95%= 0.2–0.7;

p< 0.005).

In relation to the children with a gestational age (GA)≤34

weeks, the results were significantly different between groups,

with higher percentage of normal outcomes in the treated

than in the non-treated group (OR =4.45, CI 95% =0.7–26; effect


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Fig.4. Maneuversto crawling. (16)Elementaryassistedcrawling.(17) Modified assistedcrawling.(18) Crawling withlateral support.(19) Crawling legsupport.(20) Crawling

in an ascending plane. (21) Crawling a downward slide. (22) Crawling on stairs.

Fig. 5. Maneuversto walking. (23) Elementary walk. (24) Elementary walkon upward slide.

size = 0.68CI 95% = 0.1–0.9; p=0.017 ; see Tables 4A and B). Fig. 6

shows the MRI of two patients, one of each group.

However, no significant differences were observed between the

groups ininfants with >34weeks of GA. Total IQvalues areshown in

Tables 1 and 2. In the non-treated group there was one child with

very severe mental retardation who was not able to perform the

WISC test.Thischildwasnot takenintoaccount whenthe mean val-

ues of the subtests or the total IQ were compared between groups.

No significant differences between groups for the total or the IQ

subtests were observed for all the infants and for those subgroups

with GA≤34 orGA> 34.

Interestingly, although all the children of both groups had

abnormal findings in the initial MRI evaluation, in the last MRI

study four of thirteen of the non-treated group (31%) and twelve

of twenty in the treated group (12/20 = 6 0%) showed a nor-

mal MRI (see Fig. 6), the difference between groups was not

significant ( p=0.15). The children of both groups who finished

the study with normal MRI scans also showed significant dif-

ferences in outcome: two of four in the non-treated group

(50%) and twelve of twelve in the treated group (12/12= 100%;

OR= 2, CI 95% = 0.75–5.32; effect size= 0.6CI 95% = 0.07–0.85;

p= 0.05).


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Erika Cruz-Rivero, Antonio Fernández-Bouzas †, Delia Figueroa-

Navarro,JohannaFlores-Arizmendi,Berta González-Frankenberger

†, Verónica Guidobono-Radesca, Rosa M. Hernández-Corona, Clau-

dia Jiménez-Sánchez, Alma Janeth Moreno-Aguirre, Juan José

Ortiz-Reséndiz, Erik Pasayé-Alcaraz, Tonatzin Pineda-Martínez,

Sara Elisa Ponce-Rodríguez, Eneida Porras-Kattz, Amaya Soberón-

García and Angeles Zavala. Authors also acknowledge the

anonymous reviewer for his/her suggestions, Dr. Dorothy Pless for

the revisionof theEnglishversionof the manuscript,andDr. Susana

Szava for the translation to Spanish from Hungarian of Katona’s

book Ontogenesis of the humannervous system.

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Terapia neurohabilitatoria

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