Gasparrini et al.

Italian Journal of Pediatrics (2019) 45:38

https://doi.org/10.1186/s13052-019-0629-7

RESEARCH Open Access

Long-term follow-up of newborns at

neurological risk
Enrico Gasparrini1* , Francesca Rosati2 and Maria Teresa Gaetti3

Abstract
Background: In order to give a new contribution to the knowledge of the psycho-physical, behavioral and socio-
relational development of the individuals who were born at neurological risk, we have carried out a research work
through a retrospective and observational analysis in such people, followed in their neuro-evolutionary
development from the Department of Pediatrics and Neonatology of the Hospital of Jesi.
The purpose of this work is to value the quality of life of the individuals born at neurological risk at a distance of
time from the birth.
In the literature only recently there are studies on the quality of life of some categories of people, but survey does
not seem to be performed in individuals previously born at neurological risk.
Methods: A statistical descriptive and inferential survey has been carried out on 812 individuals who were born at
neurological risk, 442 preterm newborns and 370 term newborns, followed from 1977 until to 2007. They were
classed in order to their age at the time of our observation. We have submitted the entire sample to a
Questionnaire to investigate some areas of their life, ranging from their clinical and psycho-social history to their
personal coming of life. Then the same persons, subdivided according to the various age groups, were subjected to
other Questionnaires on the quality of life, internationally used.
Results: Neurological outcomes were found in 14.7% of the preterm newborns and in 6% of the term newborns,
with a significant correlation between neurological outcomes and gestational age, low birth-weight, hypoxic-
ischemic encephalopathy and low APGAR-index. Neuro-disabilities were found prevalently belong to the small for
gestational age preterm newborns. A low quality of life emerged in those who had neurological outcomes.
Conclusions: Our study on the individuals who were born at neurological risk, analyzed at a distance, shows that a
good health is associated with a good quality of life, while a low quality of life occurs to those who had
neurological outcome, especially in the physical, cognitive, emotional and socio-relational aspects.
As far as the few neurological outcomes which we have found in this survey, we think that they are due, other
than to the natural factors, also to the high quality of the obstetric and neonatal care, to the early habilitation
physiotherapy and to the important collaboration with the family.
Keywords: Quality of life, Newborns at neurological risk, Follow-up, Neurological outcome, Neuro-evolutionary
development

* Correspondence: enrico.gasparrini@sanita.marche.it
1
Department of Pediatrics and Neonatology - Hospital of Macerata, Macerata,
Italy
Full list of author information is available at the end of the article

© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Gasparrini et al. Italian Journal of Pediatrics (2019) 45:38 Page 2 of 8

Background Although it is certainly important to establish the con-

The progress achieved in the last few decades in the pre- nections between the neuroimaging (ultrasound, com-
ventive, diagnostic and therapeutic fields regarding the puted tomography, cerebral magnetic resonance
assistance to pregnant women and the care of the new- imaging), the evoked potentials (visual, auditory, neuro-
borns have led to a significant drop in the mortality rate sensory), the electroencephalography and the type of the
of the newborns at neurological risk. However, despite brain damage, its extension and location, its onset, the
the progress in the medical field has allowed to increase type and severity of the neurological deficit, it is also
the likelihood of survival even of preterm newborns with true that this assessment does not always give satisfac-
low gestational age (< 32 weeks) and/or very low tory results, especially with regard to the minor brain in-
birth-weight (< 1500 g, called VLBW, and < 1000 g, juries (transient hyperechogenicity, microcystic
called ELBW), in recent years there has been no reduc- periventricular leukomalacia, intraventricular not exten-
tion in the incidence of developmental disorders of vari- sive hemorrhages).
ous kinds in these children [1, 2]. The neuroradiological and the electroencephalo-
So if on the one hand, thanks to recent technological graphic findings do not always correlate with the severity
and pharmacological discoveries in the prenatal, peri- of the psychomotor outcome. In fact, cases with normal
natal and neonatal care, there has been a significant re- or mildly compromised psychomotor development have
duction of the risk for mortality and permanent diseases, been described in the presence of extensive cystic leuko-
on the other hand many studies have documented that malacies and, conversely, cases of children in whom the
these persons, compared to those borns at-term, are presence of no-cystic leukomalacia has led to the devel-
more at risk for the onset of disorders of opment of cerebral palsy.
neuro-psychological development, which tend to in- It is therefore evident that the alone neurological in-
crease with the decrease of the gestational age, such as, strumental semeiology does not allow to define the cat-
for example, postural and motor deficits, dyspraxies, be- egories of newborns at neurological risk. Therefore it is
havioral changes, disorders of language, attention deficit necessary that it is always flanked by a valid neurological
and hyperactivity, relational difficulties, affective disor- clinical semeiology that, used before the development of
ders, learning difficulties, impairment of visuo-motor in- the technologies of recent years, has always had its valid-
tegration and quality of life [3]. ity [6] and, nowadays, is further enriched thanks to the
These deficits often emerge in preschool and school greater knowledges, especially in the neuro-functional
age, proving how the preterm birth has consequences field [7–11].
also on the children who do not present clear clinical Near to the relief of the cerebral lesion, which should
manifestations that can be diagnosed early. be documented in as much detail as possible, the integ-
In the light of these observations, more attention has rity of the central nervous system and the ability to com-
been put to the medium and long term effects of the pensate for the possible damage must be evaluated (the
preterm birth, not only on the level of physical and/or brain plasticity has exceptional potentialities in the first
cognitive functioning, but also on that of psychosocial months of the life). The clinical evaluation must ascer-
and emotional adaptation. In particular, it seems reason- tain the presence and the degree of the brain dysfunc-
able to argue that one of the most relevant areas in the tion regardless of whether or not macroscopically
field of the neonatology, the neuropsychiatry and the de- documented brain lesions are found.
velopmental psychology is to optimize the social and en- The scientific studies of the neurological clinical
vironmental adaptation and the quality of life related to semeiology of the newborn began in the years 1950–1960
the health status of the preterm baby. with Andrè Thomas, Saint Anne Dargassies, Joppich and
In Italy, in 2017, 458,151 children were born [4]: about Schulte, although various “neonatal reflexes” had already
10% of them were born preterm (before the 37th week been reported by Magnus and Klein in 1912 and Moro
of gestation) and 1% were born before the 32th week of had gone beyond the neurophysiological-phylogenetic
gestation [5]. meaning assigned initially to them and had suggested their
Of course the neurological risk is not due only to the use for neurological diagnostics.
preterm birth, but it may be due to family-genetic fac- But it is above all in the last fifty years that, for the greater
tors or to alterations during the pregnancy, during or survival of infants of ever lower weight and the consequent
after the delivery. need to make them a good quality of life, especially in the
In the recent years the introduction of new instrumen- neuropsychic field, more and more neurological evaluation
tal techniques for the morphological, functional and techniques have been developed to attribute also a prog-
metabolic study of the brain since the neonatal age has nostic meaning, as well as a diagnostic one.
provided an important contribution to the diagnosis and In particular, Prechtl, Cioni and Ferrari have developed
the prognosis of the neurological damage. a method for assessing the neuromotor development of
Gasparrini et al. Italian Journal of Pediatrics (2019) 45:38 Page 3 of 8

the newborn, based on the observation of the spontan- The aforementioned individuals were invited to take part
eous motility (“General Movements”). This instrument, to the study by a letter, in which they were informed that
that can be applied early also on the delicate newborns they would be contacted by one of our Operators for a
because it does not involve the manipulation of the meeting at the Department of Pediatrics and Neonatology
child, has shown a good sensitivity and a good specifi- of the Hospital of Jesi.
city, allowing a reliable predictability and an early diag- The choice of “face to face” was based on the possibil-
nosis of pathological development [7–10]. ity to obtain a higher quality of answers, better compli-
In order to give a contribution to the knowledge of the ance and a higher percentage of respondents.
psycho-physical, behavioral and socio-relational develop- We have submitted all the people who responded to
ment of the individuals who were born at neurological our invitation, regardless of age, to a Questionnaire to
risk, and, above all, to the knowledge of their quality of investigate some areas of their life, ranging from their
life at a distance of birth, induced also by the scarcity of clinical and psycho-social history to their personal com-
studies on this argument [12–14], we have carried out a ing of life (for example: health state, social position, level
retrospective and observational analysis in such people, of study, social and family relationships, enabling ther-
who had been followed-up for years in their apy, etc.).
neuro-evolutionary development from the Department We then subjected the same persons, subdivided ac-
of Pediatrics and Neonatology of the Hospital of Jesi. cording to the various age groups, to other Questionnaires
The purpose of our study was: on the quality of life, internationally used [15, 16]:

 to evaluate the quality of life of the individuals at a  The Tap QoL (TNo-AZL Preschool Children Quality
distance of time from their birth of Life Questionnaire; 1–7 years): given to the
 to consider their path of the growth and of the parents of the children who were born at
intellectual maturation neurological risk. It consists of 43 items that
 to determine their auxological development investigate the various psycho-physical areas of the
 to analyze the psychosocial and affective support subject examined. The areas concern the sleep, the
from their family and from the Socio-health physiological functions related to the gastroenteric,
Services. musculoskeletal and respiratory apparatus, the cog-
nitive, communicative, emotional and social-
Methods relational sphere.
We started our research by examining the medical records  PedsQoL (Pediatric Quality of Life Inventory, 8–14
filed in the Department of Pediatrics and Neonatology of years): it is a generic questionnaire developed on 23
the Hospital of Jesi concerning 1704 patients who were items that investigate the areas related to the
born at neurological risk, excluding those affected by gen- physical, emotional, social and scholastic functions.
etic and metabolic diseases, followed-up in the same  HU13 (Health Utilities Index Mark3, 15–17 years):
Department in the period between 1977 and 2007. 45 items that investigate the areas related to the
These people were 6% of 28,032 individuals born in physical, cognitive, emotional and pain-related
that period: 854 were born preterm and 850 were born functions.
at-term, both born at neurological risk. Most of them  SF36 and ID-5D VAS (Euro Quality 5 Dimensions
(92.8%) were born at the same Hospital (inborn), only and visuo-analogue, 18–32 years): both tests analyze,
some of them (7.2%) came from other Structures through a scale from 0 to 100, the perception of the
(outborn). state of the physical and emotional health,
The parameters that we took into consideration, con- investigating some areas of exploration: physical
cerning them, were the following: function, physical pain, general perception of own
state of health, vitality, social activities, limitations of
 Personal data (age, gender) role due to emotional problems, mental health.
 Gestational age  TAT proprioceptive test (Thematic apperception test
 Birth weight: AGA (weight between 10th and 90th or Murray test, 15–32 years): examines the psychic
percentile), SGA (<10th percentile), LGA (> 90th asset from an analytical point of view and evaluates
percentile) both the possible effects that being born at
 APGAR score at first minute < 7 neurological risk has in the parental relationship at
 Type of delivery (eutocic/distocic) the inter/intrapsychic level (“dialogue with the
 Diagnosis at birth internal parental images”), both the functional and
 Outcome in the first year of life pathological defensive mechanisms that the person
 Abilitive physiotherapy (yes / no). activates in his experiential path. In detail it is a test
Gasparrini et al. Italian Journal of Pediatrics (2019) 45:38 Page 4 of 8

Fig. 1 The outline of the individuals invited and recruited to take part to the study

that uses projection phenomena starting from the The drop-out (slightly greater for the term borns) was
tables that are presented to the individual who mainly determined by the inability to find personal informa-
elaborates a “story”, whose interpretation highlights tions (telephone numbers, addresses, etc.) and by the lack of
attitudes, conflicts, defensive mechanisms which are response from someone. These data are shown in Fig. 1.
often unconscious. It is composed from 31 tables The classification based on the degree of prematurity
and includes differentiated series that are suitable for of the individuals examined is reported in Table 1.
young or adult persons, male or female. We then subdivided these people, selected on the basis
of their age at the time of our observation, in the follow-
Therefore a descriptive and inferential statistical sur- ing group:
vey was carried out.
The absolute frequencies and the percentages accord- a) 1–7 years
ing to term and preterm newborns were calculated for b) 8–14 years
the categorical variables. The comparison between the c) 15–17 years
two groups was made by the Chi-square Test (χ2) and d) 18–32 years.
the Fischer Exact Test.
The quantitative variables were instead synthesized From the analysis carried out in the phases of the ex-
using the median as a measure of centrality and the first perimentation on 812 individuals of the sample it results
and third quartile as a measure of dispersion. The groups
were compared by the Wilcoxon-Mann-Withney Test.
Table 2 The prevalence of neurological outcomes
Neurological N° Preterm (% on N° term (% on 370)
Results Outcomes newborns 442) newborns
Invited to participate in the study 1704 individuals who Neuro-sensory 16 3.6% 9 2.4%
were born at neurological risk and followed in the period deficit
between 1977 and 2007, 812 individuals (about 50%) Neuro-motor 14 3.2% 3 < 1%
came in a year: 442 preterm borns and 370 term borns. deficit
These constitute the sample of our survey. Psycho-motor 14 3.2% 4 < 1%
delay
Table 1 The degree of prematurity of the individuals examined Language 11 2.5% 2 < 1%
Level of prematurity % Average Gestational Age delay
34+ 0–36+ 6 weeks of GA 72 35.14 ± 0.86 Epilepsy 2 < 1% 2 < 1%
32+ 0–33+ 6 weeks of GA 21 33.06 ± 0.45 Hydrocephalous 3 < 1% 0 ----
28+ 0–31+ 6 weeks of GA 6.6 29.51 ± 1.05 Walking deficit 5 < 1% 2 < 1%
< 28+ 0 weeks of GA 0.4 26.67 ± 0.52 Total 65 14.7% 22 6%
Gasparrini et al. Italian Journal of Pediatrics (2019) 45:38 Page 5 of 8

Table 3 The neurological outcomes and associated factors relationship between the parental figures, resulting from
Neurological Outcomes p an emotionally perceived pathological experience.
Hypoxic-ischemic encephalopathy 0.001 All the patients with more or less severe problems of
APGAR score at first minute < 7 0.001
neuro-evolutionary development had benefited from the
Neuro-psycho-pedagogical and social District Services,
Twin birth 0.15
even if these have not always been adequate and
Gestational age 0.001 efficient.
Kind of delivery 0.971 There were statistically significant differences between
Birth weight (SGA, AGA, LGA) 0.001 term and preterm newborns with regard to sleep disor-
ders (p 0.01) and school difficulties (0.04).
that 14.7% of the preterm newborns and 6% of the term At last, there were statistically significant differences
newborns have had pathologic outcomes (Table 2). in the level of employment: in fact, study or work 58.6%
The presence of pathologic outcomes is statistically cor- of term newborns versus 48.2% of the preterm newborns
related (p < 0.001) to the presence of hypoxic-ischemic en- (p < 0.0001).
cephalopathy at the birth, to the APGAR score of less As for the quality of life, which has been evaluated by
than 7 at the first minute of life, to the neonatal gesta- comparing it to a scale of values ranging from 0 to 100,
tional age and at to the birth weight. where 0 represents the minimum and 100 maximum
Among preterm newborns, the incidence of problems satisfaction, it has been seen that the group of preterm
increased as the neonatal gestational age was reduced newborns has presented an average value equal to 50
and, among them, the prognosis of the small for the ges- against a value equal to 69 of those born at term.
tational age (SGA) newborns was worse; on the other In detail, as reported in the Tables 4,5,6,7, among the
hand, the kind of delivery and twin birth have no signifi- group of the preterm newborns and the group of the
cance (Table 3). term newborns, the following statistically significant dif-
These results are in accordance with our previous sur- ferences emerged in the various age groups:
vey carried out on infants of low birth weight at 5 years A low quality of life has emerged in those persons who
of age [16] and with the data of the literature. had neurological outcomes. The most compromised
From the questionnaire submitted to the people who areas were related to the following aspects:
responded to our invitation regardless of the age, it has
emerged that were no statistically significant differences – physical: 27.3%.
between preterm and term newborns as regards the auxo- – social: 18%.
logical aspect. In fact, there was a normal stature-weight – cognitive: 14.3%.
growth in almost all the children examined, also if, how- – emotional: 14.2%.
ever, 6.6% of the SGA newborns had a short stature (< 3°
or -2DS) and 20% of them were obese. Discussion
Almost all the children followed in the follow-up who, From the survey carried out on individuals who were
during the first months of life, had presented signs of a born at neurological risk of our case series it emerges
predictive neurological pathology (“symptomatic-risk that few neurological outcomes are found. It is to be
children”) or an established neuro-evolutionary path- thought that this is partly due to natural factors, but
ology had been subjected to early habilitation physio- above all to the quality of the obstetric care and to the
therapy (96.8% of preterm newborns and 94.8% of term timeliness and the appropriateness of the neonatal care,
newborns respectively, p 0.21). to the early habilitation physiotherapy, to the important
All the individuals have had a psycho-social support collaboration with the family (“the therapeutic alliance”).
from their families, even if in 43% of cases it was not The data analyzed show that the satisfactory physical
found to be qualitatively valid, because of an altered state of the individuals in question (the low percentage

Table 4 TNo-AZL Preschool Children Quality of Life Questionnaire (1-7 years)

Quantitative variables: median (1 and 3 quartile) Term (n. 70) Preterm (n. 70) p
Wilcoxon test
physical impact 36 (35–36) 34 (31–36.5) 0.01
emotional impact 6 (6–6) 5 (5–6) < 0.0001
social impact 14 (13–14) 14 (12–14) 0.21
cognitive impact 8 (8–8) 7 (7–7) < 0.0001
Total score (0–100) 74.4 (73.3–74.4) 69.8 (63.4–75.6) 0.00
Gasparrini et al. Italian Journal of Pediatrics (2019) 45:38 Page 6 of 8

Table 5 Pediatric Quality of Life Inventory (8-14 years)

Quantitative variables: median (1 and 3 quartile) Term (n. 70) Preterm (n. 71) p
Wilcoxon test
physical impact 90.6 (71.9–93.8) 84.4 (78.1–87.5) 0.06
emotional impact 85 (80–85) 80 (60–90) < 0.0001
social impact 100 (0–100) 75 (10–90) < 0.0001
scholastic impact 85 (10–90) 50 (30–70) 0.08
Total score (0–100) 90 (85.2–94.7) 78.3 (71.1–83.9) < 0.0001

of neurological outcomes at a distance, stature-weight represent the privileged stage of the emersion of the
growth in the norm in the majority of cases) is associ- emotional states, it is clear that the problem has reper-
ated with an average satisfactory quality of life. cussions in the social sphere: family, friendships, school,
The areas investigated which have negative implica- work.
tions on the quality of life are related to the physical, A good contribution to overcome this anguished
cognitive, emotional and socio-relational aspects. In fact, and suffered experience of the child and of his par-
a low quality of life emerges, especially in the ents is given by processes of the humanization (care,
socio-relational and affective aspects, in those who had gentle handling, skin to skin, minimal manipulation,
neurological outcomes. etc.), which from several years are applied in the De-
Regarding the emotional aspect, that includes the basic partments of Neonatology and Neonatal Intensive
emotions (fear, anxiety, agitation, joy), analyzed through Care, especially with the NIDCAP (Newborn Individ-
various questionnaires, may be say that all these emo- ualized Developmental Care and Assessment
tions are enclosed in a sort of emotional container Program) [18, 19], method which, beyond the
whose space and whose form are shaped by the relation- stabilization of the vital functions and of the health
ship with the mother, who represents the first emotion- services, certainly of priority importance, supports
ally charged relationship. While in the normal the relational needs of the newborn and of his par-
conditions the newborn can immediately benefit from ents and encourages their affective link, using appro-
the maternal containment function, in cases where the priately the technology resources and reducing the
baby is prematurely separated from the reference figure inconveniences and the disadvantages associated with
(pre-term birth and/or neurological risk at birth, which the hospitalization [19, 20].
implies the hospitalization), he is alone to manage his
emotional states and to trace the boundaries of his in-
ternal world, often in a labile and dysfunctional way. Conclusions
This problem, as shown by our study, has repercus- From our research on a population of individuals
sions on the structuring of personal identity. born at neurological risk, it emerges that few neuro-
Also the post-natal emotional stress of the parents logical outcomes have been found in these subjects
may be associated with the behavioral disturbances and and that their quality of life, evaluated at a distance
the cognitive development of the child, together with from the birth, is in average discreet, better in term
other factors related to familiarity, both of a hereditary borns.
nature and of an educational peculiarity [17]. As it was logical to expect, a low quality of life has
What we have found in the sample is the difficulty to been demonstrated, especially in the social-relational
manage the emotions and to face up to the frustrations and affective aspects, in those who had neurological
and anxieties. Since the interpersonal relationships outcomes.

Table 6 HU13 (Health Utilities Index Mark3) (15-17 years)

Quantitative variables: median (1 and 3 quartile) Term (n. 47) Preterm (n. 36) p
Wilcoxon test
impact of auditory, visual, linguistic capacity 1 (0.93–1) 0.85 (0.78–0.93) < 0.0001
impact of motor capacity 1 (1–1) 0.75 (0.5–1) < 0.0001
impact of emotional capacity 1 (1–1) 0.75 (0.5–1) < 0.0001
impact of cognitive capacity 1 (1–1) 1 (0.95–1) 0.05
perception of pain 1 (0.75–1) 1 (0.75–1) < 0.0001
Total score (0–1) 0.96 (0.96–1) 0.91 (0.87–0.93) < 0.0001
Gasparrini et al. Italian Journal of Pediatrics (2019) 45:38 Page 7 of 8

Table 7 Euro Quality 5 Dimensions and visuo-analogue (18-32 years)

Quantitative variables: median (1 and 3 quartile) Term (n. 183) Preterm (n. 265) p
Wilcoxon test
impact of motor capacity 1 (1–1) 1 (1–1) 0.41
self-care 1 (1–1) 1 (1–1) 0.41
pain/discomfort 1 (0.6–1) 1 (0.4–1) < 0.0001
anxiety and depression 1 (0.3–1) 1 (0.6–1) < 0.0001
VAS (0–100) 88 (83–95) 85 (80–96.7) 0.24

The good results obtained are undoubtedly to be at- the Italian law (Legislative Decree of 30 June 2003, n. 196. Code on the
tributed largely to the quality and timeliness of the ob- protection of personal data).

stetric and neonatal care, to the precociousness of

habilitation physiotherapy and to the collaboration with Consent for publication
Non applicable.
the family, as well as to the humanization processes.
Since it has been shown that the humanization is a
Competing interests
model of care that takes into account the relational The authors declare that they have no competing interests.
needs of the newborn and of the parents and
strengthens their link, the psycho-physical development
of the child and increases the effectiveness of the care, Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in
we hope that these processes are always improved and published maps and institutional affiliations.
applied in every part of the world, along with an increas-
ing focus on the observation of the clinical performance Author details
1
Department of Pediatrics and Neonatology - Hospital of Macerata, Macerata,
and a further improvement of diagnostic and therapeutic Italy. 2Autonomy and Life Rehabilitation Center, Falconara, Italy. 3Department
techniques. of Pediatrics and Neonatology - Hospital of Jesi, Jesi, Italy.
Equally important is to follow the growth path of those
Received: 6 November 2018 Accepted: 4 March 2019
born at risk in its psycho-neuro-evolutionary and auxo-
logical aspects by collaborating with their families; not
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