Access to this full-text is provided by Springer Nature.
Content available from BMC Pediatrics
This content is subject to copyright. Terms and conditions apply.
R E S E A R C H A R T I C L E Open Access
Cerebral palsy in Moldova: subtypes,
severity and associated impairments
Ecaterina Gincota Bufteac
1,2*
, Guro L. Andersen
3,4
, Vik Torstein
4
and Reidun Jahnsen
5
Abstract
Background: Moldova is ranked as one of the countries in Europe with the lowest income per capita and with a
relatively high infant and maternal mortality rate. Information on neurodisabilities in general is limited, and
regarding cerebral palsy (CP) in particular, it is completely lacking. The aim of this study was therefore to make a
crude estimate of the prevalence of CP and to describe subtypes and the severity of motor impairments and
associated problems in this country.
Methods: Children with CP born 2009–2010, attending the National Hospital Institute of Mother and Child, the
reference hospital for ~ 75% of children in Moldova with neurological disabilities, were identified from medical
records.
Results: Among 207 children with CP (estimated prevalence 3.4 per 1000 live births), 185 (mean age 7.3 years; 36%
girls) had detailed information. Thirty seven (20%) children had spastic unilateral, 113 (61%) spastic bilateral, 22
(12%) dyskinetic and 9 (5%) children had ataxic CP. The subtype was unclassified in four children. Among all
children, 93 (51%) had epilepsy, 109 (59%) intellectual disability, 42 (23%) severe vision and 10 (5%) hearing
impairments while 84 (45%) children had severe speech impairments. Fifty-two (28%) children were born
prematurely, and 46 (25%) had Apgar scores below 7 at five minutes.
Conclusion: Compared to other European studies, the distribution of CP subtypes was different in Moldova.
Moreover, the estimated prevalence, the proportions with severe motor and associated impairments and of
children born at term were higher in Moldova while the proportion with low Apgar did not differ. The findings may
suggest different etiological pathways causing CP in Moldova than in other European countries. A national register
is warranted for quality assurance and improvement.
Keywords: Cerebral palsy, Moldova, Epidemiology, Subtype, Severity
Background
Cerebral palsy (CP) describes a group of permanent disor-
ders of the development of movement and posture, causing
activity limitations that are attributed to non-progressive
disturbances occurring in the developing foetal or infant
brain. The motor impairments are often accompanied by
disturbances of sensation, perception, cognition, communi-
cation, and behaviour, by epilepsy and by secondary muscu-
loskeletal problems [1].
Considering the significant differences in perinatal and
infant mortality between high- and low-income countries,
it may seem paradoxical that the prevalence of CP has
been reported to be similar, at around 2–3 per 1000 live
births both in developing countries [2,3] and in developed
countries [4,5]. However, the clinical manifestations of
CP differ significantly between low- and high income
countries [3,6,7], and some studies have reported that
perinatal asphyxia and hyperbilirubinaemia are more com-
mon causes in developing countries [2,3,7] . In studies
describing the panorama of CP, ascertainment of cases is a
challenge even in developed countries [5]. In this regard,
it is noteworthy that other studies in developing countries
have reported CP prevalence between 3.4 and 4.5 per
1000 live births [3,7].
* Correspondence: kbufteac@gmail.com;s307865@hioa.no;voinicel@usmf.md
1
Department of Health Sciences, Oslo Metropolitan University, PO box 4 St.
Olavs plass, No-0130 Oslo, Norway
2
Early Intervention Center ‘Voinicel’, Drumul Taberei str., nr.2A, Chisinau,
Moldova
Full list of author information is available at the end of the article
© The Author(s). 2018 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.
Gincota Bufteac et al. BMC Pediatrics (2018) 18:332
https://doi.org/10.1186/s12887-018-1305-6
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
Moldova is ranked as the country in Europe with the
lowest gross domestic product (GDP) i per capita, esti-
mated to around USD 5700 in 2017, compared with an
average of USD 40000 for the European Union. Thus, fi-
nancial resources for advanced medical care are limited,
even if the proportion of the GDP spent for health ex-
penditures (10%) is comparable to the proportion spent
by the Nordic countries. These limited financial re-
sources are a likely explanation of the high maternal
mortality rate of 23 deaths per 100,000 live births; five to
six times higher than in the Nordic countries, and of the
infant mortality rate of 12 deaths per 1000 live births,
being more than twice as high as in the Nordic countries
(9). The prevalence of CP and distribution of CP sub-
types, motor impairments and associated problems is
unknown, and access to orthopaedic surgery as well as
to modern treatment, such as Botulinum toxin injections
are very limited (personal observation) [8,9].
Thus, the aim of this study is to describe the pano-
rama of CP in Moldova with emphasis on CP subtypes,
the severity of the motor impairments and the occur-
rence of associated impairments, as well as how these
clinical characteristics relate to perinatal risk factors.
Methods
Design and study population
Eligible for inclusion in this cross-sectional study were
children with CP treated at the National Hospital Institute
of Mother and Child, in Chisinau, Moldova, born between
January 1st 2009 and December 31st 2010. This hospital is
the reference hospital for children with disabilities living
outside the Capital area, covering approximately 2.7
million (75%) of Moldova’s 3.5 mill inhabitants. Acquired
CP lesions after the neonatal period were excluded. Chil-
dren with neurological impairments are referred to this
hospital every six months for examination and treatment.
Children diagnosed with CP were identified by the first
author via medical records from the Departments of
child neurology (3–18 years) and of toddler neurology
(3 months to 3 years). The data were collected between
June and September 2016, when the children were 7–
8 years old. Detailed information regarding neurological
status, motor function and associated impairments was
identified by scrutinizing the medical records of each
child from several departments. Antenatal and perinatal
information was collected from the medical records at
the Maternity ward, and at the Departments of neonatal
care, premature birth and from the Neonatal Intensive
Care Unit (NICU).
Variables
CP was diagnosed and classified consistent with the rec-
ommendations proposed by the Surveillance of Cerebral
Palsy in Europe (SCPE) [10] into spastic, dyskinetic,
ataxic and not classified subtypes. The spastic subtype
was sub-classified into unilateral and bilateral subtypes,
spastic unilateral CP into right and left hemiplegia, and
spastic bilateral CP into quadriplegia and diplegia in ac-
cordance with the International Classification of Disease
10 (ICD 10) [11].
Gross motor function was classified according to the
Gross Motor Function Classification System (GMFCS)
[12] using the available information on walking and sit-
ting abilities. Fine motor function was classified accord-
ing to the Bimanual Fine Motor Function (BFMF) scale
using the available information on hand function [13].
As the data were collected from medical records of vari-
able quality, the children’s gross motor function was cat-
egorized into those who were able to walk without
assistive devices (corresponding to GMFCS level I and
II), those who were able to walk with assistive devices
corresponding to (GMFCS level III) and those who were
unable to walk even with such devices (corresponding to
GMFCS levels IV-V).
Fine motor function is described by speech therapists
in the free text of medical records. Based upon these de-
scriptions, fine motor function was classified according
to BFMF, as proposed by Andersen et al. [4]. As for
GMFCS, the BFMF classification was reduced to three
categories; i.e. BFMF level I-II, BFMF level III and BFMF
levels IV-V [4].
Associated impairments
Speech therapists tested cognitive abilities in the hospital
and described speech and feeding abilities in free text in
the medical records.
Cognitive function was assessed using the Development
Assessment of Young Children Evaluation tool (DAYC)
and classified into intellectual disability (intelligence quo-
tient (IQ) score < 70) and normal intellectual ability (IQ
score ≥70) [14].
Speech was classified on a five-level scale from zero to
four, where zero indicated normal speech, level I indicated
indistinct speech, level II obviously indistinct speech, level
III severely indistinct speech (difficult to understand) and
level IV indicated children with no speech.
Feeding ability was classified into five levels, 0 indicat-
ing that the child did not have feeding problems, level I
indicating that the child was in need of some assistance,
level II that the child was entirely dependent on assist-
ance, level III that the child was partly tube fed and level
IV that the child was mainly tube fed. No information
on gastrostomy was recorded. The five levels were then
dichotomised into two categories: independent feeding
and dependent on caregiver assistance.
Vision was described as 0 for normal, 1 for impaired
and 2 for severely impaired [10], and later dichotomised
Gincota Bufteac et al. BMC Pediatrics (2018) 18:332 Page 2 of 9
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
into 0 (0–1 normal or impaired) and 1 (2 severely
impaired).
Hearing was described as 0 for normal, 1 for impaired
and 2 for severely impaired, and later dichotomized into 0
(0–1 normal or impaired) and 1 (2 for severely impaired).
Epilepsy was defined as two unprovoked seizures, ex-
cluding neonatal and febrile seizures. Epilepsy was con-
sidered active if the child used antiepileptic drugs at the
time of the registration.
Perinatal data
Available perinatal data included gestational age (GA),
birth weight (BW) and Apgar scores at one and five mi-
nutes. Gestational age at birth is usually estimated from
ultrasonography at GA week 18–22. In this study, GA
was categorized into extremely low (ELGA < week 28,
very low (VLGA: GA week 28 (28.0) to < 32 (31 weeks;
six days), moderately low (MLGA: GA week 32 (32.0) to
37 (36 weeks, six days) and term-born (GA week 37.0 or
later). Birth weight was recorded to the nearest gram (g)
and was categorized as extremely low (ELBW < 1000 g);
very low (VLBW: 1000–1499 g); moderately low
(MLBW: 1500–2499 g) and normal (BW > 2500 g).
Apgar scores at one and five minutes were categorized
into three categories: 0–3, 4–6 and 7–10.
Statistical methods
The Statistical Package for Social Sciences (IBM SPSS
V.19) was used for data analysis, and a significance level of
0.05 was chosen. Descriptive statistics with frequency ta-
bles were performed to show proportions of subtypes and
CP severity levels, and the proportion of children with as-
sociated impairments. Differences in proportions were
evaluated using Chi-square statistics, and p-values < 0.05
were considered statistically significant.
Ethics
The study was approved by the National Committee for
Ethical Expertise in Clinical Trials (Nr. 266) and by the
Centre of Early Intervention ‘Voinicel’Ethical Commit-
tee (nr. 01/17). A statement of Agreement of Collabor-
ation between the State Medical and Pharmacy
University and the Institute of Mother and Child was
signed, and finally, permission to conduct the study was
obtained from the Ministry of Health (12th of July, nr.
08/88), from the Municipality Council of Social Protec-
tion, (13.07.2016, nr. 070117/957) and from the Ministry
of Labour, Social Protection and Family of the Republic
of Moldova.
Permission to access the children’s data was obtained
from the Republican Ethics Committee, The State Med-
ical and Pharmacy Ethics Committee, Ministry of Health
and Ministry of Labour and Social Protection and the
Directors of the Main Hospital for Children in RM- In-
stitute of Mother and Child.
Parents or primary caregivers of patients treated at this
centre sign an informed consent form stating that med-
ical data collected as part of the admission may be used
for research purposes. The use of this regularly collected
medical information in the present study was approved
as described above and did not require a new individual
consent form to be completed.
Results
In all, 207 children with CP were identified. The total
number of live births during 2009 and 2010 in Moldova
was 81,277, and a crude estimate of CP prevalence
would be 3.4 per 1000 live births if the children in this
study were recruited from 75% of the birth population.
Of the 207 children, 22 had incomplete data. Thus, the
study population comprised 185 children with a mean
age of 7.3 years (range: 6.6–7.6 years) and 67 (36%) of
these were girls. Thirty-seven children (20%) had spastic
unilateral, 113 (61%) had spastic bilateral, 22 (12%) had
dyskinetic and nine (5%) had ataxic CP. In four children
(2%), the subtype could not be classified. Mean age at
diagnosis was 23 months (range: 12-91 months). Among
children with unilateral spastic CP, the extremities of the
right side were affected in 21 (57%) and on the left side
in 16 (43%) (p= 0.502). Among those with spastic bilat-
eral CP, 19 (17%) had diplegic, while 94 (83%) had
quadriplegic CP (p= 0.001).
Table 1shows that 60 (31%) children were able to walk
independently (GMFCS level I-II), 53 children (33%)
were able to walk with assistive devices (GMFCS level
III) and the remaining 72 (36%) children were unable to
walk (GMFCS level IV-V) (p= 0.001). Table 1also shows
that 73 (40%) of the children had hand function corre-
sponding to BFMF level I or II, 47 (24%) had BFMF level
III and 65 (36%) had hand function corresponding to
level IV or V (p= 0.001). Children with unilateral CP
had better gross and fine motor function compared to
children with bilateral and dyskinetic CP (p= 0.001)
(Table 1).
Associated impairments
Table 1shows that 109 (59%) children had an intellec-
tual disability. In total, 42 (23%) had severe visual and
ten (5%) severe hearing impairment, 93 (50%) had active
epilepsy, 84 (45%) had severely impaired speech or no
speech and 80 (43%) children were unable to eat inde-
pendently (p= 0.001). Ten (5%) of the 185 children with
CP were severely affected by all of these impairments.
Table 1also shows that associated impairments were
most prevalent among children with dyskinetic and
spastic bilateral CP subtypes (p= 0.001), while they were
least prevalent among children with unilateral CP (p=
Gincota Bufteac et al. BMC Pediatrics (2018) 18:332 Page 3 of 9
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
0.041). Among children with unilateral CP, there were
no significant differences in the prevalence of associated
impairments between children with right- or left-sided
affection (p> 0.056). All ten children who were severely
affected by all associated impairments had the spastic bi-
lateral subtype. None of the 84 children with severe
speech impairment communicated with the help of aug-
mentative or alternative communication aids (i.e. pic-
tures or pictograms). The proportion of children without
any associated impairments in this study was 11%.
Perinatal risk factors
In total, 133 (72%) children with CP were born at
term, whereas 10 (5%) were born ELGA. Among chil-
dren born at term and preterm, the most common
subtype was spastic bilateral CP, accounting for 54%
and 79%, respectively (Table 2). Only one of 23
children born before GA week 32 was able to walk
without assistive devices (GMFCS level I-II), com-
pared to 11 (38%) children born moderately preterm,
and 48 (36%) children born at term (p=0.023). Five
(22%) of the 23 children born before week 32 had
good hand function (BFMF I-II); however, this pro-
portion was lower when compared to those born at
term, 54 (41%) of 133 children born ≥37 weeks had
good hand function (p< 0.001) (Table 3).
Table 4shows that epilepsy was present in a higher
proportion of children born at term compared to those
born preterm, while intellectual disability, severe vision
and hearing impairments were more prevalent in chil-
dren born before GA 28 weeks compared to those born
at term (p= 0.024).
A total of 130 (70%) children had normal BW, and six
(3%) had BW < 1000 g. Among children with normal
Table 1 Subtypes, severity and associated impairments in a cohort of 185 children with CP
CP subtypes
Unilateral N (%) Bilateral N (%) Dyskinetic N (%) Ataxic N (%) Not classified N (%) Total N (%) P-value of totals
GMFCS levels
Level I-II 33 (89) 21 (19) 0 5 (56) 1 (25) 60 (33)
Level III 4 (11) 39 (35) 4 (18) 4 (44) 2 (50) 53 (29)
Level IV-V 0 53 (28) 18 (82) 0 1 (25) 72 (38) < 0.001
BFMF levels
Level I-II 33 (91) 35 (31) 0 4 (44) 1 (25) 73 (40)
Level III 4 (10) 32 (28) 4 (18) 5 (56) 2 (50) 47 (24)
Level IV-V 0 46 (41) 18 (82) 0 1 (25) 65 (36) < 0.001
Intellectual disability
No 31 (84) 39 (35) 2 (9) 3 (34) 1 (25) 76 (41)
Yes 6 (16) 74 (66) 20 (91) 6 (67) 3 (75) 109 (59) 0.001
Active epilepsy
No 29 (78) 48 (43) 8 (36) 3 (33) 4 (100) 92 (49)
Yes 8 (22) 65 (58) 14 (64) 6 (67) 0 93 (51) < 0.001
Vision
Normal/impaired 34 (92) 80 (71) 19 (86) 7 (78) 3 (75) 143 (77)
Severely impaired 3 (8) 33 (29) 3 (14) 2 (22) 1 (25) 42 (23) 0.054
Hearing
Normal/impaired 37 (100) 104 (92) 21 (96) 9 (100) 4 (100) 175 (95)
Severely impaired 0 9 (8) 1 (5) 0 0 10 (5) 0.143
Speech impairments
Normal 11 (30) 8 (7) 1 (5) 0 0 20 (11)
Impaired, understandable 25 (68) 43 (38) 7 (32) 5 (56) 1 (25) 81 (44)
Severely impaired/no speech 1 (3) 62 (55) 14 (64) 4 (44) 3 (75) 84 (45) < 0.001
Feeding
Independent 34 (92) 56 (49) 8 (36) 5 (56) 2 (50) 105 (57)
Dependent 3 (8) 57 (51) 14 (64) 4 (44) 2 (50) 80 (43) < 0.001
Total 37 (100) 113 (100) 22 (100) 9 (100) 4 (100) 185 (100)
Gincota Bufteac et al. BMC Pediatrics (2018) 18:332 Page 4 of 9
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
BW, the most common CP subtype was spastic bilateral,
72 (64%) (p< 0.001) (Table 2).
Finally, 79 (43%) children had a low Apgar score (0–3
and 4–6) at one and 46 (25%) at five minutes (Table 3).
Low Apgar scores were associated with more severe im-
pairments of gross and fine motor function (p= 0.029)
and with spastic bilateral and dyskinetic CP (p= 0.057)
(Table 3).
Discussion
In this first study of the panorama of CP in Moldova we
found a crude prevalence estimate of 3.4 per 1000 live
births and that spastic bilateral CP was the most com-
mon subtype, accounting for nearly two-thirds of all
cases in this population of children. Only every fifth
child had the spastic unilateral CP subtype, and only one
third could walk without an assistive device. Most of the
children had significantly impaired fine motor function,
and associated problems were common. Almost half of
the children had barely understandable or no speech
and a concern is that none of them used assisted or aug-
mented communication. Only 28% of the children were
born prematurely, and around 10% of the children were
born at GA below 32 weeks, or with BW below 1500 g.
Every fourth child had Apgar scores below 7 at five
minutes.
Validity
Strengths and limitations
The strength of the study is the hospital-based cohort
from the main paediatric hospital of Moldova Institute
of Mother and Child. As this hospital cares for all chil-
dren living outside the Municipality of Chisinau, the co-
hort may be considered population-based and
representative of 75% of the population of Moldova. The
regular assessment of the children provided high-quality
clinical information that could be systematised. The
mean age of the children when the study was performed
was 7.3 years old, which represents a strength regarding
the validity of the CP diagnosis [9,15]. Access to a var-
iety of medical records also ensured ascertainment of
the cases. Nonetheless, we cannot exclude that some
children with milder forms of CP (for example, some
children with unilateral spastic CP with GMFCS and
BFMF level I), were not referred to this central hospital.
Such selection bias could, therefore, have contributed
somewhat to the low proportion of children with the
unilateral CP subtype and the high proportion of chil-
dren with severe motor impairments and associated
problems. In contrast, the crude estimate of prevalence
was high, and even in the most unlikely event that the
cases included in this study would represent all children
with CP in Moldova, the prevalence would be 2.5 per
1000 live births. The latter figure would still be high
Table 2 Children with different CP subtypes by gestational age (GA), birth weight (BW) and Apgar score
CP subtypes
Unilateral N (%) Bilateral N (%) Dyskinetic N (%) Ataxic N (%) Not classified N (%) Total N (%) P-value of totals
GA
GA < 28 weeks 1 (3) 7 (6) 1 (5) 0 1 (25) 10 (5)
GA 28–31 weeks 0 11 (10) 0 1 (11) 0 12 (7)
GA 32–36 weeks 4 (11) 23 (20) 2 (9) 1 (11) 0 30 (16)
GA ≥37 weeks 32 (86) 72 (64) 19 (86) 7 (78) 3 (75) 133 (72) 0.002
BW
BW < 1000 g 0 6 (5) 0 0 0 6 (3)
BW 1000-1499 g 1 (3) 8 (7) 1 (5) 0 1 (25) 11 (6)
BW 1500-2499 g 5 (14) 27 (24) 4 (18) 1 (11) 1 (25) 38 (21)
BW ≥2500 g 31 (83) 72 (64) 17 (77) 8 (89) 2 (50) 130 (70) 0.054
Apgar (1 min)
Apgar 0–3 1 (3) 19 (17) 1 (5) 1 (11) 1 (25) 23 (12)
Apgar 4–6 8 (22) 40 (35) 5 (23) 2 (22) 1 (25) 56 (30)
Apgar 7–10 28 (75) 54 (48) 16 (72) 6 (67) 2 (50) 106 (58) 0.057
Apgar (5 min)
Apgar 0–3 1 (3) 7 (6) 2 (9) 1 (11) 0 11 (6)
Apgar 4–6 1 (3) 30 (27) 2 (9) 0 2 (50) 35 (19)
Apgar 7–10 35 (94) 76 (67) 18 (82) 8 (89) 2 (50) 139 (75) 0.044
Total 37 (100) 113 (100) 22 (100) 9 (100) 4 (100) 185 (100)
Gincota Bufteac et al. BMC Pediatrics (2018) 18:332 Page 5 of 9
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
compared with other European countries [5,16,19].Thus,
we consider it unlikely that the main findings and conclu-
sions in this study can be completely explained by selec-
tion bias.
Another limitation is that the classification of gross
and fine motor function (GMFCS and BFMF) was made
in retrospect, based upon text descriptions in the med-
ical records. However, the main criterion in the classifi-
cation of GMFCS is the ability to walk with or without
assistive devices or not at all. Therefore, we believe that
misclassification of GMFCS is unlikely to explain the re-
sults regarding gross motor function. The classification
of fine motor function (BFMF) according to Andersen et
al. [4] is more complicated. Interestingly, the proportion
of children with severely impaired fine motor function
in this study is about the same as Andersen et al. [4].
However, it should be noted that fine motor function
was found to be more impaired in Norway compared to
other populations at that time. Thus, the findings for
fine motor function in this study should be interpreted
with caution. Assessments of cognitive abilities, speech
and feeding were performed by experienced speech ther-
apists, mostly using validated instruments, which is a
strength of this study.
Comparison with the literature
In the present study the distribution of spastic and
non-spastic CP subtypes is comparable to other studies
in Europe [4,16].
However, the proportion of children with unilateral
spastic CP is lower, while spastic bilateral (particularly
quadriplegic CP) and dyskinetic forms were higher in
our study compared to several studies in Europe and
Australia [4,16–18].
Among term born children, the proportion with dyski-
netic CP in our study (12%) was lower compared with
Himmelmann et al. (23%) [19], but higher than in two
other studies [4,19]. The percentage of children with
the ataxic subtype is similar to other studies [4].
The distribution of CP subtypes among children born
preterm in this study was comparable to the distribution
reported by Himpens et al. [16] in their metanalysis of
studies including children born later than 1980.
An important finding is that the proportion of chil-
dren who were able to walk independently (33%) was
lower in the present study than in a Norwegian study
(55%), Andersen et al. [4], and in the majority of the
studies included in the meta-analysis by Himpens et
al. [16].
Table 3 Severity of gross and fine motor impairments in children with CP by gestational age (GA), birth weight (BW) and Apgar
score
Estimated GMFCS Estimated BFMF
I-II N (%) III N (%) IV-V N (%) Total N (%) I-II N (%) III N (%) IV-V N (%) Total N (%)
GA
GA < 28 weeks 1 (2) 5 (9) 5 (7) 11 (6) 4 (6) 3 (6) 4 (6) 11 (6)
GA 28–31 weeks 0 7 (13) 5 (7) 12 (7) 1 (1) 7 (15) 4 (6) 12 (7)
GA 32–36 weeks 11 (18) 11 (21) 7 (10) 29 (15) 14 (19) 9 (19) 6 (10) 29 (15)
GA > 37 weeks 48 (80) 30 (57) 55 (76) 133 (72) 54 (74) 28 (60) 51 (78) 133 (72)
BW
BW < 1000 g 1 (2) 3 (6) 2 (3) 6 (3) 3 (4) 1 (1) 2 (3) 6 (3)
BW 1000-1499 g 2 (3) 4 (7) 5 (7) 11 (6) 3 (4) 4 (9) 4 (6) 11 (6)
BW 1500-2499 g 10 (17) 12 (23) 16 (22) 38 (21) 12 (17) 13 (28) 13 (20) 38 (21)
BW > 2500 g 47 (78) 34 (64) 49 (68) 130 (70) 55 (75) 29 (62) 46 (71) 130 (70)
Apgar (1 min)
Apgar 0–3 1 (1) 7 (13) 15 (21) 23 (13) 3 (5) 7 (15) 13 (20) 23 (13)
Apgar 4–6 16 (27) 16 (30) 24 (33) 56 (30) 20 (27) 16 (34) 20 (31) 56 (30)
Apgar 7–10 43 (72) 30 (57) 33 (46) 106 (57) 50 (68) 24 (51) 32 (49) 106 (57)
Apgar (5 min)
Apgar 0–3 1 (2) 3 (5) 7 (10) 11 (6) 1 (2) 4 (9) 6 (9) 11 (6)
Apgar 4–6 6 (10) 11 (21) 18 (25) 35 (19) 9 (12) 10 (21) 16 (25) 35 (19)
Apgar 7–10 53 (88) 39 (74) 47 (65) 139 (75) 63 (86) 33 (70) 43 (66) 139 (75)
Total 60 (100) 53 (100) 72 (100) 185 (100) 73 (100) 47 (100) 65 (100) 185 (100)
GMFCS Gross Motor Function Classification System estimated from descriptions of walking and sitting abilities
BFMF Bimanual Fine Motor Function estimated from descriptions of hand function in each hand separately
P-value GMFCS/GA,BW,Apgar 1,5 min < 0.002
Gincota Bufteac et al. BMC Pediatrics (2018) 18:332 Page 6 of 9
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
The proportion of children without any associated im-
pairments was 11% in this study compared to 28% in
Norway [4] and 48% in Sweden [19]. However, the latter
study did not include speech impairments [19]. When
we excluded speech impairments, we found that 35% of
the Moldovan children with CP had no associated im-
pairments (Table 4), which is comparable to results from
Norway (34%) [4], but lower than in Sweden and
Deutschland [19,20].
The proportion of children with severely impaired
or no speech in our study was higher than in a Nor-
wegian study [4]. This finding is reasonable, consider-
ing the low proportion of children with unilateral
spastic CP, and the high proportion of children with
severe gross motor impairments (GMFCS level IV-V)
in our study. However, it is concerning that none of
the children with severely impaired speech had any
form of assisted or alternative communication (ASC).
This finding may be partially consistent with one
study in Norway reporting that approximately 50% of
children in need of such communication did not use
ASC [21].
The proportions of children born prematurely, and
born before week 28 were lower in Moldova than in two
Nordic studies [4,19]. This may be partly explained by
lower proportions in the background population (0.27%
in Moldova versus 0.4% in Norway) [22], but more likely
by differences in perinatal and neonatal mortality. The
majority of children with CP were born at term, consist-
ent with most other studies.
Despite the higher proportions of children born at
term and with quadriplegic and dyskinetic CP in this
study, the proportion with low Apgar scores was similar
to that reported by Andersen et al. [4] and Himmelmann
et al. [19].
The most severe gross and fine motor impairments were
associated with low Apgar scores. Moreover, children born
with normal BW had more severe motor impairments in
comparison with children with low BW (≤2500 g). These
findings are consistent with another study conducted in
Moldova between 2008 and 2014 [23].
Interpretation and implications
The lower proportion of children with unilateral CP in
this study, as well as the lower proportion of children able
to walk independently (GMFCS level I-II) could partly be
explained by selection bias. It is possible that families liv-
ing in the most rural areas of Moldova who have a child
with mild unilateral CP are less likely to apply for or be re-
ferred to follow-up at the Institute of Mother and Child.
However, if there are cases missing, the prevalence of CP
must be significantly higher than our estimate. Thus, one
implication of this study is that there is a need to establish
national high-quality health registers in general, and CP
Table 4 Associated impairments by gestational age (GA) in children with CP
GA < 28 N (%) GA 28–31 N (%) GA 32–36 N (%) GA > 37 N (%) Total N (%) P-value of totals
Intellectual disability
No (> 70) 3 (30) 4 (33) 14 (47) 55 (41) 76 (41)
Yes (< 70) 7 (70) 8 (67) 16 (53) 78 (59) 109 (59) 0.553
Active epilepsy
No 8 (80) 7 (58) 19 (63) 58 (44) 92 (49)
Yes 2 (20) 5 (42) 11 (37) 75 (56) 93 (51) 0.008
Vision
Normal/impaired 6 (60) 9 (75) 24 (80) 104 (78) 143 (77)
Severely impaired 4 (40) 3 (25) 6 (20) 29 (22) 42 (23) 0.303
Hearing
Normal/impaired 9 (90) 12 (100) 30 (100) 124 (93) 175 (95)
Severely impaired 1 (10) 0 0 9 (7) 10 (5) 0.552
Speech Impairments
Normal 1 (10) 0 4 (13) 15 (11) 20 (11)
Impaired, understandable 4 (40) 7 (58) 15 (50) 55 (41) 81 (44)
Severely impaired/No speech 5 (50) 5 (42) 11 (37) 63 (48) 84 (45) 0.994
Feeding
Independent 7 (70) 6 (50) 20 (67) 72 (54) 105 (57)
Dependent 3 (30) 6 (50) 10 (33) 61 (46) 80 (43) 0.347
Total 10 (100) 12 (100) 30 (100) 133 (100) 185 (100)
GA Gestational Age (weeks) in categories (< 28 weeks of gestation, 28–31 weeks, 32–36 weeks and > 37 weeks of gestation)
Gincota Bufteac et al. BMC Pediatrics (2018) 18:332 Page 7 of 9
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
registers in particular, in Moldova. This is of the utmost
importance to provide health authorities with correct in-
formation regarding the prevalence and need for interven-
tions but also to monitor ante- and perinatal health.
Notably, a very recent Norwegian study documented the
need for access to several health registers to ensure
complete identification of cases [5].
However, although selection bias may partly explain
the low proportion of children with unilateral CP, we
consider it less likely to be the main explanation of the
difference in CP subtypes between Moldova and other
European studies. First, the crude estimate of prevalence
is higher than in other studies, which makes it unlikely
that there has been a significant underreporting of cases.
Secondly, within the group of children with bilateral CP,
the proportion with quadriplegic CP was very high, and
finally, within the group with bilateral CP, the proportion
able to walk independently was lower in our than in
other populations, Thus, another interpretation may be
related to obstetric and perinatal care. The increased
maternal and infant mortality rates in Moldova com-
pared to Norway, Sweden and Iceland, are most likely
also reflected in higher perinatal and neonatal mortality
rates. The high proportion of children with more severe
manifestations of CP in Moldova may, therefore, also be
explained by less advanced obstetric and neonatal care
in Moldova than in Nordic countries. Both the spastic
quadriplegic and dyskinetic CP subtypes are common in
deliveries complicated by hypoxia-ischemia [24]. How-
ever, low Apgar scores were not more common in this
study than in other studies. Therefore the higher propor-
tion of children with quadriplegic and dyskinetic CP
may have other causes, such as increased prevalence of
pre-pregnancy or pregnancy related maternal disorders,
congenital anomalies [25,26], perinatal infections or pla-
cental disorders. The low proportion of children born
before week 28 could, in part, be explained by different
attitudes and limited access to advanced neonatal inten-
sive care in Moldova. Thus, the other implication of this
study is that there is a need to explore whether obstetric
and neonatal care in Moldova may need to be further
improved to achieve results comparable to other Euro-
pean countries.
Finally, this study has revealed that standard classifica-
tion systems like GMFCS and BFMF, as well as motor
function assessment tools, such as Gross Motor Func-
tion Measurement (version 66 or 88) [12], are not clinic-
ally used on a regular basis. Moreover, assisted or
augmented communication was apparently not used by
children with speech problem. One implication of these
results will, therefore, be to establish a collaborative net-
work with specialists from the rehabilitation centres
throughout the country in order to improve the quality
of care for children with CP in Moldova.
Conclusion
Compared to other populations, children with CP in
Moldova more frequently present with bilateral and dys-
kinetic subtypes. In addition, severe gross motor impair-
ments and associated problems are also more common
in Moldova. Our findings suggest a higher prevalence of
CP, and the causal pathways may be different in
Moldova relative to other European countries. Children
with milder CP symptoms may be less likely to receive
specialist care. These findings suggest a need for a na-
tional health quality register [27], and provide a basis to
improve the quality of perinatal medicine and care for
children with CP.
Abbreviations
BFMF: Bimanual fine motor function; BW: Birth weight; CP: Cerebral palsy;
GA: Gestational age; GDP: Gross domestic product; GMFCS: Gross motor
function classification system; IQ: Intellectual quotient; SCPE: Surveillance of
Cerebral Palsy in Europe; USD: United States dollars
Acknowledgements
We would like to express our thanks to the Ministry of Health and
administrative staff of the ‘Institute of Mother and Child’Chisinau, Moldova,
for providing access to the medical records saved in the hospital archives.
Funding
This study was supported by a student grant from the Ministry of Foreign
Affairs of Norway and AHEAD-Moldova, Norway, within the PhD program at
Oslo Metropolitan University, Faculty of Health Sciences, Oslo, Norway.
Availability of data and materials
The datasets generated and analysed during the current study are not
publicly available due to the restrictions to share the data to the third
parties, based on the Management Committee of the Institute of Mother
and Child decision -the hospital which provided the data (written permit
from the Director of the hospital, where its specified that its forbidden to
share the data to the third parties), but are available from the corresponding
author on reasonable request.
Authors’contributions
EGB designed the study, extracted and analysed the data, performed the
statistical analyses, participated in drafting and improving the manuscript. RJ,
GA and TV contributed to the design and conceptualization of the study,
provided critical input and oversight of field work, and reviewed the final
manuscript as submitted. All authors approved the final manuscript as
submitted and agree to be accountable for all aspects of the work.
Authors’information
Ecaterina Gincota Bufteac is a medical doctor at Voinicel Early Intervention
Centre in Chisinau, Moldova and PhD candidate at Oslo Metropolitan
University, Norway,
Guro L. Andersen is a pediatrician PhD, leader of the Cerebral Palsy Registry
of Norway (CPRN) at Vestfold Hospital trust and associate professor at
Department of Clinical and Molecular Medicine, Norwegian University of
Science and Technology in Trondheim, Norway.
Vik Torstein is professor of pediatrics at Department of Clinical and Molecular
Medicine, Norwegian University of Science and Technology in Trondheim,
Norway.
Reidun Jahnsen is a physical therapist PhD and senior researcher at Oslo
University Hospital. She is leader of the national CP surveillance program
(CPOP) in Norway.
Ethics approval and consent to participate
The study was approved by the National Committee for Ethical Expertise in
Clinical Trials (Nr. 266) and by the Centre of Early Intervention ‘Voinicel’
Ethical Committee (nr. 01/17). A statement of Agreement of Collaboration
between the State Medical and Pharmacy University and the Institute of
Gincota Bufteac et al. BMC Pediatrics (2018) 18:332 Page 8 of 9
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
Mother and Child was signed, and finally, permission to conduct the study
was obtained from the Ministry of Health (12th of July, nr. 08/88), from the
Municipality Council of Social Protection, (13.07.2016, nr. 070117/957) and
from the Ministry of Labour, Social Protection and Family of the Republic of
Moldova. Permission to access the children’s data was obtained from the
Republican Ethics Committee, The State Medical and Pharmacy Ethics
Committee, Ministry of Health and Ministry of Labour and Social Protection
and the Directors of the Main Hospital for Children in RM- Institute of
Mother and Child.
Consent for publication
not applicable.
Competing interests
The authors declare that they have no competing interests.
Publisher’sNote
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
Author details
1
Department of Health Sciences, Oslo Metropolitan University, PO box 4 St.
Olavs plass, No-0130 Oslo, Norway.
2
Early Intervention Center ‘Voinicel’,
Drumul Taberei str., nr.2A, Chisinau, Moldova.
3
The Cerebral Palsy Register of
Norway (CPRN), Department of Paediatrics, Vestfold Hospital Trust, Tonsberg,
Norway.
4
Department of Clinical and Molecular Medicine, Norwegian
University of Science and Technology, PO Box 8905, 7491 Trondheim,
Norway.
5
The Cerebral Palsy Follow-up Program (CPOP), Department of
Clinical Neurosciences for Children, Oslo University Hospital, Box 4950,
Nydalen, 0424 Oslo, Norway.
Received: 16 March 2018 Accepted: 8 October 2018
References
1. Rosenbaum, P., Paneth, N., Leviton, A., Goldstein, M., Bax, M., Damiano, D., ...
Jacobsson. (2007). A report: the definition and classification of cerebral palsy
April 2006. Dev Med Child Neurol, 49, 8–14. doi:https://doi.org/10.1111/j.
1469-8749.2007.tb12610.x.
2. El-Tallawy HN, Farghaly WM, Shehata GA, Rageh TA, Metwally NA, Badry R,
Kandil MR. Cerebral palsy in Al-Quseir City, Egypt: Prevalence, subtypes, and
risk factors. Neuropsychiatr Dis Treat. 2014;Vol. 10:1267–72.
3. Stanley FJ, Blair E, Alberman E. Cerebral palsies: epidemiology and causal
pathways. London: Cambridge University Press; 2000.
4. Andersen GL, Irgens LM, Haagaas I, Skranes JS, Meberg AE, Vik T. Cerebral
palsy in Norway: prevalence, subtypes and severity. Eur J Paediatr Neurol.
2008;12(1):4–13. https://doi.org/10.1016/j.ejpn.2007.05.001.
5. Hollung SJ, Vik T, Wiik R, Bakken IJ, Andersen GL. Completeness and
correctness of cerebral palsy diagnoses in two health registers: implications
for estimating prevalence. Dev MedChild Neurol. 2017;59(4):402–6. https://
doi.org/10.1111/dmcn.13341.
6. Altonoby A, Tawfek M, Abdelaziem F, Kilany A. Establish registry of cerebral
palsy in Tanta Egypt. International Journal of Therapies & Rehabilitation
Research. 2017;6(2):174–9. https://doi.org/10.5455/ijtrr.000000260.
7. Serdaroglu A, Cansu A, Md SÖ, Tezcan S. Prevalence of cerebral palsy in
Turkish children between the ages of 2 and 16 years. Dev Med Child
Neurol. 2006;48(6):413–6. https://doi.org/10.1111/j.1469-8749.2006.tb01288.x.
8. “The Third Millenium Development Goals Report. Republic of Moldova”,
2013. www.undp.md/publications/Millenium_ROM_small.pdf
9. CIA Fact book. Retrieved from: https://www.cia.gov/library/publications/the-
world-factbook/geos/md.html, August 2018.
10. Surveillance of cerebral palsy in Europe: a collaboration of cerebral palsy
surveys and registers. Surveillance of Cerebral Palsy in Europe (SCPE). Dev
Med Child Neurol. 2000;42(12):816–24.
11. World Health Organisation. International statistical classification of diseases
and related health problems, 10
th
revision (ICD-10). Geneva: World Health
Organisation; 1992.
12. Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B.
Development and reliability of a system to classify gross motor function in
children with cerebral palsy. Devel Med Child Neurol. 1997;39(4):214–23.
https://doi.org/10.1111/j.1469-8749.1997.tb07414.x.
13. Beckung E, Hagberg G. Neuroimpairments, activity limitations, and
participation restrictions in children with cerebral palsy. Developmental
Medicine & Child Neurology. 2002;44(5):309–16. https://doi.org/10.1111/j.
1469-8749.2002.tb00816.x.
14. Simeonsson RJ, Rosenthal SL. Psychological & Developmental Assessment.
Development Assesment of young children (DAYC evaluation), vol. 386.
New York: Guilford Press; 2001. ISBN 1-57230-645-9
15. Cans C, Dolk H, Platt MJ, Colver A, Prasauskiene A, RÄGeloh-Mann IK.
Recommendations from the SCPE collaborative group for defining and
classifying cerebral palsy. Dev Med Child Neurol. 2007;49:35–8. https://doi.
org/10.1111/j.1469-8749.2007.tb12626.x.
16. Himpens E, Van den Broeck C, Oostra A, Calders P, Vanhaesebrouck P.
Prevalence, type, distribution, and severity of cerebral palsy in relation to
gestational age: a meta-analytic review. Dev Med Child Neurol. 2008;50(5):
334–40. https://doi.org/10.1111/j.1469-8749.2008.02047.x.
17. Sellier E, Horber V, KrÄGeloh-Mann I, De La Cruz J, Cans C, On behalf of the,
S. C. Interrater reliability study of cerebral palsy diagnosis, neurological
subtype, and gross motor function. Dev Med Child Neurol. 2012;54(9):815–
21. https://doi.org/10.1111/j.1469-8749.2012.04359.x.
18. Howard, J., Soo, B., Graham, H. K., Boyd, R. N., Reid, S., Lanigan, A., . . .
Reddihough, D. S. (2005). Cerebral palsy in Victoria: motor types,
topography and gross motor function. J Paediatr Child Health, 41(9–10),
479–483. doi:https://doi.org/10.1111/j.1440-1754.2005.00687.x.
19. Himmelmann K, Beckung E, Hagberg G, Uvebrant P. Gross and fine motor
function and accompanying impairments in cerebral palsy. Dev Med Child
Neurol. 2006;48(6):417–23. https://doi.org/10.1017/S0012162206000922.
20. Wichers M, Hilberink S, Roebroeck ME, Stam HJ, van Nieuwenhuizen O.
Motor impairments and activity limitations in children with spastic cerebral
palsy: a Dutch population-based study. J Rehabil Med. 2009;41(5):367–74.
https://doi.org/10.2340/16501977-0339.
21. Andersen G, Mjøen TR, Vik T. Prevalence of speech problems and the use of
augmentative and alternative communication in children with cerebral palsy: a
registry-based study in Norway. Perspectives on Augmentative and Alternative
Communication. 2010;19(1):12. https://doi.org/10.1044/aac19.1.12.
22. National Bureau of Statistics of the Republic of Moldova, statbank.statistica.
md, Annu Rep 2009, 2010.
23. Ala Curteanu, Characteristics of physical development of premature
newborns in the first 2 years of life Retrieved from: https://ibn.idsi.md/sites/
default/files/imag_file/Particularitatile%20dezvoltarii%20fizice%20a%20nou_
nascutilor.pdf
24. Meberg A, Broch H. Etiology of cerebral palsy. In: Journal of Perinatal
Medicine, vol. Vol. 32, pp. 434; 2004.
25. Smithers-Sheedy H. Declining prevalence of cerebral palsy in Europe: good
news? Dev Med Child Neurol. 2016;58(1):14–4. https://doi.org/10.1111/
dmcn.12885.
26. Jystad, K. P., Strand, K. M., Bjellmo, S., Lydersen, S., Klungsöyr, K., Stoknes, M., .
. . Vik, T. (2017). Congenital anomalies and the severity of impairments for
cerebral palsy. Dev Med Child Neurol, 59(11), 1174–1180. doi:https://doi.org/
10.1111/dmcn.13552.
27. Khandaker, G., Van Bang, N., Dũng, T. Q., Giang, N. T. H., Chau, C. M., Van
Anh, N. T., . . . Elliott, E. J. (2017). Protocol for hospital based-surveillance of
cerebral palsy (CP) in Hanoi using the Paediatric active enhanced disease
surveillance mechanism (PAEDS-Vietnam): a study towards developing
hospital-based disease surveillance in Vietnam. BMJ Open, 7(11). e017742
doi:https://doi.org/10.1136/bmjopen-2017-017742.
Gincota Bufteac et al. BMC Pediatrics (2018) 18:332 Page 9 of 9
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
1.
2.
3.
4.
5.
6.
Terms and Conditions
Springer Nature journal content, brought to you courtesy of Springer Nature Customer Service Center GmbH (“Springer Nature”).
Springer Nature supports a reasonable amount of sharing of research papers by authors, subscribers and authorised users (“Users”), for small-
scale personal, non-commercial use provided that all copyright, trade and service marks and other proprietary notices are maintained. By
accessing, sharing, receiving or otherwise using the Springer Nature journal content you agree to these terms of use (“Terms”). For these
purposes, Springer Nature considers academic use (by researchers and students) to be non-commercial.
These Terms are supplementary and will apply in addition to any applicable website terms and conditions, a relevant site licence or a personal
subscription. These Terms will prevail over any conflict or ambiguity with regards to the relevant terms, a site licence or a personal subscription
(to the extent of the conflict or ambiguity only). For Creative Commons-licensed articles, the terms of the Creative Commons license used will
apply.
We collect and use personal data to provide access to the Springer Nature journal content. We may also use these personal data internally within
ResearchGate and Springer Nature and as agreed share it, in an anonymised way, for purposes of tracking, analysis and reporting. We will not
otherwise disclose your personal data outside the ResearchGate or the Springer Nature group of companies unless we have your permission as
detailed in the Privacy Policy.
While Users may use the Springer Nature journal content for small scale, personal non-commercial use, it is important to note that Users may
not:
use such content for the purpose of providing other users with access on a regular or large scale basis or as a means to circumvent access
control;
use such content where to do so would be considered a criminal or statutory offence in any jurisdiction, or gives rise to civil liability, or is
otherwise unlawful;
falsely or misleadingly imply or suggest endorsement, approval , sponsorship, or association unless explicitly agreed to by Springer Nature in
writing;
use bots or other automated methods to access the content or redirect messages
override any security feature or exclusionary protocol; or
share the content in order to create substitute for Springer Nature products or services or a systematic database of Springer Nature journal
content.
In line with the restriction against commercial use, Springer Nature does not permit the creation of a product or service that creates revenue,
royalties, rent or income from our content or its inclusion as part of a paid for service or for other commercial gain. Springer Nature journal
content cannot be used for inter-library loans and librarians may not upload Springer Nature journal content on a large scale into their, or any
other, institutional repository.
These terms of use are reviewed regularly and may be amended at any time. Springer Nature is not obligated to publish any information or
content on this website and may remove it or features or functionality at our sole discretion, at any time with or without notice. Springer Nature
may revoke this licence to you at any time and remove access to any copies of the Springer Nature journal content which have been saved.
To the fullest extent permitted by law, Springer Nature makes no warranties, representations or guarantees to Users, either express or implied
with respect to the Springer nature journal content and all parties disclaim and waive any implied warranties or warranties imposed by law,
including merchantability or fitness for any particular purpose.
Please note that these rights do not automatically extend to content, data or other material published by Springer Nature that may be licensed
from third parties.
If you would like to use or distribute our Springer Nature journal content to a wider audience or on a regular basis or in any other manner not
expressly permitted by these Terms, please contact Springer Nature at
onlineservice@springernature.com
Available via license: CC BY 4.0
Content may be subject to copyright.