Early access to physiotherapy for infants with cerebral palsy: A retrospective chart review.

AIM: This study aimed to investigate whether children with cerebral palsy (CP) had equal access to timely physiotherapy. Additionally, to learn more about clinical characteristics of infants with CP, we explored differences in neonatal clinical history and CP profile between children referred by a neonatologist or enrolled in neonatal follow-up and those referred by other healthcare professionals as well as those referred before and after 5 months corrected age.
METHODS: We conducted a retrospective chart review study including children born in Uppsala County, Sweden, from 2010 to 2016, who had received a CP diagnosis by July 2019. Entries by doctors and physiotherapists working at Uppsala University Children's Hospital were reviewed.
RESULTS: Thirty-eight children were included (21 girls, 55.3%) in the study. Twenty-two (57.9%) were born at term. Twenty-five children (66%) had their first visit to a physiotherapist before 5 months corrected age, and this included all children (n = 22, 57.9%) referred by a neonatologist or enrolled in neonatal follow-up. The latter group had significantly earlier access to physiotherapy compared to children referred by other healthcare professionals, with a median of 1.9 (min-max: -1-4) and 7.6 (min-max: 1-24) months, respectively (p < 0.0001). Referral source explained unique variance in predicting time of referral to physiotherapist (R2 0.550, B 4.213, p < 0.0001) when controlling for both number of risk factors and severity of motor impairment. However, number of risk factor was vital for early access to physiotherapy for children referred by other health care professionals. Children referred by a neonatologist or enrolled in neonatal follow-up or referred before 5 months corrected age differed on all measured variables concerning neonatal clinical history and CP profile, compared to children referred by other healthcare professionals or after 5 months corrected age. The latter groups had milder forms of CP. In total, twenty-eight children (73.7%) were ambulatory at 2 years of age. Bilateral spastic CP was most common among those referred by a neonatologist or enrolled in neonatal follow-up or referred before 5 months corrected age, while unilateral spastic CP was most common among those referred by other healthcare professionals or after 5 months corrected age.
CONCLUSION: Infants with CP have unequal access to timely physiotherapy, and children considered at low risk for CP receive therapy later. Neonatal follow-up of infants considered at high risk for CP that involves an assessment of motor performance using an evidence-based method during the first months of life corrected age seems to be effective in identifying CP early. Conversely, measuring milestone attainment seems to be a less reliable method for early identification. To provide safe and equal care, all professionals performing developmental surveillance should receive proper training and use evidence-based assessment methods. Physiotherapy should be available prior to formal medical diagnosis.

Introduction

Cerebral palsy (CP) is a clinical diagnosis used to describe a spectrum of permanent movement disorders caused by non-progressive disturbances that occurred in the developing brain [1,2]. Although the incidence is declining due to improvements in care [2,3], CP is still considered the most common physical disability in childhood, affecting 1.4 per 1000 in high-income countries [3]. Increasing evidence points to the importance of early intervention for motor disorders in children [3-8], and children with milder CP are more responsive to early intervention [8-10]. To intervene during the child’s first months of life, to capitalize on the enhanced neuronal plasticity during this critical developmental period, is considered as best practice [3,4,6-8]. Motor training incorporating active, child-initiated, goal-oriented and task-specific movements, as well as family involvement and environmental enrichment, have shown promising results [3,7,8]. Early motor interventions aim to advance motor skills and children’s learning potentials as well as to prevent secondary negative consequences of the disorder [3,6,8,11].

In Sweden, children with motor problems are primarily identified through two different healthcare services. The Swedish Child Health Services (CHS), a voluntary free-of-charge primary healthcare service, offer a comprehensive well-child surveillance program to all children aged 0–5 years [12]. During the child’s first year of life, the program offers at least 11 scheduled health visits, which include four developmental check-ups and three medical examinations [13]. Motor development is monitored by child healthcare physicians and nurses (specialists in either pediatric care or primary healthcare) observing whether children reach motor milestones or by parental reports [12]. CHS reaches 97% of all Swedish children [14]. Children who have a neonatal clinical history that increases the risk of developmental disorders are additionally enrolled in neonatal follow-up programs guided by national guidelines and adjusted to local routines [15]. At Uppsala University Children’s Hospital, these high risk infants are routinely assessed by physiotherapists using an evidence-based assessment method measuring developmental progress and quality of movements at 2, 4 and 10 months corrected age.

Infants with CP or at risk for CP can be accurately diagnosed before 5 months corrected age using clinical reasoning and a combination of standardized tools [6]. However, these high-risk infants only constitute half of all children with CP [5,9,16-18]. Studies have shown that children without readily identifiable risks factors for CP have delayed access to intervention [16-18]. Additionally, studies have revealed that the Swedish CHS only makes minor contributions to early identification of CP and severe health problems [19,20]. Consequently, children considered at low risk for CP are deprived of interventions that are known to improve outcomes [3,8,9].

The importance of early diagnosis and intervention for children with CP has been understood for decades [2]. Nonetheless, children with CP are still identified late [2,5,16-18], and studies investigating how CP manifests during infancy and what factors affect access to intervention have been called for [17,21,22]. By retrospectively reviewing medical charts, we aimed to describe clinical characteristics of infants with CP as well as what factors enable early access to physiotherapy. We hypothesized that children referred by a neonatologist and those enrolled in neonatal follow-up would have earlier access to physiotherapy and that there would be differences in neonatal clinical history and CP profile compared healthy children born at term. Additionally, because infants can be diagnosed with CP or as being at high risk for CP before 5 months corrected age [6], we chose to investigate differences between children referred for physiotherapy before and after 5 months corrected age to learn more about what enables early access to intervention.

Methods

Study population and setting

This retrospective chart review included children born in Uppsala County from 2010 to 2016 who had received a CP diagnosis by July 2019. The children were identified through both the local CP register (n = 38), which is part of the Swedish National Cerebral Palsy Surveillance Program and Registry (CPUP) [23], and the electronic medical chart system (n = 19). As the aim of the present study was to investigate children’s access to early physiotherapy, i.e. during the first months of life, children with CP who moved into the county after 1 year of age were excluded from the study (n = 18), leaving 39 eligible children.

In Uppsala County, there are approximately 295,000 inhabitants living in either urban Uppsala or its surrounding rural areas. From 2010 to 2016, 28,691 children were born in the county [24], distributed as follows: 601 born before gestational week (GW) 31 (2.1%), 1517 between GW 32–36 (5.3%) and 26,556 born at term (92.6%). These children attended well-child visits at any of the 44 child health centers in the county. Children who met the defined criteria in the national guideline [15], including all children born before 32 weeks of gestation, were also enrolled in the neonatal follow-up program and had additional visits at Uppsala University Children’s Hospital. At 2, 4 and 10 months corrected age, the infants’ motor development was routinely assessed by physiotherapists using Structured Observation of Motor Performance in Infants (SOMP-I) [25]. SOMP-I is a non-diagnostic, primarily discriminative assessment method that measures spontaneous and volitional motor performance from term to 12 months of age aiming to identify infants in need of early motor intervention regardless of etiology [25,26]. It allows for a detailed assessment of level of motor development and quality of motor performance in different body parts in different positions. During the study period, regardless of clinical background and the etiology of motor problems, all children aged 0 to 5 years were referred to the same physiotherapy clinic at Uppsala University Children’s Hospital for assessment and intervention.

Data collection

Data collection was conducted during the summer of 2018, with a supplementary search during the summer of 2019. The latter search revealed two additional children who met the inclusion criteria, both born in the fall of 2016. The entries by doctors and physiotherapists working at the children’s hospital were reviewed using a predefined template (S1 Table) based on risk factors mentioned in the review by Novak and colleagues [6]. All data related to age were corrected for prematurity if appropriate (gestational age <37 weeks). The first author performed most of the data collection, while the last author supplemented the data when needed. Any uncertainties were discussed until consensus was reached.

Measures

Referral source was defined as the professional who referred the child to physiotherapy. The children were categorized into two groups: I) referred by a neonatologist or enrolled in neonatal follow-up or II) referred by other healthcare professionals. Neonatal clinical history was described using gestational age and number of known risk factors predictive of CP, such as stroke, infections, or seizures, before 5 months corrected age (S1 Table). Gestational age was analyzed using weeks as a continuous variable as well as categorized into extremely preterm (22–27 GW), very preterm (28–32 GW), moderately preterm (32–36 GW) or full-term (37–42 GW). Risk factors were measured as a continuous variable with the exact number of risk factors identified before 5 months corrected age. Motor severity was described using the Gross Motor Function Classification System (GMFCS) at 2 years of age [27]. Distinctions between levels are based on functional abilities, where Level I indicates the highest and Level V the lowest functional level. Children at GMFCS Level I-III are ambulatory with or without assistance, while those at GMFCS Level IV-V are considered non-ambulatory and dependent on wheeled mobility. Type of CP was described by motor type and topography.

Statistical analysis

Descriptive statistics were applied to characterize our sample and are presented as number and percentages. Mann-Whitney U tests were used to compare age (months) at first visit to a physiotherapist based on referral source. Linear regression analyses were performed to explore the relationship between age at first visit to a physiotherapist (months) and referral source (categorical). The model was adjusted for number of risk factors (continuous) and severity of motor impairment (categorical). Additionally, we investigated the interaction between referral source and number of risk factors. Gestational age was not included in the model, as preterm infants born before GW 32 are routinely enrolled in the neonatal follow-up and are hence, unless otherwise indicated, assessed by a physiotherapist at 2 months corrected age regardless of the degree of prematurity. The children’s neonatal clinical history and CP profile were compared based on referral source and access to physiotherapy before or after 5 months of age using the Mann-Whitney U test, Chi-square analysis or Fischer’s exact test. For the analysis of severity of motor impairment, the children were categorized into either ambulatory or non-ambulatory. A two-tailed p-value of <0.05 was considered statistically significant. All calculations were performed using IBM SPSS Statistics 24 for Windows (SPSS Inc., Chicago, IL, USA).

Ethical approval

Due to the retrospective nature of the study and the risk of losing participants in a small sample, we sought and received approval from the Regional Ethical Review Board in Uppsala, Sweden (reg. no. 2018/173) as well as the Heads of Operations at Uppsala University Children’s Hospital and the Habilitation Services in Uppsala to review the data without obtaining informed consent. As data contains potentially identifiable and sensitive patient information data access is limited to by request. Data are available from Uppsala University, Legal Affairs Division (contact via e-mail: registrator@uu.se), for researchers who meet the criteria for access to confidential data.

Results

Thirty-nine children met the inclusion criteria, giving a prevalence of CP in Uppsala County of 1.4 cases per 1000 or an incidence of 5.4 cases per year. In one case, local routines had not been followed and this child had delayed access to physiotherapy. Because this case was not representative of the rest of the sample, this participant was excluded from the statistical analysis. There were no missing data.

Two-thirds of the children were born at term (n = 22, 57.9%) (Table 1), and the average gestational age was 38 weeks (min-max 23–41). Slightly more than half of the children were girls (n = 21, 55.3%). Of the 38 children, 22 (58.0%) were referred for physiotherapy by a neonatologist or enrolled in neonatal follow-up (Table 1). The remaining 16 children (42.0%) were referred by other healthcare professionals, i.e., a pediatric neurologist (n = 7) or CHS (n = 9). Twenty-five children (65.8%) were referred before 5 months corrected age.

Table 1

Descriptive statistics for all children with cerebral palsy (CP) as well as divided by referral source and referred before or after 5 months corrected age.

			Referral source			Before or after 5 months
		Total	Neoa	Otherb	P-value	0–4 moc	5–24 moc	P-value
		n = 38	n = 22 (58)	n = 16 (42)		n = 25 (66)	n = 13 (34)
Sex
	Boys, n (%)	17 (44.7)	5 (22.7)	12 (75.0)		8 (32.0)	9 (69.2)
	Girls, n (%)	21 (55.3)	17 (77.3)	4 (25.0)		17 (68.0)	4 (30.8)
Birth history
	Gestational age, weeks
	Mean (SD)	35.2 (5.5)	32.6 (5.8)	38.6 (2.1)	0.004	33.3 (5.8)	38.7 (2.2)	0.009
	Median	38	30.5	39		33	39
	Min-max	23–41	23–41	33–41		23–41	33–41
	Gestational age groups
	22–27 GWd	4 (10.5)	4 (18.2)	0 (0)	0.005	4 (16.0)	0 (0)	0.015
	28–31 GWd	8 (21.1)	8 (36.4)	0 (0)		8 (32.0)	0 (0)
	32–36 GWd	4 (10.5)	2 (9.1)	2 (12.5)		3 (12.0)	1 (7.7)
	37–42 GWd	22 (57.9)	8 (36.4)	14 (87.5)		10 (40.0)	12 (92.3)
	Known risk factors
	Mean (SD)	3.6 (3.1)	5.6 (2.5)	0.9 (1.5)	< 0.0001	5.3 (2.5)	0.3 (0.5)	< 0.0001
	Median	4	6	0		6	0
	Min-max	0–9	0–9	0–5		0–9	0–1
CP profile
	Severity of motor impairment
	Ambulatory	28 (73.7)	14 (63.6)	14 (87.5)	0.143	16 (64.0)	12 (92.3)	0.118
	Non-ambulatory	10 (26.3)	8 (36.4)	2 (12.5)		9 (36.0)	1 (7.7)
	Type of CP
	Unilateral	16 (42.1)	5 (22.7)	11 (68.8)	0.012	7 (28.0)	9 (69.2)	0.026
	Bilateral	17 (44.7)	14 (63.6)	3 (18.8)		15 (60.0)	2 (15.4)
	Ataxic/dyskinetic	5 (13.2)	3 (13.6)	2 (12.5)		3 (12.0)	2 (15.4)
Physiotherapy
	First visit, months
	Mean ±SD	4.6 (5.3)	1.5 (1.2)	8.8 (5.8)	< 0.0001	1.6 (1.3)	10.2 (5.5)	< 0.0001
	Median	2	1.9	7.6		2	8.6
	Min-max	-1-24	-1-4	1–24 mo		-1-4	5–24 mo
	Referred before 5 months
	Yes	25 (65.8)	22 (100)	3 (18.8)	< 0.0001
	No	13 (34.2)	0 (0)	13 (81.3)

Results are presented in numbers and percentage. Mean and standard deviation (SD) plus median, minimum and maximum are presented when applicable. Mann-Whitney U test, Chi-square analysis or Fischer’s exact test are used to compare groups.

aNeo: Neonatologists or enrolled in neonatal follow-up.

bOther: Other healthcare professionals.

cMo: Months.

dGW: Gestational weeks.

Twenty-eight children (73.7%) were ambulatory at 2 years of age (Table 1). The largest category of children was assessed at GMFCS Level I (n = 15, 39.5%), while three were assessed at GMFCS Level V (7.9%). The remaining children were equally divided over the GMFCS Levels (II: n = 7 (18.4%), III: n = 6 (15.8%), and IV: n = 7 (18.4%)). The most common types of CP were unilateral (n = 16, 42.1%) and bilateral (n = 17, 44.7%) spastic CP (Table 1). All children with unilateral spastic CP were assessed as ambulatory with or without assistance (GMFCS Level I-III) at 2 years of age. This held true for half of the children with bilateral spastic CP (n = 8, 47.1%). Of the non-ambulatory children (GMFCS Level IV-V), nine (90.0%) were diagnosed with bilateral spastic CP.

Access to physiotherapy

Children referred by a neonatologist or enrolled in neonatal follow-up had significantly earlier access to physiotherapy compared to children referred by other healthcare professionals (p < 0.0001) (Table 1). On average, these infants were approximately two months old (min-max: -1-4) at the first visit to the physiotherapist (Table 1). The corresponding age for infants referred by other healthcare professionals was approximately 7.5 months (min-max 1–24). All children referred by a neonatologist or enrolled in neonatal follow-up had their first visit before 5 months corrected age (n = 22, 100%), while this was only true for three children (18.8%) referred by other healthcare professionals. The unadjusted regression model demonstrated that both referral source and number of risk factors were associated with early access to physiotherapy (Table 2). When the variables were entered into the adjusted regression model, referral source explained unique variance in predicting age at first visit to a physiotherapist (R2 0.550, B 4.213, p < 0.0001). There was an interaction between referral source and the number of risk factors (Table 2), and this was especially true for the children referred from other healthcare professionals (Fig 1).

Table 2

Linear regression models.

Independent variables	R2	B	95% CI	P
Unadjusted
Referral source (othera vs neob)	0.477	-7.291	(-9.88, -4.71)	< 0.0001
Number of risk factors	0.465	-1.151	(-1.58, -0.73)	< 0.0001
Severity of motor problem (GMFCSc Levels I-V)	0.152	-1.489	(-2.68, -0.30)	0.016
Interaction referral source * number of risk factors	0.378	-0.973	(-1.40, -0.55)	< 0.0001
Adjusted
Model 1	0.550			< 0.0001
Referral source (othera vs neob)		-4.213	(-7.93, -0.50)	0.027
Number of risk factors		-0.571	(-1.18, 0.04)	0.066
Severity of motor problem (GMFCSc Levels I-V)		-0.429	(-1.41, 0.55)	0.381
Model 2	0.664			< 0.0001
Referral source (othera vs neob)		-8.085	(-12.11, -4.06)	< 0.0001
Number of risk factors		-2.218	(-3.36, -1.08)	< 0.0001
Severity of motor problem (GMFCSc Levels I-V)		-0.553	(-1.42, 0.31)	0.202
Interaction referral source * number of risk factors		2.107	(0.82, 3.39)	0.002

Summary of unadjusted and adjusted linear regressions models for variables hypothesized to predict access to early physiotherapy (months corrected age), where R2 denotes explained variance in the model and B the degree of change in the outcome variable (months corrected age) for every 1-unit of change in the dependent variable.

aOther: Other healthcare professionals.

bNeo: Neonatologists or enrolled in neonatal follow-up.

cGMFCS: Gross Motor Function Classification System.

Fig 1

The interaction between referral source and number of risk factors.

The total number of known risk factors before 5 months corrected age (X-axis) and the mean corrected age at first visit to physiotherapist in months (Y-axis). The lines represent the referral source.

Comparisons of neonatal clinical history and CP profile

Referral source

Children referred by a neonatologist or enrolled in neonatal follow-up were born significantly more prematurely than children referred by other healthcare professionals (p = 0.004) (Table 1). They had more known risk factors predictive of CP (p <0.0001) (Table 1), with a mean (SD) of 5.6 (2.5) compared to 0.9 (1.5) in children referred by other healthcare professionals. No statistically significant difference was found in severity of motor impairment based on referral source (Table 1). However, more children referred by a neonatologist or enrolled in the neonatal follow-up were assessed as non-ambulatory (n = 8, 80.0%) compared to those referred by other healthcare professionals (n = 2, 20.0%). Children assessed as ambulatory with or without assistance were divided equally between the referral sources (Table 1). There was a statistically significant difference between the groups regarding type of CP (p = 0.012) (Table 1), such that the children referred by a neonatologist or enrolled in the neonatal follow-up were more often diagnosed with bilateral spastic CP (n = 14, 63.6%) and those referred by other healthcare professionals with unilateral spastic CP (n = 11, 68.8%).

Referred before and after 5 months corrected age

When analyzing differences in neonatal clinical history and CP profile in relation to whether the child had access to physiotherapy before or after 5 months of age, similar results were found. Children referred to physiotherapy before 5 months corrected age were significantly more often born prematurely (p = 0.009) and had more known risk factors predictive of CP (p < 0.0001) (Table 1). Most children (n = 9, 69.2%) referred after 5 months of age had no known risk factors predictive of CP (Table 1), while the corresponding figure (mean (SD)) for those referred before 5 months corrected age was 5.3 (2.5). For the children referred by other healthcare professionals, the number of risk factors was vital for early access to physiotherapy (Fig 1). Additionally, children referred after 5 months corrected age had milder forms of CP, where all, except one, were ambulatory with or without assistance at 2 years of age (n = 12, 92.3%) (Table 1). No statistically significant difference was found in severity of motor impairment when comparing the two groups. However, the majority (n = 9, 90.0%) of the children assessed as non-ambulatory had their first visit to physiotherapists before 5 months of age. Regarding type of CP, there was a statistically significant difference between the two groups (p = 0.026) (Table 1), such that those referred before 5 months corrected age were more often diagnosed with bilateral spastic CP (n = 15, 60.0%). Among those referred after 5 months corrected age, unilateral spastic CP was most common (n = 9, 69.2%).

Discussion

Our study confirmed our hypothesis that children referred by a neonatologist and those enrolled in neonatal follow-up had earlier access to physiotherapy compared to children referred by other healthcare professionals, even when the number of known risk factors and the severity of motor impairment were controlled for. However, the number of risk factors seemed to be vital for early access to physiotherapy for the children that were not NICU graduates. Furthermore, the groups differed on all variables in regards in neonatal clinical history and CP profile. The prevalence of CP was similar to figures reported in other high-income countries [3], and only a little more than half of the children were referred by a neonatologist or enrolled in neonatal follow-up. Children born at term constituted 58% of all CP cases. Among all the children, 66% had access to physiotherapy before 5 months corrected age.

Similar to Boychuck and colleagues’ [17] findings, referral source and number of known risk factors predicted earlier access to physiotherapy. It is important to acknowledge that children who require neonatal intensive care are considered to be at high risk for CP and are routinely enrolled in neonatal follow-up programs [6]. In this setting, professionals know they are assessing high-risk children. The children may also have more severe impairments, which may partly explain why CP in these children are identified earlier [17]. Additionally, in neonatal follow-up, children are assessed by physiotherapists using evidence-based assessment methods [15]. Being trained and skilled in assessing early motor performance using evidence-based assessment methods seemed to improve early identification of children with CP.

However, only slightly more than half of all children with CP are enrolled in neonatal follow-up [5,9,16-18]. For the remaining children, age at referral varies considerably [16-18]. In this connection, the primary healthcare services, including CHS, show the greatest delays [16-19]. Although the Swedish CHS is striving to improve their methods and the infants in our study were identified at an earlier age than in previous studies [16-19], the children were nevertheless referred later than high-risk infants and with greater variability. In our study, the children who were not NICU graduates had few, if any, known risk factors for CP, but having more risk factors led to earlier access to physiotherapy. Furthermore, the majority of all children were assessed as ambulatory at 2 years of age. Not having identifiable risk factors for CP as well as having a high functional level often leads to delayed referral for intervention [5,9,18,28]. Adding this to the relatively low prevalence of CP indicates that very few healthcare professionals will ever be the first assessor of an infant with emerging CP. This highlights the challenge of early identification of children with CP outside neonatal follow-up. Thus, our question should be: How can we enable early identification of children with CP without known risk factors for CP? In Sweden, healthcare professionals working within CHS could play a pivotal role, as nearly all children pass through this service. However, to enable this, we need to learn more about early signs of CP and its development during the first year of life.

Additionally, we need to consider how motor development is assessed within CHS. We know that, when our aim is early identification of children with CP, assessments focusing on motor milestones are not reliable [9]. Some children with CP may have near normal milestone attainment over the first year of life [2,9], and this is especially true for children with mild unilateral CP [9]. Merely assessing how far the child has come in its development can lead to a false impression of typical development, and this is why assessing quality of movement is recommended [7,9,16]. Children with unilateral or bilateral spastic CP, especially those with a milder motor impairment, are usually identified late [18,28]. Being observant of early quality deviations such as persistent asymmetries, especially early hand preference [6,9,10,22], irrespective of motor delay, should warrant a more thorough examination and prompt referral to physiotherapy.

To enable timely identification of children with CP, evidence-based assessment methods should be an integrated part of developmental surveillance. Standardizing care could potentially reduce variability across organizations and professionals [29], hence increasing equality and patient safety. Furthermore, using such methods improves accuracy, enables earlier identification (including mild delays or suspected deviations) and provides more information compared to clinical judgement alone [6,9,30,31]. Not using such methods will delay identification of children with CP [16-18], consequently depriving children of interventions known to be beneficial [3,4,6,8]. The fact that the rate of CP is falling and that CP severity is lessening further highlight this need [3]. A recent scoping review suggested that feasible methods for well-child surveillance are lacking [22]. Johansen and colleagues [32], however, showed that when child health nurses used SOMP-I in routine well-child surveillance, the method appeared to be clinically useful. Providing child healthcare professionals with an evidence-based assessment method may enable earlier identification of children with CP.

All professionals performing developmental surveillance should receive adequate training, use evidence-based assessment methods when available and be skilled in discriminating atypical movement from variations in typical movement [6]. However, it is important to remember that proper assessment of infants using any standardized method is an acquired skill requiring practice over time [29]. Nurses learning to use SOMP-I stressed that becoming a proficient assessor requires training and practice [33]. Furthermore, infants displaying aberrant motor performance should have access to physiotherapy prior to any formal medical diagnosis, as mild cases without any risk factors can be particularly difficult to diagnose [9]. Important to note is that the linear serial model of referral should be avoided, as it prolongs lead time and delays intervention [16,17].

Limitations

Our results are based on a small clinical population from one Swedish county. Nevertheless, the prevalence of CP was similar to figures reported elsewhere, indicating that it is a representative sample. However, a larger sample could have revealed statistically significant differences between severity of the motor problems and referral source or access to physiotherapy before or after 5 months corrected age. Furthermore, the youngest children were only 2 years of age when we conducted the initial search, which entails the risk that not all children with CP were identified. However, no child was identified after 2 years of age, and only two children meeting the inclusion criteria were identified in the supplementary search. The retrospective design limited our access to the entries made at the children’s hospital, possibly resulting in missed information from other sources, such as CHS. Furthermore, the review of the medical charts was mainly performed by the first author. To reduce the risk of bias, a template was used when collecting the data (S1 Table).

Clinical implications

Early identification and timely intervention are widely accepted as best practice for children with CP. Our study indicates that a neonatal follow-up program that includes infants at high risk for CP as well as those born before 32 weeks of gestation and that involves an assessments of motor performance using an evidence-based method during the first months of life corrected age is effective in identifying children with CP early. However, infants have unequal access to timely physiotherapy, and children considered at low risk for CP receive therapy later. The high variability in referral practices suggests that knowledge of CP characteristics in infants varies widely across organizations and professionals. It is especially children without readily identifiable risk factors who have delayed access to intervention, indicating that the current CHS practice of measuring milestone attainment does not effectively identify CP. This is concerning, given CHS’s key role in early identification of developmental disorders.

To provide high quality care that is equal and safe, all professionals working with developmental surveillance, regardless of organizational level, need appropriate knowledge of typical and atypical motor development, including early clinical signs of CP. Without continuous professional development initiatives to increase such knowledge, children will continue to experience delayed access to physiotherapy. Evidence-based assessment methods should be used when available, as these improve early identification and support clinical decision-making. Furthermore, when aberrant motor performance is observed, the child should be promptly referred to physiotherapy, regardless of formal medical diagnosis.

Template for data collection.

(DOCX)

Click here for additional data file.

15 Feb 2021

PONE-D-20-28394

Unequal access to timely physiotherapy for children with Cerebral Palsy: a retrospective chart review

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

Reviewer #2: Partly

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: No

Reviewer #2: No

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Reviewer #1: Yes

Reviewer #2: Yes

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The authors retrospectively reviewed patient data from two health care systems in a county in Sweden in the aim to assess whether children with cerebral palsy (CP) have equal access to timely physiotherapy. They concluded from the data that Children with CP have unequal access to physiotherapy. The authors emphasized the importance of timely access of physiotherapy to children with CP. The data and results might be helpful for the improvement of local health policy for children with CP.

The authors provided detailed descriptive results of data. However, the description of data collection is not detailed. Several aspects of information as the following should be described:

(1) as a retrospective review, do you have a data collection guidance or standard, which is like on what data to be reviewed , how to collect data, and data quality control, before the formal data review? if so, please provide a data collection flow chart.

(2) as described in the manuscript, the first author reviewed most of the data from two different health care systems, is there the possibility of any potential bias on reviewing data from two different health care systems mostly by one researcher, has any potential bias been considered to be controlled before formal data review, has any preventive method been used to control the bias?

(3) the authors did not mention any data missing in the manuscript. How has data missing been handled if you did have the cases of missing data?

As to statistical analysis, the authors used Kruskal-Wallis H Test but without providing any justification for the selection of this method.

As to results, the authors found that both referral source and number of risk factors have significant influences to the first visit to physiotherapy (see Table 2), and concluded that “children referred from the child health services have the most delayed access” (see abstract conclusion). A likely scenario is that number of risk factors dominates the decision of the first visit to physiotherapy but children with CP from the child health services have the fewer number of risk factors compared to other referral sources, and the fewer number of risk factors caused the delay of referral of children with CP to physiotherapy by the child health services. If the number of risk factors was controlled, is the conclusion “children referred from the child health services have the most delayed access” still correct?

Reviewer #2: The purpose of the review is to provide the editors with an expert opinion regarding the validity and quality of the manuscript under consideration. The review should also supply authors with explicit feedback on how to improve their papers so that they will be acceptable for publication in PLOS ONE. As you write, consider the following points:

• What are the main claims of the paper and how significant are they for the discipline?

I appreciate the opportunity to review the manuscript named “Unequal access to timely physiotherapy for children with Cerebral Palsy: a retrospective chart review”

-The authors claims to investigate whether children with cerebral palsy (CP) in Sweden have equal access to timely physiotherapy. Additionally, the children’s birth history and CP profile are described to understand typical features that might enable earlier identification for children with CP in the future. Equity in care is important and it is clearly of interest to know if it is provided for children with CP, as that would be a prerequisite in order to correctly target suitable measures. However, I would also suggest nuancing the results with regard to motor function and need of physiotherapy, further discussed in comments below.

• Are the claims properly placed in the context of the previous literature? Have the authors treated the literature fairly?

-Yes, however the literature may also provide further information for nuancing according to gross motor function, mentioned above.

• Do the data and analyses fully support the claims? If not, what other evidence is required?

-Data sufficiently supports the claims. Multilevel regressions may be considered.

• PLOS ONE encourages authors to publish detailed protocols and algorithms as supporting information online. Do any particular methods used in the manuscript warrant such treatment? If a protocol is already provided, for example for a randomized controlled trial, are there any important deviations from it? If so, have the authors explained adequately why the deviations occurred?

-No need.

• If the paper is considered unsuitable for publication in its present form, does the study itself show sufficient potential that the authors should be encouraged to resubmit a revised version?

-Yes, I suggest a revised version to be resubmitted

• Are original data deposited in appropriate repositories and accession/version numbers provided for genes, proteins, mutants, diseases, etc.?

-Not applicable

• Are details of the methodology sufficient to allow the experiments to be reproduced?

-Yes

• Is the manuscript well organized and written clearly enough to be accessible to non-specialists?

-The manuscript should be revised more thoroughly for structure and readability, suggestions follows below.

Although confidential comments to the editors are respected, any remarks that might help to strengthen the paper should be directed to the authors themselves.

Explicit feedback for improvement:

I thank you for letting me read and comment on your work, which I find important and interesting. I start of with general comments and proceed with specific comments referring to line numbers.

I would recommend you to ethically reconsider some of the presented data due to confidentiality of the participants, further commented below.

I would think it is of interest to nuance the discussion regarding need for physiotherapy and motor function. This study, like earlier cited studies shows roughly that when disability is not expected or fairly invisible, diagnosis/referral is more likely to be delayed. Conceivably these children are not the ones most in need of physiotherapy, thus, the consequences of less early physiotherapy may not be quite generalizable for all children with CP. For ease of reading, consider using the same wording throughout the document, e.g. medical history/complicated birth history, and also to provide both numbers and percentages.

Introduction:

51: Please provide a reference for this statement.

52-53: Children with complicated birth history are enrolled to neonatal follow-up, which may be confused with information in methods, lines 79-80 where neonatal follow-up is only for children born <32 weeks. Please clarify criteria for neonatal follow-up

54-56: I would appreciate a more specific description of the knowledge gap – why this needs to be explored again but specifically for physiotherapy.

57: “Improve outcomes” is very general, please specify/exemplify interventions and outcomes and possibly for which children (GMFCS)

63: Is it possible that early motor interventions are more important for children with GMFCS III-V, and thereby lessening the impact of the inequality in timely physiotherapy, as all but one(!) from the well child visits had GMFCS I-II? While such information should not lead to disregarding of inequality, it would all the same nuance the picture.

Method:

72-74: Exclusion criteria seems to exclude all children not born in Uppsala regardless of when they moved to Uppsala? Please clarify the exclusion criteria and the reasons for it as excluded children correspond to almost 50% of your current sample

78-79: Do all term born children always participate in the well child program?

79-80: Please clarify which children receives neonatal follow-up and how neonatologist differs from neuropediatrician. According to line 52-53, neonatal follow-up would not only include <32 weeks. Do the preterm children also participate in the well child program? 82: The neuropediatricians seem to be part of the neonatal follow-up, which further complicates the relevance of this division of referral source, see lines 52 and 79.

102: Please consider if multilevel analysis would be useful, e.g. multivariable logistic regressions.

109, Ethics: I disagree with your statement that all data are presented on group level. Some groups consists of single children. In a fairly small community of children with CP and their parents, in a named region in Sweden, there would be a significant risk that individual children are identified by some of these data. This would be particularly unfortunate since no informed consent is collected.

Results:

117-118: Please clarify the meaning of “missed early” and why this is reason for exclusion.

Table 1: In the rows you explain that you report n (%), however the percentages are summed up by column. I would recommend you to reconsider this way of presenting in order to gain readability

120-121: Please explain the relevance of the difference between being referred by neonatologist or neuropetiatrician – are these children not part of the same neonatal follow-up? Also, is it possible that CHS does not refer to physiotherapist directly, but via e.g. neuropediatricians, thus contributing to the delay?

Table 2: It would be helpful if you explain H and Df among the abbreviations in the table and also elaborate the table heading so that the table can be understood separately from the text. GMFCS is quite close to significant regarding first visit to physiotherapy – I propose you add to the discussion whether your results actually show that there is no difference with regard to GMFCS or if the results may be due to power-issues.

Discussion:

169: It is a bit unclear if you refer to the Ref 12 or to own results (or both)

172: As mentioned above, I find it a difficult to follow this grouping of children due to referral source – which are the children who are not from CHS and not in the neonatal follow-up There is a lack of consistency and/or a need of a more concise description throughout the manuscript

175-176: Again, as mentioned earlier, I would suggest you elaborate around this matter. While it is important to provide equal care, as to receive early FT assessment, there may also be limited consequences for children with mild motor difficulties to be referred to physiotherapy at a higher age, because of their fairly good motor function(?). Other difficulties associated with CP may be prioritized when motor function is good, such as e.g. speech or cognition.

178: Please clarify if the early interventions refer to physiotherapy or other interventions. Please consider discussion about power in your study when discussing GMFCS as not significantly associated with early referral to physiotherapist.

205-206: It seems in this statement like all children are not included in the neonatal follow-up – is that right and if so, please state this more clearly. According to the introduction line 52 all children with complicated birth history are routinely included.

206: Please specify which interventions and which guidelines you refer to.

216: Please specify the kind of review you refer to.

220-232: To implement use of evidence based motor assessment tools within CHS seems to be a suitable suggestion in order to early detect more children with presumed CP. I suggest you emphasize this even more. (As there is a shortage of specialist CHS nurses in primary care, maybe such assessment could be introduced as a cooperation task for primary health care physiotherapists in order to widen their area of responsibility and thereby strengthening their professional role?)

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Reviewer #1: Yes: Yanlong Song

Reviewer #2: No

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Submitted filename: PlosOne.pdf

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31 Mar 2021

Response to reviewers comments regarding manuscript PONE-D-20-28394

We would like to start by thanking the academic editor and the reviewers for their valuable and constructive feedback! Below you find our response to their recommended and suggested revisions. Based on the feedback from the reviewers the revisions are extensive. We have refined our aim and research questions to be more concise, and as a result we needed to redo the statistical analysis as well as edit tables and exclude the figure. To address these changes as well as to meet the requests by the reviewers we have rewritten parts of the introduction and discussion as well.

We have highlighted the changes in the manuscript in yellow. Given the extensive revision of the manuscript it has also been edited for language. These language changes are not highlighted to improve the readability of the text. If necessary, we can provide the manuscript with these tracked changes. Added text is highlighted in yellow, while removed text appears as strikethrough and also highlighted in yellow.

Journal Requirements

(1) Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming.

We have edited the manuscript to meet PLOS ONE’s style requirements.

(2) In your Methods section, please provide additional information regarding the participant inclusion and exclusion criteria. Furthermore, we note that you have reported significance probabilities of 0 in places. Since p=0 is not strictly possible, please correct this to a more appropriate limit, eg 'p<0.0001'

We have edited this throughout the manuscript.

(3) We note that the grant information you provided in the ‘Funding Information’ and ‘Financial Disclosure’ sections do not match. When you resubmit, please ensure that you provide the correct grant numbers for the awards you received for your study in the ‘Funding Information’ section.

As none of the authors have received any specific funding for this work, we have removed the previous reported funding bodies and instead ticked the box for ‘The author(s) received no specific funding for this work.’ Could you please update the financial disclosure in the online submission form to: “The authors received no specific funding for this work”? Thank you in advance!

(4) Thank you for stating the following in the Competing Interests section: "SOMP-I is owned by Barnens rörelsebyrå ekonomisk förening (economic association) Uppsala, Sweden. Kine Johansen is a partner of Barnens rörelsebyrå. All other authors have no conflicts of interest to disclose." Please confirm that this does not alter your adherence to all PLOS ONE policies on sharing data and materials, by including the following statement: "This does not alter our adherence to PLOS ONE policies on sharing data and materials.”

We have updated the statement regarding competing interests to adhere to PLOS ONE policies and guidelines, see below. The statement is included in the cover letter. Please change the online submission form on our behalf.

I have read the journal's policy and I, Kine Johansen, the last authors of this manuscript have the following competing interests to declare: Structured Observation of Motor Performance in Infants (SOMP-I), the assessment methods used in clinical practice at Uppsala University Children’s Hospital and tested within the child health services is owned by Barnens rörelsebyrå ekonomisk förening (economic association) Uppsala, Sweden. Kine Johansen is one of the owners of Barnens rörelsebyrå. This does not alter our adherence to PLOS ONE policies on sharing data and materials. The two other authors have no competing interests to disclose.

(5) We note that you have indicated that data from this study are available upon request. PLOS only allows data to be available upon request if there are legal or ethical restrictions on sharing data publicly.

We have updated the data availability statement to adhere to PLOS guidelines, see below. The statement is included in the cover letter. Please change the online submission form on our behalf. We have also added this information to the section ‘Ethical approval’ in the manuscript.

Data cannot be shared publicly because it includes potentially identifying and sensitive patient information, therefore access is limited to by request by the Regional Ethical Review Board in Uppsala, Sweden (reg. no. 2018/173). Data are available from Uppsala University, Department of Women’s and Children’s Health (contact via e-mail: kine.johansen@kbh.uu.se) for researchers who meet the criteria for access to confidential data.

Review comments to the Author

Reviewer #1

The authors provided detailed descriptive results of data. However, the description of data collection is not detailed. Several aspects of information as the following should be described:

(1) As a retrospective review, do you have a data collection guidance or standard, which is like on what data to be reviewed, how to collect data, and data quality control, before the formal data review? if so, please provide a data collection flow chart.

Besides the inclusion and exclusion criteria and the data collection template (S1 Table), we did not have a data collection guidance on standard. Hence, we cannot provide a data collection flow chart.

(2) As described in the manuscript, the first author reviewed most of the data from two different health care systems, is there the possibility of any potential bias on reviewing data from two different health care systems mostly by one researcher, has any potential bias been considered to be controlled before formal data review, has any preventive method been used to control the bias?

All data collected and used in this study is based on data from hospital stays and visits to the Uppsala University Children’s Hospital. All children with motor problems were during the study period referred for to the same pediatric physiotherapy clinic located at the children’s hospital. CP type and typography as well as the Gross Motor Function Classification System (GMFCS) level was collected from the assessment by the pediatric neurologist around 2 years of age. No data were collected from the child health services.

(3) The authors did not mention any data missing in the manuscript. How has data missing been handled if you did have the cases of missing data?

As all data are based on medical records and we only used data available from the records we did not have any missing data. We have added a sentence in the first section of the results section.

(4) As to statistical analysis, the authors used Kruskal-Wallis H Test but without providing any justification for the selection of this method. As to results, the authors found that both referral source and number of risk factors have significant influences to the first visit to physiotherapy (see Table 2), and concluded that “children referred from the child health services have the most delayed access” (see abstract conclusion). A likely scenario is that number of risk factors dominates the decision of the first visit to physiotherapy but children with CP from the child health services have the fewer number of risk factors compared to other referral sources, and the fewer number of risk factors caused the delay of referral of children with CP to physiotherapy by the child health services. If the number of risk factors was controlled, is the conclusion “children referred from the child health services have the most delayed access” still correct? The number of risk factors plays a considerable part in referral to physiotherapy. However, as the separate variables are dependent on each other, i.e. if a child have more risk factors they are more likely to be admitted to the NICU and hence be included in the neonatal follow-up, we cannot do this kind of analysis.

We agree with reviewer 1 that referral source and the number of risk factors are dependent on each other. As reviewer propose children with more risk factors were admitted to the neonatal intensive care unit and had earlier access to physiotherapy. To analyze this relationship we performed a multivariate regression analyses controlling for the number of risk factors and severity of the motor problem. We found that referral source contributed with unique variance compared to the number of risk factors. Our interpretation of these findings are that our current system of identifying CP in high risk infants is effective, i.e. a generous neonatal follow-up program which includes children with known risk factors predictive of CP as well as those born before 32 weeks of gestation and that involves an early assessment of motor performance. After redefining our aim and research questions we removed the Kruskal-Wallis H Test from our analysis.

Reviewer #2

• Are the claims properly placed in the context of the previous literature? Have the authors treated the literature fairly? Yes, however the literature may also provide further information for nuancing according to gross motor function, mentioned above.

We have refined the aim and research questions, and rewritten the introduction, results and discussion. Hopefully this has provided a more nuanced picture of motor function and the need of timely motor interventions. The effects of early motor interventions holds for both gross and fine motor function.

• Do the data and analyses fully support the claims? If not, what other evidence is required? Data sufficiently supports the claims. Multilevel regressions may be considered.

Thank you for the suggestion. We have redone our statistical analysis and included a univariate and multivariate regression analyses.

• Is the manuscript well organized and written clearly enough to be accessible to non-specialists? The manuscript should be revised more thoroughly for structure and readability, suggestions follows below.

Response to explicit feedback for improvement:

- I would recommend you to ethically reconsider some of the presented data due to confidentiality of the participants, further commented below.

We have address this in the comments below.

- I would think it is of interest to nuance the discussion regarding need for physiotherapy and motor function. This study, like earlier cited studies shows roughly that when disability is not expected or fairly invisible, diagnosis/referral is more likely to be delayed. Conceivably these children are not the ones most in need of physiotherapy, thus, the consequences of less early physiotherapy may not be quite generalizable for all children with CP.

We have address this in the comments below.

- For ease of reading, consider using the same wording throughout the document, e.g. medical history/complicated birth history, and also to provide both numbers and percentages.

We have changed medical history/complicated birth history to neonatal clinical history as well as added both number and percentages throughout the manuscript.

Introduction

• 51: Please provide a reference for this statement.

We have added a reference as suggested.

• 52-53: Children with complicated birth history are enrolled to neonatal follow-up, which may be confused with information in methods, lines 79-80 where neonatal follow-up is only for children born <32 weeks. Please clarify criteria for neonatal follow-up.

We have rewritten the ‘Introduction’ as well as the ‘Study population and setting’ to clarify the inclusions criteria for neonatal follow-up in Uppsala County.

• 54-56: I would appreciate a more specific description of the knowledge gap – why this needs to be explored again but specifically for physiotherapy.

We have refined the aim and research question and highlighted the knowledge gap in the last section of the introduction.

• 57: “Improve outcomes” is very general, please specify/exemplify interventions and outcomes and possibly for which children (GMFCS)

Early intervention is in this manuscript primarily referring to early motor interventions. We have added two sentences elaborating on this in the first section of the introduction.

According to Novak et al (2020) the following features are common for effective motor interventions for children with CP: ‘practice of real-life tasks and activities, using self-generated active movements, at a high intensity, where the practice directly targets the achievement of a goal set by the child (or a parent proxy if necessary). The mechanism of action is experience-dependent plasticity. Motivation and attention are vital modulators of neuroplasticity, and successful task-specific practice is rewarding and enjoyable to children, producing spontaneously regular practice.’

Given that children with less severe motor impairment are more likely to be able to produce active goal-directed movements, they are also those who are more responsive to early motor interventions (Morgan et al., 2018; Sakzewski et al., 2019). Early motor interventions aim to improve motor outcomes as well as to prevent secondary negative consequences of not being able to move age-appropriately.

Early motor intervention programs have been associated with beneficial effects of both motor and cognitive outcomes (Hadders-Algra, 2021; Morgan et al., 2016).

• 63: Is it possible that early motor interventions are more important for children with GMFCS III-V, and thereby lessening the impact of the inequality in timely physiotherapy, as all but one(!) from the well child visits had GMFCS I-II? While such information should not lead to disregarding of inequality, it would all the same nuance the picture.

Literature suggests that children with milder CP are more responsive to early motor interventions than children with more severe forms of CP (Morgan et al., 2018; Sakzewski et al., 2019). So, in contrast with reviewer 2s suggestion, children with milder motor impairments would benefit more from early intervention. Our experience from clinical practice is that children with less severe motor impairments do show aberrant motor development, but this does not necessarily mean that the child is delayed. We have added a sentence with references addressing that children with milder CP are more responsive to early intervention in the first section of the introduction. We have also added a section in the discussion addressing that children with milder CP and especially those with unilateral CP might have near to normal motor milestones acquisition and the need to assess quality of movement to enable early identification of infants with CP.

Method

• 72-74: Exclusion criteria seems to exclude all children not born in Uppsala regardless of when they moved to Uppsala? Please clarify the exclusion criteria and the reasons for it as excluded children correspond to almost 50% of your current sample

As the aim of our study was to investigate children’s access to early physiotherapy, i.e. during the first months of life, children with CP who moved into the county after 1 year of age were excluded from the study. We have added this to the text.

• 78-79: Do all term born children always participate in the well child program?

Yes, the Swedish child health services are offered to all children aged 0-5 years and has an attendance rate of 97%. We have added this in the introduction.

• 79-80: Please clarify which children receives neonatal follow-up and how neonatologist differs from neuropediatrician. According to line 52-53, neonatal follow-up would not only include <32 weeks. Do the preterm children also participate in the well child program? 82: The neuropediatrician seem to be part of the neonatal follow-up, which further complicates the relevance of this division of referral source, see lines 52 and 79.

We have removed the national guideline to follow-up infants born before 28 weeks of gestation when describing neonatal follow-up in the introduction, and instead explained the inclusion criteria for neonatal follow-up in Uppsala County in the “study population and setting” section. All children are offered the well-child surveillance, and CHS reaches 97% of all Swedish children 0-5 years of age. We have rewritten this section of the introduction to make this more concise.

The neonatologist work with newborn infants that are in need of neonatal intensive care. Given that these children are at increased risk for later developmental disorders these high-risk infants are routinely enrolled in neonatal follow-up programs. In Uppsala County, the neonatologist is the responsible physician at the follow-up. If a neurological impairment or disability is suspected the child is referred to a neurologist, which work at another department and is not a part of the neonatal follow-up. As we have changed our aim, research questions and results, this step in the children’s clinical journey is no longer investigated in our study and we have removed this from the text.

After redefining our aim, we divided the children into those who had been referred by the neonatologist or enrolled in the neonatal follow-up and those referred from other healthcare professionals. Hopefully this division makes it clearer.

• 102: Please consider if multilevel analysis would be useful, e.g. multivariable logistic regressions.

We added a univariate and multivariate regression analyses as suggested.

• 109, Ethics: I disagree with your statement that all data are presented on group level. Some groups consists of single children. In a fairly small community of children with CP and their parents, in a named region in Sweden, there would be a significant risk that individual children are identified by some of these data. This would be particularly unfortunate since no informed consent is collected.

We agree and to avoid identifications of individual children, we have collapsed some variables to have more children in every groups.

Results

• 117-118: Please clarify the meaning of “missed early” and why this is reason for exclusion.

We have rewritten this sentence and added another to provide more clarity. However, we cannot describe this in more detail as it could lead to identification of this child.

• Table 1: In the rows you explain that you report n (%), however the percentages are summed up by column. I would recommend you to reconsider this way of presenting in order to gain readability

We agree and have edited this in table 1.

• 120-121: Please explain the relevance of the difference between being referred by neonatologist or neuropediatrician – are these children not part of the same neonatal follow-up? Also, is it possible that CHS does not refer to physiotherapist directly, but via e.g. neuropediatrician, thus contributing to the delay?

The neonatologist work with newborn infants that are in need of neonatal intensive care. Given that these children are at increased risk for later developmental disorders these high-risk infants are routinely enrolled in neonatal follow-up programs. In Uppsala County, the neonatologist is the responsible physician at the follow-up. If a neurological impairment or disability is suspected the child is referred to a neurologist, which work at another department and is not a part of the neonatal follow-up. As we have changed our aim, research questions and results, this step in the children’s clinical journey is no longer investigated in our study and we have removed this from the text.

In regards to referral from the CHS to the pediatric neurologist. Linear serial models of referrals are known to delay access to intervention for children with CP, so this is definitively a warranted concern. In our sample, all children were referred to the neurologist due to other medical concerns, such as seizures. However, after redefining our aim, we divided the children into those referred by neonatologists or enrolled in neonatal follow-up and those referred from other healthcare professional this is no longer of importance as they now are presented as one group. We have added a sentence in the discussion that linear serial model of referral should be avoided as it can prolong lead time and delay intervention.

• Table 2: It would be helpful if you explain H and Df among the abbreviations in the table and also elaborate the table heading so that the table can be understood separately from the text. GMFCS is quite close to significant regarding first visit to physiotherapy – I propose you add to the discussion whether your results actually show that there is no difference with regard to GMFCS or if the results may be due to power-issues.

We have removed table 2 from the manuscript and added a discussion in ‘Limitations’ regard sample size.

Discussion

• 169: It is a bit unclear if you refer to the Ref 12 or to own results (or both)

We are referring to Ref 12 and have rewritten this sentence to convey the correct meaning.

• 172: As mentioned above, I find it a difficult to follow this grouping of children due to referral source – which are the children who are not from CHS and not in the neonatal follow-up. There is a lack of consistency and/or a need of a more concise description throughout the manuscript.

After redefining our aim, we divided the children into those referred by a neonatologist or enrolled in neonatal follow-up or those referred by other healthcare professionals. Hopefully this division makes the groups easier to follow when reading the manuscript.

• 175-176: Again, as mentioned earlier, I would suggest you elaborate around this matter. While it is important to provide equal care, as to receive early FT assessment, there may also be limited consequences for children with mild motor difficulties to be referred to physiotherapy at a higher age, because of their fairly good motor function(?). Other difficulties associated with CP may be prioritized when motor function is good, such as e.g. speech or cognition.

All children should have equal access to physiotherapy/early motor interventions. Knowing that milder forms of CP are more responsive to early motor interventions (Morgan et al., 2018; Sakzewski et al., 2019), stress the importance of identifying these children early. At this point we are missing the children where our intervention could have the largest effect. Delayed access to physiotherapy can lead to delayed motor development as well as muscle weakness, contractures and loss of function (Ulrich, 2010). Furthermore, as motor abilities are needed to explore the world, solve problems and make discoveries (Johnston, 2009; Von Hofsten, 2004), early motor problems are likely to affect child development. Already from an early age these motor behaviors and the children’s perceptual-motor experiences within cultural and social contexts form their cognition (Johnston, 2009; Von Hofsten, 2004). Moreover, as neuronal plasticity is enhanced during the first months of life and goal-directed actions lead to structural and functional changes in the brain motor interventions can impact how the brain organizes itself (Johnston, 2009; Novak et al., 2017). This is likely why early motor interventions programs have shown to be beneficial for children’s cognitive outcomes (Hadders-Algra, 2021; Morgan et al., 2016).

Due to the course of development of speech, early intervention in this regards is not relevant during the first months of a child’s life.

• 178: Please clarify if the early interventions refer to physiotherapy or other interventions.

We have removed this section of the discussion.

• Please consider discussion about power in your study when discussing GMFCS as not significantly associated with early referral to physiotherapist.

We have discussed this in the ‘Limitations’ section.

• 205-206: It seems in this statement like all children are not included in the neonatal follow-up – is that right and if so, please state this more clearly. According to the introduction line 52 all children with complicated birth history are routinely included.

We have deleted this section of the discussion.

• 206: Please specify which interventions and which guidelines you refer to.

We have rewritten this section and added the name of the guidelines we refer to.

• 216: Please specify the kind of review you refer to.

We have rewritten this sentences to convey the correct meaning.

• 220-232: To implement use of evidence based motor assessment tools within CHS seems to be a suitable suggestion in order to early detect more children with presumed CP. I suggest you emphasize this even more. (As there is a shortage of specialist CHS nurses in primary care, maybe such assessment could be introduced as a cooperation task for primary health care physiotherapists in order to widen their area of responsibility and thereby strengthening their professional role?)

When rewriting the discussion we emphasize CHS as the arena where we can do most to improve timely identification of children with CP. We also highlight the benefits and challenges of using evidence-based assessment methods in well-child surveillance. In Sweden, child health nurses outnumber pediatric physiotherapists. Additionally, the CHS reaches 97% of all children aged 0-5 years of age, while physiotherapist only see children on a referral-basis. By introducing an evidence-based assessment method and training of child health nurses, we would potentially be able to reduce the unequal access for early intervention. This holds not only for CP, but for other developmental disorders as well. As we all realize the unleashed potential of the CHS as an arena for early identification of children with motor problems, there are continuously quality improvement projects to increase the cooperation between child health nurses and pediatric physiotherapists.

Sincerely,

Kine Johansen

Physiotherapist specialised in paediatrics, PhD

Corresponding author

Department of Women’s and Children’s Health

References

Hadders-Algra, M. (2021). Early Diagnostics and Early Intervention in Neurodevelopmental Disorders—Age-Dependent Challenges and Opportunities. Journal of Clinical Medicine, 10(4), 861. https://doi.org/10.3390/jcm10040861

Johnston, M. V. (2009). Plasticity in the developing brain: implications for rehabilitation. In Developmental Disabilities Research Reviews (Vol. 15, Issue 2, pp. 94–101). John Wiley and Sons Inc. https://doi.org/10.1002/ddrr.64

Morgan, C., Darrah, J., Gordon, A. M., Harbourne, R., Spittle, A., Johnson, R., & Fetters, L. (2016). Effectiveness of motor interventions in infants with cerebral palsy: a systematic review. Developmental Medicine & Child Neurology, 58(9), 900–909. https://doi.org/10.1111/dmcn.13105

Morgan, C., Fahey, M., Roy, B., & Novak, I. (2018). Diagnosing cerebral palsy in full-term infants. Journal of Paediatrics and Child Health, 54(10), 1159–1164. https://doi.org/10.1111/jpc.14177

Novak, I., Morgan, C., Adde, L., Blackman, J., Boyd, R. N., Brunstrom-Hernandez, J., Cioni, G., Damiano, D., Darrah, J., Eliasson, A. C., De Vries, L. S., Einspieler, C., Fahey, M., Fehlings, D., Ferriero, D. M., Fetters, L., Fiori, S., Forssberg, H., Gordon, A. M., … Badawi, N. (2017). Early, accurate diagnosis and early intervention in cerebral palsy: Advances in diagnosis and treatment. In JAMA Pediatrics (Vol. 171, Issue 9, pp. 897–907). American Medical Association. https://doi.org/10.1001/jamapediatrics.2017.1689

Novak, I., Morgan, C., Fahey, M., Finch-Edmondson, M., Galea, C., Hines, A., Langdon, K., Namara, M. M., Paton, M. C., Popat, H., Shore, B., Khamis, A., Stanton, E., Finemore, O. P., Tricks, A., te Velde, A., Dark, L., Morton, N., & Badawi, N. (2020). State of the Evidence Traffic Lights 2019: Systematic Review of Interventions for Preventing and Treating Children with Cerebral Palsy. In Current Neurology and Neuroscience Reports (Vol. 20, Issue 2, pp. 1–21). Springer. https://doi.org/10.1007/s11910-020-1022-z

Sakzewski, L., Sicola, E., Verhage, C. H., Sgandurra, G., & Eliasson, A. C. (2019). Development of hand function during the first year of life in children with unilateral cerebral palsy. Developmental Medicine and Child Neurology, 61(5), 563–569. https://doi.org/10.1111/dmcn.14091

Ulrich, B. D. (2010). Opportunities for early intervention based on theory, basic neuroscience, and clinical science. Physical Therapy, 90(12), 1868–1880. https://doi.org/10.2522/ptj.20100040

Von Hofsten, C. (2004). An action perspective on motor development. In Trends in Cognitive Sciences (Vol. 8, Issue 6, pp. 266–272). Trends Cogn Sci. https://doi.org/10.1016/j.tics.2004.04.002

Submitted filename: Response to Reviewers.docx

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5 May 2021

PONE-D-20-28394R1

Early access to physiotherapy for infants with Cerebral Palsy: a retrospective chart review

PLOS ONE

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Reviewer #1: The authors have revised the manuscript thoroughly, and overall revisions are clear and logical. A main point I still have is on the regression analysis. Firstly, the authors did not state the regression models they used are linear or nonlinear. Secondly, the names of regressions the authors used, univariate regression and multivariate regression, are confusing. In both regression analysis, there is only one outcome variable (age at the first visit to a physiotherapist), thus the regressions should be named as simple (linear, I assume) regression for that with only one predictor and multiple (linear, I assume) regression for that with more than one predictors. Thirdly, as to the multivariate regression, the authors did not include an interaction item on referral source * number of risk factors. As mentioned before, I think there may exist interaction effect between referral source and number of risk factors. I am interested in that if the interaction item on referral source * number of risk factors was added in the multivariate regression, how would the results be?

Reviewer #2: Thank you for the opportunity to re-review this manuscript. Major revisions are made to the manuscript, which greatly have improved it's quality, readability and arguments. All my queries are addressed. I have no further comments.

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6 Jun 2021

Response to reviewers comments regarding manuscript PONE-D-20-28394R2

We would again like to thank the reviewers for their valuable and constructive feedback! Below you find our response to the queries. We have highlighted the changes in the manuscript in yellow. Added text is highlighted, while removed text appears as strikethrough.

Journal Requirements

(1) Please review your reference list.

We have reviewed the references and it is complete and correct. Small changes have been made in the text. Additionally, we have replaced reference 6, with a recently published paper (reference 8).

Removed

Reference 6. Morgan C, Darrah J, Gordon AM, Harbourne R, Spittle A, Johnson R, et al. Effectiveness of motor interventions in infants with cerebral palsy: a systematic review. Dev Med Child Neurol. 2016;58: 900–909. doi:10.1111/dmcn.13105.

Replaced

Reference 8. Morgan C, Fetters L, Adde L, Badawi N, Bancale A, Boyd RN, et al. Early intervention for children aged 0 to 2 years with or at high risk of cerebral palsy: international clinical practice guideline based on systematic reviews. JAMA Pediatr. 2021. doi: 10.1001/jamapediatrics.2021.0878.

Review comments to the Author

Reviewer #1

(1) The authors have revised the manuscript thoroughly, and overall revisions are clear and logical. A main point I still have is on the regression analysis. Firstly, the authors did not state the regression models they used are linear or nonlinear. Secondly, the names of regressions the authors used, univariate regression and multivariate regression, are confusing. In both regression analysis, there is only one outcome variable (age at the first visit to a physiotherapist), thus the regressions should be named as simple (linear, I assume) regression for that with only one predictor and multiple (linear, I assume) regression for that with more than one predictors. Thirdly, as to the multivariate regression, the authors did not include an interaction item on referral source * number of risk factors. As mentioned before, I think there may exist interaction effect between referral source and number of risk factors. I am interested in that if the interaction item on referral source * number of risk factors was added in the multivariate regression, how would the results be?

As reviewer #1 assumed, we have used a linear regression model. We have added this to the text. To further clarify our analysis, we have changed the wording from univariate and multivariate to unadjusted and adjusted regression models. For the third point, we will start by thanking the reviewer! This was important and has added valuable information about our sample and our results. We have included the interaction item in the regression analysis and added a figure to illustrate the interaction between referral source and number of risk factors. Text addressing these results have be added where appropriate. Additionally, we have changed the order of the variable “referral source”, so that the NICU graduates are used as the reference.

Sincerely,

Kine Johansen

Physiotherapist specialised in paediatrics, PhD

Corresponding author

Department of Women’s and Children’s Health

Submitted filename: Respons to reviewers.docx

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15 Jun 2021

Early access to physiotherapy for infants with cerebral palsy: a retrospective chart review

PONE-D-20-28394R2

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17 Jun 2021

PONE-D-20-28394R2

Early access to physiotherapy for infants with cerebral palsy: a retrospective chart review

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