Thorax and pelvis kinematics during walking,a comparison between children with and without cerebral palsy: A systematic review

Abstract

BACKGROUND:

Dysfunctional postural control and pathological thorax and pelvis motions are often observed in children with cerebral palsy (CP) and can be considered as an indicator of diminished dynamic stability.

OBJECTIVE:

The aim of this study was to identify the differences between children with CP and typically developing children in three-dimensional thorax and pelvis kinematics during walking.

METHODS:

Three electronic databases were searched by using different combinations of keywords. The methodological quality of the studies was assessed by two researchers with the Strobe quality checklist.

RESULTS:

Ten studies (methodological quality: 32% to 74%) with in total 259 children with CP and 220 typically developing children (mean age: 7.6 to 13.6 year) were included. Compared to typically developing children, children with bilateral CP showed an increased range of motion of the thorax, pelvis and spine during walking. The results of the children with unilateral CP were less clear.

CONCLUSION:

In general, children with bilateral CP showed larger movement amplitudes of the trunk compared to children without CP. This increase in movement amplitudes could influence the dynamic stability of the body during walking. In children with unilateral CP, the results were less obvious and further research on this topic is required.

Keywords

Cerebral palsy gait analysis kinematics thorax spine

1 Introduction

Cerebral palsy (CP) is one of the most common causes of severe motor disability in childhood, with a prevalence varying between 1.5 and 3 per 1000 live births (Himpens et al., 2010). The motor disorders of cerebral palsy are often accompanied by disturbances of sensation, perception, cognition, communication, and behaviour, by epilepsy, and by secondary musculoskeletal problems (Rosenbaum et al., 2007). Despite that the damage remains stable, the clinical consequences may vary with time (Romkes et al., 2007). The Surveillance of cerebral palsy in Europe (SCPE) created a classification system in which CP is divided into several categories: spastic unilateral (USCP), spastic bilateral (BSCP), ataxic and dyskinetic cerebral palsy or a mixed type (McManus, Guillem, Surman, & Cans, 2006).

Complex motor problems such as abnormal gross motor functioning, abnormal fine motor functioning and abnormal motor control are the core features of CP and may lead to gait difficulties (Rosenbaum et al., 2007). Clinical gait laboratories focussed mainly on the lower limbs. This is based on the assumption that the trunk does not contribute actively to gait. The trunk greatly influences the dynamics of the rest of the body, as it accounts for more than half of the body mass. Locomotor control is believed to rely on active neuromuscular control of trunk motion to maintain stability during walking (Winter, MacKinnon,Ruder, & Wieman, 1993). The central nervous system prioritize stability of the trunk over other inferior segments, implying that the stability of body segments would follow a kinematic chain, whereas upper components, i.e. the trunk, are more stable than lower ones, i.e. lower extremities.

The mobility of children with CP may range from an independent walker to assistance dependent or wheeled mobility (Rodby-Bousquet & Hagglund, 2012). Beckung et al. (2008) described the walking ability of children with CP from the SCPE database of which 50% were able to walk, 20% were able to walk but needed a walking aid and the remaining 30% were unable to walk. Children with CP walk with a higher energy cost in comparison to non-disabled children and walking with assistive devices requires even more energy. Rodby-Bousquet and Hagglund (2012) hypothesise that the child’s gross motor function, CP subtype, age, different distances and environments influence the walking performance in children with CP (Rodby-Bousquet & Hagglund, 2012).

Stability during walking is maintained by the locomotor control, which depends on the active control of trunk motion (Degelaen et al., 2012). Postural control aims to maintain the body gravity centre within the support base and is essential for ADL-activities (de Graaf-Peters et al., 2007; van der Heide & Hadders-Algra, 2005). Dysfunctional postural control and motion is often observed in children with CP (Degelaen et al., 2012; Molenaers et al., 2006; van der Heide & Hadders-Algra, 2005) and trunk stabilization is one of the primary goals in the treatment in this group of children. To the best of our knowledge, no systematic literature review is available about the 3D-kinematics of the trunk in children with and without CP. This systematic review focus on studies which used 3D gait analysis, because these techniques can be used to characterize and quantify the dysfunctions of gait in children with CP. In addition, it is also a source of specific information for therapeutic treatment goals and clinical practice (Degelaen et al., 2012; Heyrman, Feys, Molenaers, Jaspers, Monari, et al., 2013).

The aim of this systematic review is to provide a summary of the evidence concerning the differences in trunk kinematics between children with CP and children without neurological disorder determined by three-dimensional (3D) movement analysis. The research question is: “What are the differences in thorax and pelvis kinematics during walking between children with CP and typically developed children?”

2 Method

2.1 Search strategy

Two independent researchers (BDK and LVG) conducted an extensive search in three relevant databases: Web Of Science, PubMed and PEDro (last search 3rd December 2014). The search strategy consisted of different combinations of keywords related to the research-question (Table 1). ‘Cerebral palsy’, ‘walking’, ‘gait’ and ‘biomechanical phenomena’ were used as MeSH-terms for the PubMed database.

The publications were screened subsequently by title, abstract and full text. Additionally, related articles and reference lists of important studies were screened for relevant publications.

2.2 Selection criteria

Published experimental studies, written in English and published after 2000, which made a comparison between children with CP and typically developed children in 3D kinematics of the trunk and/or pelvis during walking, were included. Studies that only measured healthy children or only children with CP without a control group were excluded. All participants had to be less than nineteen years old and must not have undergone surgery or orthopaedic interference, which could affected their walking pattern, in the year preceding the study. The participants had to undergo a gait analysis on a treadmill or walkway, barefoot, with an ankle foot orthosis (AFO) or with a dynamic foot orthoses. The use of other assistive device (e.g. crutches) and any walking direction different from forward was not allowed.

2.3 Methodological quality assessment

Two researchers (BDK and LVG) evaluated, independently, the methodological quality with the Strobe quality checklist (Strobe-statement, 2015). Due to irrelevance, the items “Reasons for non-participation at each stage”, “the flow diagram”, “reporting of category boundaries when continuous variables were categorised” and “estimates of absolute risk” were not applied. The total score was calculated without these items. The maximum score for each article was twenty-six for the assessment of the cross-sectional studies and twenty-seven for the assessment of the case-control studies. The Cohen’s Kappa was calculated to describe the inter-rater reliability.

2.4 Data extraction

Data were extracted by two researchers (BDK and LVG) independently. For each study the characteristics of the participants (number of subjects, age, height, weight, sex, CP subtype and severity), of the intervention (walking surface, gait speed and footwear) and of the outcomes (kinematic values) were collected. Only the results related to the research question of this systematic review (kinematics of the trunk, pelvis, spine and thorax as defined in 3.3.3.) were reported.

3 Results

3.1 Search results

The initial search yielded a total of 372 articles (Appendix 1). After screening on title and abstract, ten articles were selected for further screening. Two articles that didn’t meet the inclusion criteria were excluded after reading the full-texts. Two additional articles, found after screening the references and the related articles, were added to the selection. Finally, a total of ten articles (eight cross-sectional studies and two case-control studies) were enrolled in this systematic review (Fig. 1).

3.2 Methodological quality analysis

The methodological quality of the articles was between 34.62% and 79.63% (Appendix 2 and 3). The lower scores are mainly due to inadequate title and limited information about the description of the setting and the sensitivity analysis, especially the study of Molenaers et al. (2006) which is a published congress contribution. There was decided to exclude none of the articles based on the qualitative analysis because the scores on the items most relevant for this systematic review (objectives, description of participants, data sources, quantitative variables, outcome data, key results and interpretation) were satisfying. The inter-rater reliability was good (Cohen’s Kappa level of agreement between the 2 reviewers) was 0.77 (Range 0.70 to 0.87).

3.3 Descriptive analysis

The characteristics of the study participants and intervention of the selected studies were reported in Table 2.

3.3.1 Study participants

In total 259 children with CP and 220 typically neurologically developed children were included. Seven out of ten studies included exclusively children with diplegia (Akalan, Temelli, & Kuchimov, 2009; Carriero, Zavatsky, Stebbins, Theologis, & Shefelbine, 2009; Cimolin et al., 2007; Degelaen et al., 2012; Galli et al., 2014; Heyrman, Feys, Molenaers, Jaspers, Monari, et al., 2013; Romkes et al., 2007), in which five authors reported that it was the spastic form (Carriero et al., 2009; Cimolin et al., 2007; Degelaen et al., 2012; Heyrman, Feys, Molenaers, Jaspers, Monari, et al., 2013; Molenaers et al., 2006). Two studies included only children with hemiplegia, with one of both confirming that it was the spastic hemiplegia (Salazar-Torres, McDowell, Kerr, &Cosgrove, 2011; Schweizer, Brunner, & Romkes, 2014). The final study included children with spastic hemiplegia and children with spastic diplegia(Molenaers et al., 2006). The mean age of the participants ranged from 7.6 years to 12.24 years for the children with CP and from 7.8 years to 13.6 years for typically developing children. If reported the majority of the children with CP were boys (53 girls and 111 boys) (Degelaen et al., 2012; Heyrman, Feys, Molenaers, Jaspers, Monari, et al., 2013; Romkes et al., 2007; Salazar-Torres et al., 2011; Schweizer et al., 2014). In five studies the sex of the participants was not reported (Akalan et al., 2009; Carriero et al., 2009; Cimolin et al., 2007; Galli et al., 2014; Molenaers et al., 2006).

3.3.2 Type of intervention

All ten interventions consisted of walking at a self-selected, normal or comfortable speed over a walkway. In four out of ten interventions the intervention was performed barefoot (Cimolin et al., 2007; Galli et al., 2014; Heyrman, Feys, Molenaers, Jaspers, Monari, et al., 2013; Romkes et al., 2007). In the studies of Molenaers et al. (2006) and Schweizer et al. (2014), only the children with CP conducted the intervention initially barefoot and subsequently with (hinged) ankle-foot orthoses (Molenaers et al., 2006; Schweizer et al., 2014). In the study of Degelaen et al. (2012) both, children with CP and children with typical neurological development, conducted the intervention initially barefoot followed by walking with ankle-foot orthoses (Degelaen et al., 2012). Three studies didn’t mention the footwear used during the analysis (Akalan et al., 2009; Carriero et al., 2009; Salazar-Torres et al., 2011).

3.3.3 Outcome: Difference in kinematics between healthy controls and patients

All studies evaluated the differences in three-dimensional (3D) kinematics between children with CP and children without CP during walking. Different optoelectric systems were used to measure the 3D kinematics (e.g. Elite system BTS, Milan, Italy and Vicon Oxford Metrics, Oxford, UK) and different outcomes were calculated based on different marker placements.

Only for the trunk a clear definition was found in the study of Schweizer et al. (2014) (Schweizer et al., 2014). For the other various segments, a definition is suggested based on the descriptions of all ten included articles as the thorax, spine and pelvis.

Thorax: The upper part of the trunk between the neck and the abdomen

Spine: The spinal or vertebral column

Pelvis: The space or compartment surrounded by the pelvic girdle (bony pelvis). The pelvic bones and sacrum form the pelvic girdle.

Trunk: The entirety of the thorax, spine and pelvis (Schweizer et al., 2014).

According to these definitions the results of the studies of Galli et al. (2014) and Degelaen et al. (2012) became classified under the term “thorax” despite the use of the term “trunk” in the article (Degelaen et al., 2012; Galli et al., 2014).

3.3.3.1. Thorax. Six studies examined the kinematics of the thorax (Table 3) (Degelaen et al., 2012; Galli et al., 2014; Heyrman, Feys, Molenaers, Jaspers, Monari, et al., 2013; Molenaers et al., 2006; Romkes et al., 2007; Schweizer et al., 2014). These studies agreed that the absolute ROM of the thorax in the three planes (transverse, coronal and sagittal) was greater in children with diplegia compared to typically developing children. Heyrman et al. (2013) found a difference in the relative ROM in the coronal and sagittal plane, but these differences were only significant between the control group and children with GMFCS II. This ROM was larger in the children with spastic diplegia GMFCS II compared to the control group (Heyrman, Feys, Molenaers, Jaspers, Monari, et al., 2013). The study of Schweizer et al. (2014) indicated that the ROM of the thoracic lateroflexion was smaller in the control group compared to the affected side in the hinged ankle-foot orthoses (hAFO) condition in children with hemiplegia. The mean internal rotation of the thorax was increased in children with hemiplegia and the thorax rotated more on both sides and in both conditions, barefoot walking and walking with hAFO, in children with hemiplegia compared to the control group (Schweizer et al., 2014).

3.3.3.2. Spine. Only three studies measured the movements of the spine (Table 4) (Heyrman, Feys, Molenaers, Jaspers, Monari, et al., 2013; Romkes et al., 2007; Schweizer et al., 2014). Romkes et al. (2007) found a significant larger spinal tilt in children with diplegic CP, compared to children without CP. In contrast, Heyrman et al. (2013) found only a difference in the range of the kyphosis of children with GMFCS II and normal developing children (Heyrman, Feys, Molenaers, Jaspers, Monari, et al., 2013; Romkes et al., 2007). The motion in the coronal plane was smaller in the control group than in the children with diplegic CP in the study of Romkes et al. (2007) (Romkes et al., 2007) and Schweizer et al. (2014) found that the typically developing children had less spine rotation on both sides during walking than hemiplegic children with hAFO (Schweizer et al., 2014).

3.3.3.3. Pelvis. The kinematics of the pelvis has been studied more extensively (Akalan et al., 2009; Carriero et al., 2009; Cimolin et al., 2007; Heyrman, Feys, Molenaers, Jaspers, Monari, et al., 2013; Romkes et al., 2007; Salazar-Torres et al., 2011; Schweizer et al., 2014) than the other segments of the trunk in children with CP (Table 5). The results of the different studies correspond well: each of the four studies that measured the kinematics of the pelvis in children with diplegic CP indicated that there is a significant difference between the ROM of the pelvis tilt between the two groups. The children with diplegia had, in average, an increased anterior tilt during walking and furthermore the ROM of the pelvis tilt was increased (Carriero et al., 2009; Cimolin et al., 2007; Heyrman, Feys, Molenaers, Jaspers, Monari, et al., 2013; Romkes et al., 2007). Only Akalan et al. (2009) found an increased pelvic tilt in the stance phase and found no increased ROM of the pelvic tilt in diplegic children with increased femoral anteversion (Akalan et al., 2009). Schweizer et al. (2014) found an increased external rotation on the hemiplegic side and an increased internal rotation on the unaffected side for both conditions (barefoot walking and walking with hAFO). Salazar-Torres et al. (2011) compared for how many standard deviations the results of the children with hemiplegic CP differed from the results of the normally developing children. In the majority of the spastic hemiplegic children (60.4%) the pelvic tilt range increased, only 14.3% walked with increased pelvic obliquity range, 25.3% walked with reduced pelvic obliquity range and 23.1% walked with increased pelvic rotation. Of the 91 children in this study with spastic hemiplegic CP: 28.6% walked with a certain degree of anterior tilt, 61.6% walked with a certain level of pelvic retraction of the affected side, 36.3% walked with the affected side down and 22% walked with the affected side up (Salazar-Torres et al., 2011).

3.3.3.4. Trunk. Only one study reported the movement amplitudes of the trunk (Table 6) (Schweizer et al., 2014). This study had no exact quantitative results displayed in the article, there was only reported that children with hemiplegia showed more tilt of the entire trunk (pelvis, thorax and spine) on both sides and to both conditions, barefoot walking and walking with hAFO, compared to children without CP (Schweizer et al., 2014).

4 Discussion

This systematic review identified ten articles that compared the kinematics of the thorax and pelvis in children with and without CP. The results indicate increased movement amplitude of the trunk (thorax, spine and pelvis) in children with CP compared with typically neurologically developed children. The increased movement amplitude of the trunk is considered an indicator of diminished dynamic stability (Heyrman, Feys, Molenaers, Jaspers, Monari, et al., 2013).

4.1 Comparison between children with diplegia and typical neurological developed children

Children with diplegia have an increased ROM of the thorax, the pelvis and the spine in the sagittalplane. The ROM of the thorax is also increased in the two other planes in children with diplegia. Degelaen et al. (2012) argued that the frontal motion control is programmed first, and subsequent sagittal motion control must take into account previously occurring effects on sagittal control due to frontal commands. Even though the frontal motion control is programmed first, a greater difference in absolute ROM of the thorax in the frontal plan compared to the sagittal plane between children with and without CP of the type diplegia was found first by Degelaen et al. (2012) and confirmed by this systematic review. Degelaen et al. (2012) declared that “This alteration of the walking strategy may represent compensation by reduction in the distal degree of freedom, which is typical in children with CP and manifests notably with equinus in order to ensure both foot clearance at the onset of the swing phase and forward progression throughout this phase.” (Degelaen et al.,2012).

In addition to the increased ROM of the pelvis in the sagittal plane, Heyrman et al. (2013) and Akalan et al. (2009) found a double bump pattern of the pelvis to anterior tilt only in children with spastic diplegia, although Heyrman et al. (2013) recognized this only at GMFCS II (Akalan et al., 2009; Heyrman, Feys, Molenaers, Jaspers, Monari, et al., 2013). Also in the graphs in the article of Romkes et al. one could recognise a double bump pattern of the pelvis (Romkes et al., 2007). The first bump of the pelvis to anterior tilt is during midstance, the second during initial swing. The double bump pattern of the pelvis in the sagittal plane is a possible CP (spastic diplegia) effect, since it does not occur in typically developing children. It is possibly related to the inability to dissociate pelvic and hip movements because of weak hip extensors and/or spastic hip flexors (Akalan et al., 2009).

4.2 Comparison between children with hemiplegia and typical neurological developed children

The results of the children with hemiplegia are less clear. In this review, three articles that included results of children with hemiplegia were incorporated. One of the three studies did not specify that these results of the kinematics were significant (Molenaers et al., 2006). A second study calculated no means per group (CP-group and control group) but compared instead for how many standard deviations the pelvic kinematics of each child with hemiplegia differed from the results of normally developing children. The third article presented the results in a graphical overview and discussed them, but this article gave no exact value of the measurements (Schweizer et al., 2014). Other articles could not confirm the results of the third article for lack of well-documented studies on children with hemiplegia. Further research that describes the differences between the kinematics of the entire trunk of children with CP type hemiplegia andchildren without CP, is required.

Only the study of Schweizer et al. (2014) compared children with hemiplegia that walked with AFO’s to typically developing children that walked barefoot. The study concluded that the ROM of the thoraciclateroflexion and the spine rotation showed a clinically relevant increase compared to the control group. This increase was not observed in the hemiplegia group that walked barefoot. Molenaers et al. (2006) is of the opinion that: “Providing stability in the distal joints through the application of AFO’s improved pelvic stability, but provoked more trunk motion. Increased trunk ROM might be considered as a compensatory strategy for the reduced ankle power generation at push-off, caused by AFO’s, combined with increased step lengths and walking velocity” (Molenaers et al., 2006).

4.3 Comparison between children with different GMFCS levels

The study by Heyrman et al. (2013) made a distinction between GMFCS I and GMFCS II in the interpretation of the results. Children with GMFCS II showed significantly increased ROM at almost alllevels (thorax tilt, thorax lateral bending, thorax rotation, pelvic tilt, spine kyphosis and lordosis) compared to typically developing children, while only case of lateral thorax instability was observed in children with GMFCS I during walking (Heyrman, Feys, Molenaers, Jaspers, Monari, et al., 2013). Based on this article, it can be concluded that the ability to control the trunk movements varies between children with different degrees of motor involvement in children with spastic diplegia.

4.4 Methodological considerations

The gait analysis was performed in the same way in all studies by walking over a walkway at a self-selected, normal or comfortable speed. The footwear was not indicated in three studies, but in the other studies gait analysis was always completed barefoot and occasionally followed by additional trials in which the children walked with orthoses. In all studies the differences in 3D kinematics during walking was measured with 3D movement analysis (Elite system BTS, Milan, Italy; Vicon Oxford Metrics, Oxford, UK). 3D movement analysis is used to assess the dysfunctions during gait quality and quantity in children with CP (Degelaen et al., 2012; Heyrman, Feys, Molenaers, Jaspers, Monari, et al., 2013). For directing the treatment for the lower limbs of children with CP, 3D movement analysis is considered a standard tool. Moreover the surplus value of 3D movement analysis has also been demonstrated for upper limb pathology (Heyrman, Feys, Molenaers, Jaspers, Van de Walle, et al., 2013).

4.5 Limitations of this review

In all articles included in this systematic review, the trunk is divided into one, two or three rigid structures for the measurement of the 3D kinematics. Actually the trunk is a multiple segmental structure. A simplification of the trunk results in loss of information on small segmental movements (Heyrman, Feys, Molenaers, Jaspers, Van de Walle, et al., 2013). In addition, there is no consensus regarding the definition of the various segments (trunk, thorax and spine), which makes generalisation difficult. Terms such as trunk and thorax are often used interchangeably. None of the ten articles clarified the definitions of every segment. Only the trunk is defined by Schweizer et al. (2014) as a combination of, respectively, the thorax, spine, and pelvis (Schweizer et al., 2014). There is a need for a well-defined description of the segments in 3D gait analysis. Furthermore, there are differences between the included studies in marker placement, the number of included segments and the definition of anatomical axes. To optimize upcoming research, one optimal trunk model should be developed. Some studies included in this systematic review used the Plug-in Gait model or anatomical landmarks of the upper body for the measurements of the 3D kinematics of the trunk.

A limitation of most of the articles included in this systematic review is that spatiotemporal parameters like e.g. step length and walking speed were not taken into account. However a previous study of Schwartz et al. (2008) indicated that walking speed influences the kinematic parameters of typically developing children in both the frontal, sagittal and transversal plane (Schwartz, Rozumalski, & Trost, 2008). Five studies examined the spatiotemporal parameters and concluded that the walking speed is lower in children with spastic diplegia compared to typically developing children (Akalan et al., 2009; Carriero et al., 2009; Galli et al., 2014; Heyrman, Feys, Molenaers, Jaspers, Monari, et al., 2013).

4.6 Clinical implications and implications for further research

In one of the recent studies of Heyrman et al. (2014), it was concluded that movements of the trunk during walking are not only compensatory but the trunk movements also reflect an underlying trunk control deficit (Heyrman et al., 2014). Children with CP have marked difficulties in adapting the degree of postural muscle contraction to the specifics of the situation. They show mild to moderate problems in recruiting direction-specific activity and show dysfunctions in the fine-tuning of postural adjustments (de Graaf-Peters et al., 2007). Improving segmental trunk postural control should be an important goal of the therapy. This objective can be achieved either by training or by compensation with the use of trunk support (Curtis et al., 2015).

Literature on the integration of this 3D kinematics with the kinetics and EMG signals is still missing. In CP, impaired trunk control has been shown to affect performance of activities of daily life (Brogren, Hadders-Algra, & Forssberg, 1998; Prosser, Lee, Barbe, VanSant, & Lauer, 2010). In order to provide the best therapeutic setting for children with CP, the relation between dynamic stability and increased trunk motion need to be more clarified. Further research on this subject could provide more insight into trunk control in both healthy children and children with CP (Galli et al., 2014).

5 Conclusion

Overall findings indicate a difference in kinematics of the thorax, spine, pelvis and trunk in children with and without CP during walking, particularly in terms of increased movement amplitudes in children with CP type diplegia compared to typically neurologically developed children. The increased movement amplitude of the trunk is considered an indicator of diminished dynamic stability. These increased trunk ROM can also be considered as a compensatory strategy for the reduction of ankle power generation at push off. This could either be caused by the biomechanical constraints associated by the AFO’s or by the spastic muscles. Gait characteristics of CP children are determined largely by spasticity in muscles whose action is marked in the sagittal (psoas, hamstring, gastrocnemius) and frontal (hip adductors) planes. The spastic types of CP are characterized by imbalances in muscle activity across joints (Cobeljic, Bumbasirevic, Lesic, & Bajin, 2009).

With growth, the imbalance between agonist and antagonist often progresses to muscle contracture, joint and bony deformities. Because this implicates a reduction of the distal degree of freedom in the lower limbs, children may search for other movement strategies to ensure forward progression in stance and foot clearance in swing. Improving dynamic stability and maintaining the overall mobility should be important goals of the therapy. In the future, researchers should use a generally accepted definition of the various segments as well as a generally accepted trunk model in 3D motion analysis of the trunk and integrated kinetics and EMG signals in order to have a better inside into the organization and effect of trunk motion on gait and other functional activities. Longitudinal studies were trunk motion, muscle activity and joint mobility are taken into account should give us the possibility to have a better inside into the development of different motor strategies (compensatory or lack of dynamic stability) in children with CP.

Conflict of interest

We confirm that there are no conflicts of interest associated with this publication and there has been no financial support for this work that could have influenced its outcome.

Footnotes

Appendix

Appendix 3

Quality assessment of included studies: Strobe quality checklist for case-control studies

		Schweizer K.	Degelaen M.	Total
		et al. (2014)	et al. (2012)	(max. value 2)
1. Title and abstract	A	0	0	0
	B	1	1	2
2. Background/rationale		1	1	2
3. Objectives		1	1	2
4. Study design		1	0	1
5. Setting		1	0	1
6. Participants	A	1	1	2
	B	1	0	1
7. Variables		1	1	2
8. Data sources/ measurement		1	1	2
9. Bias		1	1	2
10. Study size		1	0	1
11. Quantitative variables		1	1	2
12. Statistical methods	A	1	1	2
	B	1	0	1
	C	0	0	0
	D	1	0	1
	E	0	0	0
13. Participants	A	0.5	0	0.5
	B	NA	NA	NA
	C	NA	NA	NA
14. Descriptive data	A	1	1	2
	B	0	0	0
15. Outcome data		1	1	2
16. Main results	A	0	0	0
	B	NA	NA	NA
	C	NA	NA	NA
17. Other analyses		0	0	0
18. Key results		1	1	1
19. Limitations		1	0	1
20. Interpretation		1	1	2
21. Generalizability		0	0	0
22. Funding		1	0	1
Total (max 29)			21.5	13
Percentage score			74.13	44.82
Cohen’s Kappa level			0.741	0.721

All the items could score a maximum of 1 point when all the criteria were fulfilled, 0.5 points when only a part of the criteria were reached and 0 points when none of the criteria were fulfilled. NA = not applicable. The total score (with a maximum value of 30) was calculated without the non-applicable item.

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