The association between crawling as a first mode of mobilisation and the presentation of atraumatic shoulder instability: a retrospective cohort study

Abstract

Background and purpose

To investigate if there is an association between whether an infant crawls as their first mode of mobilisation and the subsequent presentation of atraumatic shoulder instability.

Patients and methods

A retrospective cohort of 50 consecutive patients who had presented to a national specialist centre for shoulder instability with a diagnosis of atraumatic instability was compared with a cohort of 50 participants who did not have shoulder instability. Primary outcomes were presence of atraumatic shoulder instability and whether or not the patient crawled as their first mode of mobility. A Pearson chi-squared test was used to evaluate associations.

Results

There was a significant association between crawling and shoulder instability (X²(1) ≥ 11.93, p = 0.001) with a higher prevalence of non-crawlers in the group with shoulder instability compared to the control group.

Interpretation

There may be an association between developmental milestones and atraumatic shoulder instability. It cannot be concluded from this study whether association is causal and additional research is needed to further investigate this relationship. Asking patients presenting with shoulder instability about their developmental milestones as part of a full subjective history could guide a more targeted sensorimotor rehabilitation programme.

Introduction

Atraumatic shoulder instability is defined as a symptomatic abnormal motion at the glenohumeral joint, causing pain or a sense of joint displacement (subluxation or dislocations) ¹ with no preceding traumatic event. Ninety-five per cent of shoulder dislocations are attributed to a traumatic event, with the remaining 5% atraumatic. ² Overall prevalence of atraumatic shoulder instability in the United Kingdom is not known. However, despite being a small cohort, these patients have the potential to generate high healthcare costs and socioeconomic burden per patient, ³ via regular presentation to Accident and Emergency departments and reduced work or school attendance.

Classification of shoulder instability using the Stanmore triangle ¹ is widely accepted, with those classified as Type III presenting with no structural pathology and an element of abnormal muscle recruitment at the shoulder girdle. Currently high-level evidence for the treatment and management of type III atraumatic shoulder instability is lacking. ⁴ The 2019 British Elbow and Shoulder Society guidelines ⁵ have recommended that conservative management should be the first line of management in this cohort; however, currently this is predominantly based on expert opinion, cohort studies and trials with short-term outcomes.

The reason why some people develop abnormal muscle recruitment at their shoulder is not fully understood and the evidence to support any one theory is extremely limited. A high prevalence of both localised shoulder and global soft tissue laxity has been reported in patients presenting with shoulder instability. ⁶ This leads to a theory that secondary poor joint proprioception ⁷ could affect sensorimotor pathways and cause abnormal muscle recruitment. The increased degrees of freedom at the shoulder joint and subsequent displacement of the humeral head from the glenoid could also cause a protective muscle recruitment or spasm at the shoulder girdle. There may be additional or alternative reasons for abnormal muscle recruitment at the shoulder girdle. Anecdotal reports at the Royal National Orthopaedic Hospital from patients and their parents of poor childhood coordination, and of ‘bottom shuffling’ instead of crawling, led to our hypothesis that there may be an association between developmental milestones and the later presentation of atraumatic shoulder instability. There have been no studies investigating the relationship between developmental milestones and shoulder dysfunction.

It is observed in clinical practice that patients with atraumatic shoulder instability commonly have generalised joint hypermobility (GJH). Joint hypermobility results from ligamentous laxity, which is usually determined by the genes that encode for connective tissue. ⁷ In a systematic review of the literature, Clark and Kattab ⁸ concluded that there was a paucity of literature relating to an association between GJH, joint hypermobility syndrome, impaired motor control, motor delay and developmental coordination disorder in children. They report that there is evidence that joint hypermobility is associated with motor delay and motor control impairments in young children, but this is limited and not conclusive.

The primary aim of this study was to investigate whether there is an association between whether an infant crawls as their first mode of mobilisation and the later presentation of atraumatic shoulder instability. A secondary aim was to see if there was an association between whether the patient was hypermobile and whether they crawled, which would lead to the hypothesis that hypermobility is what links the two variables.

Methods

Ethics

This project was registered as a service evaluation by the host institution and no ethical approval was required.

Design

A retrospective review of patient records formed the basis of this study. A dataset was recorded for all patients attending a physiotherapy led shoulder instability clinic which included a question regarding the gross motor developmental milestone of crawling. This question was added in February 2012, which is when records were reviewed from. The review of the patient records ceased after 50 patients had been included. The review of records was performed by the lead author (DW).

Participants

Shoulder instability group. Patients referred to a national specialist centre for atraumatic shoulder instability between February 2012 and February 2014 who were triaged onto a non-surgical pathway to a physiotherapy led clinic were included. Demographics of the participants can be found in Table 1. Patients whose first point of contact at the hospital was at a physiotherapy led clinic were included. Patients whose first point of contact was with a surgical consultant were not included, because they did not typically ask about crawling in their assessment. Following assessment, the type of shoulder instability was classified as per the Stanmore Triangle ¹ and patients classified as having Type III/II or Type III instability were included in this retrospective study. Patients who did not know whether they crawled or not (typically those who did not attend with a parent) were excluded from the study.

Table 1.

Demographics.

	Instability group	Normal group
Gender	Male = 11 Female = 39	Male = 4 Female = 46
Age (years)	No. of participants	No. of participants
<18	32	0
18–24	12	2
25–34	3	20
35–44	3	17
45–54	0	8
55–64	0	3
Median	17	Data not available
Mean	17.5	Data not available
SD	6.31	Data not available
Minimum	9	Data not available
Maximum	39	Data not available

Normal group. Staff members of the therapy department (allied health professionals) were invited to complete an online survey. Exclusion criteria were if they had any history of shoulder instability.

Outcomes

Participants were asked if they crawled and if they did crawl whether they crawled first or walked first. Patients who crawled as their first mode of ambulation were categorised as ‘Crawled’. Those patients who did not crawl at all or walked first were categorised as ‘Not Crawled’. The patient groups were also asked the age at which they started independent walking. It was an assumption that if the infant walked before they crawled, they did not spend a significant time crawling.

The presence of GJH was assessed in the patient group using the Beighton score. ⁹ Those with a score of >4 were categorised as hypermobile and those with a score of <4 were categorised as not hypermobile. ¹⁰ Since this study was carried out the nosology for diagnosing hypermobility has been updated. ⁷ It is possible that these patients would now fit into a diagnosis of either Hypermobile Elhos Danlos or Hypermobility Spectrum Disorder. However, the subjective information which would have allowed us to categorise these patients using the new nosology was not gathered at the time of data collection. Therefore, for the purpose of this article the generic term hypermobility will be used to describe those patients who fulfilled the criteria for diagnosing GJH.

Data analysis

The association between the presence of atraumatic shoulder instability (yes/no) and whether the subject crawled as their first mode of mobility (crawled/not crawled) was analysed using a Pearson chi-squared test of univariate regression.

In the patient group a Pearson chi-squared test was also used to evaluate associations between whether the participant crawled (yes/no) and the presence of hypermobility (yes/no).

The mean age of independent walking was also calculated for both groups.

Data were analysed using SPSS (version 16.0).

Results

Demographics

Table 1 contains patient demographics.

The proportion of male to female was similar in both groups.

Age of independent walking

Mean age of independent walking in the patient group was 12 months (SD 3.04) and 12.98 months (SD 3.30) in the normal group. There was no significant difference between groups (p = 0.13).

Crawling

There was a significant association between crawling and shoulder instability (X²(1) ≥ 11.93, p = 0.001) with a higher prevalence of non-crawlers in the group with shoulder instability compared to the group of normals. This can be seen in Figures 1 and 2.

Figure 1.

Instability group’s first mode of mobility. Crawled: n = 33; Not Crawled: n = 17.

Figure 2.

Normal group’s first mode of mobility. Crawled: n = 48; Not Crawled: n = 2.

Hypermobility and first mode of mobility

There was no significant association between hypermobility and the patient’s first mode of locomotion (X²(1) ≥ 1.739, p = 0.227). Prevalence of hypermobility in the group of crawlers compared to non-crawlers can be seen in Figures 3 and 4.

Figure 3.

Presence of hypermobility in crawling group. Hypermobile: n = 19.

Figure 4.

Presence of hypermobility in non-crawling group. Hypermobile: n = 13.

Discussion

A retrospective cohort of patients with atraumatic shoulder instability was used to fulfil the primary aim of this study which was to investigate if there is an association between whether an infant crawls as their first mode of mobilisation and the later presentation of atraumatic shoulder instability. A secondary aim was to see if there was an association between whether or not the patient was hypermobile and whether they crawled, which would lead to the hypothesis that hypermobility could be what links the two variables. There was a significant association between crawling and shoulder instability with a higher prevalence of non-crawlers in the group with shoulder instability compared to the group of normals, which addressed the primary aim. There was no significant association between hypermobility and the patient’s first mode of locomotion which addressed the secondary aim.

This is the first known study investigating the association between developmental milestones and shoulder instability and so it is not possible to discuss how these results compare with existing evidence. Nof and Rosenthal ¹¹ reported an association between age of independent walking and temporomandibular joint dysfunction, which is in agreement with the current study that there may be a link between developmental milestones and dysfunctional neuromuscular presentations. The lack of association between GJH as measured by the Beighton Score ⁹ and crawling is in agreement with studies which report no association between developmental coordination delay and joint hypermobility,^10,12,13 but conflicts with the studies which do suggest an association.^14,15 However, it should be taken into consideration that the above studies measured joint hypermobility and a measure of coordination delay concurrently, whereas this study measured joint hypermobility at a much later date (age range 9 to 39) which cannot confirm or exclude the presence of absence of hypermobility as an infant. Mean age of independent walking in our patient cohort was 12.02 (SD 3.04) months which falls within normal limits (8.2 to 17.6 months) ¹⁶ and 12.98 in the normal group. There was no significant difference between groups. This suggests that not all gross motor milestones were affected in the shoulder instability group.

There are several possible alternative explanations for these findings. Firstly, patients with type III shoulder instability may have had developmental coordination delay causing both a lack of crawling and an impairment of their neuromuscular coordination at their shoulder. Secondly, lack of crawling due to developmental coordination delay or another unknown reason may have meant the patients missed out on a key neurodevelopmental activity which may be necessary for developing normal muscle coordination at the shoulder girdle. As well as more global reasons for delayed or lack of crawling, there are a number of localised causes such as obstetric brachial plexus injury, none of which we specifically asked about in our dataset. Alternatively, localised tissue laxity at the shoulder could be associated with the lack of crawling. A limitation of this study was that specific shoulder laxity was not assessed, as it does not form part of the Beighton assessment. It is likely that the patients had localised laxity, as anecdotally this is a common finding in this cohort, but this study’s methods means this remains unknown. It also means that we cannot exclude an association between tissue laxity at the shoulder and lack of crawling. Tissue laxity could be the cause of both difficulty with crawling and shoulder instability. Tissue laxity has been reported to reduce proprioception ⁷ which could impair sensorimotor control. Motor function relies on an effective and integrated sensory system. Type III shoulder instability is defined by the lack of structural findings. Muscle structure and electromyography studies are normal, but muscle recruitment, tone and sequencing are frequently affected. This suggests an issue with either sensory systems or the systems which integrate the sensory and motor pathways, although there is also the potential effect of psychosocial factors (which are anecdotally commonly observed in this cohort) on sensorimotor systems. Finally, a concurrent but non causal association between tissue laxity and neurodevelopmental delay must also be considered secondary to pleiotropy, where one gene can influence more than one seemingly unrelated traits.

There were a number of limitations in this study. A retrospective study design means that no causal associations can be extracted. As these data were non-parametric, a sample size calculation was not appropriate, but it is acknowledged that a larger cohort may have elicited a different result. The samples were not matched, for example the majority of the instability group were under 18, whereas the majority of the normal group were between 25 and 44. Matching the samples would have reduced the influence of confounding variables. With regards to outcome measures, a Beighton score in children and adolescents ≥6 is now considered more relevant in new published guidelines. ¹⁷ More than two-thirds (32/50) of the patient cohort patients were <18 and half of these patients (18/32) were classified as hypermobile using the ≥5 cut off. This may have overestimated the number of hypermobile patients in the sample. However, 12 of these potentially wrongly classified patients were crawlers and 6 were classified as non-crawlers, which meant the overall result would not have changed. The Beighton score has been reported to be a valid and reliable measure of joint hypermobility.¹⁸

It was also assumed that if a child walked before he/she crawled that they did not spend significant amount of time crawling. This information was unknown, and this assumption could have led to an overestimation of the number of non-crawlers and a type 1 error. Patients were only included in the study if they attended with a parent who had knowledge of their developmental milestones which introduced sampling bias and may account for the high number of children and adolescents included in the study. Eighteen patients were excluded (26.5% of total sampled). The definition of crawling was not made clear to the participants. There is a chance this could have led to an overestimation of the numbers of crawlers and a type 2 error. Showing them a video of crawling, for example, could have reduced this error, and should be considered for any future replication of this study.

A significant limitation of the study was the risk of recall bias from the parents which could have affected the accuracy of the results. Parents were being asked to recall their child’s developmental milestones from an average of 17.5 years previously. There is some evidence that parents can reliably recall developmental milestones, with Majnemer and Rosenblatt ¹⁹ reporting parents accurately recalled age of walking. However, there are other studies that conclude that recall is poor and that factors such as existence of siblings could affect its reliability.^20,21 None of these studies look at recall over a period of time greater than five years. Participants could have been informed in advance of the questions to allow them to access records or photographs, which would have increased the accuracy of their responses. There was reduced risk of recall bias with the normal group as they had the opportunity to contact their parents or access records. This however also makes comparison between the groups questionable.

It must also be acknowledged that the use of allied health professionals as the normal group may have introduced additional bias, as some of them may have had access to, and background knowledge of, the study hypothesis. Using a patient group without shoulder instability would reduce this bias.

Whether these results can be translated to the whole population of patients with atraumatic instability of the shoulder is questionable. Patients are usually referred to a tertiary centre when they are not progressing with treatment locally. Therefore, it is likely that the cohort included in this study was not representative of the whole shoulder instability population and may represent a specific sub-cohort.

This is a pragmatic, unfunded study that was developed in response to anecdotal evidence of patients with atraumatic shoulder instability not crawling. The purpose of this study was not to identify a causal relationship between not crawling and shoulder instability, but to shed some light on the phenomenon. This research highlights that there may be an association between not crawling and shoulder instability and therefore further investigations into causal relationships of this phenomenon are warranted.

Implications for clinical practice

Current British Elbow and Shoulder Society guidelines (2019) for the management of atraumatic shoulder instability recommend that conservative treatment in the form of predominantly an exercise-based approach should be the first line of management in this cohort. ⁵ This study does not provide any evidence that would warrant any change in practice. It does however generate an insight into the association between crawling and shoulder instability and therefore asking about developmental milestones as part of a comprehensive subjective assessment could help to identify type III shoulder instability.

Conclusion

This study reports that there may be an association between the neurodevelopmental milestone of crawling and atraumatic shoulder instability. Whilst it is not possible to derive from this data that the association is causal, this research does generate some important questions surrounding this relationship. More research is warranted to further investigate this association, which may help us to understand the role of the sensorimotor systems in atraumatic shoulder instability. A better understanding of the reason for the impaired motor control that is frequently evident in atraumatic shoulder instability may guide more targeted treatment programmes.