Introduction

Musculoskeletal injuries are a well-known but rather neglected complication of epileptic seizures and particularly tonic–clonic seizures; they significantly reduce the quality of life for the affected patients. Despite growing scientific interest, the number of studies addressing these injuries and their risk factors is limited. Among the vast spectrum of different musculoskeletal injuries, shoulder injuries account for a major percentage; these include fractures of the humerus, scapula or clavicle, acute or recurrent shoulder dislocations, rotator cuff lesions, or a combination of these injuries [1, 2]. Detailed descriptions of specific shoulder lesion characteristics are difficult to obtain from large cohorts or cross-sectional studies which focus primarily on other epidemiological aspects; these lesions are included in broader categories such as, “upper extremity injuries” or “other fractures”. In contrast, the few studies dedicated to the orthopedic treatment of shoulder injuries in patients affected by seizures are abundant in terms of details, but limited sample size and lacking in information concerning the neurological history [3,4,5,6,7,8]. The aim of this study was to analyse the epidemiology of a large cohort of patients suffering from seizure-related shoulder injuries and to provide detailed information on trauma dynamics and specific lesion characteristics.

Methods

The goal of this study was to describe the epidemiology and the specific features of shoulder injuries occurring during seizures in a selected subgroup of patients with epilepsy.

A screening for upper limb injuries was performed on all patients referring to a tertiary epilepsy center from January 2015 to June 2020 with an anamnestic questionnaire completed at the time of stationary admittance or during outpatient consultations, under the supervision of a clinician. For patients ruled in during this screening phase, relevant clinical and radiological records were collected and reviewed to investigate dynamics and characteristics of shoulder injuries.

Adult patients suffering from a bony or soft tissue shoulder injury sustained during a seizure were considered for inclusion. Patients with injuries sustained in paediatric age, caused by other aetiologies than a seizure or affecting other regions of the body were excluded.

Data collected during clinical care were integrated by telephonic interviews to gather full information on the injury in terms of trauma dynamics, bone or soft tissue involvement, affected side, as well as the type and direction of instability for glenohumeral dislocations. If surgical treatment was required, the type of intervention and possible subsequent complications were recorded.

Demographic data, as well as data regarding diagnosis and treatment of epilepsy and information on shoulder injuries, were entered into a spreadsheet for analysis. Statistical analysis was performed using GraphPad Prism v 6.0 software (GraphPad Software Inc.). The Shapiro–Wilk normality test was used to evaluate the normal distribution of the sample. Continuous variables were expressed as the mean ± standard deviation (SD) or medians and first and third quartiles [Q1–Q3], as appropriate. The differences between the groups of patients for continuous variables were evaluated with unpaired Student’s t test or Mann–Whitney test according to the characteristics of the data distribution. Categorical variables are expressed in numbers of cases and frequencies; their differences were tested using with the chi-squared test or Fisher’s exact test. Variables significant at univariate analysis were inserted in a multivariable logistic regression model to correct for confounding and avoid multiple test correction and to estimate multivariate odds ratios (ORs) for evaluating the association between covariates and development of recurrent instability, of perioperative complications and of recurrent instability as a complication after surgical treatment. For all analyses, the significance level was set at p value lower than 0.05.

This audit of data collected during clinical care was approved by the local medical ethics committee (Ethikkommission an der Medizinischen Fakultät der Rheinischen Friedrich-Wilhelms-Universität Bonn, No. ID 245/19).

Results

Demographics, clinical history, and trauma dynamics

Approximately 15,000 clinical consultations were evaluated in the screening phase and 106 patients with shoulder injuries met the inclusion criteria. Baseline neurological diseases included focal epilepsies (45%), unknown epilepsy types (32%), genetic generalized epilepsies (19%), and acute symptomatic seizures (4%). Average age at the time of injury was 39.7 ± 17.5 years and a male predominance was recorded (65%). No significant differences were encountered in the average age of the male and female patients. Bilateral injuries occurred in 29 patients (27.4%) and, of those, 17 patients had bilateral shoulder injuries which occurred simultaneously (Fig. 1). In 23.6% of the cases, shoulder injury occurred during the first seizure. At the moment of injury, 52.8% were not taking any antiepileptic drugs (AEDs), either because their epilepsy was not yet diagnosed, or because the medication had been discontinued due to low patient compliance, or a medical withdrawal from the medication was attempted.

Fig. 1
figure 1

Pie charts illustrating the affected side and the distribution of bilateral lesions in the study cohort

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A description of the trauma dynamics derived from direct observation by witnesses or during in-hospital monitoring was available for 76 patients (Table 1); in 47 cases (61.8%), the shoulder injury was caused solely from the muscular activation during the seizure without any external acting force or fall. In the remaining 29 cases (38.2%), the shoulder injury was caused by uncontrolled falls with direct impact on the shoulder joint. No patients sustained a shoulder lesion after a fall on the outstretched hand. The subgroup of patients experiencing shoulder injuries due to muscular activation was younger at the time of injury (p = 0.0054). Bilateral shoulder injuries and shoulder dislocations occurred much more frequently within the subgroup of patients experiencing shoulder injuries due to muscular activation (p = 0.011 and p < 0.0001, respectively), whereas fractures occurred much more frequently within the subgroup of patients experiencing shoulder injuries due to uncontrolled falls with impact on the shoulder (p = 0.0149).

Table 1 Trauma dynamics in the study population
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Specific injuries subgroups and treatment results

The detailed description of the incidence of specific injuries (fractures, soft tissue injuries, combined and bilateral events) as well as the subgroup analysis of associations between demographic variables and different lesions are presented in Appendix A. Figure 2 and Table 2 summarize different aspects related to shoulder instability and illustrate risk factors for the development of recurrent instability. Data regarding surgical procedures and complications were available for 57 of the 64 surgically treated patients and are presented in Appendix B. The overall postoperative complication rate was 38.7%, with recurrence of instability being the most frequently reported complication (62.5%).

Fig. 2
figure 2

Pie charts illustrating different aspects related to shoulder instability. A Percentage of patients affected by shoulder instability. B Distribution of soft tissue and bony lesions. C Distribution of recurrent instability. D Direction of instability

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Table 2 Univariate and multivariate analyses of risk factors for the development of recurrent instability
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Discussion

This study analysed the epidemiology, dynamics of injury, specific lesion characteristics and treatment results of a large cohort of patients suffering seizure-related shoulder injuries, confirming the extremely high frequency of bilateral injuries and posterior shoulder dislocations in this selected group of patients as compared to the general population.

Furthermore, two new relevant findings emerged from analysis of the collected data:

  1. (1)

    Uncontrolled muscle activation during a seizure is a distinctive dynamic of injury in patients with seizures, accounting for more than the half of all shoulder lesions, especially in younger patients. This can lead both to anterior and posterior dislocations or fracture-dislocations and is frequently cause of bilateral lesions and of instability recurrence after surgery.

  2. (2)

    Shoulder injury treatment in epilepsy patients is burdened by a high complication rate, especially after patients undergo surgery for instability; a recurring instability developed in almost two-thirds of those patients who underwent operative treatment.

Shoulder injuries in epilepsy patients

When compared to the general population, epilepsy patients are more prone to suffer accidental injuries and fractures [3, 9,10,11], which significantly influences their quality of life [12]. Although among orthopaedic surgeons it is well known, that seizures can lead to severe shoulder injuries, more detailed knowledge on epidemiology and lesion characteristics in this selected subgroup of patients bases entirely on classic papers describing case series extracted from the records of patients treated mainly surgically at highly specialized orthopedic departments [5, 6]. This findings are confirmed in more recent literature mainly by numerous technical or clinical reports, which cannot deliver epidemiological data or information on the relative relevance of different lesions [13,14,15,16,17,18,19].

On the other hand, in cross-sectional studies on large cohorts of epileptic patients, shoulder injuries are rarely reported as an independent diagnosis and details on specific lesions characteristics, such as the direction of shoulder instability, are omitted [3, 4].

This study screened a large cohort of patients referring to a tertiary center for diagnosis and treatment of epilepsy and first reports the demographic characteristics of a large cohort of 106 patients, specifically investigating epidemiological aspects and differentiating the type of shoulder injuries. Here, a vast spectrum of different shoulder injuries emerged, ranging from isolated unilateral soft tissue lesions to bilateral humeral fracture-dislocations, including acute and recurrent instability in both anterior and posterior direction. Notably, the percentage of patients suffering from “rare” injuries, such as posterior dislocations and bilateral shoulder lesions was confirmed to be higher compared to the literature data from cohorts without seizures [6, 8, 14, 20,21,22,23,24,25,26].

Thangarajah et al. analyzed a consecutive series of 33 epileptic patients with 49 unstable shoulders who were referred to a specialized orthopaedic unit for treatment of recurrent instability and reported a mean age at the time of the index dislocation of 20 years [5]; as opposed to this, Bühler and Gerber reported a mean age of 43.5 years for 26 consecutive patients with epilepsy with 34 unstable shoulders, which comes closer to the values we encountered in our cohort (age: 39.7 ± 17.5 years) [6]. Our study revealed a difference in the average age of the patient group that experienced isolated soft tissue injuries (age: 32.4 ± 17.5 years); this was significantly lower than that for the overall patient population with shoulder injuries and, in particular, than the patient subgroup with fractures (age: 44.9 ± 15.7). In agreement with these findings, Robinson et al. noted in their series of 26 patients sustaining a complex posterior fracture dislocation, that the eleven patients who sustained an injury during a seizure were slightly younger than the remaining study patients [7]. A male dominance was documented in previous reports as well as in our study [5,6,7, 27].

The direction of instability differs between published reports [5, 6]. Although posterior shoulder dislocations are frequently described as being associated with seizures [6, 7, 21, 24, 27], the direction of instability in both the aforementioned patient groups was predominantly anterior [5, 6]. Our study confirmed that the dominant direction of shoulder instability in patients affected by seizures is anterior (58.6%); however, the rate of patients experiencing posterior dislocations was found to be extremely high in this selected group of patients (35.7%). Trauma dynamics did not appear to play a significant role in determining the direction of dislocation of patients who experienced uncontrolled muscle activation during a seizure: both anterior and posterior dislocations were reported.

Overall, posterior shoulder dislocations are a very rare occurrence which pose a constant challenge to the orthopaedic surgeon, since they can often be missed at initial presentation [8, 20]. The relationship between these rare types of dislocation and seizures has been previously defined [8, 28,29,30]. In our study, four patients experienced a posterior dislocation after directly falling on the shoulder, which confirms that powerful muscular contraction is just one of the possible injury dynamics in patients with these rare lesions.

One recommendation derived from this data collection is that a clinical examination by means of observation, palpation, passive, and active mobilisation of any painful areas should be carried out after every seizure, followed by a radiological examination of the injured regions. This is mandatory since the pain derived from fractures or dislocations can sometimes be misinterpreted for postictal muscle soreness and rhabdomyolysis as a consequence of muscle contractions [2].

Bilateral shoulder injuries are considered extremely rare and are found in literature almost always as case reports, associated with seizures [6, 14, 21,22,23,24, 27], electrocution [25], or with high-speed motor vehicle accidents or falling on both arms [26]. A recent series investigated 17 surgically treated patients who sustained a bilateral humerus fracture caused either by falling on both arms or motor vehicle accident, without history of seizures: the reported average age was 68 years, notably higher than what we encountered in our subgroup of 13 patients who sustained a bilateral humeral fracture (age: 41.5 ± 13.0 years) [26]. When considering all our 29 patients experiencing bilateral injuries, mean age dropped to 33.6 years. These data confirm that seizures are a risk factor for sustaining this rare injury also in the younger patients.

Risk factors and treatment options

Several studies have investigated the risk factors that are associated with seizure-related injuries with seizure frequency and their generalized onset considered to be most important. Furthermore, seizure type (atonic, tonic, myoclonic, and in particular, tonic–clonic seizures), the number of antiepileptic drugs, a less independent living situation and psychiatric comorbidities have been mentioned as further, possible risk factors for seizure-related injury [12, 31,32,33,34,35]. Inappropriate patient positioning, such as forcing a lateral decubitus during the tonic–clonic phase of the seizure, could also increase the risk of shoulder dislocations [4].

As opposed to previously published data, drug-naïve patients with their first tonic–clonic seizure and without a prior history of epilepsy were not the only group of patients who reported a shoulder injury during a seizure [36]. Only one-quarter of our patients suffered a soft tissue shoulder injury during their first seizure and only 11% of the patients who were diagnosed with a fracture experienced it during their first seizure.

An increased fracture incidence for epilepsy patients has been described and quantified with a relative risk between 1.91 and 2.45 [3, 37,38,39]. Numerous risk factors explain this association: first, seizures (in particular tonic, atonic, tonic–clonic or myoclonic seizures) can lead to unprotected falls and subsequent fractures; second, uncontrolled muscle contractions during a seizure can lead to an enormous increase in the load transmitted to bones and joints, resulting in burst fractures of the spine and in joint dislocations or fracture-dislocations [40, 41]. Furthermore, some AEDs may have sedative effects increasing the risk of uncontrolled falls [42,43,44], whereas other reduce bone mineral density [45, 46]. In our cohort, 48% of the patients were taking AEDs when the injury occurred, which did not affect the dynamics and types of lesions. Nevertheless, the response to therapy, as well as the patients’ compliance with AEDs also plays a role in limiting seizure-related injuries [47, 48]. This aspect appeared also in our cohort, with twelve patients with epilepsy (11.3%) experiencing seizure-related shoulder injuries after discontinuing their AEDs (medical indication or non-compliance).

Treatment choice depends on the patient’s characteristics and type of shoulder injury. Regardless of the type of surgical procedure, treating shoulder injuries in epilepsy patients is difficult due to a high complication rate, with recurrence of instability occurring in almost two-thirds of patients undergoing stabilization procedures. Therefore, extreme caution is advised when planning and conducting surgery, in addition to properly consulting and educating the patient prior to surgery. Furthermore, the findings of this study highlight the role of a specialised neurological evaluation, appropriate AED treatment, and an evaluation of early epilepsy surgery or vagus nerve stimulation in drug-resistant patients. A neurologist should always be involved in treating these patients whether they present first to outpatient orthopaedic clinics or the emergency department [5].

The limitations of this study include the heterogeneous nature of the investigated cohort, with variable patients and lesions characteristics, which makes grouping and categorisation difficult. Furthermore, diagnosis and treatment of shoulder lesions occurred at different institutions, which may have different diagnostic protocols, treatment standard and orthopedic expertise, possibly leading to some variability in the lesions’ classification, decision-making, treatment choice, and complication rate. Moreover, this study did not yet collect long-term follow-up radiological data, thus not being able to show if epilepsy and seizures affect long-term radiological outcomes and osteoarthritis progression. Finally, some relevant data could neither be retrieved through examination of clinical records nor via telephonic interview; this led to some missing data and the subsequent exclusion of some patients from subgroup analysis.

Conclusions

Epilepsy is associated with a high risk of musculoskeletal injuries, and shoulder lesions are common after seizures. Bilateral injuries and posterior dislocations, rarely observed in the general population, occur with a high frequency after seizures. The role of uncontrolled muscle activation was confirmed as a distinctive dynamic of injury in young patients with seizures, leading both to anterior and posterior dislocations and threatening the results of surgical stabilization procedures. A high complication rate was documented after treatment: this calls for appropriate preoperative counselling and a multidisciplinary approach to minimize recurring tonic–clonic seizures.