Humeral Retroversion in Children with Shoulder Internal Rotation Contractures Secondary to Upper-Trunk Neonatal Brachial Plexus Palsy

Pearl, Michael L. MD; Batech, Michael DrPH; van de Bunt, Fabian MD

Journal of Bone & Joint Surgery - American Volume:
doi: 10.2106/JBJS.15.01132
Scientific Articles
Abstract

Background: The most common sequela of neonatal brachial plexus palsy is an internal rotation contracture of the shoulder that impairs function and leads to skeletal deformation of the glenohumeral joint. Treatment options include release, transfers, and humeral osteotomy, all ultimately striving for better function through increased external rotation. Prior studies have shown that neonatal brachial plexus palsy alters humeral retroversion but with conflicting findings. We studied retroversion in children with internal rotation contractures from neonatal brachial plexus palsy to clarify its effect on version and surgical planning.

Methods: Bilateral shoulder and elbow magnetic resonance imaging scans of 21 children with neonatal brachial plexus palsy were retrospectively analyzed. Retroversion referenced to the transepicondylar line at the elbow was measured with respect to 2 different proximal reference axes, the longest diameter of an axial cut of the proximal part of the humerus (the skew axis) and the line perpendicular to the articular surface (the humeral center line). Glenoid version and glenohumeral morphology type (concentric glenoid, posterior-concentric glenoid, biconcave, or pseudoglenoid) were also determined. All geometric variables were assessed for correlation with patient age and the severity of the internal rotation contracture.

Results: Retroversion on the involved side was decreased at 6° compared with 19° (p = 0.003), as measured between the skew axis and transepicondylar line. Retroversion referenced to the humeral center line was also decreased at −2° (anteversion) compared with 20° (p < 0.001). Patient age was inversely correlated with retroversion, but was only significant for the skew axis (r = −0.497, p = 0.022), decreasing in linear regression by 2.4° per year (p = 0.038). Humeral retroversion did not correlate with the severity of the internal rotation contracture, glenoid version, or glenoid morphology type.

Conclusions: Humeral retroversion is likely to be less on the affected side in children with internal rotation contractures from upper trunk neonatal brachial plexus palsy and merits consideration in surgical planning.

Level of Evidence: Prognostic Level IV. See Instructions for Authors for a complete description of levels of evidence.

Author Information

1Department of Orthopaedics, Kaiser Permanente, Los Angeles, California

2Division of Biostatistics, Department of Research and Evaluation, Kaiser Permanente Southern California, Pasadena, California

3Department of Orthopaedics, Vrije Universiteit, Amsterdam, the Netherlands

E-mail address for M.L. Pearl: michael.l.pearl@kp.org

E-mail address for M. Batech: michael.batech@kp.org

E-mail address for F. van de Bunt: fabianvdbunt@gmail.com

Article Outline

The most common sequela of neonatal brachial plexus palsy is an internal rotation contracture of the shoulder that leads to skeletal deformation of the glenohumeral joint1. The resultant dysplasia of the glenoid has been well characterized by increased retroversion, the formation of a pseudoglenoid, and posterior displacement of the dysplastic humeral head relative to the scapula2-4. The humeral head deformity shows a loss of normal symmetry and flattening of the anterior articular surface5,6. Less well understood are the consequences of the contracture on the version of the humerus, with conflicting findings in the few available published reports7-9.

Shoulder motion is the sum of the combined movement between the scapulothoracic and glenohumeral articulations and the geometry of the constituent skeletal segments. All other factors being equal, a shoulder with greater humeral retroversion will have greater external rotation. The internal rotation contracture of neonatal brachial plexus palsy accordingly reflects a diminished range of external rotation that has, among its component parts, changes in the glenohumeral joint and version of the humerus. The measured external rotation is the parameter most used to indicate a surgical procedure for these patients, so a better understanding of its component parts, inclusive of humeral retroversion, merits further consideration.

Normal humeral retroversion is extremely variable, as has been shown in numerous previous studies, ranging from −28° (anteversion)10 to 92° in fetal bones11-13, reflecting not only individual variation14-16, but also how version changes from fetal life through development12,13, how it varies by ethnicity11, and how it responds to environmental factors such as dedicated throwing sports17-23. Adding to the complexity of measuring version, many different methodologies have been used in variable ways (direct measurement, radiography, computed tomography [CT], ultrasonography), and the version angle itself has also been defined differently with respect to variable reference axes. Furthermore, it has been shown that version changes even within the same methodology depending on orientation and slice level chosen with three-dimensional imaging24.

Only a few studies have measured both sides in the same “normal” individual10,22,23,25-31; most observed little to no difference between sides, and even those that did find a difference found only a difference of <10°. In contrast, multiple studies of dedicated throwing athletes have shown a difference in retroversion of ≥10° between both arms that is evident by the patient age of 12 years17,18,20-23. Accordingly, one would expect that children with neonatal brachial plexus palsy would also show asymmetry of version from the altered mechanical forces resultant from their neurological injury. Three reports in the literature have detailed findings on retroversion in this population but with conflicting results. Scaglietti8 described a radiographic method for analyzing version. The diagrams from his study clearly depict backward rotation of the proximal segment (increased retroversion) from this condition, although no numerical values were presented. In a magnetic resonance imaging (MRI) study of 33 infants, van der Sluijs et al. corroborated these findings, showing increased retroversion in the involved arm (28° in the involved arm compared with 22° in the uninvolved arm)7. However, Sheehan et al. more recently reported on an older group of 13 children, with a mean age (and standard deviation) of 11.8 ± 3.3 years, finding a decrease in retroversion in the affected arm9.

The treatment options of children with internal rotation contracture secondary to neonatal brachial plexus palsy include soft-tissue procedures (releases and tendon transfers) and bone realignment procedures such as a rotational osteotomy of the humerus32-37. The indications for one procedure or another vary from center to center, but all ultimately strive for better function through an improved position of the hand in space. How this is achieved for each patient must necessarily relate to the specifics of his or her anatomy, including humeral retroversion. Toward the goal of better understanding how humeral retroversion may play a role in surgical planning, we studied humeral retroversion in 21 young children who were under evaluation for treatment of internal rotation contractures secondary to unilateral neonatal brachial plexus palsy.

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Materials and Methods

In our medical center, children with passive external rotation with the arm by the side that is near neutral (0°) or less are candidates for intervention, either Botox (onabotulinumtoxinA; Allergan) injection (used off-label) or arthroscopic release and/or muscle transfer. A rotational osteotomy of the humerus is recommended for children who present with glenohumeral deformity at the age of ≥8 years. Children of families who elect intervention are offered MRI for surgical planning purposes.

With institutional review board approval, 29 bilateral shoulder and elbow MRI scans of children with unilateral internal rotation contractures from upper plexus (C5-6 or C5-7) palsies were retrospectively accessed from a consecutive series of patients who had undergone treatment at our facility from February 2010 to October 2014. Children who had undergone a prior surgical procedure or treatment other than physical therapy were excluded from this analysis. Eight of these MRI scans were found deficient in some way that compromised completion of our detailed measurement protocol (e.g., poor study because of motion artifact or incomplete visualization of the entire glenohumeral joint or humerus, scapula, proximal part of the humerus, and epicondyles for both the involved and uninvolved sides). We present the findings in the 21 remaining subjects (Table I). Passive external rotation was measured with the patient arm in adduction at the time of the surgical procedure or injection, under general anesthesia, by the same orthopaedic surgeon using a handheld goniometer.

MRI studies were performed on a 1.5-T MRI unit (Signa; GE Medical Systems) with use of Signa 5X software. Three-dimensional axial gradient-echo images (38-ms repetition time, 15-ms echo time, 20° flip angle, 2 signals acquired, 2-mm section thickness with 0-mm spacing, 120-mm field of view, and 256 × 160 matrix) were made of both shoulders in the axial plane. Children were not moved in the gantry between securing images from the shoulder and corresponding elbow to preserve the coordinate system of the humerus. Children younger than 7 years of age, or those unable to remain still, were imaged under general anesthesia. For small children, both arms against the side of the body were imaged simultaneously, positioned as well as possible parallel to each other and coaxial to the gantry. If this was not possible because of the child’s size or contracture severity, the shoulder and elbow of one arm were imaged first and then the shoulder and elbow of the other arm were imaged.

MRI DICOM (Digital Imaging and Communications in Medicine) files were imported into OsiriX (Pixmeo). Files were first de-identified and were saved numerically as a database of 21 randomized subjects. Axial plane sequences from the uninvolved and involved sides that best represented the subcoracoid slice for determination of glenohumeral parameters were selected and then were exported as TIFF (tagged image file format) files5, which were imported into The Geometer’s Sketchpad (version 5.03; McGraw-Hill Education).

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Measurement of Retroversion

Retroversion was measured with respect to two different proximal reference axes and the transepicondylar line distally. The first proximal reference axis was chosen to provide continuity with the earlier reports of Scaglietti and van der Sluijs et al. using a line along the longest axis of the proximal part of the humerus7,8. From the methodology presented by those earlier authors, their axis choice was based on visual approximation. To improve the precision and reproducibility of this determination, we defined this axis geometrically, in accord with a prior study (Fig. 1)5, as a line segment that spanned the greatest distance from the periphery of the greater tuberosity to the medial articular surface, and designated it as the skew axis. This axis is separate and distinct from the second proximal reference axis that we studied, the humeral center line, which is the perpendicular projection from the margins of the articular surface, a common choice in prior studies on retroversion18,23,28,29,36.

Glenoid version and glenohumeral morphology type (concentric glenoid, posterior-concentric glenoid, or pseudoglenoid) were also determined2,4,5. By convention, humeral retroversion is presented as a positive value (negative values reflecting anteversion).

Version (in relation to both proximal reference axes) was measured twice by two investigators and was repeated at an interval of no less than 2 weeks to assess inter-investigator and intra-investigator reliability. Investigators were blinded from each other’s measurements and clinical details while making version measurements.

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Statistical Analysis

Standard descriptive measures were reported for retroversion of the involved and uninvolved sides and their difference within the study population. Pearson product-moment or Spearman rank correlation coefficients were estimated between each of these and age, passive external rotation, glenoid version, and glenohumeral morphology type as appropriate on the basis of the underlying distribution of the continuous data. Comparison of means between glenoid types was made using the parametric t test, analysis of variance (ANOVA), or Kruskal-Wallis test, as appropriate. Paired data (i.e., involved measurements compared with uninvolved measurements made on the same subject) were compared using paired t tests or paired-samples Wilcoxon signed-rank tests, as appropriate. Simple linear regression assessed the relationship between version differences and age. Inter-investigator and intra-investigator reliability was assessed using intraclass correlation coefficients38 with 95% confidence interval (95% CI) limits. Normality in all scenarios was assessed for parametric assumptions using the Shapiro-Wilk normality test, and all tests were two-sided and were considered significant at the 5% type-I error rate.

All analyses were conducted using R statistical software (version 3.1.1; The R Foundation for Statistical Computing).

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Results

The mean age of the children was 3.2 ± 3.3 years (range, 0.5 to 10.1 years) (Table I). The mean internal rotation contracture was −11° (range, −60° to 20°). There were 1 biconcave glenoid, 12 pseudoglenoids, 4 concentric-posterior glenoids, and 4 concentric glenoids. The mean glenoid retroversion on the uninvolved side was 6° (range, −5° to 16°). The mean glenoid retroversion on the involved side was 27° (range, −1° to 58°). The mean paired difference in glenoid retroversion (involved − uninvolved) was 22° (range, −6° to 55°). The glenoid retroversion on the involved side was negatively correlated with passive external rotation (r = −0.507, p = 0.019) (Table II). Age was weakly associated with glenoid retroversion, but this was not significant (p = 0.318).

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Humeral Retroversion by Skew Axis

Retroversion as measured between the skew axis and transepicondylar line was decreased on the involved side, with a mean of 6° for the involved humeri compared with a mean of 19° for the uninvolved humeri (p = 0.003), with a wide range for both of the humeri (Fig. 2). The mean paired difference (involved − uninvolved) was 13° (range, −16° to 52°), although, in some children, retroversion was increased on the involved side (Table I). There was no significant correlation between retroversion and the range of passive external rotation, glenoid retroversion, or glenoid morphology type (p > 0.05 for all comparisons). Age was negatively correlated with humeral retroversion on the involved side only (r = −0.497, p = 0.022), decreasing in the linear regression analysis by 2.4° per year (p = 0.038) (Fig. 3).

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Humeral Retroversion by Humeral Center Line

Retroversion as measured between the humeral center line and the transepicondylar line was decreased on the involved side, with a mean of −2° on the involved side compared with 20° on the uninvolved side (p < 0.001) (Fig. 4). The mean paired difference was 22° (range, −15° to 40°). There was no significant correlation between humeral retroversion and the range of passive external rotation, glenoid retroversion, or glenoid morphology type (p > 0.05 for all comparisons). There was no correlation between age and humeral retroversion using the humeral center line reference axis (r = −0.123, p = 0.594). Although not significant (p = 0.556), linear regression showed a decrease of 0.7° per year.

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Interrater and Intrarater Reliability

All measurements of version were done independently twice by two of the authors to assess repeatability and reliability of the measurements. Intraclass correlation coefficients showed good to excellent reliability and were as follows. For retroversion measured by the skew axis, the intraclass correlation coefficient for interrater reliability on the involved side was 0.944 (95% CI, 0.897 to 0.970; p < 0.001). The intraclass correlation coefficient for interrater reliability on the uninvolved side was 0.867 (95% CI, 0.754 to 0.928; p < 0.001). The intraclass correlation coefficient for intrarater reliability on the involved side was 0.949 (95% CI, 0.881 to 0.979; p < 0.001) for examiner 1 and 0.973 (95% CI, 0.935 to 0.989; p < 0.001) for examiner 2. The intraclass correlation coefficient for intrarater reliability on the uninvolved side was 0.825 (95% CI, 0.620 to 0.925; p < 0.001) for examiner 1 and 0.930 (95% CI, 0.828 to 0.972; p < 0.001) for examiner 2 (Table III).

For retroversion measured by the humeral center line, the intraclass correlation coefficient for interrater reliability on the involved side was significant at 0.881 (95% CI, 0.778 to 0.936; p < 0.001). The intraclass correlation coefficient for interrater reliability on the uninvolved side was significant at 0.863 (95% CI, 0.640 to 0.938; p < 0.001). The intraclass correlation coefficient for intrarater reliability on the involved side was significant at 0.950 (95% CI, 0.879 to 0.980; p < 0.001) for examiner 1 and 0.959 (95% CI, 0.889 to 0.984; p < 0.001) for examiner 2. The intraclass correlation coefficient for intrarater reliability on the uninvolved side was significant at 0.968 (95% CI, 0.923 to 0.987; p < 0.001) for examiner 1 and 0.951 (95% CI, 0.881 to 0.980; p < 0.001) for examiner 2 (Table III).

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Discussion

The first two reports on humeral retroversion in children with neonatal brachial plexus palsy showed that retroversion was increased in this patient population7,8. However, we found a reduction of retroversion, by 13° to 22° depending on the reference axes selected, in a cohort of young children under evaluation for internal rotation contractures from this injury. Our findings are in agreement with another recent study on this subject by Sheehan et al., who reported a reduction in retroversion of 17° in an older group of children, with a mean age of 11.8 years (range, 6.7 to 18.7 years)9. The mean age of subjects in our study was 3.2 years, with most of our patients <5 years of age and all patients ≤10.1 years of age. To the extent that the existing literature presents conflicting information, our study weighed strongly toward establishing that version decreases with this injury.

Humeral retroversion is greatest at birth11-13, gradually decreasing to adult values through growth, under the influence of internal and external forces encountered by the arm. The young throwing athlete manifests increased retroversion by countering natural forces that reduce retroversion with the external rotation torque generated during the throwing motion17,18,20-23. All children with healthy arms also do this to some extent through normal developmental activities. The affected arm of the child with neonatal brachial plexus palsy likely experiences diminished use and altered external forces contributing to the reduction in retroversion observed in the current study.

This information may alter surgical indications for some patients, but definitive recommendations will require further study. Most treating surgeons presently favor soft-tissue procedures for patients who present with an internal rotation contracture and minimal deformity of the glenohumeral joint. However, if it were known that such a patient also had markedly decreased humeral retroversion, a rotational osteotomy might be much more compelling. At a minimum, the prevailing recommendation to reserve humeral osteotomy for patients with the most advanced glenohumeral deformity merits reconsideration.

The complexities in measuring humeral version and the deformities that result from this condition perhaps explain the conflicting findings in the earlier literature on this subject. The developing proximal humeral articular surface often warps in the presence of an internal rotation contracture, losing symmetry, with its new shape having a long axis (the skew axis) that is directed posteriorly relative to the original orientation of the articular surface5,6. In the present study, retroversion measured on the involved side relative to the skew axis was, on average, 8° more than version referenced to the humeral center line, with a maximum difference of 42°. In contrast, retroversion measured on the uninvolved side using these different proximal reference axes had a negligible difference (<2°).

A potential limitation of the methods used in this study was the superposition of two-dimensional images slices from the proximal and distal ends of the humerus to define the retroversion angle. All existing methodologies have their limitations, but a method based on a three-dimensional reconstruction of the entire humeral bone would potentially offer the truest value of retroversion. The methods of Sheehan et al. explore the potential of such a method, statistically defining the orientation of the bone from a three-dimensional model constructed by manually segmenting the relevant anatomy9. However, the clinical utility and relevance of these statistically calculated axes remain to be established. We therefore chose to pursue a method that was consistent with the earlier literature on this subject, adding precision to the method of defining the proximal reference axis, aiming for consistency between subjects and between sides in each subject. Our reliability data suggest that these efforts were successful.

Neither the severity of the internal rotation contracture nor the extremity of the glenoid version or glenoid deformity type was correlated with the reduction in humeral retroversion. It is possible that our small sample size was underpowered to identify correlations that exist. Alternatively, it is also possible that activity-related extrinsic factors are responsible for this altered development. Just as the external rotation torque from the throwing motion alters humeral growth, increasing retroversion17,18,20-23, one could speculate that the less-used limb of a child with neonatal brachial plexus palsy would experience less external rotation torque, resulting in decreased retroversion. Further biomechanical study is required to determine which activities impart this torque. Increasing evidence from animal models further supports the theory that some of the glenohumeral version changes with this injury stem from altered use of the limb39-42.

In conclusion, we observed that humeral retroversion on the affected side commonly decreased in the presence of an internal rotation contracture secondary to neonatal brachial plexus palsy. Some earlier studies have suggested otherwise, but we believe that those conflicting results were likely due to a measurement methodological artifact. Clinical evaluation of humeral retroversion may become an increasingly important part of surgical planning, but how and if this should change surgical indications require further study.

NOTE: The authors thank Justin Klein for illustrations.

Investigation performed at the Kaiser Permanente Los Angeles Medical Center, Los Angeles, California

Disclosure: There was no external source of funding for this work. The Disclosure of Potential Conflicts of Interest forms are provided with the online version of the article.

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