Correlation between the morphology of the biceps groove and injuries to the biceps pulley and the long head tendon of the biceps

DOI: https://doi.org/10.21203/rs.3.rs-2077535/v1

Abstract

Purpose: The morphometric parameters of the osseous structures of the biceps groove were measured to investigate their correlation with the structural injury of the trochlear and the long head tendon of the biceps. 

Methods: A total of 126 patients undergoing arthroscopic rotator cuff repair surgery had their biceps tendons and bicipital groove morphologies prospectively evaluated on a 3D reconstruction model of the humeral head. The width of groove, depth of groove, opening angle, medial wall angle, and inclination angle of the bicipital groove were measured for each patient. During the surgery, the type of injury to the biceps pulley and the degree of biceps longus tendon injury were assessed. The correlations of these injury assessments with bicipital groove measurements were analyzed. 

Results: The average width of groove was 12.52 mm ± 2.11 mm. The average depth was 4.88 mm ± 1.38 mm. The average inclination angle was 26.27° ± 8.10°. The average opening angle was 89.77° ± 18.40°. The average medial wall angle was 40.57° ± 7.93°. Significant biceps pulley structural injury was observed in 66 patients, and their Martetschlager classifications were as follows: type I injury in 12 patients, type II injury in 18 patients, and type III injury in 36 patients. The Lafosse grades of long head tendon injury were as follows: 72 cases were grade 0 injury, 30 cases were grade I injury, and 18 cases were grade II injury. We found no significant correlation between the opening width, depth, inclination angle, opening angle, and medial wall angle of bicipital groove and injuries of the pulley and the long head of the biceps tendon. Conclusion:This study does not find a correlation between the injury of the pulley or the long head of the biceps tendon and bicipital groove morphology.

Introduction

Lesions of the long head of the biceps tendon (LHBT) are a common source of pain in the shoulder anterior [13], and often present concomitantly with other shoulder pathologies. Lafosse et al. reported that 45% of patients with rotator cuff tears also had LHBT lesions [4]. Instability is a common cause, and the biceps groove, the bony channel where LHBT leaves the shoulder joint, is an important stabilizing structure for LHBT [5]. From a morphological point of view, a shallow and wide biceps groove may be a risk factor for LHBT instability and further lesions. Many previous studies have discussed the relationship between biceps groove morphology and LHBT lesions [2, 5, 6], but reports have been inconsistent. From a methodological perspective, most of the studies were based on CT or MRI cross-sectional images [7], and an improper arm position during scanning or variations in the scanning plane angle may render the cross-sections taken from the biceps groove incomparable. The three-dimensional (3D) reconstruction technology of CT bone can superimpose a series of two-dimensional images and reconstruct the three-dimensional structure, allowing for a more intuitive observation of the bone structure from multiple angles [8]. Through the specific fault angle cutting method, an accurate cross-section can be taken for a better view of the biceps groove, which can improve the measurement accuracy and enhance comparability between different individuals.

Before LHBT enters the biceps groove, there exists the long head tendon pulley structure, which is a soft tissue stable structure. The relationship between pulley structure injury and LHBT lesions has attracted increasing attention in recent years [9]. Trauma, degeneration, and intra-articular impingement can all lead to pulley structure injury [10]. As the two important structures that jointly maintain LHBT stability, the morphology of the inter-tubercular sulcus of the humerus may also be a risk factor for pulley structure injury. Therefore, it is necessary to perform further research on this.

In this study, patients undergoing arthroscopic shoulder surgery were subjected to a preoperative CT scan, and a 3D model of the proximal humerus was constructed. The width, depth, angle of inclination, angle of opening, and medial wall angle of the biceps groove were measured. Their correlation with pulley structure and LHBT lesions was also investigated.

Data And Methods

1. Inclusion and exclusion criteria

The inclusion criteria were: (1) no prior surgery and injury to the dominant shoulder; (2) no obvious surgical contra-indication in preoperative examination; (3) no contra-indication of radiological examination; (4) patient agreed to participate in the study and filled out an informed consent form. 

The exclusion criteria were: (1) the primary disease was an inflammatory disease, such as giant rotator cuff tear, etc., that the researchers decided as unsuitable for inclusion; (2) patient had participated in other clinical trials within the previous three months; (3) other conditions deemed unsuitable for inclusion in this study as judged by the investigator.

2    Reconstruction of a 3D model of the proximal humerus

2.1    Acquisition of imaging data

The shoulder joint of the patient was CT scanned, with the affected shoulder placed on the side of the body, and a 3D model of the biceps groove was constructed based on CT scan data. A 64-slice CT scanner (SOMATOM Perspective, China) was used, covering the upper end of the humerus. The layer thickness was 0.625 mm, the layer spacing was 0.95 mm, and each pixel of the obtained image was 512 × 512. After scanning, the CT images were preprocessed in CT workstation, and CT data obtained were stored in the DICOM format.

2.2    Three-dimensional reconstruction of proximal humeral model

DICOM scan data were imported into Mimics 21.0 software. Threshold analysis was performed using the threshold tool, which was set at 245. The humeral boundary was isolated, the joining images were excised using the zone growth tool, and the excess structures were isolated. The layers were edited one by one, with the remnants replenished and the noise removed. The model was further optimized in Geomagic Warp reverse engineering software. The software was used to fill holes, remove noise, and repair boundaries to smooth the model, resulting in a 3D model of the humeral head containing the tackle structure, as displayed in Fig. 1.

3    Research design

3.1    Positioning the measurement plane

The depth of the internodular sulcus was defined as the distance from the highest point of the lesser nodule to the bottom of the biceps groove [11, 12]. It is critical to locate the measurement plane passing through the highest point of the tuberosity and the bottom of the biceps groove. Previous studies based on CT or MRI data were prone to errors because they only relied on imaging cross-sectional images to select the measurement plane, which could be affected by body position and the angle of administration. In this study, 3-MATIC software was used to set up a humerus model parallel to the humerus shaft Reference line (L1). The highest point of the tuberosity was selected as the reference plane S1 perpendicular to L1, and the section S2 of the humerus shaft passing through the highest point of the tuberosity was obtained. This plane was defined as the measurement plane passing through the highest point of the lesser tubercle and the sulcus floor, and measurements of the bony parameters of the internodular sulcus opening were performed on S2 as shown in Fig. 2.

3.2    Measurement of the bony structure of biceps groove

(1) Width of groove (WG)

On S2 plane, the width of the groove refers to the straight line distance between the vertices of the large and small nodules.

(2) Depth of groove (DG)

The depth of the biceps groove is the length of a straight line perpendicular to the vertex of the nodules.

(3) Opening Angle of biceps groove (OA)

The lowest point of the biceps groove was selected, and a tangent line was made along the lateral wall of the nodules. The angle between the two points was the opening angle of the biceps groove.

(4) Medial Wall Angle of biceps groove opening (MWA)

The lowest point of the biceps groove was made parallel to the vertex of the nodules, and the tangent line of the lowest point of the biceps groove along the medial wall of the small nodules was made. The angle between the two was the medial wall angle of the biceps groove, as depicted in Fig. 3.

3.3    Measurement of inclination angle of intertubercular sulcus opening

In this study, the angle between the two lines of the large and small nodules and the transverse line of the humerus shaft was defined as the opening inclination angle of the intertubercular sulcus. Since the connection of the vertices of the large and small nodules is not in the same plane in 3D, the connection L1 of vertices of the large and small nodules were directly projected, and the projected line L2 and the vertical segmentation plane S1 of humerus bone were established, in UG (Unigraphics NX Siemens USA) software. The angle between L2 and S1 was measured to obtain the opening inclination angle of the intertubercular sulcus, as demonstrated in Fig. 4.

4    Arthroscopy

Arthroscopy is considered the gold standard for evaluating pulley and LHBT injury. In this study, arthroscopy was performed by the same senior shoulder surgeon to observe the degree of LHBT injury in the glenohumeral joint and classify the pulley structure injury.

4.1    Classification of pulley structure injury

The method proposed by Martetschläger [13]  was used to classify pulley structure injury, as illustrated in Fig. 5.

    Type I: medial pulley structure injury (medial coracohumeral ligament and/or superior glenohumeral ligament)

    Type II: lateral pulley structure injury (lateral coracoid brachial ligament)

    Type III: combined injury of internal and lateral pulley structure

4.2    Classification of injury of LBHT

The method proposed by Lafosse [13] was used to classify LBHT injury, as shown in Fig. 6.

    Grade 0: no injury to long head tendon of biceps

    Grade I: minor injury (less than 50% local loss or erosion of tendon)

    Class II: major injury (extensive absence or erosion of more than 50% of the tendon)

5    Statistical analysis

 Statistical analyses were performed using SPSS 23.0 software. Empirical measurements with a normal distribution and homogeneity of variance were reported as mean ± standard deviation (x ̅±s), or as median and quartile spacing otherwise. Differences between groups were compared by independent sample T-test. Count data were represented with frequency table, composition ratio, etc. Correlations were performed using the Spearman correlation test. Differences less than 0.05 (P < 0.05) were considered statistically significant.

Results

1     Demographic Data

 A total of 126 patients in Shanghai Guanghua Hospital of Integrated Traditional Chinese and Western Medicine from January 2021 to June 2021 that satisfied the criteria were included in this study, comprising 72 male patients and 54 female patients. There were 40 cases in the left shoulder and 86 cases in the right shoulder. The patients were 31–78 years old, with an average of 61.05 ± 11.91 years old, and the disease duration was 0.1–3 years, at an average of 1.6 ± 2.26 years.

 2     Biceps groove opening morphology

 The width of the internodular sulcus opening ranged from 8.90 mm to 17.24 mm, averaging 12.52 mm ± 2.11 mm. The biceps groove depth ranged from 3.16 mm to 9.24 mm, averaging 4.88 mm ± 1.38 mm. The inclination angle of the biceps groove ranged from 12.66° to 40.41°, averaging 26.27° ± 8.10°. The biceps groove opening angle ranged from 40.96° to 112.69°, averaging 89.77° ± 18.40°. The inner wall angle ranged from 30.90° to 64.34°, averaging 40.57° ± 7.93°. Table 1 summarizes these measurements.

 Table 1. General data and morphological parameters statistics of biceps groove.

 

n = 126

Age/year  

61.05 ± 11.91

Gender/(Male:Female)

72:54

Course/year  

1.6 ± 2.26

Shoulder/case (right:left)

43:20

Biceps groove opening width/mm  

12.52 ± 2.11

Biceps groove opening depth/mm  

4.88 ± 1.38

Biceps groove opening inclination angle/ °  

26.27 ± 8.10

Biceps groove opening angle/ °  

89.77 ± 18.40

Internal wall angle/ ° of biceps groove opening  

40.57 ± 7.93

3     Arthroscopy 

Sixty patients showed no obvious pulley structure injury, while the remaining 66 patients showed obvious pulley structure injury.According to Martetschläger classification system, twelve patients had a type I injury, 18 patients had a type II injury, and 36 patients had a type III injury.

There were 54 patients with LHBT structure injury. According to the Lafosse classification system, 30 patients had a grade I injury and 24 patients had a grade II injury. Table 2 and Fig. 7 summarize the arthroscopy results.

 Table 2. Classification of pulley injury and LHBT injury.

 

No injury

I

II

III

Martetschlager parting

60

12

18

36

Lafosse classification

72

30

24

-

4     Correlation between pulley structure injury and biceps longus muscle injury

 According to the gamma test, the correlation between pulley structure injury and biceps long head muscle injury was statistically significant (P < 0.01), with a gamma coefficient of 0.639. These quantities exhibited a positive correlation trend.

 5     Correlation between biceps groove osseous structure and LHBT injury

 All patients were divided into LHBT-injured and non-LHBT-injured groups. After examination, we found no statistical differences in the width, depth, inclination angle, opening angle, and medial wall angle of the biceps groove between the two groups (P > 0.05). Table 3 summarizes the result of this examination.

 Table 3.    Comparison of bony structural parameters of biceps groove between the two groups

 

LHBT-injured group

Non-injured group

P

Width of intertubercular sulcus opening

13.61 ± 2.23

11.80 ± 1.75

0.057

Depth of biceps groove opening

4.92 ± 1.25

4.85 ± 1.51

0.915

Angle of inclination of biceps groove opening

22.60 ± 2.38

28.72 ± 7.22

0.098

Angle of biceps groove opening

90.73 ± 17.37

89.13 ± 19.80

0.855

Medial wall angle of biceps groove opening

42.68 ± 7.69

44.16 ± 8.36

0.694

 Spearman correlation test was performed between LHBT injury degree and biceps groove morphology, and we found that the correlation between LHBT injury degree and the width, depth, inclination angle, opening angle, and medial wall angle was not statistically significant (P > 0.05). Table 4 summarizes the correlation result.

 Table 4. Correlation between osseous structure of biceps groove and LHBT injury grade.

Parameter

r

P

Width of intertubercular sulcus opening

0.139

0.558

Depth of biceps groove opening

0.054

0.822

Angle of inclination of biceps groove opening

0.296

0.205

Angle of biceps groove opening

0.006

0.979

Medial wall angle of biceps groove opening

0.037

0.876

 6     Correlation between biceps groove bony structure and pulley structure injury

 All 126 patients were divided into the injured pulley structure group and the non-injured group. After examination, there was no statistically significant difference in the width, depth, inclination angle, opening angle, and medial wall angle of the biceps groove between the two groups (P > 0.05). Table 5 summarizes the correlation result.

 Table 5. Comparison of bony structural parameters of biceps groove between the two groups.

 

Pulley injury group

Non-injured group

P

Width of intertubercular sulcus opening

12.39 ± 2.54

12.68 ± 1.57

0.764

Depth of biceps groove opening

5.02 ± 1.77

4.70 ± 0.71

0.620

Angle of inclination of biceps groove opening

26.18 ± 9.34

26.39 ± 6.85

0.955

Angle of biceps groove opening

88.72 ± 20.16

91.05 ± 17.12

0.787

Medial wall angle of biceps groove opening

44.09 ± 9.80

42.94 ± 5.31

0.756

 Spearman correlation test was performed between the pulley structure injury type and the morphology of the biceps groove, and the correlation between the pulley structure injury type and the width, depth, inclination angle, opening angle, and inner wall angle was not statistically significant (P > 0.05). Table 6 summarizes the correlation result.

 Table 6. Correlation between osseous structure of biceps groove and injury degree of pulley structure.

Parameter

r

P

Width of intertubercular sulcus opening

0.124

0.604

Depth of biceps groove opening

0.042

0.860

Angle of inclination of biceps groove opening

0.202

0.394

Angle of biceps groove opening

0.170

0.472

Medial wall Angle of biceps groove opening

0.033

0.891


Discussion

The biceps groove is the most important bony stabilizing structure for LHBT. The morphologies of the biceps groove reported by different studies are quite different. Taking the depth of the biceps groove as an example, the average values of the biceps groove varied from 4.2 to 5.8 mm in different studies [5, 6, 14, 15], while the value in this study was 4.88 mm. This variation could come from demographic variations in the subjects, such as race, ethnicity, and other factors, or from variations in the measurement method adopted. Previous morphological studies of the biceps groove utilized MRI or CT images of the humerus in cross-section. MRI has natural shortcomings in visualizing bone structure, which may affect the stability of the measurement, especially given that the biceps groove is a long strip that requires a consistent and comparable measurement plane, ideally the humeral cross-section through the highest point of the humeral tuberosity [12]. Obtaining a true cross-section perpendicular to the longitudinal axis of the humerus is difficult due to the differences in position and image scanning parameters during examination. In addition, defining the measurement level in continuous two-dimensional images is difficult, and the determination of the measurement level in previous reports was unclear. According to Joseph et al., [14] MRI biceps groove data from the 4th to 6th layers of the proximal humerus were used, and since they could not guarantee that the same layer was selected, it was difficult to make transverse comparisons between different individuals. Given the above reasons, this study constructed a three-dimensional model of the proximal humerus using thin-slice CT scanning, which allowed us to choose the measurement plane more intuitively and accurately on the model, thus avoiding measurement error and facilitating the horizontal comparison of different studies.

 There remains controversy about the correlation between the morphological differences of the biceps groove and LHBT lesions. Yoo et al. [6] compared the intraoperative stability of LHBT with the morphological measurement of the biceps groove based on MRI and found that a shallow biceps groove, large opening angle, and small angle of medial wall were high-risk factors for LHBT instability. Urita et al. [15] used CT  data to show that there was no significant correlation between the morphological parameters and LHBT lesions except for the bony spur in the medial wall of the biceps groove and the injury of the subscapularis tendon. Uluckoy et al. [5] also found that, except for subscapular tendinopathy, the shape of biceps sulci had little relationship with LHBT stability. Our study also found no correlation between the morphology of the biceps groove and LHBT injury, suggesting that the osseous structure is not the only and decisive stabilizing factor of LHBT lesions.

 The pulley structure of LHBT comprises the superior glenohumeral ligament (SGHL), the coracohumeral ligament (CHL), the supraspinatus muscle, and the subscapularis tendon, which is a soft tissue stabilizing device before the biceps long head tendon enters the bone pulley groove. Pulley structure injury is an important reason for the anterior pain of the shoulder joint [10]. Recently, more attention has been paid to pulley injury. Habermeyer classification is a commonly used clinical injury classification system for pulley structures [16]. This system was derived from Martetschlager et al. [17], and it was accurate, easy to use, and has a short processing time. In the present study, the proportion of pulley structure injury reached 55%, which was much higher than the 7% reported by Baumann [9]. This may be because this study enrolled more patients who required rotator cuff repair, whereas Baumann included a larger number of diagnostic arthroscopy cases. Considering that the biceps groove and the trochlea structure are the bone and soft tissue stabilizing structures of LHBT respectively, they may influence each other in the development of LHBT lesions. In the present study, we only found a positive correlation between trochlea structure injury and LHBT injury, but no correlation between biceps groove morphology and LHBT injury.

 This study has many shortcomings. All patients included in this study had rotator cuff tears, shoulder impingement, or other serious cases requiring surgery, and these diseases are high-risk factors of LHBT and pulley injuries [18] and could interfere with the analysis results. Second, due to the limited workload and research time of 3D reconstruction, this study could only include 126 cases, which may affect the validity of the conclusions. Finally, the accuracy of the study and the comparability between individuals were improved by positioning and measurement on the 3D model. However, most of the measurement parameters used for comparison were still measured in 2D studies. Further exploration is required to verify the advantages of 3D modeling in studying the biceps groove.

 In conclusion, pulley structure and LHBT injuries commonly accompany rotator cuff injuries. There are variations in the biceps groove of the humerus in humans, but the correlation between the trochlear structure and LHBT injury was not found in this study.

Abbreviations

LHBT: Lesions of the long head of the biceps tendon; 3D: three-dimensional; WG: Width of groove; DG: Depth of groove; OA: Opening Angle of biceps groove; MWA: Medial Wall Angle of biceps groove opening

Declarations

Supplementary Information

The online version contains supplementary material available at   

Acknowledgements

no.

Authors’ contributions

Xiaoye Tang performed the data analyses and wrote the manuscript; JiaLu Zhang contributed signifcantly to analysis and manuscript preparation; Jiechao Zhang and Yong He helped perform the analysis with constructive discussions. The author(s) read and approved the fnal manuscript.

Funding

This work was supported by Scientific and Technological Innovation Action Plan Medical Innovation Research Project of Shanghai Science and Technology Committee, Shanghai 21Y11911400

Availability of data and materials

All data generated or analysed during this study are included in this published article [and its supplementary information files]

Ethics approval and consent to participate

This study protocol was reviewed and approved by the Ethics Committee of Guanghua Hospital affiliated to Shanghai University of Traditional Chinese Medicine, All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Author details

All authors are from Department of Orthopaedic Surgery, Guanghua Hospital affiliated to Shanghai University of Traditional Chinese Medicine

References

  1. Macdonald P, Verhulst F, Mcrae S, et al. Biceps Tenodesis Versus Tenotomy in the Treatment of Lesions of the Long Head of the Biceps Tendon in Patients Undergoing Arthroscopic Shoulder Surgery: Blinded Blinded Controlled Trial.[Z]. 2020.48, 1433-1449.
  2. van Deurzen D F P, Garssen F L, Kerkhoffs G M M J, et al. Clinical relevance of the anatomy of the long head bicipital groove, An Evidence-based review. Clinical Anatomy (New York, N.Y.), 201,34(2):199-208.
  3. Ding D Y, Garofolo G, Lowe D, et al. The biceps tendon: from proximal to distal: Journal of bone and joint surgery. American volume,2014,96(20):e176.
  4. Lafosse L, Reiland Y, Baier G P, et al. Anterior and posterior instability of the long head of the biceps tendon in rotator cuff tears: a new classification based on arthroscopic observations.[J]. Arthroscopy : the journal of arthroscopic & related surgery : official publication of the Arthroscopy Association of North America and the International Arthroscopy Association, 2007, 23 (1) : 73-80.
  5. Ulucakoy C, Kaptan A Y, Yapar A, et al. The effect of bicipital groove morphology on the stability of the biceps long head tendon.[J]. Archives of Orthopaedic and trauma surgery, 2021141 (8) : 1325-1330.
  6. Yoo J C, Iyyampillai G, Park D, et al. The influence of bicipital groove morphology on the stability of the long head of the biceps tendon.[J]. Journal J orthopaedic surgery (Hong Kong),2017,25(2):613377483.
  7. Leite M J, Sa M C, Lopes M J et al. Coracohumeral distance and coracoid overlap as predictors of subscapularis and long head of the biceps Injuries and injuries [J]. Journal of shoulder and shoulder surgery,2019,28(9):1723-1727. (in Chinese)
  8. Gauci M, Deransart P, Chaoui J, et al. Three-dimensional geometry of the normal shoulder: Journal of shoulder and shoulder surgery,2020,29(12):e468-e477. (in Chinese)
  9. Baumann B, Genning K, Bohm D, et al. Arthroscopic prevalence of pulley lesions in 1007 consecutive patients.[J]. Journal of shoulder and elbow Surgery, 2008, (1) : 14 to 20.
  10. Martetschlager F, Tauber M, Injuries and experimental studies of tyrosine tyrosine tyrosine [J]. Journal of experimental myocardium,2016,35(1):19-27.
  11. Abboud J A, Bartolozzi A R, Widmer B J, et al. Bicipital groove morphology on MRI has no correlation to intra-articular biceps tendon pathology.[Z]. 2010.19, 790-794.
  12. Chen Changfa, one of the Kings. Anatomical observation of biceps groove of humerus and its clinical significance [J]. Chinese Journal of Clinical Anatomy,1991(03):151.
  13. Martetschlager F, Zampeli F, Tauber M, et al. Multiple approaches to / / gastronomic approaches to the Biceps Pulley: Research progress in the field of prospective research [J]. JSES international,2020,4(2):318-323.
  14. Abboud J A, Bartolozzi A R, Widmer B J, et al. Bicipital groove morphology on MRI has no correlation to intra-articular biceps tendon pathology.[Z]. 2010.19, 790-794.
  15. Urita A, Funakoshi T, Amano T, et al. Predictive factors of long head of the biceps tendon disorders-the bicipital groove morphology and subscapularis Tendon tear.[J]. Journal of shoulder and elbow surgery,2016,25(3):384-389.
  16. Habermeyer P, Magosch P, Pritsch M, et al. Anterosuperior impingement of the shoulder as a result of pulley lesions: A study on the potential of arthroscopic surgery [J]. Journal of shoulder and shoulder surgery,2004,13(1):5-12.
  17. Martetschlager F, Zampeli F, Tauber M, et al. Multiple approaches to / / gastronomic approaches to the Biceps Pulley: Research progress in the field of prospective research [J]. JSES international,2020,4(2):318-323.
  18. Braun S, Horan M P, Elser F, Gastronomic approach to gastronomic approaches [J]. Chinese journal of sports medicine,2011,39(4):790-795.