Efficacy of management of associated dysfunctions on rotator cuff and long head of the biceps: systematic review

Background The important functional role the rotator cuff (RC) and biceps play in the shoulder, the close anatomical relationship between them and the high incidence of injuries require an appropriate multidisciplinary therapeutic approach after a rigorous assessment. The objective is to identify and analyze surgical interventions, whether or not followed by a postsurgical one, of associated dysfunctions on the RC and long head of the biceps (LHB) and their effectiveness in improving shoulder functionality. Methods A systematic review based on PRISMA protocol was conducted using PubMed, Web of Science, PEDro, Scopus, CINAHL, and Dialnet until 22 April 2021. The main inclusion criteria were as follows: randomized clinical trials including subjects diagnosed with RC and LHB lesions who had surgical and/not post-surgical treatments. The methodological quality of trials was evaluated by the PEDro scale. Data were shown in 3 pre-established tables: (1)sample data, diagnostic methods, dysfunctions and injury frequency, interventions, outcome measures and results; (2)significance and effectiveness of interventions; and (3)comparison of the effectiveness of interventions. Results Eleven studies were selected. The methodological quality of ten of them was assessed as good and one excellent (PEDro scale). All articles had surgical treatments and ten had postoperative management. All trials used arthroscopy and two open surgery too. Single-row, double-row and transosseous repair were used for RC lesions, while SLAP repair, tenotomy, and tenodesis were applied to LHB injuries. Measured parameters were functionality, pain, Popeye’s sign, strength, range of motion, satisfaction degree, biceps cramping, and quality of life. All approaches in general, surgical plus postsurgical, were always effective to the parameters measured in each study. Seven trials compared tenotomy and tenodesis: four of them obtained statistically significant differences in favor of tenodesis in Popeye’s sign, cramping, satisfaction degree, and/or forearm supination strength; and one, in favor of tenotomy in cramping. All studies measured functionality using functional assessment scales. The most widely used was the Constant Score. Conclusions Surgical plus post-surgical interventions in associated dysfunctions on RC and LHB were effective. Tenodesis obtained better results than tenotomy in Popeye’s sign, satisfaction, and forearm supination strength. However, there was no difference regarding biceps cramping. Supplementary Information The online version contains supplementary material available at 10.1186/s13018-021-02621-0.


Introduction
The rotator cuff (RC), which plays a fundamental role in the stability of the shoulder joint complex, allows its optimal functionality by also orienting the upper limb in the three axes of space [1]. It consists of supraspinatus, infraspinatus, teres minor and subscapularis muscles [2], although some authors [3] include the long head of the biceps (LHB) due to its important stabilizing role in the glenohumeral joint [3].
Currently, there is a high index of omalgias, some of them due to both the general involvement of RC and, in particular, the long head of the biceps tendon (LHBT). In relation to the RC, the dysfunction affects 5.7 million Americans of over 60 years of age, accounting for 10% of the population [4]. In fact, said dysfunction has even been increasing in recent decades [5], which also implies an increase in treatments, as it is almost the most prevalent condition treated using orthopedic surgery [6]. On the other hand, LHBT pathologies (tenosynovitis, partial or total tendon tears, subluxations, or dislocations [7]) rarely appear in isolation and are commonly associated with RC [8] due to the close anatomical relationship between the two structures [9].
The frequent involvement of shoulders are the third cause of consultation in primary care and causes pain, stiffness, weakness, or joint instability that results in a detriment in the patient's quality of life [10]. So much so, that approximately 1% of adult populations in developed countries have shoulder disorders [4]. In half of these, the symptoms persist over a long period of time [11], which leads to a significant consumption of care and socio-economic resources, as well as production losses due to absenteeism. Thus, due to the important functional role the RC and biceps play in the shoulder [1], the close anatomical relationship between them [9], the high incidence of injuries [11], and the high prevalence of orthopedic surgeries that treat such dysfunctions [6]; these structures need to be addressed to obtain appropriate multidisciplinary diagnoses and interventions, i.e., surgical and conservative treatment, the latter including physiotherapy.
Consequently, the recovery rate of the patient will increase, the need for health care will decrease, and labor productivity will improve, which translates into a reduction in health costs.
Therefore, the aim of this systematic review was to identify and analyze surgical interventions, whether or not followed by a postsurgical one, of associated dysfunctions on the rotator cuff and long head of the biceps and their effectiveness in improving shoulder functionality.

Methods
The method used in this systematic review is based on the PRISMA statement [12].

Data sources and search strategy
An electronic search of PubMed, Web of Science, PE-Dro, Scopus, CINAHL, and Dialnet was carried out from inception through April 22, 2021. Mesh terms (Medical Subject Headings) for English language and other terms of interest for frequency of use, or Decs Terms (Descriptores en Ciencias de la Salud) for Spanish database and search strategies are shown in Table 1.

Study selection and inclusion/exclusion criteria
The selected studies had to meet the following inclusion criteria: (1) studies published until April 22, 2021; (2) population: adults with lesions diagnosed for both RC tendons and LHBT, without racial or gender limits; (3) intervention: surgical treatment, whether it had a postsurgical intervention or not, of RC tendons and LHBT pathologies, to achieve one or more of the following objectives: to decrease pain, to increase range of motion (ROM), patient strength and functionality; (4) study design: randomized clinical trials with a minimum score of 6 in the PEDro scale; (5) language: studies reported in English and Spanish.
The exclusion criteria were as follows: studies that included subjects with any neurogenic disorder or with tumors that affected the shoulder.
The title and summary of the found articles determined whether they fulfilled the inclusion criteria in a first phase. Subsequently, we reviewed the full text of the pre-selected studies and documented the reason for excluding the discarded records.

Data extraction
Data extraction was carried out by one reviewer (RA) and verified by a second reviewer (VP). Disagreements between reviewers were resolved by a third reviewer (GC), who assessed the information independently to resolve the discrepancies.
A pre-designed table detailed information on study features, participant characteristics, diagnostic methods, dysfunctions and injury frequency, surgical and postsurgical interventions, outcome measures (functional rating scales like Constant or tools like dynamometers, among others) and results (e.g., pain, ROM, patient strength, and functionality).
The methodological quality data were collected in a standardized table. See the section "Quality appraisal."

Quality appraisal
The methodological quality of trials was assessed by using the Physiotherapy Evidence Database (PEDro) scale [13], which evaluates both the internal validity of the study and the adequacy of the statistical information to interpret the results [14]. The scale is composed of 11 items, although the first criterion is not included in the final marker [14], so the maximum score is 10. All PE-Dro items assess the risk of bias of the selected studies, as shown in the results section of the key for Table 3. They were considered as excellent quality between 9 and 10 points, good quality between 6 and 8 points, fair quality for 4-5 points, and poor methodological quality for below 4 points.
The evidence levels determined by the authors of the included studies will also be considered.

Search results
The initial search produced 245 results. Following the removal of duplicates, 206 articles were screened by title, abstract, and full-text, due to as follows: not including subjects with lesions diagnosed for both RC tendons and LHBT, not having surgical treatment, not having ≥ 6 score in PEDro scale, not publishing in English or Spanish. Finally, 11 studies [15][16][17][18][19][20][21][22][23][24][25] were included in this review. Figure 1 shows study selection process based on PRISMA [12].

Quality assessment
The items: "subjects were randomly allocated to groups (in a crossover study, subjects were randomly allocated an order in which treatments were received)" [2]; "measures of at least one key outcome were obtained from more than 85% of the subjects initially allocated to groups" [8]; "all subjects for whom outcome measures were available received the treatment or control condition as allocated or, where this was not the case, data for at least one key outcome was analyzed by intention to treat" [9]; "the results of between-group statistical comparisons are reported for at least one key outcome" [10]; and "the study provides both point measures and measures of variability for at least one key outcome" [11], stood out as they were carried out in every study [15][16][17][18][19][20][21][22][23][24][25]. By contrast, item "there was blinding of all therapists who administered the therapy" [6], did not score.
As for the subjects' age, the mean was 59.37 years, the one performed by Mardani-Kivi et al. [23] was the youngest (55 years) while that of the longest-lived patients was by Franceschi et al. [15] (63.25 years).
With respect to the involvement of the dominant arm, seven [15][16][17][22][23][24][25] studies reflected whether it corresponds or not. In all of them, the involvement of the dominant arm was more common, it was 72.37% of the study sample, the highest frequency being 82% [22] and the lowest 56% [23].
• Active elbow flexion and extension were allowed, but terminal extension was restricted. Passive ER (1 day after surgery).
• At 6 weeks, the sling was removed, and overhead stretching were started (rope and pulley).
• Isoinertial strengthening and rehabilitation of RC, deltoid, and scapular stabilizers were initiated (10 or 12 weeks post-operation).
• Heavy manual work and overhead activities were allowed after 6 to 10 months after surgery. There was a statistically significant difference in total postoperative UCLA scores and ROM (p < 0.05).
Franceschi et al. [16] To determine whether or not to detach the biceps tendon from the glenoid after tenodesis performed with the inclusion of the biceps in the RC suture results in an improved outcome. Level of evidence: not specified. • EG1: arthroscopy; RC repair and tenodesis without tenotomy of LHBT.
• Active elbow flexion and extension were allowed, but terminal extension was restricted.
• At 6 weeks, the sling was removed, and overhead stretching were started (rope and pulley).
• Isoinertial strengthening and rehabilitation of RC, deltoid, and scapular stabilizers were initiated (10 or 12 weeks post-operation).
• Heavy manual work and overhead activities were allowed after 6 to 10 months after surgery.  (depending on the patient's age: > 50, tenotomy).
• Afterwards, pulley exercises were prescribed to increase their range of flexion.
• Home-based active assisted shoulder exercises; 3 times daily, each session 20 min.
• Elastic band exercises, strengthening exercises for the muscles stabilizing the scapula, were initiated 2 months after the operation.
• All sports activities were permitted after 6 months.
The 12 months post-operatively: no significant differences were found in ROM, pain and functional scores between the groups (p > 0.05). Popeye´s deformity was 3 times higher in group I than in group II (19.6% vs 5.6%) p = 0.04. Besides, group II showed greater forearm supination power (0.818 ± 0.108) than group I (0.998 ± 0.015, p = 0.02).
Zhang et al. [19] To compare the clinical outcomes between tenotomy and tenodesis for the treatment of LHB lesions in patients > 55 • EG2: arthroscopy; RC repair and LHBT tenotomy with tenodesis. Postoperative rehabilitation: • All the patients followed the routine rehabilitation procedures after RC repair.
• For tenotomy group: immobilization of their elbow motion for 1 week.  • Active ROM and gentle strength training 6 weeks post operation.
• Unrestricted use of the biceps muscle was not allowed until 16-20 weeks post operation.
Postoperative rehabilitation: • Immobilization in abduction: 4 weeks for a partial-thickness and small (< 1 cm) tear, 5 weeks for a medium (1-3 cm) tear, and 6 weeks for a large to massive tear (> 3 cm).
• Shrugging of both shoulders, active elbow flexion/extension, active forearm supination/ pronation, and active hand and wrist motion were encouraged immediately after surgery.
• Active-assisted shoulder ROM exercises were encouraged after weaning from the brace.
• Muscle strengthening exercises were started at 9 to 12 weeks postoperatively.
• All sports activities were permitted from 6 months after surgery.  • EG2: arthroscopy; RC repair and LHBT tenotomy and tenodesis. Postoperative rehabilitation: • Immobilization was maintained with a 20°a bduction pillow for 3 weeks.
• Pendulum exercises were allowed, starting from the first post-operative day.
• After the immobilization period, passive and assisted exercises in forward flexion and external rotation were initiated.
• Strengthening exercises were restricted until 6 weeks after the surgical procedure.
The follow-up was 6 and 24 months.   • Pull over was forbidden up to 6 weeks to prevent damage of the healing area.

Comparison between groups
• After 6 weeks, the sling was removed and pull over was started with the help of tackles.
• Isotonic strengthening of fixator muscles of RC, deltoid, and scapula were started at 10th to 12th postoperative weeks.
• This rehabilitation process was continued for 6 months.
• Heavy hand work and pull over activities were allowed after 6 to 10 postoperative months.  • The first 6 weeks after surgery, a sling with abduction pad was used.
• Active flexion and extension of the elbow were allowed, but terminal extension was forbidden.
• After 6 weeks, the sling was removed.
• Isotonic strengthening of the fixator muscles of RC, deltoid, and scapula was started at 10 to 12 postoperative weeks.
• This rehabilitation process was continued for 6 months.
• Heavy manual work and overhead activities were allowed only after sufficient muscle strengthening at approximately 6-10 months after surgery. the shoulder and elbow were started and gradually increased.
• Full-weight loading of the RC and biceps was not allowed until at least 3 months after surgery.  [17]; and that of ST and subscapularis tendon (SbT) in 18% [16]. Finally, the three tendons (ST, IT, and SbT) were affected in 27% [16].
Van Deurzen et al.
Criteria: (1) Eligibility criteria were specified. (2) Subjects were randomly allocated to groups (in a crossover study, subjects were randomly allocated an order in which treatments were received). (3) Allocation was concealed. (4) The groups were similar at baseline regarding the most important prognostic indicators. (5) There was blinding of all subjects. (6) There was blinding of all therapists who administered the therapy 7. There was blinding of all assessors who measured at least one key outcome. (8) Measures of at least one key outcome were obtained from more than 85% of the subjects initially allocated to groups. (9) All subjects for whom outcome measures were available received the treatment or control condition as allocated or, where this was not the case, data for at least one key outcome was analyzed by "intention to treat." (10) The results of between-group statistical comparisons are reported for at least one key outcome. (11) The study provides both point measures and measures of variability for at least one key outcome
Only five studies [15,16,18,23,25] compared the pre-and post-intervention of each experimental group ( Table 4). The measured parameters were ROM, pain, and patient satisfaction. Related to the functionality, Constant, UCLA, SST, and ASES scales were used. Two articles [15,16] found significant differences in each intervention. Each group showed a statistically significant improvement in ROM and UCLA.
One [18] obtained significant improvements in pain, in Constant, and in ASES scales in every experimental group. Another one [23] found significant differences in each intervention in Constant, SST, pain, and satisfaction. Both groups improved these mentioned parameters. One [25] showed substantial improvements in Constant Score in both groups. Table 4 summarizes the significance and effectiveness of interventions of these 5 studies.
Specifically, in [15], group II intervened through biceps tenotomy and RC repair and showed statistically significantly better results in UCLA scores and ROM than group I, which operated through type II SLAP repair and RC repair. In [18], group II intervened through tenodesis with tenotomy showed greater forearm supination power than group I, which operated through tenotomy (p = 0.02). In [21], the incidence of Popeye's sign was significantly higher in group II, operated through tenotomy, than group I, intervened through tenotomy and tenodesis. In [22], the incidence of Popeye's sign was significantly higher in group I of tenotomy than in group II of tenodesis, while the incidence of biceps brachii cramping was higher in the tenodesis (p = 0.043). In another one [23], Popeye's sign and biceps brachii cramping were significantly higher in group I of arthroscopic tenotomy than in group II of open subpectoral tenodesis, and patient satisfaction was significantly higher in tenodesis.

Discussion
This systematic review compiled the randomized clinical trials that included subjects with lesions diagnosed for RC and LHB, identifying and analyzing surgical and post-surgical approaches, if the latter was specified, as well as their efficacy on associated dysfunctions on both structures. Thus, sample data, diagnostic methods, dysfunctions and injury frequency, interventions, outcome measures, and results obtained were extracted. Secondarily, the functional evaluation methods on associated dysfunctions on RC and LHB were analyzed.
Regarding the methodological quality, this systematic review required randomized clinical trials to score at least 6 out of 10 on the PEDro scale [13], i.e., good methodological quality. It is noteworthy that 3 out of 10 scoring items are related to blinding (5, 6, and 7), which is difficult to meet in the surgical and post-surgical procedures addressed [27]. Thus, these items did not score particularly well. In particular, the blinding of clinicians who administered the therapy did not score any points. However, regarding the patients, three of the included studies [18,20,22] were blinded despite the handicap. The methodological quality of Castricini et al. [22] was even assessed as excellent since, in addition to the patients, it blinded the evaluators of the intervention. Thus, said author ensured that the results of the interventions were not conditioned by the subjects and also decreased the probability of clinical trial bias.
Since the PEDro scale determines the probability of the result validity and that it contains sufficient information to guide clinical practice [13], the good methodological quality of the selected studies evidenced these attributes. This is complemented by the evidence levels In relation to the sample, RC and LHB dysfunctions can occur at any age, although the mean of these studies is around 60 years, consistent with the reduction of the blood supply characteristic of age [28], which contributes to tendon degeneration [29]. As for sex, there are no major differences between men and women. This equity is refuted in the study of Razmjou et al. [30] in which the associated lesions affected the male population more significantly. However, Lee et al. [18], in which the study sample was consecutive, the high incidence percentage of women (77%) may be due to the increase of calcium and/or hydroxyapatite deposits on tendons because of the hyperparathyroidism in menopausal women [31]. Likewise, seven studies [15][16][17][22][23][24][25] mentioned the involvement of the dominant arm, this being the injury with a large percentage, surpassing 80% [22,24] of cases. This high incidence is due to the degeneration of RC tendons because of the overuse of the dominant arm in activities of daily life. This explains what happens more in workers and athletes [11] whose requirements are greater.
With respect to the methods of evaluation and diagnosis, some clinicians use special tests for RC tears [32] and for biceps [23]. In addition to these tests, it is convenient to use complementary imaging tests rather than giving additional information, thus obtaining, a more accurate diagnosis. In relation to this review, all the analyzed studies have used complementary imaging tests. The most commonly used was MRI, since it allows to recognize factors of poor prognosis, such as tedious retraction, atrophy, and fat infiltration of the muscular tummy, and identify lesions associated to the glenohumeral joint [33]. Likewise, Iannotti et al. [33] described a sensitivity of MRI of 89% and a specificity of 100% in the detection of rotator tears not subjected to previous surgery. Ardic et al. [34] show MRI and US had a comparable high accuracy for identifying the biceps pathologies and RC tears. Despite this, MRI was superior to ultrasonography in many shoulder structures [34]. Nevertheless, MRI is still a costly method [35] of somewhat limited availability and may be contraindicated for medical reasons or for claustrophobia [36].
On the other hand, the relationship between RC and LHB was proposed. The associated pathologies were RC tears and LHBT tears, subluxations, or dislocations. In the case of a single injured tendon, the supraspinatus is the most frequently affected [18] and it is associated with partial or total tears of biceps tendon. However, when the injury affects the SbT, it is very probable that there is an instability-like dysfunction of the LHB, due to the intimate morpho-functional relationship existing between the structures in relation to the reflex pulley [37] charged with maintaining the integrity of LHB. In the case of an involvement of 2 tendons, the association of ST and IT is the most commonly related to LHB tendinopathy [7].
As for the surgical treatment applied to restore RC dysfunctions, all trials [15][16][17][18][19][20][21][22][23][24][25] used the arthroscopy technique. Compared with traditional open techniques, arthroscopic repairs offer patients smaller incisions and less soft-tissue trauma, which result in improved postoperative pain and rehabilitation [38]. Besides, seven papers [15-18, 22, 24, 25] used suture anchors in RC lesion. Regarding the type of suture anchor, three [16,17,24] used metallic anchors and two [15,22] biodegradable anchors. As for the anchor composition, each material has its inherent advantages and disadvantages. For example, metallic suture anchors are opaque in X-rays and are hence easily evaluated in the clinical setting. However, these pose challenges in revision RC surgery [38], including distortion of preoperative MRI and necessity of removal before a new anchor can be put in place [38]. On the other hand, bio-absorbable anchors are radiolucent in X-rays and have less distortion on MRI [38]. Nevertheless, there are cases of an exaggerated immune response resulting in significant osteolysis, chondrolysis, and premature anchor failure [38].
Regarding LHB surgical treatment, there is no consensus on which technique is the most effective, since some authors, such as Walch et al. [39], defended tenotomy as producing more satisfactory results, while others, such as Checchia et al. [40], also obtained results in patients treated with LHB tenodesis. However, tenodesis seems to prevent complications associated with tenotomy, such as Popeye's sign, atrophy, and muscle weakness [41]. This fact is corroborated in this review, in which the incidence of Popeye's sign is significantly higher in the tenotomy group [18,[21][22][23].
In relation to this postoperative intervention, physiotherapy currently addresses shoulder dysfunction through numerous procedures [42][43][44], in accordance with authors such as Kuhn et al. [45]. This study [45] considers joint mobilizations, massage, transcutaneous electrical stimulation nerve stimulation, US, laser treatment, extracorporeal shockwave [46], and a flexibility and strength exercise program [45,47]. Scientific evidence demonstrates that the combination of exercise and manual therapy significantly decreases pain and increases functionality [45]. Therefore, the selected trials [15][16][17][18][19][20][22][23][24][25], included flexibility and strength exercise programs and joint mobilizations performed from the first day in order to increase recovery speed and decrease the period of disability [48]. The role of the scapula in omalgia is considered especially relevant nowadays due to moving the upper extremity through its greatest ROM, the shoulder complex (thorax, humerus, and scapula) must work in a synchronized manner [49]. Thus, optimal shoulder functionality is directly related to adequate scapular biomechanics [50]. For this reason, some authors such as Struyf et al. [46], Moezy et al. [51], and Baskurt et al. [52] add, to the rehabilitation of shoulder pathology, scapular stabilization exercise programs [15][16][17][18]53].
To assess treatment efficacy, the authors measured pain, ROM, muscle strength, absence or presence of Popeye's sign, biceps brachii cramping, quality of life, and degree of satisfaction separately. The sum of the mentioned parameters, except for Popeye's sign, biceps cramping, and quality of life, involves the way the global functionality of the shoulder is addressed. Even so, every study used functional rating scales that offered a single score, even if independently rated items had been included. All clinical interventions from the included studies [15][16][17][18][19][20][21][22][23][24][25] improved those parameters separately, as well as global functionality through rating scales, so any intervention of associated dysfunctions on the RC and LHB is effective from a clinical perspective. As to the shoulder rating scales used, the authors mainly used the Constant Score as a functional assessment method to determine the significant differences. This scale is employed in shoulder pathologies, especially RC [54,55]. Its frequent use is because it is easy to complete and interpret [55] and it is also extremely useful in monitoring RC dysfunctions [55].
Regarding the strengths of the study, it should be noted that randomized clinical trials were only included to minimize the risk of review bias, in addition to a requirement of a minimum of 6 points on the PEDro scale, that is, that the methodological quality was good. On the other hand, the search was carried out with no time limit (i.e., without applying any time filter in the databases), to obtain more scientific evidence, as well as assess the new healthcare trends. Finally, this review provides detailed information on the functional assessment tools used by every author. This highlights the importance of these methods, which contain both objective and subjective data from clinicians and patients themselves (patient-reported outcome measures).
Regarding the limitation of the study, the authors considered that the surgical techniques used in the studies, as well as the items addressed and the measurement systems applied, were broadly heterogeneous, thus preventing any meta-analysis. On the other hand, one of the included articles [21] did not specify the physiotherapeutic intervention in detail. Based on this, the authors propose a review that focused its attention on the physiotherapeutic protocol used in the combined impacts of RC tendons and LHBT prospectively. After analyzing the results obtained in this study, a new systematic review addressing "the efficacy of treatment on RC and superior labral dysfunctions" could be of interest. We also consider more randomized clinical trials where surgical techniques and associated conservative clinical procedures are homogenized to be necessary (e.g., corticosteroid injections or physiotherapy) in order to obtain robust evidence of the effectiveness of the interventions. This would enable the creation of quality clinical action protocols.
In conclusion, this systematic review analyzed the efficacy of surgical and post-surgical interventions used, when the latter were specified, in the joint dysfunctions of the tendons attached to the RC and the LHBT.