Introduction

Although alterations in scapular motion can be observed in asymptomatic shoulders, these are more commonly described in the presence of painful conditions [1–4]. Because of the conflicting evidence regarding the causal relationship of scapular altered motion and pain, this issue is still under debate [5].

Symptom modification tests are frequently used to assess possible association between scapular motion and pain. This approach aligns well with recent proposals on applying a classification system that is based on movement-impairment rather than pathoanatomical findings [6, 7]. The Scapular Assistance Test (SAT) is one of these tests in which the scapula is manually assisted by the examiner into upward rotation and posterior tilt while the patient actively elevates the arm [8, 9]. The SAT is considered positive when a reduction of at least two points on the 11-point numerical pain rating scale occurs during assisted elevation as compared to elevation without assistance [8]. A positive SAT may suggest inadequate strength and/or activation of the serratus anterior and lower trapezius [8].

A recent study [10] reported a large variability in the clinical presentation in patients with shoulder pain, and described that factors related to range of motion, rotator cuff function and scapular motion were associated with shoulder pain, dysfunction of the upper limbs, and psychological aspects. The clinical presentation of individuals with shoulder pain is usually characterized by painful elevation of the arm, dysfunction, altered scapular motion, non-optimal activation of the scapular muscles, and more recently, by psychological aspects such as pain catastrophizing [1, 2, 11–13]. The heterogeneity of the clinical presentation and interactions among the different factors have not been previously investigated and may influence the result of the SAT. This study will enhance the knowledge to better understand how the SAT may guide the clinical decision-making in the management of individuals with shoulder pain.

Therefore, the aim of this study was to determine predictive factors related to the SAT in individuals with shoulder pain during arm elevation, and to analyze how these predictors interact in a nonlinear manner to discriminate the result of a positive and negative SAT.

Materials and methods

Results

A total of 236 individuals were recruited. Fig 1 brings the flow chart of the study. Eighty-four individuals completed the study. The characteristics of the individuals and predictors are presented in Table 1. Individuals with a positive SAT presented angular onset of pain higher in the range of arm flexion as compared to those with a negative SAT (p<0.05, mean difference: 20.35°, 95% CI: 4.70°; 36.01°). Individuals with a positive SAT presented less disability of the upper limbs when compared with individuals with negative SAT (p<0.05, mean difference: 7.58 points, 95% CI: 0.08; 15.08). Individuals with a positive SAT also presented lower score in the PCS than individuals with a negative SAT (p<0.05, mean difference: 7.62 points, 95% CI: 2.56; 12.68). There was no difference for the other outcomes (Table 1).

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Fig 1. Flow chart of the study.

https://doi.org/10.1371/journal.pone.0276662.g001

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Table 1. Characteristics of the participants and predictive factors.

https://doi.org/10.1371/journal.pone.0276662.t001

The classification tree selected the angular onset of pain during arm elevation as the first predictor variable of the SAT (Fig 2). Individuals with an angular onset of pain below or equal 65° of arm elevation will present a negative SAT. However, this variable alone did not entirely explain the occurrence of a positive SAT, and scapular dyskinesis was selected as the second predictor. Details about tree divisions, with the respective predictors’ cutoff points and the number and percentage of individuals classified in each subgroup according to the selected predictors are presented in Fig 2.

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Fig 2. Classification tree of the occurrence of a positive and negative Scapular Assistance Test.

The bolded category in each node corresponds to the predicted category. Abbreviations: SAT, Scapular Assistance Test; DASH, Disabilities of the Arm, Shoulder and Hand; PCS, Pain Catastrophizing Scale. Blue boxes indicate leaves of the tree. Gray boxes indicate intermediate nodes of the tree.

https://doi.org/10.1371/journal.pone.0276662.g002

The predictive model correctly classified 47 of the 47 individuals with positive SAT, and 31 of the 37 individuals with negative SAT. Overall, the predictive model obtained an average accuracy of 92.9% and ROC area of 0.96.

Discussion

The findings of this study demonstrated that a positive SAT may be influenced by different interactions of contributing factors. The angular onset of pain during arm elevation was the main predictor of a positive SAT selected by the CART. However, this variable alone did not entirely explain the occurrence of a positive SAT, and other predictors (scapular dyskinesis, pain catastrophizing, pain at rest and strength of the serratus anterior and lower trapezius muscles) were selected by the classification tree. Interestingly, pain catastrophizing was selected multiple times and may be considered an important predictor for a positive SAT. The cutoff points defined by the CART analysis may help clinicians to target factors that may be related to the occurrence of a positive SAT.

Those individuals with an angular onset of pain below 65° of arm elevation had a negative SAT. This finding is not surprising since contribution of the scapula is low at the initial ranges of arm elevation [36, 37]. In addition, pain and functionality of the arm may be better perceived above 65° where most daily and labor activities are performed [38], and contribute to a positive SAT from the interaction with the other predictors used in this study. The presence of dyskinesis combined with low pain catastrophizing (≤ 6 points at the PCS) contributed to a positive SAT above 65°. This indicates that the pain of these patients is likely influenced by altered scapular motion [9]. However, due to the chronicity of pain of the individuals in the current study, central impairments on pain modulation may be present and different phenotypes of people with shoulder pain may exist [39]. Taking all together, it is valid to observe other factors besides the biomechanical ones. Individuals with score above 6 points in the PCS, presence of pain at rest, and strength of the serratus anterior below 11.3 kilograms force also had higher likelihood of presenting a positive SAT.

Pain catastrophizing levels above 30 points indicate individuals susceptible to be catastrophizers [28]. Our study shows that mild levels of pain catastrophizing may moderate the probability of a positive SAT. For example, increased pain catastrophizing levels combined with intermediate values of serratus anterior strength (11.3 to 17.8 kilograms force) were associated with a negative SAT, but lower pain catastrophizing levels combined with higher values of serratus anterior strength (> 17.8 kilograms force) were associated with a positive SAT. The serratus anterior is an important scapular mover [21], and any change in pain or range of shoulder elevation during the assistance of the scapula has already been associated as a predictor of better outcome after physical therapy management for shoulder pain [40]. For individuals with pain during movement of the arm and scapular dyskinesis, pain catastrophizing may be more relevant as higher levels of pain catastrophizing were associated with a negative SAT.

When scapular dyskinesis is not present, strength of the lower trapezius should be assessed along with pain catastrophizing and strength of the serratus anterior. It is worthy to note that pain at rest was only selected when scapular dyskinesis was present, and that strength of the lower trapezius was only selected in the absence of scapular dyskinesis. Based on the muscle position, the lower trapezius muscle is most aligned to execute scapular upward rotation during arm abduction when compared to flexion [22]. However, SAT was performed during flexion of the arm in the current study. Future research may apply the SAT during abduction to investigate possible deficits in the lower trapezius muscle strength. Kibler [9] suggested that a positive SAT was related to a deficit in muscle activation or strength of the scapular muscles. However, recent studies [25, 41] did not identify differences in the serratus anterior and lower trapezius muscle strength between those with a positive and negative SAT. In the current study, muscle strength of the serratus anterior and lower trapezius alone could not explain the occurrence of a positive SAT. The inclusion of pain catastrophizing by the CART suggests that the SAT may be influenced not only by biomechanical variables but also by psychological factors.

Although the participants in this study presented high muscle strength, we cannot talk about muscle activation. Serratus anterior and lower trapezius muscles may not be properly activated during elevation of the arm. Clinicians should also be aware that previous studies have shown that individuals with a positive SAT are more likely to present greater scapular anterior tilt (Ribeiro et al., 2020) and pectoralis minor tightness (Grimes et al., 2020).

Negative psychological factors have been reported in individuals with shoulder pain. These factors include emotional aspects such as anxiety and depression, [42] kinesiophobia, [43] fear and avoidance beliefs [44] and pain catastrophization [29]. Recently, individuals with worse psychological profile were shown to present worse function and higher shoulder pain intensity [13]. In the present study, individuals with negative SAT presented higher pain catastrophizing thoughts when compared to individuals with a positive SAT. Clinicians should pay attention to individuals with a negative SAT as they may benefit of an approach that targets psychological factors in addition to therapeutic exercises. Further research should investigate the influence of other psychological factors, such as kinesiophobia, self-efficacy, optimism and resilience that may also predict the SAT result.

From the resulting tree, the cutoff points adjusted during the training stage are accurate since the classification leaves (in blue) mostly separate the two classes accordingly. Analyzing the tree, two leaves presented a misclassification of 6 individuals: (i) 5 individuals in the leaf that used the PCS with a cutoff point above 8 points; and (ii) 1 individual in the leaf that used the PCS with a cutoff point above 15 points. Both leaves are predominantly composed of individuals with positive SAT meaning that these leaves are better suited to classify individuals with positive SAT.

In summary, the resulting tree has 7 levels that combine the following variables: angular onset of pain, presence of scapular dyskinesis, pain catastrophizing, serratus anterior and lower trapezius muscle strength. Based on the results, these variables may be considered the most relevant to distinguish individuals with a positive and negative SAT. The high accuracy of the model indicates that the classification of individuals in positive or negative SAT was not random, nor was it affected by the imbalance between the number of individuals with positive or negative SAT. It is important to note that patients with negative SAT presented worse function, but also higher levels of pain catastrophizing when compared to positive SAT. Function of the upper limbs as evaluated by the DASH was not a relevant variable in the tree. This study suggests that biomechanics may not explain the SAT result alone, but there may be influence of patients’ belief in relation to their pain with regards to magnification, rumination and hopelessness. These findings are in line with another study [12] reporting that PCS explains function variance more than biological factors such as MRI data.

This study has some limitations. Although a 2-point decrease in pain intensity was considered for a positive SAT, the points on the numerical pain rating scale was not registered. The SAT was performed during flexion of the arm and our findings cannot be extrapolated to other planes of arm elevation. Some patients reported pain during execution of the muscle strength tests, and this may have influenced the results. Future studies should explore the contribution of other psychological factors to the contribution to SAT results such as positivism, resilience and self-efficacy. Finally, one should notice that this study does not allow a causal relationship to be made between the clinical variables.

Conclusion

The SAT result was influenced by different interactions of contributing factors, such as angular onset of pain during arm elevation, scapular dyskinesis, pain catastrophizing, pain at rest and serratus anterior and lower trapezius muscle strength. This indicates that the SAT result may be explained not only by biomechanical variables, but also by psychological factors. Disability of the upper limbs does not seem to contribute to the SAT result.

Supporting information