Keywords
rotator cuff injuries/diagnosis - rotator cuff injuries/epidemiology - rotator cuff
injuries/surgery - wound healing
Introduction
The incidence of rotator cuff injuries has grown exponentially as the life expectancy
of the population increases. Several technical explanations have been given to justify
this increase. The issue revolves around the degenerative aspects related to the aging
process of the organism, associated with some life habits, such as sports practice,
profession, diet, use of medications, and the presence of associated diseases in addition
to genetic issues, which has not received much attention in publications to date.
Anatomical variations also participate in this process. Therefore, there are many
factors that may influence the development of rotator cuff tendon injuries.
Hamada et al.[1] studied the histology of the human supraspinatus tendon, subdividing it into portions
and observed that, in the youth, the tendon is organized into wavy layers and that
in the older patients, this pattern changes to homogeneous, emaciated, and with hyaline
degeneration ([Figure 1]).
Fig. 1 In the young, the tendon insertion is organized in distinct layers (a) in the elderly,
there is disorganization (b).
Uthoff and Ishii[2] analyzed the histology of tendinous insertion in the larger tubercle and observed,
in the youth, the existence of a layered organization pattern. In the elderly, a disorganization
occurs that is considered a degenerative process ([Figure 2]). The author described the inflammatory reaction in the partial lesion of the rotator
cuff as an attempt by the organism itself to heal it. However, Yamaguchi et al.[3] histologically studied the natural evolution of these lesions in a series of 58
cases and, in none of them, it was possible to observe the reduction of the size of
the lesion. This fact shows that spontaneous healing of the rotator cuff is something
that should not be expected by patients, let alone by surgeons.
Fig. 2 Organization of the fibers of the supraspinatus tendon in layers in the young, and
its progressive disorganization in the adult.
Does the progressive increase in the incidence of injuries in the general population
lead us to ask about what is considered normal for a determined age? How many carriers
of cuff injury are asymptomatic? Milgron et al.[4] stated that the prevalence of lesions increases significantly in the population
after 70 years of age, and it is more frequent on the dominant side, a fact that has
been proven by other authors.[5] In the seventh decade of life, this incidence increases to more than 80%.
During the last two decades, methods of treatment of cuff injuries have evolved substantially.
The surgeries, which have previously been done openly, have started, in most reference
centers, to be done arthroscopicly. Different types of sutures emerged, and high-strength
threads began to be used routinely.
Local Factors
The main factors associated with rotator cuff healing are injury size, muscle quality
(atrophy and fatty degeneration), tendon quality, presence of delamination, and shoulder
morphology.
Injury Size
The first characteristic evaluated by most surgeons is the size of the lesion. The
analysis, however, should be performed by evaluating the size of the lesion in the
sagittal plane and coronal plane (medial retraction or tendon shortening), since they
are independent characteristics with respect to the healing rate. From a general point
of view, the increase in lesion size negatively influences healing rates, ranging
from 97%, for small lesions, to only 6%, for large or massive lesions, in some series.
[6]
[7]
[8]
[9]
[10]
Size Evaluated in the Sagittal Plan
Wylie et al.,[11] when evaluating the healing rate in this plan, showed that lesions ≥ 2.2 cm had
a healing rate of 49%, and in lesions ≤ 2.2 cm the rate rose to 71%. Considering this
cutoff value, the hypothesis was postulated that an injury exceeding 2 cm already
presents significant involvement of the infraspinal,[12] which alters the kinematics of the humean head, generating unbalance in the forces.[13] This fact would put the repair at risk, thus justifying the increased risk of healing
failure in lesions larger than 2.0 cm.
Evaluated Size in Coronal Plan (Shortening)
Myotendinous shortening is considered a direct result of muscle retraction. However,
Meyer et al.[14] showed that, although the shortening is predominantly of muscle mass, retraction
is also caused by shortening of the tendon itself, both due to the remaining substance
in the tubercule after the initial injury and, in advanced stages, the resorption
of the tendon itself. In a subsequent analysis, Tashjian et al.,[6] showed that patients with lesions in which the myotendinous junction (MTJ) is lateral
to the face of the glenoid, the healing rate was 93%, while in patients with preoperative
MTJ medial to the glenoid face, the healing rate was 55%. The analysis then concluded
that the position of MTJ is an independent factor in healing. From the point of view
of the size of the retraction itself, Wylie et al.[11] showed that lesions with shortening in relation to the footprint ≥ 2 cm presented
a healing rate of 47%, as opposed to 76% healing in lesions with retraction ≤ 2 cm.
Muscle Quality (Fatty Atrophy and Degeneration)
When one thinks of rotator cuff healing, one goal to be achieved is the healing of
the tendon-bone interface. Given this fact, most studies focus on methods to strengthen
or positively interfere with this interface. However, analyzing large lesions, Jeong
et al.[15] observed that muscle quality is more important than tendon quality in the new rupture
index. According to the authors, the occupancy rate of the supraspinatus below 43%
in relation to the totality of the supraspinatus fossa and a degree of fatty infiltration
≥ 2 according to Goutallier are independent risk factors for further rupture of the
rotator cuff, with sensitivity of 98% and specificity of 83.6%. A systematic review
by Khair et al.,[16] corroborates this fact, indicating that the quality of the preoperative muscle plays
an important role in the rate of tendon healing. Low stages of Goutallier (0–1) are
associated with low rates of new rupture (25%); in contrast, high stages (2–4) have
high rates of rupture (59%).
Histological and Macroscopic Tendon Quality
Regarding the analysis of the histological and macroscopic quality of the tendon,
it has been suggested that a worse quality tendon would lead to worse healing rates.
However, Mazzoca et al.[17] showed that there is no correlation between the macroscopic appearance of the tendon
in the arthroscopy, or in the histological analysis, and healing. Furthermore, they
showed that the macroscopic appearance is not correlated with the histological quality
of the tendon, and there is no association between the degree of histological tendinopathy,
the macroscopic appearance and the healing index or clinical results of the repair.
Therefore, the abnormal appearance should not influence negatively the stress or technique
of repair.
Delamination
A chronic complete lesion is considered delaminated when there is a horizontal cleavage
area in the ruptured tendon. The rotator cuff is composed of five layers, namely:
the most superficial is composed of coracoumeral ligament fibers; the second layer
is composed of parallel fibers between the supra and infraspinal; the third is composed
of small fascicles that intersect the cuff tendons at an angle of 45 degrees; the
fourth is composed of extracapsular loose connective tissue that previously connects
with the deep portion of the coracoumeral ligament; and, finally, the fifth layer
is basically composed of a joint capsule. The second and third layers are thicker,
presenting different directions of collagen fibers.[18] It is precisely between these layers that tendon delamination occurs. In a recent
study, Boileau et al.[19] showed a prevalence of 32% delamination, all of which involved a posterior component
of the deep layer. This study showed that, in general, delamination has a deleterious
effect on the healing rate, especially in large lesions. Kwon et al.,[20] in a study with 1,043 patients, confirmed the significantly lower healing rate in
delaminated tendons, if the analysis is performed using a single variable. However,
when performing multivariate analysis, it was noticed that delamination is not an
independent risk factor for healing failure.
Shoulder Morphology
Heuberer et al.[21] analyzed the morphology of the acronym and correlated it with the chance of developing
subacromial impact, impacto rotator cuff injury and arthropathy. There were three
ways to evaluate acromial morphology, namely: critical shoulder angle (CSA), acromial
index (AI) and lateral acromion angle (LAA). The authors concluded that the best way
to predict the appearance of cuff-related lesions or the development of osteoarthrosis
is through the CSA. This angle, which was described by Moor et al.,[22] has great benefit for combining the lateral extension of the acromion with glenoid
angulation. It is calculated on anteroposterior radiography by the angle between the
line of the lower edge to the upper edge of the glenoid and the line of the lower
edge of the glenoid to the most inferolateral point of the acromion ([Figure 3]). In the referred study, the authors demonstrated an association between rotator
cuff injury for CSA > 35° and glenohumeral arthrosis in CSA < 30°. This fact has been
demonstrated by other authors.[23]
Fig. 3 Critical shoulder angle.
A biomechanical study conducted by Gerber et al.[24] deepened the subject, demonstrating that CSA > 38° requires an increase of up to
33% in supraspinatus activity for shoulder stabilization during 6°-61° abduction.
This fact could explain the findings of Moor et al.[22] and predict probable change in the healing rates of these patients. In fact, Garcia
et al.[25] found a 14-fold vezes higher risk of rerupture ruptura in patients with CSA > 38°.
A recent systematic review on the subject also confirmed the hypothesis, showing that
CSA > 38° is associated with lower healing rate.[26] However, due to the heterogeneity of the relevant literature in the review in question,
the strength of this finding is considered limited.
Systemic Factors
We will discuss here the various systemic factors that can influence tendon-bone or
tendon-tendon healing.
Chronic alcohol use is an important factor regarding the increased incidence of injury
as well as the severity of rotator cuff injury in both genders. The association between
alcohol consumption and rotator cuff injuries showed that, in wine drinkers, there
was more massive lesions than small lesions.[27]
In relation to smoking, it is known that nicotine acts in the expression of the so-called
MMP-9, which is an enzyme involved in the degradation of the extracellular matrix,
in tenocytes. This factor leads to the modification of the modulus of elasticity of
the tendon and, according to Park et al.,[28] is an important risk factor for the spread of the lesion.
Regarding the influence of diabetes mellitus on the prognosis of cuff repair, it is
known that the persistence of hyperglycemia in the postoperative period increases
the possibility of non-healing of reconstructed the tendons. Therefore, blood glucose
control after surgery becomes fundamental.[29]
The association between arterial hypertension and cuff injuries showed that, in relation
to normotensive patients, hypertensive patients have twice as many large lesions and
four times as many massive lesions.[30]
Cholesterol also influences the prognosis by increasing tendon stiffness through changes
in its modulus of elasticity.[31]
Obese patients, those with increased body mass index, also present increased incidence
and severity of rotator cuff injuries.[32]
Immunobiological factors, by interfering with the mechanisms associated with muscle
homeostasis, aggravate the process of fatty degeneration, which, in sua turn, determines
the worsening of the prognosis of tendon healing.[33]
Finally, age, which is an inexorable factor, also influences through the natural process
of tendon degeneration, the modulus of elasticity in the rotator cuff.
Chung et al.[34] analyzed the main prognostic factors associated with poor results after surgical
reconstruction of the rotator cuff. The mean age of the patients evaluated was 63.7
years. The authors observed the incidence of 39.8% of failure in the repair of rotator
cuff lesions. The worst prognostic factors considered were fatty degeneration of the
infraspinal muscle and reduction of subacromial space by cephalic migration of the
humeral head.
Cho et al.[35] studied the factors that affect the integrity of rotator cuff reconstruction. The
patients were divided into three groups, namely: < 50 years of age group I), between
51 and 60 years of age (group II), and > 60 years of age (group III). They observed
that the older the age, the lower the incidence of healing ([Table 1]). Nevertheless, the study recommends the reconstruction of lesions in elderly patients
due to clinical improvement.
Table 1
|
Groups:
|
< 50
|
51–60
|
> 60 years
|
|
N
|
49
|
68
|
52 patients
|
|
Healing
|
87.8%
|
79.4%
|
65.4%
|
|
N-healing
|
12.2%
|
20.6%
|
34.6%
|
Deer et al.[36] evaluated the integrity of the repair and its relationship with the function on
the shoulders of patients submitted to arthroscopic reconstruction after 65 years
of age. For the study, the authors used the same sonographer to perform all imaging
tests and found an incidence of 75% of tendon integrity with the University of California
Los Angeles Shoulder Score (UCLA) improvement from 17 points to 32 points, which represents
85% of good and excellent results. There was also a significant reduction in the level
of pain when the visual analog scale was used.
Dezaly et al.[37] conducted a prospective, comparative, randomized study of two groups of patients.
Group I underwent rotator cuff reconstruction, acromioplasty, and tenotomy of the
long portion of the brachial biceps. Group II underwent biceps tenotomy and acromioplasty,
without cuff reconstruction. There were 103 patients evaluated and, although the postoperative
recovery time was shorter in group II, as expected, both the functional result by
the Constant score (82 in group I and 73 in group II) and the subacromial distance
measured in the imaging exams were favorable to group I. Interestingly, the best results
were observed in the reconstructions of the most retracted lesions, suggesting that
elderly patients with small lesions should be treated conservatively.
Many studies[38] have suggested that increasing age is related to a reduction in the potential for
tendon healing, while biomechanical studies suggest that the reason for this should
be due to an unfavorable environment, such as low-tissue perfusion and the reduction
in the number of undifferentiated cells.
Perioperative Factors
The systemic and local factors mentioned above are inherent to the patient, and, therefore,
in general, difficult to control on the part of the surgeon. For this reason, factors
related to surgical techniques are of crucial importance in the results, since at
this point the surgeon can actively act in the improvement of healing. Here, a good
choice, focused on technical knowledge, can increase healing rates.
Single Row x Double Row
Apreleva et al.[39] showed that rotator cuff repair with single row (SR) anchors can restore only 67%
of normal footprint, which could be an explanation for healing failures. Considering
this, Lo and Burkhart[40] created the double row (DR) of anchors technique. This technique consists of using
a row of medial anchors, next to the joint margin, and another row in the lateral
aspect of the footprint. In this way, the width from medial to lateral is reestablished
in an attempt to recreate the insertion of the rotator cuff and thus optimize the
healing potential. From a biomechanical point of view, the addition of a second row
of anchors increases the number of attachment points, increasing the initial strength
of the construction, decreasing the load that each knot/anchor needs to resist and
decreasing stress at the point of contact between each suture in the cuff. Biomechanical
studies supported the technique, demonstrating a significant decrease in gap interval
formation and strain deformation, associated with increased strength and initial stiffness,
when compared to the single row technique.[41]
Despite demonstrating a biomechanical advantage, the clinical value of the technique
is controversial, with an important part of the trials stating that there are no improvements
in quality of life or clinical scores, despite an advantage in the healing rate of
DR over SR.[42] A recent Brazilian study, with results of 1 to 4 years of the double row technique
corroborates this fact, demonstrating no statistically significant difference in UCLA
and American Shoulder and Elbow Score (ASES) scores between the two techniques.[43]
Given the above, to decide about the real advantage of the technique, and which patient
would benefit from it, Xu et al.[44] performed a meta-analysis, with randomized clinical trials of levels 1 and 2 evidence,
comparing the two methods. They concluded that, although the DR technique presented
a lower rate of new rupture (23.8% DR x 40.2% SR), better ASES and improvement in
medial rotation amplitude, there is no difference in the Constant score, UCLA score,
anterior elevation, lateral rotation and muscle strength when compared to the SR technique
in the overall analysis of the results. However, when analyzing subgroups by lesion
size, in large lesions > 3 cm, DR repair showed statistically significant improvement
in healing, UCLA and ASES. This result is corroborated by other authors, such as the
summary of meta-analyses performed by Spiegl et al.[45] and the meta-analysis produced only with level 1 trials of evidence, conducted by
Sheibani-Rad et al.[46]
Arthroscopic x Open
The most used methods for rotator cuff reconstruction are open, mini-open and arthroscopic.
Both the mini-open and arthroscopic techniques maintain the integrity of the deltoid
origin. In contrast, in the open technique, part of the deltoid is deserted from the
edge of the acromion. Theoretically, this would be the main disadvantage of open reconstruction;
however, a study by Cho et al.,[47] in postoperative magnetic resonance imaging (MRI) analysis, showed no significant
difference between open and arthroscopic techniques regarding complications such as
detachment of deltoid origin or muscle changes. Another disadvantage of the open technique
would be increased pain in the initial postoperative phase, since it requires greater
mobilization of soft tissues. This fact was also not confirmed, as demonstrated in
meta-analysis with level 1 randomized controlled studies conducted by Ji et al.[48]
Regarding healing rates, a recent meta-analysis with high-quality studies and 770
patients showed similar healing rates between mini-open and arthroscopic techniques.[49] Moreover, there was no significant difference in clinical scores between the techniques.
Despite the similarity between the clinical results and healing rates, it is worth
remembering that the arthroscopic technique offers advantage by providing easy access
to glenohumeral joint associated with better cosmetic results.
Postoperative Factors
Chemical Factors: Anti-inflammatory
Healing is a gradual process, composed of overlapping phases, and the inflammatory
phase is mandatory. Any factor that slows or alters its progress can affect it. Most
studies on the subject are in vitro or with animal models and, as found by Constantinescu
et al.,[50] in a systematic review, the current literature does not provide enough evidence
for or against the use of nonsteroidal antiinflammatory drugs (NSAIDs). It is worth
noting that this review found only one level 1 randomized clinical trial of evidence.
The study in question, conducted by Oh et al.,[51] compared the analgesic side effects in the use of celecoxib (selective inhibitor
COX-2), ibuprofen (non-selective NSAID), and tramadol (opioid). No significant differences
were found between medications. In a second time, retrospectively, the healing rates
were evaluated by MRI and ultrasound (US), and an important negative effect was observed
with the use of selective COX-2 inhibitor (new rupture: 37% celecoxib × 7% ibuprofen × 4%
tramadol). Therefore, despite presenting similar analgesia in the postoperative period,
when compared with other NSAIDs and opioids, selective COX-2 inhibitors should not
be used, since they can act negatively on healing after rotator cuff repair.
Mechanical Factors
The way to conduct the postoperative period may interfere with the healing process
of the rotator cuff after a surgical reconstruction. Rehabilitation protocols consider
the need for initial protection of reconstruction, associated with the intention of
restoring shoulder function, preventing joint stiffness and muscle atrophy. Shoulder
joint stiffness still has unclear etiology, but may be related to prolonged immobilization
or conservative rehabilitation programs.[52] Biomechanical studies show that early loading is harmful to the organization of
collagen fibers, and can generate microdamage at the bone/tendon interface, thus preventing
the integration of collagen fibers into the bone or even complete healing failure.[53]
Early Mobilization vs. Late Mobilization
The protocols can be divided basically into two categories: early passive motion (EPM)
and immobilization with delayed range motion (DRM).[54] The EPM protocol consists of minimal immobilization with sling, in which commuting
movements are allowed plus passive movements of range of motion such as lateral rotation
and elevation from the first postoperative day. On the other hand, the DRM protocol
imposes the use of sling without passive movements, and only commuting exercises up
to 2 to 4 weeks postoperatively are allowed. Performing analysis and review of published
meta-analyses, Houck et al.,[55] concluded that the EPM protocol improves the range of motion, but increases the
risk of further rupture of the cuff. It is noteworthy that, although shoulder stiffness
is an important problem in the postoperative period of rotator cuff surgery, it is
considered a complication, different from the recurrence of rupture, which is considered
a treatment failure.
Sling Time
One of the first questions of the patients in the preoperative consultation concerns
the time of use of the sling. There is a lot of divergence in the literature regarding
the minimum time of use associated with better rotator cuff healing. Koh et al.[56] showed, in a level 1 study of evidence, that there are no benefits in healing when
comparing immobilization for 4 weeks and immobilization for 8 weeks. Therefore, the
literature does not support the use of sling for more than 4 weeks.
Velpeau Sling vs. Abduction Sling
Basically, anti-rotational sling keeps the arm close to the body in medial rotation.
The abduction sling maintains the shoulder in various abduction and lateral rotation
configurations. In the biomechanical analysis, Jackson et al.[57] found the optimal position to create the lowest level of supraspinatus and infraspinatus
tension. This position would be with elevation of 21 to 45° and lateral rotation of
18 to 23°. However, in practice, the results do not prove the benefits of this position.
Some authors show that there was no significant difference in clinical aspects or
in the rate of new rupture. Other studies favorable to the use of abduction slings
show advantages from the clinical point of view of pain and function, without evaluation
of the the results in healing rates.[58] It is worth mentioning that, in general, studies on sling immobilization are based
on the responses of patients' self-assessment in relation to the amount of time of
use of the type; however, an important question is whether these patients actually
use the sling as reported. Based on this questioning, Grubhofer et al.[59] showed, evaluating the use of abduction slings with digital sensors, that only 48%
of patients used the sling in a way they considered satisfactory (> 80% of the time).
Moreover, when comparing the data obtained by the sensors and the patient information,
the discrepancy was frightening, especially in patients who did not use the sling
as recommended. The authors, therefore, suggest caution with the results of studies
on type and time of use of slings.
Genetic Factors
Figueiredo et al.,[60] identified genetic factors associated with susceptibility of rotator cuff injury,
reinforcing the role of extracellular matrix homeostasis in this context.
Final Considerations
The present review article allowed us to broaden the understanding of the factors
that interfere in the healing process of rotator cuff tendons. It was clear that there
are many variables, being local, systemic, mechanical, chemical, genetic or associated
with life habits. Pre, peri, and postoperative factors have a decisive influence on
this process. As a final message, it is suggested that the treatment of rotator cuff
lesions be done individually, considering all the factors previously described and,
in elderly patients, before the surgical option, that the attempt of conservative
treatment should be considered.
