Rotator cuff tears and tendinopathy - Is platelet rich plasma (PRP) helpful? Read this important updated version.

A review of published randomized trials and meta-analyses indicates that non-operative treatment is effective for the majority of patients with conditions of the rotator cuff, including rotator cuff tears.

Local corticosteroid injections are sometimes used in non-operative treatment, however they apparently have no biologic effect in terms of regenerating or reversing the degenerative changes occurring in rotator cuff tendons and their clinical benefit usually wears off quickly.

It has been suggested that local injection of platelet-rich plasma (PRP) may promote stem and progenitor cell proliferation, modulate inflammatory responses, stimulate angiogenesis, enhance the proliferation of tenocytes, stimulate the production of extracellular matrix proteins, protect against oxidative stress, and inhibit inflammation (see Platelet-Rich Plasma in Orthopaedic Surgery: A Critical Analysis Review) and that these effects may benefit patients with rotator cuff tendinopathies before structural failure of the rotator cuff occurs. 

 The authors of Subacromial injection of platelet-rich plasma provides greater improvement in pain and functional outcomes compared to corticosteroids at 1-year follow-up: a double-blinded randomized controlled trial attempted to answer this question in a randomized clinical trial of patients between 18 and 50 years old (mean age 28 years) who had both a clinical and magnetic resonance imaging diagnosis of supraspinatus tendinopathy refractory to conservative treatment. 

A total of 50 patients received a single subacromial injection of PRP, whereas 50 patients received a single subacromial corticosteroid injection. All the patients completed 12 months of clinical follow-up. 

At 12 months, in comparison to the those receiving cortisone, patients in the PRP group showed a significantly greater improvement in 

the VAS score: 1.68 vs. 2.3

the American Shoulder and Elbow Surgeons (ASES) score, 89.8  vs. 78.0 

the Single Assessment Numeric Evaluation (SANE) score, 89.2 vs. 80.5 

and the the Pittsburgh Sleep Quality Index (PSQI) score, 2.72 vs. 4.02 

The overall failure rate was significantly higher in the corticosteroid group (30%) than in the PRP group (12%) (P < .01).

It was particularly interesting to note that the difference in the course of the two groups was not evident until 6 months after the injection. As Michael Pearl pointed out, it is possible that the PRP folks would have gotten better anyway (i.e. the PRP may not have had an effect). We'd need a saline injected control arm to examine that possibility.

It does seem that the corticosteroid injected group tended to do less well with time and their greater failure rate may be related to the adverse effects of cortisone on tendons. As Dr Pearl says "An alternative explanation could be that cortisone is deleterious and the PRP less interfered with the natural history.  " 

It is notable that the ASES score difference between 3 and 12 months (85 to 90) does not exceed the minimal clinically important difference for ASES of 15. 

Comment: This double blinded randomized clinical trial showed that young patients with rotator cuff tendinosis having subacromial injection of PRP did better than comparable patients having subacromial injection of cortisone. It does not show that patients having subacromial injection of PRP would do better than those with no treatment or with a placebo control. Keep in mind that these patients had an average age of 28, folks who have a lot of potential for recovery with time and rehab.

A possible benefit of PRP in cuff tendinosis cannot be extrapolated to the treatment of cuff tendons with structural failure, as demonstrated by the authors of Subacromial Platelet-Rich Plasma Injections Produce Significantly Worse Improvement in Functional Outcomes in Patients With Partial Supraspinatus Tears Than in Patients With Isolated Tendinopathy who found that  improvement in the ASES score was significantly greater in the group without tears than in the group with partial cuff tears (PTRCTs) at all follow-up times. 94% of the patients in the isolated tendinopathy group but less than half of patients in the PTRCTs group achieved a substantial clinical benefit at 12 months follow-up. 

Furthermore, a review of published randomized controlled trials and meta-analyses failed to demonstrate a clinically significant benefit to the patient of the use of PRP in conjunction with surgical repair of a torn rotator cuff.

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Here are some videos that are of shoulder interest
Shoulder arthritis - what you need to know (see this link).
How to x-ray the shoulder (see this link).
The ream and run procedure (see this link).
The total shoulder arthroplasty (see this link).
The cuff tear arthropathy arthroplasty (see this link).
The reverse total shoulder arthroplasty (see this link).
The smooth and move procedure for irreparable rotator cuff tears (see this link).
Shoulder rehabilitation exercises (see this link). 

PRP for Cuff Disease: Data Fragility of a Level I Study

Allogeneic Platelet-Rich Plasma Versus Corticosteroid Injection for the Treatment of Rotator Cuff Disease A Randomized Controlled Trial

These authors investigated the safety and efficacy of a fully characterized allogeneic pure PRP injection into the subacromial space of patients with "rotator cuff disease" in comparison with corticosteroid injection. Inclusion criteria: ≥18 years ofd age, unilateral shoulder pain for at least 3 months, a Neer or Hawkins impingement sign,  either a painful arc or a positive result on the Jobe test. Exclusion criteria included previous subacromial injections within the past 3 months, a history of shoulder trauma, a full-thickness rotator cuff tear as demonstrated with magnetic resonance imaging (MRI) or ultrasonography, and limitation of both active and passive movement of the glenohumeral joint of 25% in at least 2 directions as compared with the contralateral shoulder or with normal values.

60 patients with rotator cuff disease were randomly assigned to receive a subacromial injection of either 4 mL of allogeneic pure PRP or a 4-mL mixture of 1 mL of 40-mg/mL triamcinolone acetonide and 3 mL of 2% lidocaine under ultrasonographic guidance. 

The authors concluded that " Constant score at 1 month did not significantly differ between the PRP and corticosteroid groups. At 6 months, the DASH (Disabilities of the Arm, Shoulder and Hand) score, overall function, and external rotation were significantly better in the PRP group than in the corticosteroid group, and the other clinical outcomes did not show significant differences. All pain measurements, the strength of the supraspinatus and infraspinatus, and 5 functional scores also improved slowly and steadily after injection, becoming significantly better at 6 months compared with those before the injection, whereas those in the corticosteroid group responded promptly but did not further improve. Allogeneic PRP injections for the treatment of rotator cuff disease are safe but are not definitely superior to corticosteroid injections with respect to pain relief and functional improvement during 6 months. The DASH score, overall function, and external rotation were significantly better in the PRP group than in the steroid group at 6 months. Generally, PRP slowly but steadily reduced pain and improved function of the shoulder until 6 months, whereas corticosteroid did not."

Comment: Let's take a look at the DASH data. Recalling that a lower DASH score is good, we can see that at later time points the average DASH scores for the available patients are lower (i.e. better).

A few blog posts ago we discussed data fragility (see this link). Fragility is an indication of how sensitive the result is to the loss of patients to followup. 

In this study, we see that the average DASH score for the patients available at each time point after treatment is related to the percentage of patients lost to followup. The best (lowest) DASH score is at 6 months when 24% of the original patients were not included. The conclusion that the DASH improved with time is fragile because it is possible that the missing 24% could have had higher (worse) DASH scores at 6 months - we just don't know. 

It is also of interest that the percent of patients lost to followup (especially at 6 months) is quite different for the PRR and the steroid groups as shown below.

This limitation is not discussed in the limitations discussion of the paper.

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‘‘Stem Cell Treatments Flourish With Little Evidence That They Work’’

This was a headline in the May 13, 2019 New York Times. You must read the full article in this link.

Here is a nice review: The role of biologic agents in the management of common shoulder pathologies: current state and future directions
Here are their conclusions regarding platelet rich plasma (PRP). Given the wide variety of clinical results for PRP injections for various shoulder pathologies, expectations must be tempered by clinicians and patients. Although basic science literature supports a potential role in the management of rotator cuff tears, robust clinical data are lacking to support their widespread use.

Here are their conclusions regarding "stem cells" or "cell based therapy" or Bone marrow aspirate concentrate (BMAC). BMAC has the unique advantage of containing a very small population of mesenchymal stem cells and a high proportion of various growth factors, but its true clinical efficacy is still largely unknown. High-quality studies with appropriate control groups are needed to better define its clinical role. A critical deficiency in the current literature is the lack of information correlating the composition and/or biologic activity of marrow-derived cells and clinical outcomes. Furthermore, obtaining BMAC is an expensive procedure with unknown cost-effectiveness.

One of the key issues is the direct to consumer advertising of stem cell and related therapies See this link.

Comment: Currently we are seeing aggressive marketing and patient demand that has led to the indiscriminate use of cell therapy for a wide range of musculoskeletal conditions. It is of note that in many cases the high cost of these procedures is covered by the patient because insurance companies have not been convinced of their effectiveness. Because of the lack of data on their value to the patient, we avoid these interventions in our patients.

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Are PRP, stem cells, or biomaterials of value in rotator cuff repair?

Biologics for Rotator Cuff Repair A Critical Analysis Review

In their introduction, the authors state that "Despite an increase in the number of operations performed and enhanced surgical techniques, unacceptably high rates of failure of up to 94% still occur." They point out that this has driven intense scientific and commercial interest in "biologics" (platelet-rich plasma, stem cells, and biomaterials) as a possible means for enhancing the healing of attempted cuff repairs.

In their review, these authors note that

(1) among the many types of biologic augmentation, there is considerable heterogeneity of the content, quality, and quantity of growth factors used in platelet-rich plasma and bone marrow aspirate concentrate, and conclusions from individual studies may not necessarily be generalizable to other formulations within the group.

(2) current Level-I evidence suggests that universal use of platelet-rich plasma provides no significant clinical benefit in rotator cuff repair.
(3) although some evidence exists for the use of stem cells from bone marrow aspirate concentrate and the use of biologic grafts, results from Level-I studies are lacking and 

(4) level-I trials focused on the evaluation of clinical outcomes (i.e. using the Simple Shoulder Test, the American Shoulder and Elbow Surgeons score, the University of California at Los Angeles  shoulder score, or the Constant score) should be performed to help to determine the appropriate use of biologic augmentation in rotator cuff surgical procedures.

Comment: As these authors indicate, all of the scientific and commercial interest in biologics needs to be evaluated in terms of well controlled studies showing that clinical outcomes are better for patients receiving biologics in comparison to comparable patients not receiving them. These studies need to be carried out in recognition of the observation that over 10 million individuals are living with cuff tears and at most 4% of them get surgery each year. It is commonly observed that patients with cuff tears can respond to physical therapy. Furthermore, patients are commonly clinically improved after cuff repair surgery whether or not the surgery is successful in restoring the integrity of the cuff. From a clinical standpoint, therefore, biologics are going to need to make a big difference in order to justify their cost.

For a perspective on cuff repair as well as a Robert Frost poem, readers are invited to visit this post:

Rotator cuff repair - failure with continuity

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Does PRP help patients having rotator cuff repair?

Platelet-rich plasma in fibrin matrix to augment rotator cuff repair: a prospective, single-blinded, randomized study with 2-year follow-up

These authors point out that "despite improvements in the mechanical constructs used to repair rotator cuff tears, retear remains a significant issue. Retear rates ranging from 10%-90% depending on the size of the tear, age of the patient, amount of fatty infiltration, and type of repair have been reported. Higher failure rates in patients older than 65 years have been consistently demonstrated".

They sought to test the concept that application of autologous platelet-rich plasma in fibrin matrix (PRPFM) improves clinical outcomes in patients undergoing arthroscopic rotator cuff repair using a prospective, randomized, single-blinded study of 76 patients. The treatment group underwent arthroscopic rotator cuff repair with PRPFM. 

The control group did not receive the PRPFM. 

The Simple Shoulder Test scores showed no incremental benefit of PPFM: the improvement was from 45% to 96% for the control group and from 49% to 96% in the PRPFM group. 

Strength of the supraspinatus at 24 months by dynamometer testing was 99.8% in the control group and 96.3% in the PRPFM group. Infraspinatus strength was 104% in the control group and 103% in the PRPFM group

MRI's suggested a 19% retear rate for the control group and 7.4% for the PRPFM technique at 6 months.

All of their results showed no statistically significant benefit of PRPFM.

Comment: This is a valuable randomized trial that shows that showed no evidence of added clinical benefit for the PRPFM. If the study had not included the control group, one might conclude that cuff repair with PRPFM argumentation was a "clinically viable technique" because the patients were improved. However, with the inclusion of the control group, it became evident that the addition of PRPFM did not benefit the patients.

It is of interest that in spite of the apparently greater rate of retears in the control group, there was no difference in clinical outcomes.

The authors do not provide the incremental time involvement and the incremental cost of the PRPFM approach (see the details at the end of this post below).

In any event, evidence of incremental value for PRPFM was lacking.

Preparation of PRPFM: "Eighteen milliliters of whole blood was drawn from patients by use of sterile technique, transferred to a specially designed tube for centrifugation in a Drucker 755VES general-purpose centrifuge,

and spun for 6 minutes at 1100 RPM. During centrifugation, the heavier red and white blood cellular components moved to the bottom of the tube while the lighter platelets remained at the top in the plasma. A polyester separator gel in the tube sealed the red blood cells and the white blood cells to prevent contamination with the platelets. After processing, 4-4.5 cm3 of leukocyte-poor PRP was transferred to 2 separate tubes containing trace amounts of calcium chloride to replace the calcium that was bound by the citrate and was spun for an additional 15 minutes at 1450 RPM. This second, faster spin using the same centrifuge caused the fibrinogen in the plasma to form a 2-cm3 solid PRPFM in disk-like form. The PRPFM was then removed and fashioned on the back table to fit the size and shape of the tear.


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Is there such a thing as injection arthropathy?

We often see patients whose physicians have tried to delay the need for arthroplasty through the use of injections (steroids, PRP, hylaluronic acid) The safety and efficacy of these injections is unclear (see this link, this link, this link, this link, this link, and this link). Laboratory investigations, such as Lidocaine Potentiates the Chondrotoxicity of Methylprednisolone (see this link), may be of relevance.
Not infrequently we'll see patients in whom the first or second injection helped, but from #3 on, there was no appreciable benefit. Occasionally we see shoulders that have had multiple injections and changes in the shoulder radiographs that are not typical of osteoarthritis. This is not intended to imply a cause/effect relationship.

Here's a recent example.

A very active young man sustained a hard fall on his shoulder. He received a series of intra articular injections as he documented for us here:

His current shoulder radiographs are shown here:

While this use of injections is common practice, we were struck by the cystic changes in the bone on both sides of the joint - changes that are not typical of post-traumatic arthritis in our experience. It is surely not possible to know if there was an association between these changes and the injections.

For comparison, the x-rays below show the more typical appearance of osteoarthritis.

Here are some quotes from the American Academy of Orthopaedic Surgeons 2013 guidelines (see this link) regarding the use of injections for arthritis of the knee:

Procedural Treatments: Recommendations 8-11
RECOMMENDATION 8
We are unable to recommend for or against the use of intraarticular (IA) corticosteroids for patients with symptomatic osteoarthritis of the knee.
Strength of Recommendation: Inconclusive
Description: Evidence from a single low quality study or conflicting findings that do not allow a recommendation for or against the intervention. An Inconclusive recommendation means that there is a lack of compelling evidence that has resulted in an unclear balance between benefits and potential harm.
Implications: Practitioners should feel little constraint in following a recommendation labeled as Inconclusive, exercise clinical judgment, and be alert for emerging evidence that clarifies or helps to determine the balance between benefits and potential harm. Patient preference should have a substantial influencing role.

RECOMMENDATION 9
We cannot recommend using hyaluronic acid for patients with symptomatic osteoarthritis of the knee.
Strength of Recommendation: Strong
Description: Evidence is based on two or more “High” strength studies with consistent findings for recommending for or against the intervention. A Strong recommendation means that the quality of the supportingevidenceishigh. Aharmsanalysisonthisrecommendationwasnotperformed.
Implications: Practitioners should follow a Strong recommendation unless a clear and compelling rationale for an alternative approach is present.

RECOMMENDATION 10
We are unable to recommend for or against growth factor injections and/or platelet rich plasma for patients with symptomatic osteoarthritis of the knee.
Strength of Recommendation: Inconclusive
Description: Evidence from a single low quality study or conflicting findings that do not allow a recommendation for or against the intervention. An Inconclusive recommendation means that there is a lack of compelling evidence that has resulted in an unclear balance between benefits and potential harm.
Implications: Practitioners should feel little constraint in following a recommendation labeled as Inconclusive, exercise clinical judgment, and be alert for emerging evidence that clarifies or helps to determine the balance between benefits and potential harm. Patient preference should have a substantial influencing role. 

Here is an interesting recent post about platelet rich plasma (see this link).

The bottom line is that we do not know (1) how injections affect the natural history of shoulder arthritis or (2) what regimen of injections is likely to maximize safety and efficacy.

The patients we most commonly see in our office have advanced arthritis with virtually complete loss of the cartilage over the glenoid and humeral head. In such cases it seems unlikely that injections will change the subsequent course of the disease.

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Rotator cuff repair, can the healing be enhanced?

Re-establishing the complex anatomy of the tendon attachment to bone is a major challenge in orthopedics. 

The authors of Augmentation of Tendon-to-Bone Healing review some of the methods currently under investigation for increasing the quality of this complex healing challenge.

They looked at a number of different approaches. These are listed below along with their conclusions.

Osteoinductive Growth Factors
Transforming growth factor, bone morphogenetic protein, fibroblast growth factor, and granulocyte colony-stimulating factor have shown some positive effects on the repair and healing of tendon and bone tissues in animal model studies.

Platelet-Rich Plasma
Although basic-science studies suggest positive effects on tendon-to-bone healing, clinical evidence from controlled human trials involving rotator cuff tendons does not show any superiority of platelet rich plasma augmented repairs over conventional methods.

Gene Therapy
Viral or nonviral vehicles can be used genetically modify cells to express growth factor at the tendon-bone insertion site. Before gene transfer can be tried as a therapeutic method to improve tendon-to-bone healing in humans, questions regarding safety and regulatory issues need to be answered.

Enveloping The Grafts With Periosteum
While enveloping the grafts with periosteum appears to be a promising approach, clinical evidence supporting its use in humans to augment tendon-to-bone healing is lacking.

Osteoconductive Materials
Calcium or magnesium-based osteoconductive materials are readily available and relatively inexpensive compared with other biological treatment modalities. Further research is required to prove them as biocompatible and effective treatment alternatives to reconstruct the tendon-to-bone interface in humans.

Cell-Based Therapies
The knowledge about the conditions that are required to choose a certain type of stem cell, optimum cell amount, and delivery vehicles, is limited. Serious concerns exist regarding their potential for differentiation into undesirable lineages, which could result in tumor-like growth.

Biodegradable Scaffolds And Biomimetic Patches
Biocompatible and biodegradable scaffolds with porous ultrastructure permit invasion and easy attachment of cells, while creating an environment suitable for cell proliferation and differentiation as demonstrated in models. The success of these approaches will require a thorough understanding of the structure-function relationship at the native insertion site, as well as the elucidation of the mechanisms governing interface regeneration.

Low-Intensity Pulsed Ultrasound
Low-intensity pulsed ultrasound may promote osteoblast and fibroblast proliferation, which may contributes to improved collagen formation and bone remodeling.

Extracorporeal Shockwave Treatment
Extracorporeal shockwave treatment can affect bone by exertion of direct pressure or by causing cavitation. These factors may create an environment with a better blood supply and increased bone and collagen formation, which may create a stronger tendon-to-bone interface.

Effects Of Various Loading Methods And Immobilization On Interface Healing
On the basis of animal models, neither strict immobilization nor immediate initiation of rehabilitation and loading appear to be beneficial after surgical repair, but rather a balance between the modalities is needed to optimize the healing enthesis and obtain a stronger interface.

Coated Sutures And Interference Screws
As with other growth factor delivery vehicles, challenges remain, including timing, dosages, degree of elution, sustainability of the release, effects of coating on fixative materials, and safety.

Delayed Interface Healing
Research is attempting to identify molecules and/or conditions that may delay the healing of the tendon-bone interface. Evidence from animal model studies has also shown that conditions that negatively impact bone formation and fracture-healing, such as uncontrolled diabetes mellitus, nicotine, and nonsteroidal anti-inflammatory drugs, also negatively affect tendon-to-bone healing.

Conclusion:

Knowledge about the complexity of tendon-to-bone healing is still limited and mainly based on animal studies. Rigorous clinical trials must be conducted to determine the value - benefit/(cost+risk) - of these approaches.

As we've pointed out in prior posts, atraumatic failure of the rotator cuff insertion is a degenerative process. Even if we could artificially manipulate the environment at the site of surgical reattachment, we not be able to "un-degenerate" the tendon or to prevent repeat failure after surgery.

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Not much support for the use of biologics in rotator cuff repair.

Application of biologics in the treatment of the rotator cuff, meniscus, cartilage, and osteoarthritis.

Abstract: "Advances in our knowledge of cell signaling and biology have led to the development of products that may guide the healing/regenerative process. Therapies are emerging that involve growth factors, blood-derived products, marrow-derived products, and stem cells. Animal studies suggest that genetic modification of stem cells will be necessary; studies of cartilage and meniscus regeneration indicate that immature cells are effective and that scaffolds are not always necessary. Current preclinical animal and clinical human data and regulatory requirements are important to understand in light of public interest in these products."

With respect to rotator cuff repair, however, the authors conclude that 'synthesis of all the studies illustrates that there is no clear advantage to using PRP (platelet rich plasma) as a surgical adjunct to rotator cuff repair'. A similar statement was made about mesenchymal stem cells.

Comment: While there is no question that platelets, growth factors and stem cells are part of the body's response to injury and healing process, there are many complexities in trying to improve on nature's finely tuned healing response.

As pointed out the Rotator Cuff Tear Book, we consider rotator cuff repair when tendon of good quality can be brought to bone of good quality without undue tension on the repair. We then intentionally create a injury to the bone in the form of trough into which the tendon is secured. By creating this trough, we cause local bleeding and start the response to injury with the natural influx of platelets, growth factors, and stem cells.

More details on cuff repair technique are shown here.

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Platelet-Rich Plasma (PRP): failure to make a difference

Platelet-Rich Plasma Injections in the Treatment of Chronic Rotator Cuff Tendinopathy A Randomized Controlled Trial With 1-Year Follow-up

There is a lot of interest in platelet-rich plasma (PRP) as a treatment of rotator cuff tear pathologies.

Even our own Academy states "Treatment with platelet-rich plasma holds great promise. Currently, however, the research studies to back up the claims in the media are lacking. Although PRP does appear to be effective in the treatment of chronic tendon injuries about the elbow, the medical community needs more scientific evidence before it can determine whether PRP therapy is truly effective in other conditions.   Even though the success of PRP therapy is still questionable,...."

These authors conducted a Level 1 randomized controlled trial of 40 patients, 18 to 70 years of age, with (1) a history of shoulder pain for >3 months during overhead-throwing activities, (2) MRI findings of RCT or partial tendon ruptures, and (3) a minimum 50% reduction in shoulder pain with subacromial injections of an anesthetic. Patients were randomized into a PRP group (n = 20) or placebo group (n = 20). Patients received an ultrasound-guided injection into the subacromial space that contained either 5 mL of PRP prepared from autologous venous blood or 5 mL of saline solution. All patients underwent a 6-week standard exercise program. 

While both the treatment and control groups showed significant improvements compared with baseline at all time points, comparison of the patients revealed no significant difference between the treatment and control groups in WORC, SPADI, and VAS scores at 1-year follow-up. The authors concluded that at 1-year follow-up, a PRP injection was found to be no more effective in improving quality of life, pain, disability, and shoulder range of motion than placebo in patients with chronic RCT who were treated with an exercise program.

Comment: the key finding here is that the placebo group improved as much as the PRP group, so claims that 'the patient got better after PRP, does not prove that PRP was effective.

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