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Technologies to Augment

Rotator Cuff Repair


Anand M. Murthi, MD*, Manesha Lankachandra, MD

KEYWORDS
 Rotator cuff repair  Platelet-rich plasma  Allograft scaffold  Synthetic scaffold  Stem cells

KEY POINTS
 The consensus of the current literature seems to be that platelet-rich plasma (PRP) may provide
some clinical benefit in rotator cuff repair, but there remains high variability among different
PRP products and preparations.
 Like PRP, the efficacy of the bone marrow aspirate concentration preparation depends on the
expression of various cytokines and signaling molecules and the product used.
 Various scaffolds and grafts, both biological and synthetic, are available to provide structural
support for the repair. Their effects and results vary depending on graft type.

Retear rates after rotator cuff repair vary widely, After physical reattachment of rotator cuff
depending on the tear type and size as well as tendons to their insertion sites, the cells and bio-
patient factors, such as age and health comor- logical factors involved in healing the repaired
bidities. Earlier research has shown that pain re- bone to tendon interface derive from surround-
lief and satisfaction can reliably be achieved ing connective tissues.
despite tendon healing.1–3 A 2014 meta- PRP is an autologous blood product with
analysis of level I and II data showed some signif- platelet concentrations greater than the baseline
icant difference in some outcome measures, but values.7 It is created through plasmapheresis
these differences did not reach clinical impor- whereby platelets and plasma are separated
tance. Importantly, the influence of age and from white blood cells (WBCs) and red blood
occupation were not evaluated, and most of cells. Commercial preparation methods vary,
the studied tears were small. Patients with intact with varying amounts of platelets and WBCs in
repairs were also found to have greater strength the final product. Moreover, most users do not
than those with retears.4 The goal of surgical ro- perform cell counts on the whole blood or PRP
tator cuff repair remains a tension-free repair products to evaluate these differences clinically.
that can withstand the functional demands of pa- The optimal ratio of PRP products has not
tients during the postoperative healing and been established, but a recent basic science
rehabilitative phase. Tendon to bone healing is study does suggest that leukocyte-poor PRP
notoriously fickle, and the fibrous scar tissue promotes more normal collagen matrix synthesis
that creates this repair lacks the mechanical and decreases more potentially harmful cyto-
strength and elasticity of native tendon.5,6 New kines and inflammatory markers than high-
technologies seek to improve tendon to bone leukocyte PRP preparations.8
healing with the addition of platelet-rich plasma In the perioperative setting, PRP is used to
(PRP), stem cells, and biological and synthetic stimulate healing at the tendon-bone interface.
grafts (Figs. 1 and 2). In a meta-analysis of 5 studies, Chahal and

The authors declare no potential conflict of interest related to this article.


Department of Orthopaedics, MedStar Union Memorial Hospital, 3333 North Calvert Street, Suite 400, Baltimore,
MD 21218, USA
* Corresponding author. Department of Orthopaedics, MedStar Union Memorial Hospital, 3333 North Calvert
Street, Suite 400, Baltimore, MD 21218.
E-mail address: amurthi14@hotmail.com

Orthop Clin N Am 50 (2019) 103–108


https://doi.org/10.1016/j.ocl.2018.08.005
0030-5898/19/ª 2018 Elsevier Inc. All rights reserved.
104 Murthi & Lankachandra

investigators to subgroup PRP and platelet-rich


fibrin; they found that although the use of PRP
resulted in improved healing rates and func-
tional outcomes, the use of platelet-rich fibrin
had no beneficial effect on tendon healing or
outcomes.
A 2012 study of 37 patients also evaluated the
effects of platelet-rich fibrin on repair integrity
following rotator cuff repairs at high risk of
failure (older patients, larger tears, and higher
Goutallier scores). Retear rates were higher in
the study group versus the control group. Func-
tional outcome scores were similar in the two
groups.12
The consensus of current literature seems to
be that PRP in rotator cuff repair does provide
some clinical benefit, improving healing rates in
tears of various sizes and with variable patient
factors. That this consensus has changed consid-
erably over the past decade shows the evolving
Fig. 1. A synthetic graft outside of the body, ready to nature of both PRP products and how they are
be passed into the subacromial space through a lateral being used by surgeons. There are still no clear
portal.
guideline regarding the characterization of PRP
products, both in clinical use and scientific
colleagues9 showed patient-reported outcomes reporting. That some PRP-related products
were no different between the two groups and (platelet-rich fibrin, for example) are clearly not
the risk of retear was not significantly changed. beneficial also underscores the heterogeneity
A larger meta-analysis of 11 studies also similarly of PRP preparations and the difficulty in making
showed no difference in retear rates and patient generalizations regarding the use of PRP in rota-
outcomes in patients treated with PRP and con- tor cuff repair.
trols.10 There was, however, a statistically signif- Similar to PRP, the use of stem cell prepara-
icant reduction in retear rates with larger tears tions at the bone-tendon repair interface also
(greater than 3 cm) that were treated with seeks to create a favorable milieu of chemical
double-row repair and PRP. A 2018 meta- signaling. Snyder and Burns’13 crimson duvet is
analysis of PRP and platelet-rich fibrin by Hurley a well-known technique to create a collection
and colleagues11 showed that the use of PRP of stem cells and cytokines at the repair site, us-
improved tendon healing rates in tears of all ing similar principles as microfracture. Basic sci-
sizes. The increase in the number of studies ence research in a rat model showed increased
available for review regarding the use of PRP mesenchymal stem cells in the drilling group
products over recent years allowed the versus the control group, and the ultimate force

Fig. 2. (A) The same graft now placed against the bursal side of the rotator cuff repair. (B) It is tied down against
the tendon bone interface.
Technologies to Augment Rotator Cuff Repair 105

to failure was significantly higher in the drilling


group at 4 and 8 weeks.14 A similar study in rab-
bits also showed increased force to failure at 8
and 16 weeks, and histologic analysis showed
thicker collagen bundles and more fibrocartilage
in the microfracture group.15
In humans studies, clinical outcomes have
been similar in patients undergoing microfrac-
ture or other marrow-stimulating tech-
niques.16–18 Milano and colleagues17 reported
on 80 patients, 40 who were randomized to
receive microfracture with rotator cuff repair
and 40 patients who underwent cuff repair
alone. At a mean follow-up of roughly 2 years,
Constant scores were similar in the two groups.
There was no difference in healing rates be-
tween the two groups, though subgroup analysis
did show better healing rates for large tears in
the microfracture group. Taniguchi and col-
leagues18 also showed improved repair integrity
in large and massive cuff tears using bone
marrow stimulation, despite similar results be-
tween groups in small and medium tears.
Mesenchymal stem cells from bone marrow
can also be collected and concentrated from Fig. 4. Bone marrow aspirate harvest from the greater
bone marrow and injected back at the site of tuberosity. A Jamshidi needle is used through a lateral
repair (Fig. 3). Like PRP, there are multiple sys- portal; no other incisions are necessary.
tems from multiple companies. Like PRP, the ef-
ficacy of the bone marrow aspirate concentration
preparation depends on the expression of stem cells in the setting of chronic rotator cuff
various cytokines and signaling molecules. tear.
The site of harvest of these bone marrow cells Although mesenchymal stem cells from bone
also varies. Bone marrow aspirate is commonly marrow concentrate can differentiate into
harvested from the greater tuberosity (Fig. 4), tendon cells, the clinical significance of this
which minimizes donor site morbidity and in- finding in rotator cuff surgery is unclear. Animal
creases surgical time. However, Hernigou and studies have shown that the bone marrow–
colleagues19 showed that bone marrow aspirate derived cells were active at the site of repair,
from this site might have fewer mesenchymal but results regarding improvement in the me-
chanical strength of the repair are mixed.20–22
In humans, 2 recent studies show decreased
retear rates in both primary and revision settings
using bone marrow aspirate.19,23
In addition to maximizing the biological com-
ponents of the repair, various scaffold and
grafts, both biological and synthetic, are avail-
able to provide structural support for the repair.
This support becomes especially important
when patient factors result in poor-quality tissue
at the site of repair. Neviaser and colleagues24
initially described the use of graft material in ro-
tator cuff repair in the 1970s to bridge in irrepa-
rable repair. This idea has recently been taken
further with the idea of superior capsular recon-
struction; but graft material is more commonly
used to reinforce a repair with poor quality tis-
Fig. 3. Bone marrow aspirate concentrate injected sue, rather than to bridge a gap between tendon
into and around the synthetic graft and repair. and bone. The use of grafts as scaffolds can
106 Murthi & Lankachandra

generally be split into products that use biolog- augmented with a polyhydroxyalkanoate mesh.
ical material, usually human or animal extracel- There was no difference in gap formation after
lular matrix, and those that use synthetic cyclic loading.
materials. Human studies show generally favorable out-
In vitro research has shown that the structural comes with the use of biological grafts. In one of
makeup and mechanical properties of both bio- the few randomized controlled trials, Barber and
logical and synthetic grafts is relatively dissimilar colleagues30 showed American Shoulder and
from native rotator cuff tendon. Smith and col- Elbow Surgeons (ASES) and Constant scores
leagues25 evaluated 7 scaffolds, comparing their were improved and cuff integrity was better
mechanical properties with a cadaver supraspi- maintained in patients who underwent repair
natus tendon. Synthetic grafts fared better in plus augmentation with dermal allograft of their
load to failure tests when compared with biolog- large (2 tendons) rotator cuff tears versus those
ical grafts, but neither matched native supraspi- who underwent repair alone. Intact repairs
natus tendon. The investigators suggested that were found in 85% of the augmentation group
one reason for this dissimilarity may lie in the versus 40% of the control group at a mean of
origin of these grafts for uses outside of the 14 months postoperatively. The investigators
shoulder, and further research into grafts also note that operative time was generally
designed to mimic the rotator cuff tendons increased by 30 to 60 minutes in the augmenta-
may hold promise. tion group.
Histologic studies show evidence of increased Other retrospective studies using biological
cell adhesion and proliferation, depending on grafts for bridging augmentation, especially in
the graft type.26 Arnoczky and colleagues27 the setting of massive rotator cuff tears, also
recently performed a retrospective study of 7 show good results. In a study of 45 patients
patients who underwent rotator cuff procedures with massive rotator cuff tears treated arthro-
with a bovine collagen graft and then underwent scopically with a regenerative tissue matrix allo-
a repeat surgery with biopsy. At 5 weeks, bi- graft augmentation using a bridging construct,
opsies showed host fibroblasts within the Wong and colleagues31 show improved Univer-
collagen implant. At 8 weeks, there was further sity of California, Los Angeles and ASES scores
host incorporation within the implant with linear as well as improved functionality at 2 years post-
organization of the host collagen fibers. At operatively. The average postoperative ASES
3 months, biopsies showed further host incorpo- score in this group was 84.1, and it is important
ration of the implant as well as implant degrada- to note that the technique used in this report
tion. At 6 months, the remnants of the implant involved bridging deficient rotator cuff tendons
were gone and the tissue samples had the orga- rather than augmenting tendon to bone repair.
nized appearance of tendon, densely organized In a study of 24 patients with massive rotator
with parallel bundles of collagen fibers. In this cuff tears treated using a mini open technique
study, at no point was there inflammatory or with regenerative tissue matrix allograft, Gupta
foreign body reaction within the sampled tissue. and colleagues32 showed improved the Short
The is a paucity of human studies on host Form 12 (SF-12) and ASES scores at 3 years post-
response to synthetic scaffolds, but a canine operatively. The mean ASES scores improved
study showed improved biomechanical function from 66.6 to 88.7, and the mean SF-12 scores
at 12 weeks. In this study, 8 dogs underwent improved from 48.4 to 56.8. Neither of these re-
bilateral shoulder surgery, with one side ports had control groups, and it is important to
repaired and the other repaired and augmented note that the surgical technique used involved
with a polymer scaffold. At time zero, repair with bridging a bone to tendon gap versus purely
augmentation increased load to failure; at an augmentation of a tenuous repair.
12 weeks, there was less tendon retraction and In a revision setting, Petri and colleagues33
greater cross-sectional area. Histologic samples showed significant improvement in the func-
at 12 weeks also showed fibrous tissue ingrowth tional portion of the ASES after open, revision,
with an overall compatible host response.28 A biological patch augmentation. Patient satisfac-
similar study in rats using a polycarbonate poly- tion in this series was also high, with no patients
urethane patch showed no inflammatory requiring further surgery. In a larger review of 24
response at 6 weeks as well as significant host patients undergoing revision open rotator cuff
tissue ingrowth.29 Regarding the initial repair repair with dermal allograft augmentation,
strength using a synthetic scaffold, a small 10 patients had MRI evidence of a retear
cadaver study showed the ultimate load to fail- at 50 months.34 Based on ASES and simple
ure was improved by 25% for rotator cuff repairs assessment numeric evaluation (SANE) scores,
Technologies to Augment Rotator Cuff Repair 107

excellent results were achieved in 24% of pa- 7. Hsu WK, Mishra A, Rodeo SR, et al. Platelet-rich
tients, good in 13%, fair in 21%, and poor in plasma in orthopaedic applications: evidence-
42%. Interestingly, this study compared these based recommendations for treatment. J Am
outcomes with historical control of revision sur- Acad Orthop Surg 2013;21:739–48.
gery without augmentation and found no signif- 8. Cross JA, Cole BJ, Spatny KP, et al. Leukocyte-
icant improvements. reduced platelet-rich plasma normalizes matrix
For synthetic scaffolds, one of the only studies metabolism in torn human rotator cuff tendons.
with a control group compared open rotator cuff Am J Sports Med 2015;43:2898–906.
repair, repair with a collagen scaffold, and repair 9. Chahal J, Van Thiel GS, Mall N, et al. The role of
with a synthetic scaffold. The polypropylene platelet-rich plasma in arthroscopic rotator cuff
patch augmentation of rotator cuff repair repair: a systematic review with quantitative synthe-
demonstrated significant improvement in the sis. Arthroscopy 2012;28:1718–27.
36-month outcome in terms of function, 10. Warth RJ, Dornan GJ, James EW, et al. Clinical and
strength, and retear rate.35 Other case series structural outcomes after arthroscopic repair of full-
as well have shown decreased pain, increased thickness rotator cuff tears with and without
range of motion, and improvement in patient- platelet-rich product supplementation: a meta-
reported outcomes.36–38 Even in revision set- analysis and meta-regression. Arthroscopy 2015;
tings, case series have shown good results with 31:306–20.
synthetic grafts. Although retear rates in this 11. Hurley ET, Lim FD, Moran CJ, et al. The efficacy of
population remain high, shoulder outcome platelet-rich plasma and platelet-rich fibrin in
scores significantly improved.39 arthroscopic rotator cuff repair: a meta-analysis of
Recent technology may allow improved heal- randomized controlled trials. Am J Sports Med
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ologics and grafting can allow surgeons to platelet-rich fibrin matrix on repair integrity of at-
choose the appropriate augmentation tech- risk rotator cuff tears. Am J Sports Med 2012;40:
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rotator cuff repair patients. Many of these newer 13. Snyder S, Burns J. Rotator cuff healing and the
technologies still need to be studied in a pro- bone marrow “crimson duvet.” From clinical obser-
spective fashion to allow for a thorough under- vations to science. Tech Shoulder Elbow Surg 2009;
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while factoring in the potential for added cost 14. Kida Y, Morihara T, Matsuda K, et al. Bone marrow-
and risks. derived cells from the footprint infiltrate into the
repaired rotator cuff. J Shoulder Elbow Surg 2013;
22:197–205.
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