13 Rotator Cuff Healing and The Bone Marrow Crimson Duvet From Clinical Observations To Science 1171446194
13 Rotator Cuff Healing and The Bone Marrow Crimson Duvet From Clinical Observations To Science 1171446194
13 Rotator Cuff Healing and The Bone Marrow Crimson Duvet From Clinical Observations To Science 1171446194
130 | www.shoulderelbowsurgery.com Techniques in Shoulder & Elbow Surgery Volume 10, Number 4, December 2009
Techniques in Shoulder & Elbow Surgery Volume 10, Number 4, December 2009 Rotator Cuff Healing and the ‘‘Crimson Duvet’’
FIGURE 1. This patient had his rotator cuff repaired on November 28, 2002 using 2 triple-loaded suture anchors on the tuberosity
adjacent to the medial border of the footprint. The magnetic resonance imaging (MRI) at 4 and 6 weeks postoperation showed the
tuberosity was devoid of tissue. At 6 weeks and there after the footprint of the cuff attachment was reestablished and continues to
mature until the final MRI at 2 years postoperation.
Clinical Impressions Leading to Understanding Second Look at Cases With Early, Mid,
the Function of Bone Marrow Clot and and Late Visual Evaluation
the Crimson Duvet There were also several observations made during the
‘‘second look’’ arthroscopic evaluations. On one occasion, a
Sequential Magnetic Resonance Imaging
patient had a suspected infection at 2 weeks postoperatively
The development and maturation of the Crimson duvet and was taken to surgery for an arthroscopic evaluation and
was first appreciated by observing the sequential magnetic lavage and debridement. The evaluation documented that the
resonance imaging (MRI) scans performed every few weeks earlier bare tuberosity was covered with a rich vascular blanket
postoperatively to determine the course of healing. The patient covering and nearly obscuring the cuff edge and suture line
was a 53-year-old radiologist with a 2.5 cm rotator cuff tear (Fig. 2).
repaired with 2 triple-loaded suture anchors. He volunteered A second case example was that a 52-year-old female
to have sequential MRI scans postoperatively to follow who was involved in a motor vehicle accident 4 weeks
cuff healing. His preoperative scan documented a large full- postoperatively and in a 2-anchor rotator cuff repair. She had
thickness tear including the supra and infraspinatus attach- bleeding in her bursa and the MRI suggested that she had torn
ments with minimal retraction (Fig. 1). At surgery, the part of her cuff repair but the adjacent area was healing well
tuberosity was debrided and small bone marrow vents were (Fig. 3). Her redo cuff repair at 8 weeks documented that the
created. The cuff edge was attached just lateral to the cartilage entire tuberosity was covered with a healthy looking tissue
using 2 triple-loaded suture anchors and simple sutures. The (Fig. 4). When it was debrided, the previously placed bone
first postoperative scan was performed at 4 weeks. The cuff marrow vents had robust cores of fibrovascular tissue
edge appeared well fixed to the edge of the cartilage and there connected to the overlying Crimson duvet (Fig. 5).
was a moderate bursal effusion but there was not soft tissue
over the tuberosity. At 6 weeks, the effusion was resolving but
the tuberosity was still bare. At 8 weeks a soft tissue signal Opportunistic Biopsies of Tissue on Tuberosity
(footprint) was evident covering the entire tuberosity. In the Finally, there were 2 opportunities for a biopsy of the
ensuing months the new ‘‘footprint’’ became increasingly more healing Crimson duvet. The first was a 40-year-old male who
dense and by 3 months had the MRI appearance of a relatively had a ‘‘seroma’’ at 5 weeks postoperation. The MRI was
normal rotator cuff attachment. A scan performed 2 years worrisome but the arthroscopic evaluation and cultures ruled
postoperatively revealed that the cuff attachment was robust out infection. Biopsies were taken from the soft tissue covering
and sound. the tuberosity area that had been prepared earlier with abrasion
Since this interesting sequence, we have had occasion to and bone marrow vents. The micropathology showed a rich
evaluate several hundred postoperative MRI scans and have fibrin matrix infiltrated with healthy fibroblasts and lympho-
noted that by and large the footprint area of the rotator cuff has cytes and an abundant array of vascular elements. There were
been completely restored when we have debrided the no inflammatory cells present (Fig. 6).
remaining torn cuff, abraded the bone, and created bone The second case was a 46-year-old male who had a rotator
marrow vents facilitating the formation of the Crimson duvet. cuff repair but partially re-tore the tendon 3 months later
FIGURE 3. This patient had an motor vehicle accident at 4 FIGURE 5. After debridement of the ‘‘Crimson duvet’’ lateral to
weeks postoperation and re-tore her rotator cuff repair. The the anterior anchor the previously placed ‘‘bone marrow vents’’
magnetic resonance imaging at 8 weeks shows the injured area could be seen filled with a rich fibrovascular core of tissue. The
lateral to the anterior anchor and another portion of the cuff that area of the tuberosity that had been abraided but without
remained intact adjacent to the posterior anchor. ‘‘Vents’’ did not have significant soft tissue attached.
FIGURE 6. A biopsy of the ‘‘Crimson duvet’’ from the tuberosity lateral to the anchors at 5 weeks postoperation shows a healthy fibrous
clot with a plethora of blood vessels, fibroblast and lymphocytes.
pump is turned off, bone marrow will flow from the vents many such ‘‘signaling molecules’’ within a fracture clot, the
and form the Crimson duvet covering the rotator cuff majority of which are still poorly understood. As the signals are
(Figs. 11, 12). sent, inflammatory cells arrive and secrete vital cytokines such as
interleukins 1 and 6, factors that also support tissue neoangio-
genesis. In true fracture settings, this system will continue,
DISCUSSION creating and remodeling bone back to bone. In the damaged local
Study of the basic principles of bone fracture healing has environment of a rotator cuff tear, this regenerative process of
revealed the importance of the callus/clot to the local healing cell signaling, proliferation, differentiation, and vascularization is
response. A fracture disrupts blood vessels within and around also crucial when bone-to-tendon healing is to be achieved.
the bone, setting off a series of events that progress over
several stages from hematoma to mature remodeled bone
tissue. Similarly, creation of a Crimson duvet in the shoulder Microfracture and Formation of ‘‘Super Clot’’
accesses this same healing process and directs it to the for Cartilage Regeneration
damaged rotator cuff tissue. According to Steadman et al,6 full-thickness articular
In rotator cuff repair, when the small bone vents cartilage defects rarely heal spontaneously and most chondral
‘‘fracture’’ the greater tuberosity, the first response is the defects most often eventually cause degenerative changes.
creation of a marrow-generated hematoma. As vessels within Other than joint replacement, techniques to treat full-thickness
the bone bleed, marrow cells also egress, and a clot forms chondral defects include drilling abrasion, autografts, allo-
adjacent to the rotator cuff-bone interface. This hematoma grafts, and cell transplantation. Dr Richard Steadman devel-
creation is the first of several discrete stages of bony healing.5 oped the technique for microfracture to enhance chondral
Fracture clots with degranulating platelets are the source of the resurfacing by providing a suitable environment for new tissue
signaling molecules such as transforming growth factor-b and formation and taking advantage of the body’s own healing
platelet-derived growth factor, which not only regulate the potential. Variable angle, sharp-tip metal awls are used to
proliferation of cells but also regulate the differentiation of make multiple perforations into the subchondral bone plate.
committed MSCs into more mature functional cells suited to
their environment, that is, fibroblasts. In fact, these are just 2 of
FIGURE 10. To create a ‘‘Crimson duvet’’ multiple perforations FIGURE 12. When the fluid pressure is lowered at the conclusion
are placed through the cortical bone of the tuberosity into the of the case the bone marrow flows out of the bone marrow vents
bone marrow space. to form the ‘‘Crimson duvet.’’
remains only 1 piece of the puzzle as bridging fibrocartilage is increased stiffness of the musculotendinous unit. Tension
unlikely to form if degenerative tendon is compressed against measurements for 1 and 2 cm excursion were taken at the time
sclerotic tuberosity. Uhthoff proposes maximizing healing of initial tendon release and compared with the measurement
potential by preserving bursal tissue and releasing bone taken 40 weeks later at the time repair was performed. The
marrow stem cells from tuberosity.15 In the bursa, vascular tension increased over 7-fold for 1 cm excursion. After 40
invasion and fibroblast proliferation appear to aid healing as weeks, the musculotendinous unit was so stiff that it could no
seen in the histologic analysis of a rabbit model and human longer be mobilized at 2 cm.
specimens.3,4,16 Similar analysis proves that exposure of Human in vivo data also show the significant difference in
subcortical bone allows an influx of fibroblasts and vessels tension in medially based single row versus double row repair
leading to a fibrocartilaginous bridge to the tendon stump. In constructs.23 A tensiometer was used to measure the tension of
addition to exposed cancellous bone, venting the bone marrow the cuff musculotendinous unit when the edge was reduced
would allow an influx of stem cells to magnify the vascular to the articular margin and the lateral footprint of greater
and fibrocartilage response. Timing to fixation may also play tuberosity. The average force required to bring the edge of a
a role as the work by Matsumoto, Zumstein, Gladstone and small tear (<20 mm) to the margin was 1.25 N compared with
Gerber illustrates that muscle atrophy is not reversed after 9.08 N for lateral tuberosity. Tears that retracted >20 mm
fixation and often progresses.17–20 In essence, a timely, required 3 N to the margin and 13.75 N to the lateral tuberosity.
biomechanically sound repair of the rotator cuff that exploits The amount of retraction of the tendon in combination with the
the biologic benefits of the subcortical bone, that is, bone inelasticity of a chronic tear can lead to excessively high-
marrow stem cells, should lead to improved healing and a tension repairs, which may be a setup for nonhealing. A lower-
superior clinical result according to Uhthoff’s study. tension medially based repair construct in combination with
the released MSCs and growth factors in the Crimson duvet
Histology of Cuff Tendon Repair may give the tendon the most optimal environment in which
Christian Gerber21 was the first to evaluate the histology to heal.
of the rotator cuff tendon repair by establishing the first animal
model for cuff repair research, the Alpine sheep. The Bone Marrow Cell Concentrations
infraspinatus tendon of this sheep is similar to the human in the Humeral Greater Tuberosity
supraspinatus. As he was developing the model for new suture Bradley et al24 studied the composition of bone marrow
constructs for repair, he studied the histology of sheep aspirate (BMA) from the proximal humerus to determine the
infraspinatus tendon repair to bone. Like Uhthoff’s study in composition and feasibility as a handy source for the harvest of
rabbits, Gerber also found the tendon stump to initially have MSCs to aid rotator cuff healing. They noted that earlier work
decreased vascularity and reduced numbers of fibrocytes, has been limited to characterization of cellular components in
although this began to improve after 2 weeks. By 6 weeks, BMA from the iliac crest and vertebral body.25–27 An earlier
fibroblasts and vessels were present in large numbers. In fact, clinical study used MRI to identify hematopoietic marrow in
at the tendon-bone junction, vessels extend from the bone the humerus of 99% of patients aged 13 to 83 years old, but the
marrow into the scar tissue, indicating healing from the cellular make-up or the amount of stem cells in humeral bone
tuberosity. By 6 months, the granulation tissue developed into marrow was not evaluated.28 Bradley et al postulated that if the
tissue with parallel-oriented collagen fibers, whereas osteo- humerus provides a source of stem cells to aid in tissue repair,
blasts formed a new bone mass embedding the fibers, with a then obtaining BMA during shoulder arthroscopy would
layer of dense fibrocartilage covering it, as it does in the become a relatively simple and convenient procedure to aid
normal tendon-bone interface. the repair process.
Their study included 12 male and female patients aged 21
Tuberosity and Rotator Cuff Blood Flow to 75 years undergoing rotator cuff repair or shoulder
In a clinical study conducted at the Hospital for Special instability repair. Approximately 10 mL of bone marrow was
Surgery, the investigators documented that the important blood aspirated into a syringe with 100 U/mL of heparin from the
supply for rotator cuff healing did originate from the greater humeral metaphysis of each patient through the greater
tuberosity bone and not from the cuff tendon. They evaluated tuberosity. The BMA was processed at UPMC Hillman Center.
13 patients each having undergone a single row arthroscopic The results of the aspirates were compared with investigations
rotator cuff repair. At 3 months postoperation, they quantified published earlier quantifying progenitor cells in BMA from the
in vivo vascularity of the rotator cuff and the surrounding area iliac crest.26,29,30 There were 518 ± 707 MSCs/mL, of humeral
using lipid microsphere-enhanced ultrasound evaluation. The BMA. These numbers are compared with Muschler’s publica-
conclusion of their study was that the rotator cuff is relatively tion26 in which he reported 301 colony-forming units /mL of
avascular after repair at 3 months, a robust vascular response iliac crest BMA. MSCs and colony-forming units are
occurs at the suture anchor site in the greater tuberosity, and essentially the same term according to Bradley. They conclude
that an intact repair may be necessary to foster angiogenesis at that a similar amount of connective tissue progenitor cells can
the repair site. The data suggest that the repaired rotator cuff be obtained from the humerus as the iliac crest. It is noted that
tendon is relatively avascular and that the blood supply to the the standard deviations of ESCs and MSCs are larger than the
tendon-bone interface comes from the tuberosity.22 values themselves. It is likely that there are differences in the
amount of progenitor cells found in each individual patient’s
Muscle Atrophy, Fat Infiltrate, and Cuff Tension bone marrow, especially because of age.26
Dr Christian Gerber20 has also used a sheep model to
evaluate the effect of chronic tear on the infraspinatus muscle Growth Factors Enhancement From Acromial
belly. Histologic analysis shows that as the muscle fibers Cancellous Bone
atrophy, fat and connective tissue then infiltrate the inter- The presence of high levels of growth factors following
fascicular and intrafascicular spaces left behind, leading to opening of the cancellous bone in the acromion was shown by
Randelli et al.31 Twenty-three patients were involved and fluid 6. Steadman JR, Rodkey WG, Rodrigo JJ. Microfracture: surgical
was collected from the subacromial space postoperation using technique and rehabilitation to treat chondral defects. Clin Orthop
a suction drain. This fluid was compared with a sample of Relat Res. 2001;391(suppl):S362--369.
peripheral venous blood taken at the same time. The samples 7. Knutsen G, Engebretsen L, Ludvigsen TC, et al. Autologous
were compared for concentrations of growth factors using chondrocyte implantation compared with microfracture in the
enzyme-linked immunosorbent assay. Platelet-derived growth knee: a randomized trial. J Bone Joint Surg Am. 2004;86:455--464.
factor-AB, fibroblast growth factor basic, and transforming 8. Steadman RJ, Rodkey WG, Singleton SB, et al. Microfracture
growth factor-b1 were all significantly higher in the sub- technique for full thickness chondral defects: technique and clinical
acromial fluid than in the blood. This suggests that opening the results. Oper Tech Orthop. 1997;7:300--305.
cancellous bone of the acromion as well as the tuberosity
9. Steadman RJ, Briggs KK, Rodrigo JJ, et al. Outcomes of microfracture
releases a significant quantity of growth factors into the
for traumatic chondral defects of the knee: average 11-year follow-up.
subacromial environment. It is expected that these growth Arthroscopy. 2003;19:477--484.
factors will potentiate the healing of the repaired rotator cuff.
10. Bae D, Yoon K, Song S. Cartilage healing after microfracture in
osteoarthritic knees. Arthroscopy. 2009;22:367--374.
11. Sano H, Uhtoff HK, Backman DS, et al. Structural disorders at the
CONCLUSIONS insertion of the supraspinatus tendon. J Bone Joint Surg Br. 1998;80:
The information presented in this paper is a compilation 720--725.
of observations, impressions, surgical case reviews, literature, 12. Sano H, Ishii H, Trudel G, et al. Histologic evidence of degeneration at
and scientific data gleaned by the authors over more than 20 the insertion of 3 rotator cuff tendons: a comparative study with human
years performing arthroscopic rotator cuff repairs. During this cadaveric shoulders. J Shoulder Elbow Surg. 1999;8:574--579.
time we have witnessed many new and creative concepts 13. Choi HR, Kondo S, Hirose K, et al. Expression and enzymatic activity
evolve that were designed to enhance and improve cuff of MMP-2 during healing process of the acute supraspinatus tendon
healing. Biologic repair of all living tissues consistently tear in rabbits. J Orthop Res. 2002;20:927--933.
requires 5 key elements: stabilization, inflammation, revascu-
14. Sano H, Ishii H, Yeadon A, et al. Degeneration at insertion weakens
larization, cellular repopulation, and remodeling. We must
tensile strength of the supraspinatus tendon: a comparative mechanical
understand and respect these principles. The unacceptable and histologic study of the bone-tendon complex. J Orthop Res.
numbers of failed repairs noted in the literature for both using 1997;15:719--726.
arthroscopic and open cuff techniques demands that we pursue
better methods that improve our patient’s outcomes. It is 15. Uhthoff HK, Traudel G, Himori K. Relevance of pathology and basic
research to the surgeon treating rotator cuff disease. J Orthop Sci.
evident that we need to study, understand, and learn to take
2003;8:449--456.
advantage of the body’s natural healing potential. All too
often, a new and often more expensive technology is touted to 16. Ishii H, Brunet JA, Welsh RP, et al. ‘‘Bursal reactions’’ in rotator cuff
be a revolution in surgical care only to be abandoned when it is tearing, the impingement syndrome and calcifying tendinitis.
shown to be little more than a different surgical exercise. The J Shoulder Elbow Surg. 1997;6:131--136.
simple and predictable concept of puncturing small holes or 17. Matsumoto F, Uhthoff HK, Trudel G, et al. Delayed tendon
bone marrow vents in the prepared tuberosity, fixing the cuff reattachment does not reverse atrophy and fat accumulation of the
securely with minimal tension, and facilitating the bone supraspinatus. J Orthop Res. 2002;20:357--363.
marrow to flow and cover the repaired cuff forming a healing 18. Zumstein MA, Jost B, Hempel J, et al. The clinical and structural long-
blanket or Crimson duvet seems to be the best current method term results of open repair of massive tears of the rotator cuff. J Bone
we know to achieve this goal. No doubt the future will include Joint Surg Am. 2008;90:2423--2431.
additional methods to enhance and support healing but until 19. Gladstone JN, Bishop JY, Lo IK, et al. Fatty infiltration and atrophy
they are proven and available we should do our best to provide of the rotator cuff do not improve after rotator cuff repair and
the best possible biologic environment for the cuff to heal and correlate with poor functional outcome. Am J Sports Med. 2007;35:
avoid unnecessary additional surgical trauma. 719--728.
20. Gerber C, Meyer DC, Schneeberger AG, et al. Effect of tendon release
and delayed repair on the structure of the muscles of the rotator cuff:
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