Beneficial Effects of Autologous Bone Marrow-Derived Mesenchymal Stem Cells in Naturally Occurring Tendinopathy
Publication Date
September 25, 2013
Journal
PLOS ONE
Authors
Roger Kenneth Whealands Smith, Natalie Jayne Werling, Stephanie Georgina Dakin, Rafiqul Alam, et al
Volume
8
Issue
9
Pages
e75697
DOI
https://dx.plos.org/10.1371/journal.pone.0075697
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0075697
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/24086616
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3783421
Europe PMC
http://europepmc.org/abstract/MED/24086616
Web of Science
000325218700110
Scopus
84884537375
Mendeley
http://www.mendeley.com/research/beneficial-effects-autologous-bone-marrowderived-mesenchymal-stem-cells-naturally-occurring-tendinop-5
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Mendeley | Further Information

{"title"=>"Beneficial Effects of Autologous Bone Marrow-Derived Mesenchymal Stem Cells in Naturally Occurring Tendinopathy", "type"=>"journal", "authors"=>[{"first_name"=>"Roger Kenneth Whealands", "last_name"=>"Smith", "scopus_author_id"=>"7410288089"}, {"first_name"=>"Natalie Jayne", "last_name"=>"Werling", "scopus_author_id"=>"55895186000"}, {"first_name"=>"Stephanie Georgina", "last_name"=>"Dakin", "scopus_author_id"=>"14017759600"}, {"first_name"=>"Rafiqul", "last_name"=>"Alam", "scopus_author_id"=>"55863200000"}, {"first_name"=>"Allen E.", "last_name"=>"Goodship", "scopus_author_id"=>"7006369437"}, {"first_name"=>"Jayesh", "last_name"=>"Dudhia", "scopus_author_id"=>"7003495983"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84884537375", "doi"=>"10.1371/journal.pone.0075697", "pui"=>"369882992", "issn"=>"19326203", "pmid"=>"24086616", "scopus"=>"2-s2.0-84884537375"}, "id"=>"6549a5d4-c3f3-3862-9b7c-1c54e2463076", "abstract"=>"Tendon injuries are a common age-related degenerative condition where current treatment strategies fail to restore functionality and normal quality of life. This disease also occurs naturally in horses, with many similarities to human tendinopathy making it an ideal large animal model for human disease. Regenerative approaches are increasingly used to improve outcome involving mesenchymal stem cells (MSCs), supported by clinical data where injection of autologous bone marrow derived MSCs (BM-MSCs) suspended in marrow supernatant into injured tendons has halved the re-injury rate in racehorses. We hypothesized that stem cell therapy induces a matrix more closely resembling normal tendon than the fibrous scar tissue formed by natural repair. Twelve horses with career-ending naturally-occurring superficial digital flexor tendon injury were allocated randomly to treatment and control groups. 1X10(7) autologous BM-MSCs suspended in 2 ml of marrow supernatant were implanted into the damaged tendon of the treated group. The control group received the same volume of saline. Following a 6 month exercise programme horses were euthanized and tendons assessed for structural stiffness by non-destructive mechanical testing and for morphological and molecular composition. BM-MSC treated tendons exhibited statistically significant improvements in key parameters compared to saline-injected control tendons towards that of normal tendons and those in the contralateral limbs. Specifically, treated tendons had lower structural stiffness (p<0.05) although no significant difference in calculated modulus of elasticity, lower (improved) histological scoring of organisation (p<0.003) and crimp pattern (p<0.05), lower cellularity (p<0.007), DNA content (p<0.05), vascularity (p<0.03), water content (p<0.05), GAG content (p<0.05), and MMP-13 activity (p<0.02). Treatment with autologous MSCs in marrow supernatant therefore provides significant benefits compared to untreated tendon repair in enhancing normalisation of biomechanical, morphological, and compositional parameters. These data in natural disease, with no adverse findings, support the use of this treatment for human tendon injuries.", "link"=>"http://www.mendeley.com/research/beneficial-effects-autologous-bone-marrowderived-mesenchymal-stem-cells-naturally-occurring-tendinop-5", "reader_count"=>72, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>6, "Researcher"=>6, "Student > Doctoral Student"=>8, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>4, "Student > Master"=>16, "Other"=>3, "Student > Bachelor"=>8, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>6, "Researcher"=>6, "Student > Doctoral Student"=>8, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>4, "Student > Master"=>16, "Other"=>3, "Student > Bachelor"=>8, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>7, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>20, "Medicine and Dentistry"=>25, "Arts and Humanities"=>1, "Sports and Recreations"=>2, "Veterinary Science and Veterinary Medicine"=>10, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>1, "Social Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>25}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Sports and Recreations"=>{"Sports and Recreations"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>20}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>7}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Arts and Humanities"=>{"Arts and Humanities"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>10}}, "reader_count_by_country"=>{"Austria"=>1, "United Kingdom"=>2, "Italy"=>1, "France"=>1}, "group_count"=>4}

CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1215317"], "description"=>"<p>Representative microscopic images of von Kossa and Oil-Red-O staining to confirm osteogenic and adipogenic differentiation of plastic adherent bone marrow derived cell populations (scale bars 100 µm). A higher magnification inset is shown in the adipogenesis image to demonstrate the presence of intracellular lipid droplets. Chondrogenic differentiation was confirmed by the formation of dense cell pellets (haematoxylin and eosin staining) that were positive for Safranin O (orange-red stain) (scale bars 1 mm). All respective controls (non-induced cultures) are shown in the upper row panels.</p>", "links"=>[], "tags"=>["differentiation", "putative", "marrow"], "article_id"=>807792, "categories"=>["Biological Sciences"], "users"=>["Roger Kenneth Whealands Smith", "Natalie Jayne Werling", "Stephanie Georgina Dakin", "Rafiqul Alam", "Allen E. Goodship", "Jayesh Dudhia"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0075697.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Trilineage_differentiation_of_putative_bone_marrow_MSCs_/807792", "title"=>"Trilineage differentiation of putative bone marrow MSCs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-25 01:32:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/1215320"], "description"=>"<p>Representative ultrasonographic appearance of (A) stem cell injected horses and (B) control (saline-injected) horses at the time of injection and at the conclusion of the study (6 months). Both transverse and longitudinal images are shown to illustrate the injury which is visible as a hypo-echoic area (arrows) denoting the loss of extracellular matrix, which is not present at 6 months. The linear organization of the healed tendon is apparent in the longitudinal images at 6 months.</p>", "links"=>[], "tags"=>["superficial", "flexor"], "article_id"=>807795, "categories"=>["Biological Sciences"], "users"=>["Roger Kenneth Whealands Smith", "Natalie Jayne Werling", "Stephanie Georgina Dakin", "Rafiqul Alam", "Allen E. Goodship", "Jayesh Dudhia"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0075697.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ultrasonography_of_the_superficial_digital_flexor_tendon_/807795", "title"=>"Ultrasonography of the superficial digital flexor tendon.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-25 01:32:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/1215321"], "description"=>"<p>(A) Cross-sectional areas were measured ultrasonographically at the time of implantation (Stem Cell 1, Saline 1 and Contra 1) and at 6 months (Stem Cell 6, Saline 6 and Contra 6). (B) Relative change in cross-sectional area between groups. The Wilcoxon Signed-Rank test showed that there was no difference in cross-sectional area between 1 and 6 months for either the stem cell treated group or the saline group, or between the contralateral limbs in each group. Contralateral limbs were therefore combined from both groups for statistical analysis. The values for normal horses are shown as mean (thick dashed line) with two standard deviations (thin dashed lines). * p = 0.006, ** p= 0.003, ***p<0.045.</p>", "links"=>[], "tags"=>["superficial", "flexor"], "article_id"=>807796, "categories"=>["Biological Sciences"], "users"=>["Roger Kenneth Whealands Smith", "Natalie Jayne Werling", "Stephanie Georgina Dakin", "Rafiqul Alam", "Allen E. Goodship", "Jayesh Dudhia"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0075697.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cross_sectional_area_of_the_superficial_digital_flexor_tendon_/807796", "title"=>"Cross-sectional area of the superficial digital flexor tendon.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-25 01:32:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/1215322"], "description"=>"<p>SDFTs were subjected to mechanical testing within 2 h of post euthanasia to determine (A) structural stiffness and (B) material stiffness (modulus), which was calculated by expressing the ratio of the structural stiffness to the ultrasonographically-determined cross-sectional area. Structural stiffness was significantly reduced in stem cell treated tendons and closer to that of the uninjured (contralateral) tendons. * p=0.015.</p>", "links"=>[], "tags"=>[], "article_id"=>807797, "categories"=>["Biological Sciences"], "users"=>["Roger Kenneth Whealands Smith", "Natalie Jayne Werling", "Stephanie Georgina Dakin", "Rafiqul Alam", "Allen E. Goodship", "Jayesh Dudhia"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0075697.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Biomechanical_properties_of_tendons_/807797", "title"=>"Biomechanical properties of tendons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-25 01:32:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/1215328"], "description"=>"<p>(A) Organisation and (B) crimp as assessed by blinded scores were taken from two separate histological sections for each tendon. Representative micrographs of haematoxylin and eosin stained histological SDFT sections from the treated and remote (less injured) sites in both MSC-treated and saline-treated groups are shown in the panels on the right. Normal tendon has a score of zero and the higher the score the more disrupted the tendon matrix and less crimp pattern, respectively. (A) * p = 0.003; ** p < 0.002; (B) * p = 0.046; ** p < 0.0001 (scale bars 50 µm).</p>", "links"=>[], "tags"=>[], "article_id"=>807803, "categories"=>["Biological Sciences"], "users"=>["Roger Kenneth Whealands Smith", "Natalie Jayne Werling", "Stephanie Georgina Dakin", "Rafiqul Alam", "Allen E. Goodship", "Jayesh Dudhia"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0075697.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Morphological_parameters_of_tendons_/807803", "title"=>"Morphological parameters of tendons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-25 01:32:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/1215329"], "description"=>"<p>Both (A) cellularity scores and (B) DNA content demonstrated reduced cellularity in MSC-treated tendons. The values for normal horses are shown as mean (thick dashed line) with two standard deviations (thin dashed lines). (A) * p=0.007; ** p=0.001; (B) * p=0.037; ** p<0.001.</p>", "links"=>[], "tags"=>[], "article_id"=>807804, "categories"=>["Biological Sciences"], "users"=>["Roger Kenneth Whealands Smith", "Natalie Jayne Werling", "Stephanie Georgina Dakin", "Rafiqul Alam", "Allen E. Goodship", "Jayesh Dudhia"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0075697.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cellularity_of_tendons_/807804", "title"=>"Cellularity of tendons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-25 01:32:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/1215330"], "description"=>"<p>There was reduced vascularity in the MSC-treated tendons, similar to normal tendon, compared to saline-injected controls. * p = 0.026; ** p = 0.004.</p>", "links"=>[], "tags"=>[], "article_id"=>807805, "categories"=>["Biological Sciences"], "users"=>["Roger Kenneth Whealands Smith", "Natalie Jayne Werling", "Stephanie Georgina Dakin", "Rafiqul Alam", "Allen E. Goodship", "Jayesh Dudhia"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0075697.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Vascularity_of_tendons_/807805", "title"=>"Vascularity of tendons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-25 01:32:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/1215331"], "description"=>"<p>Concentrations for (A) hydroxyproline and (B) sGAGs are shown. The values for normal horses are shown as mean (thick dashed line) with two standard deviations (thin dashed lines). Note that the sGAG content of MSC-treated tendons was closer to the normal range and not significantly different from the relatively uninjured contralateral limbs (p = 0.24). * p = 0.05.</p>", "links"=>[], "tags"=>[], "article_id"=>807806, "categories"=>["Biological Sciences"], "users"=>["Roger Kenneth Whealands Smith", "Natalie Jayne Werling", "Stephanie Georgina Dakin", "Rafiqul Alam", "Allen E. Goodship", "Jayesh Dudhia"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0075697.g008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Compositional_analysis_of_tendons_/807806", "title"=>"Compositional analysis of tendons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-25 01:32:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/1215333"], "description"=>"<p>(A) Tissue-linked fluorescence and (B) MMP-13 activity. The increased MMP-13 activity seen in the saline-treated group matched the lower tissue-linked fluorescence suggesting greater remodelling of the collagen matrix in the saline-treated compared to the MSC-treated tendons. (A) * p = 0.039; ** p = 0.003; (B) * p = 0.045; ** p = 0.015.</p>", "links"=>[], "tags"=>["re-modelling", "injured", "cells", "treated"], "article_id"=>807808, "categories"=>["Biological Sciences"], "users"=>["Roger Kenneth Whealands Smith", "Natalie Jayne Werling", "Stephanie Georgina Dakin", "Rafiqul Alam", "Allen E. Goodship", "Jayesh Dudhia"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0075697.g009"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Collagen_re_modelling_in_injured_and_stem_cells_treated_tendons_/807808", "title"=>"Collagen re-modelling in injured and stem cells treated tendons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-25 01:32:54"}

PMC Usage Stats | Further Information

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Relative Metric

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