Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
BMC Musculoskeletal Disorders
Published in: BMC Musculoskeletal Disorders 1/2018

Open Access 01-12-2018 | Research article

The effect of autologous platelet rich plasma on tenocytes of the human rotator cuff

Authors: Stephan Pauly, Franka Klatte-Schulz, Katharina Stahnke, Markus Scheibel, Britt Wildemann

Published in: BMC Musculoskeletal Disorders | Issue 1/2018

Login to get access

Abstract

Background

Platelet rich plasma (PRP) is widely used in rotator cuff repairs but its effect on the healing process is unclear. Several cell culture studies on the effect of allogenic PRP have reported promising results but are not transferable to clinical practice.
The aim of the present study is to assess the possible effect of autologous PRP on rotator cuff tendon cells. The amount of growth factors involved with tendon-bone healing (PDGF-AB, IGF-1, TGF-β1, BMP-7 and -12) is quantified.

Methods

Rotator cuff tissue samples were obtained from (n = 24) patients grouped by age (>/< 65 years) and sex into four groups and cells were isolated and characterized. Later, autologous PRP preparations were obtained and the effect was analyzed by means of cell proliferation, collagen I synthesis and expression of collagen I and III. Furthermore, the PRPs were quantified for growth factor content by means of platelet-derived growth factor (PDGF-AB), insulin-like growth factor (IGF-1), transforming growth factor (TGF-β1), as well as bone morphogenetic protein (BMP) -7 and − 12.

Results

Cell proliferation and absolute synthesis of collagen I were positively affected by PRP exposure compared to controls (p < 0.05), but expression and relative synthesis of collagen I (normalized to cell proliferation) were significantly reduced.
PRP contained high amounts of IGF-1 and lower levels of TGF-β1 and PDGF-AB. The amounts of BMP-7 and -12 were below the detection limits.

Conclusions

PRP is a source of growth factors such involved with tendon-bone healing. PRP had an anabolic effect on the human rotator cuff tenocytes of the same individual in vitro by means of cell proliferation and absolute, but not relative collagen I synthesis.
These results encourage further studies on clinical outcomes with more comparable standards in terms of preparation and application methods.

Level of evidence

Controlled laboratory study.
Literature
1.
Barber FA. Platelet-rich plasma for rotator cuff repair. Sports Med Arthrosc. 2013;21:199–205.CrossRef
2.
Bayne O, Bateman J. Long term results of surgical repair of full thickness rotator cuff tears. In: Bateman J, Welsh R, editors. Surgery of the shoulder. Philadelphia: The C.V. Mosby Company, Inc; 1984.
3.
Boileau P, Brassart N, Watkinson DJ, Carles M, Hatzidakis AM, Krishnan SG. Arthroscopic repair of full-thickness tears of the supraspinatus: does the tendon really heal? J Bone Joint Surg Am. 2005;87:1229–40.PubMed
4.
Boswell SG, Schnabel LV, Mohammed HO, Sundman EA, Minas T, Fortier LA. Increasing platelet concentrations in leukocyte-reduced platelet-rich plasma decrease collagen gene synthesis in tendons. Am J Sports Med. 2014;42:42–9.CrossRef
5.
Cai YZ, Zhang C, Lin XJ. Efficacy of platelet-rich plasma in arthroscopic repair of full-thickness rotator cuff tears: a meta-analysis. J Shoulder Elb Surg. 2015;24:1852–9.CrossRef
6.
Cenni E, Avnet S, Fotia C, Salerno M, Baldini N. Platelet-rich plasma impairs osteoclast generation from human precursors of peripheral blood. J Orthop Res. 2010;28:792–7.PubMed
7.
Chahal J, Van Thiel GS, Mall N, Heard W, Bach BR, Cole BJ, Nicholson GP, Verma NN, Whelan DB, Romeo AA. The role of platelet-rich plasma in arthroscopic rotator cuff repair: a systematic review with quantitative synthesis. Arthroscopy. 2012;28:1718–27.CrossRef
8.
Chen L, Dong SW, Tao X, Liu JP, Tang KL, Xu JZ. Autologous platelet-rich clot releasate stimulates proliferation and inhibits differentiation of adult rat tendon stem cells towards nontenocyte lineages. J Int Med Res. 2012;40:1399–409.CrossRef
9.
Chen M, Xu W, Dong Q, Huang Q, Xie Z, Mao Y. Outcomes of single-row versus double-row arthroscopic rotator cuff repair: a systematic review and meta-analysis of current evidence. Arthroscopy. 2013;29:1437–49.CrossRef
10.
Chung SW, Oh JH, Gong HS, Kim JY, Kim SH. Factors affecting rotator cuff healing after arthroscopic repair: osteoporosis as one of the independent risk factors. Am J Sports Med. 2011;39:2099–107.CrossRef
11.
Clayton RA, Court-Brown CM. The epidemiology of musculoskeletal tendinous and ligamentous injuries. Injury. 2008;39:1338–44.CrossRef
12.
Cross JA, Cole BJ, Spatny KP, Sundman E, Romeo AA, Nicholson GP, Wagner B, Fortier LA. Leukocyte-reduced platelet-rich plasma normalizes matrix metabolism in torn human rotator cuff tendons. Am J Sports Med. 2015;43:2898–906.CrossRef
13.
de Mos M, van der Windt AE, Jahr H, van Schie HT, Weinans H, Verhaar JA, van Osch GJ. Can platelet-rich plasma enhance tendon repair?A cell culture study. Am J Sports Med. 2008;36:1171–8.CrossRef
14.
DeFranco MJ, Bershadsky B, Ciccone J, Yum JK, Iannotti JP. Functional outcome of arthroscopic rotator cuff repairs: a correlation of anatomic and clinical results. J Shoulder Elb Surg. 2007;16:759–65.CrossRef
15.
DeHaan AM, Axelrad TW, Kaye E, Silvestri L, Puskas B, Foster TE. Does double-row rotator cuff repair improve functional outcome of patients compared with single-row technique? A systematic review. Am J Sports Med. 2012;40:1176–85.CrossRef
16.
Flury M, Rickenbacher D, Schwyzer HK, Jung C, Schneider MM, Stahnke K, Goldhahn J, Audige L. Does pure platelet-rich plasma affect postoperative clinical outcomes after arthroscopic rotator cuff repair? A Randomized Controlled Trial. Am J Sports Med. 2016;44:2136–46.CrossRef
17.
Giusti I, D'Ascenzo S, Manco A, Di Stefano G, Di Francesco M, Rughetti A, Dal Mas A, Properzi G, Calvisi V, Dolo V. Platelet concentration in platelet-rich plasma affects tenocyte behavior in vitro. Biomed Res Int. 2014;2014:630870.PubMedPubMedCentral
18.
Goutallier D, Postel JM, Bernageau J, Lavau L, Voisin MC. Fatty muscle degeneration in cuff ruptures. Pre- and postoperative evaluation by CT scan. Clin Orthop Relat Res. 1994;(304):78-83.
19.
Grasso A, Milano G, Salvatore M, Falcone G, Deriu L, Fabbriciani C. Single-row versus double-row arthroscopic rotator cuff repair: a prospective randomized clinical study. Arthroscopy. 2009;25:4–12.CrossRef
20.
Gulotta LV, Rodeo SA. Growth factors for rotator cuff repair. Clin Sports Med. 2009;28:13–23.CrossRef
21.
Gwinner C, Gerhardt C, Haneveld H, Scheibel M. Two-staged application of PRP in arthroscopic rotator cuff repair: a matched-pair analysis. Arch Orthop Trauma Surg. 2016;136:1165–71.CrossRef
22.
Hilber F, Loibl M, Lang S, Kerschbaum M, Brockhoff G, Angele P, Zellner J, Schmitz P, Nerlich M, Worlicek M. Leukocyte-reduced platelet-rich plasma increases proliferation of tenocytes treated with prednisolone: a cell cycle analysis. Arch Orthop Trauma Surg. 2017;137:1417–22.CrossRef
23.
Isaac C, Gharaibeh B, Witt M, Wright VJ, Huard J. Biologic approaches to enhance rotator cuff healing after injury. J Shoulder Elb Surg. 2012;21:181–90.CrossRef
24.
Jo CH, Kim JE, Yoon KS, Shin S. Platelet-rich plasma stimulates cell proliferation and enhances matrix gene expression and synthesis in tenocytes from human rotator cuff tendons with degenerative tears. Am J Sports Med. 2012;40:1035–45.CrossRef
25.
Kevy SV, Jacobson MS. Comparison of methods for point of care preparation of autologous platelet gel. J Extra Corpor Technol. 2004;36:28–35.PubMed
26.
Klatte-Schulz F, Gerhardt C, Scheibel M, Wildemann B, Pauly S. Relationship between muscle fatty infiltration and the biological characteristics and stimulation potential of tenocytes from rotator cuff tears. J Orthop Res. 2014;32:129–37.CrossRef
27.
Klatte-Schulz F, Pauly S, Scheibel M, Greiner S, Gerhardt C, Hartwig J, Schmidmaier G, Wildemann B. Characteristics and stimulation potential with BMP-2 and BMP-7 of tenocyte-like cells isolated from the rotator cuff of female donors. PLoS One. 2013;8:e67209.CrossRef
28.
Klatte-Schulz F, Pauly S, Scheibel M, Greiner S, Gerhardt C, Schmidmaier G, Wildemann B. Influence of age on the cell biological characteristics and the stimulation potential of male human tenocyte-like cells. Eur Cell Mater. 2012;24:74–89.CrossRef
29.
Kovacevic D, Rodeo SA. Biological augmentation of rotator cuff tendon repair. Clin Orthop Relat Res. 2008;466:622–33.CrossRef
30.
Li X, Xu CP, Hou YL, Song JQ, Cui Z, Yu B. Are Platelet Concentrates An Ideal Biomaterial for Arthroscopic Rotator Cuff Repair? A Meta-Analysis of Randomized Controlled Trials. Arthroscopy. 2014;30(11):1483–90.CrossRef
31.
Lorbach O, Baums MH, Kostuj T, Pauly S, Scheibel M, Carr A, Zargar N, Saccomanno MF, Milano G. Advances in biology and mechanics of rotator cuff repair. Knee Surg Sports Traumatol Arthrosc. 2015;23:530–41.CrossRef
32.
Magalon J, Bausset O, Serratrice N, Giraudo L, Aboudou H, Veran J, Magalon G, Dignat-Georges F, Sabatier F. Characterization and comparison of 5 platelet-rich plasma preparations in a single-donor model. Arthroscopy. 2014;30:629–38.CrossRef
33.
Marx RE. Platelet-rich plasma: evidence to support its use. J Oral Maxillofac Surg. 2004;62:489–96.CrossRef
34.
Mazzocca AD, McCarthy MB, Chowaniec DM, Cote MP, Romeo AA, Bradley JP, Arciero RA, Beitzel K. Platelet-rich plasma differs according to preparation method and human variability. J Bone Joint Surg Am. 2012;94:308–16.CrossRef
35.
Milgrom C, Schaffler M, Gilbert S, van Holsbeeck M. Rotator-cuff changes in asymptomatic adults. The effect of age, hand dominance and gender. J Bone Joint Surg Br. 1995;77:296–8.CrossRef
36.
Molloy T, Wang Y, Murrell G. The roles of growth factors in tendon and ligament healing. Sports Med. 2003;33:381–94.CrossRef
37.
Ogata S, Uhthoff HK. Acromial enthesopathy and rotator cuff tear. A radiologic and histologic postmortem investigation of the coracoacromial arch. Clin Orthop Relat Res. 1990;(254):39-48.
38.
Osti L, Papalia R, Del Buono A, Denaro V, Maffulli N. Comparison of arthroscopic rotator cuff repair in healthy patients over and under 65 years of age. Knee Surg Sports Traumatol Arthrosc. 2010;18:1700–6.CrossRef
39.
Pauly S, Gerhardt C, Chen J, Scheibel M. Single versus double-row repair of the rotator cuff: does double-row repair with improved anatomical and biomechanical characteristics lead to better clinical outcome? Knee Surg Sports Traumatol Arthrosc. 2010a;18:1718–29.CrossRef
40.
Pauly S, Klatte F, Strobel C, Schmidmaier G, Greiner S, Scheibel M, Wildemann B. BMP-2 and BMP-7 affect human rotator cuff tendon cells in vitro. J Shoulder Elb Surg. 2011;21:464–73.CrossRef
41.
Pauly S, Klatte F, Strobel C, Schmidmaier G, Greiner S, Scheibel M, Wildemann B. Characterization of tendon cell cultures of the human rotator cuff. Eur Cell Mater. 2010b;20:84–97.CrossRef
42.
Perser K, Godfrey D, Bisson L. Meta-analysis of clinical and radiographic outcomes after arthroscopic single-row versus double-row rotator cuff repair. Sports Health. 2011;3:268–74.CrossRef
43.
Prasathaporn N, Kuptniratsaikul S, Kongrukgreatiyos K. Single-row repair versus double-row repair of full-thickness rotator cuff tears. Arthroscopy. 2011;27:978–85.CrossRef
44.
Randelli P, Arrigoni P, Ragone V, Aliprandi A, Cabitza P. Platelet rich plasma in arthroscopic rotator cuff repair: a prospective RCT study, 2-year follow-up. J Shoulder Elb Surg. 2011;20:518–28.CrossRef
45.
Rodeo SA. Biologic augmentation of rotator cuff tendon repair. J Shoulder Elb Surg. 2007;16:S191–7.CrossRef
46.
Sadoghi P, Lohberger B, Aigner B, Kaltenegger H, Friesenbichler J, Wolf M, Sununu T, Leithner A, Vavken P. Effect of platelet-rich plasma on the biologic activity of the human rotator-cuff fibroblasts: a controlled in vitro study. J Orthop Res. 2013;31:1249–53.CrossRef
47.
Saltzman BM, Jain A, Campbell KA, Mascarenhas R, Romeo AA, Verma NN, Cole BJ. Does the Use of Platelet-Rich Plasma at the Time of Surgery Improve Clinical Outcomes in Arthroscopic Rotator Cuff Repair When Compared With Control Cohorts? A Systematic Review of Meta-analyses. Arthroscopy. 2016;32(5):906-18. https://​doi.​org/​10.​1016/​j.​arthro.​2015.​10.​007. Epub 2015 Dec 23.
48.
Saridakis P, Jones G. Outcomes of single-row and double-row arthroscopic rotator cuff repair: a systematic review. J Bone Joint Surg Am. 2010;92:732–42.CrossRef
49.
Seeherman HJ, Archambault JM, Rodeo SA, Turner AS, Zekas L, D'Augusta D, Li XJ, Smith E, Wozney JM. rhBMP-12 accelerates healing of rotator cuff repairs in a sheep model. J Bone Joint Surg Am. 2008;90:2206–19.CrossRef
50.
Sheibani-Rad S, Giveans MR, Arnoczky SP, Bedi A. Arthroscopic single-row versus double-row rotator cuff repair: a meta-analysis of the randomized clinical trials. Arthroscopy. 2013;29:343–8.CrossRef
51.
Sheth U, Simunovic N, Klein G, Fu F, Einhorn TA, Schemitsch E, Ayeni OR, Bhandari M. Efficacy of autologous platelet-rich plasma use for orthopaedic indications: a meta-analysis. J Bone Joint Surg Am. 2012;94:298–307.CrossRef
52.
Slater M, Patava J, Kingham K, Mason RS. Involvement of platelets in stimulating osteogenic activity. J Orthop Res. 1995;13:655–63.CrossRef
53.
Sorensen AK, Bak K, Krarup AL, Thune CH, Nygaard M, Jorgensen U, Sloth C, Torp-Pedersen S. Acute rotator cuff tear: do we miss the early diagnosis? A prospective study showing a high incidence of rotator cuff tears after shoulder trauma. J Shoulder Elb Surg. 2007;16:174–80.CrossRef
54.
Tashjian RZ, Hollins AM, Kim HM, Teefey SA, Middleton WD, Steger-May K, Galatz LM, Yamaguchi K. Factors affecting healing rates after arthroscopic double-row rotator cuff repair. Am J Sports Med. 2010;38:2435–42.CrossRef
55.
56.
Tsai AD, Yeh LC, Lee JC. Effects of osteogenic protein-1 (OP-1, BMP-7) on gene expression in cultured medial collateral ligament cells. J Cell Biochem. 2003;90:777–91.CrossRef
57.
Vavken P, Sadoghi P, Murray MM. The effect of platelet concentrates on graft maturation and graft-bone interface healing in anterior cruciate ligament reconstruction in human patients: a systematic review of controlled trials. Arthroscopy. 2011;27:1573–83.CrossRef
58.
Vavken P, Sadoghi P, Palmer M, Rosso C, Mueller AM, Szoelloesy G, Valderrabano V. Platelet-rich plasma reduces Retear rates after arthroscopic repair of small- and medium-sized rotator cuff tears but is not cost-effective. Am J Sports Med. 2015;43(12):3071–6.CrossRef
59.
Violini S, Ramelli P, Pisani LF, Gorni C, Mariani P. Horse bone marrow mesenchymal stem cells express embryo stem cell markers and show the ability for tenogenic differentiation by in vitro exposure to BMP-12. BMC Cell Biol. 2009;10:29.CrossRef
60.
Warth RJ, Dornan GJ, James EW, Horan MP, Millett PJ. Clinical and structural outcomes after arthroscopic repair of full-thickness rotator cuff tears with and without platelet-rich product supplementation: a meta-analysis and meta-regression. Arthroscopy. 2015;31:306–20.CrossRef
61.
Yamaguchi K, Ditsios K, Middleton WD, Hildebolt CF, Galatz LM, Teefey SA. The demographic and morphological features of rotator cuff disease a comparison of asymptomatic and symptomatic shoulders. J Bone Joint Surg Am. 2006;88:1699–704.CrossRef
62.
Yeh LC, Tsai AD, Lee JC. Bone morphogenetic protein-7 regulates differentially the mRNA expression of bone morphogenetic proteins and their receptors in rat achilles and patellar tendon cell cultures. J Cell Biochem. 2008;104:2107–22.CrossRef
63.
Zhang Q, Ge H, Zhou J, Cheng B. Are platelet-rich products necessary during the arthroscopic repair of full-thickness rotator cuff tears: a meta-analysis. PLoS One. 2013;8:e69731.CrossRef
Metadata
Title
The effect of autologous platelet rich plasma on tenocytes of the human rotator cuff
Authors
Stephan Pauly
Franka Klatte-Schulz
Katharina Stahnke
Markus Scheibel
Britt Wildemann
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Musculoskeletal Disorders / Issue 1/2018
Electronic ISSN: 1471-2474
DOI
https://doi.org/10.1186/s12891-018-2339-5

Other articles of this Issue 1/2018

BMC Musculoskeletal Disorders 1/2018 Go to the issue

Research article

Pharmacological effects of N-[2-[[2-[2-[(2,6-dichlorophenyl)amino]phenyl]acetyl]oxy]ethyl]hyaluronamide (diclofenac Etalhyaluronate, SI-613), a novel sodium hyaluronate derivative chemically linked with diclofenac

Research article

Lower extremity joint contracture according to ambulatory status in children with Duchenne muscular dystrophy

Research article

The use of bidirectional rapid reductor in minimally invasive treatment of bicondylar tibial plateau fractures: preliminary radiographic and clinical results

Research article

Treatment of aneurysmal bone cysts using endoscopic curettage

Research article

The association between subgroups of MRI findings identified with latent class analysis and low back pain in 40-year-old Danes

Study protocol

Protocol for the Individual Placement and Support (IPS) in Pain Trial: A randomized controlled trial investigating the effectiveness of IPS for patients with chronic pain