No healing improvement after rotator cuff reconstruction augmented with an autologous periosteal flap

  • C. HolweinEmail author
  • B. von Bibra
  • P. M. Jungmann
  • D. C. Karampinos
  • K. Wörtler
  • M. Scheibel
  • A. B. Imhoff
  • S. Buchmann



To show descriptive clinical and magnetic resonance (MR) imaging results after an additional periosteal flap augmentation in mini-open rotator cuff reconstruction and to evaluate potential healing improvement at long-term follow-up.


Twenty-three patients with degenerative rotator cuff tears were followed after receiving a mini-open single-row repair with a subtendinous periosteal flap augmentation. Data were collected preoperatively, after 12 months and after 11 years. Clinical examination, simple shoulder test (SST), Constant–Murley Score (CS), ultrasonography examination and 3T MR imaging were performed.


Out of 23 patients, 20 were available for short-term and 19 for final follow-up at a median of 11.5 years (range 10.4–13.0). Questions answered with “yes” in SST improved from baseline 5.0 (range 1.0–8.0) to short 10.5 (range 8.0–12.0) and final follow-up 12.0 (range 7.0–12.0). CS improved from 53.5 (range 25.0–66.0) to 80.8 (range 75.9–89.3) and finally to 79.8 points (range 42.3–95.4). Improvement was highly significant (p < 0.05). Severe retears were found in 9/19 patients. Ossifications along the refixed tendon were noticed in 8/19 cases. Ossifications did not correlate with clinical outcome. At final follow-up, patients with retears seemed likely to have lower strength values in CS (mean ± SD) than patients without retears (7.3 ± 4.1 vs. 12.8 ± 5.3; p < 0.05).


No positive effect on improving healing response in rotator cuff refixation with a periosteal flap augmentation could be found. Retear rate is comparable to that of conventional rotator cuff refixation in the published literature. Ossifications along the tendon, without negatively affecting the clinical outcome, were seen. This invasive technique cannot be advised and should not be used anymore.

Level of evidence



Rotator cuff repair Rotator cuff healing Periosteal flap Tendon augmentation 



No one of the authors has received personal financial support related to this study.

Compliance with ethical standards

Conflict of interest

Authors C. Holwein, B. von Bibra, P. M. Jungmann, D. C. Karampinos, K. Wörtler, M. Scheibel declare that they have no conflict of interest. Author A. B. Imhoff is a consultant for Arthrosurface, Arthrex, and mediBayreuth. Author S. Buchmann is a consultant for Arthrex.

Ethical approval

The study was granted approval by Ethics Commission School of Medicine Technical University of Munich with the related number 70/15s.


  1. 1.
    Agout C, Berhouet J, Bouju Y, Godeneche A, Collin P, Kempf JF et al (2018) Clinical and anatomic results of rotator cuff repair at 10 years depend on tear type. Knee Surg Sports Traumatol Arthrosc 26:2490–2497CrossRefGoogle Scholar
  2. 2.
    Allen MR, Hock JM, Burr DB (2004) Periosteum: biology, regulation, and response to osteoporosis therapies. Bone 35:1003–1012CrossRefGoogle Scholar
  3. 3.
    Apostolakos J, Durant TJ, Dwyer CR, Russell RP, Weinreb JH, Alaee F et al (2014) The enthesis: a review of the tendon-to-bone insertion. Muscles Ligaments Tendons J 4:333–342CrossRefGoogle Scholar
  4. 4.
    Badhe SP, Lawrence TM, Smith FD, Lunn PG (2008) An assessment of porcine dermal xenograft as an augmentation graft in the treatment of extensive rotator cuff tears. J Shoulder Elbow Surg 17:35S–39SCrossRefGoogle Scholar
  5. 5.
    Barnes LA, Kim HM, Caldwell JM, Buza J, Ahmad CS, Bigliani LU et al (2017) Satisfaction, function and repair integrity after arthroscopic versus mini-open rotator cuff repair. Bone Jt J 99-B:245–249CrossRefGoogle Scholar
  6. 6.
    Bartl C, Kouloumentas P, Holzapfel K, Eichhorn S, Wortler K, Imhoff A et al (2012) Long-term outcome and structural integrity following open repair of massive rotator cuff tears. Int J Shoulder Surg 6:1–8CrossRefGoogle Scholar
  7. 7.
    Bateman JE (1963) The diagnosis and treatment of ruptures of the rotator cuff. Surg Clin North Am 43:1523–1530CrossRefGoogle Scholar
  8. 8.
    Beitzel K, Solovyova O, Cote MP, Apostolakos J, Russell RP, McCarthy MB et al (2013) The future role of mesenchymal stem cells in the management of shoulder disorders. Arthroscopy 29:1702–1711CrossRefGoogle Scholar
  9. 9.
    Bell S, Lim YJ, Coghlan J (2013) Long-term longitudinal follow-up of mini-open rotator cuff repair. J Bone Jt Surg Am 95:151–157CrossRefGoogle Scholar
  10. 10.
    Bonnevialle N, Bayle X, Faruch M, Wargny M, Gomez-Brouchet A, Mansat P (2015) Does microvascularization of the footprint play a role in rotator cuff healing of the shoulder? J Shoulder Elbow Surg 24:1257–1262CrossRefGoogle Scholar
  11. 11.
    Brunner UH (2002) Klinische Untersuchung der Schulter. In: Habermeyer P (ed) Schulterchirurgie, vol 1. Urban and Fischer, Auflage, pp 45–69Google Scholar
  12. 12.
    Buchmann S, Sandmann GH, Walz L, Reichel T, Beitzel K, Wexel G et al (2015) Growth factor release by vesicular phospholipid gels: in-vitro results and application for rotator cuff repair in a rat model. BMC Musculoskelet Disord 16:82CrossRefGoogle Scholar
  13. 13.
    Cai YZ, Zhang C, Jin RL, Shen T, Gu PC, Lin XJ et al (2018) Arthroscopic rotator cuff repair with graft augmentation of 3-dimensional biological collagen for moderate to large tears: a randomized controlled study. Am J Sports Med 46:1424–1431CrossRefGoogle Scholar
  14. 14.
    Chang CH, Chen CH, Su CY, Liu HT, Yu CM (2009) Rotator cuff repair with periosteum for enhancing tendon-bone healing: a biomechanical and histological study in rabbits. Knee Surg Sports Traumatol Arthrosc 17:1447–1453CrossRefGoogle Scholar
  15. 15.
    Charles MD, Christian DR, Cole BJ (2018) The role of biologic therapy in rotator cuff tears and repairs. Curr Rev Musculoskelet Med 11:150–161CrossRefGoogle Scholar
  16. 16.
    Chen CH, Chang CH, Su CI, Wang KC, Liu HT, Yu CM et al (2010) Arthroscopic single-bundle anterior cruciate ligament reconstruction with periosteum-enveloping hamstring tendon graft: clinical outcome at 2 to 7 years. Arthroscopy 26:907–917CrossRefGoogle Scholar
  17. 17.
    Chen CH, Chang CH, Wang KC, Su CI, Liu HT, Yu CM et al (2011) Enhancement of rotator cuff tendon-bone healing with injectable periosteum progenitor cells-BMP-2 hydrogel in vivo. Knee Surg Sports Traumatol Arthrosc 19:1597–1607CrossRefGoogle Scholar
  18. 18.
    Chen CH, Chen WJ, Shih CH, Yang CY, Liu SJ, Lin PY (2003) Enveloping the tendon graft with periosteum to enhance tendon-bone healing in a bone tunnel: a biomechanical and histologic study in rabbits. Arthroscopy 19:290–296CrossRefGoogle Scholar
  19. 19.
    Ciampi P, Scotti C, Nonis A, Vitali M, Di Serio C, Peretti GM et al (2014) The benefit of synthetic versus biological patch augmentation in the repair of posterosuperior massive rotator cuff tears: a 3-year follow-up study. Am J Sports Med 42:1169–1175CrossRefGoogle Scholar
  20. 20.
    Collin P, Colmar M, Thomazeau H, Mansat P, Boileau P, Valenti P et al (2018) Clinical and MRI outcomes 10 years after repair of massive posterosuperior rotator cuff tears. J Bone Jt Surg Am 100:1854–1863CrossRefGoogle Scholar
  21. 21.
    Colnot C, Zhang X, Knothe Tate ML (2012) Current insights on the regenerative potential of the periosteum: molecular, cellular, and endogenous engineering approaches. J Orthop Res 30:1869–1878CrossRefGoogle Scholar
  22. 22.
    Constant CR, Murley AH (1987) A clinical method of functional assessment of the shoulder. Clin Orthop Relat Res 214:160–164Google Scholar
  23. 23.
    Degen RM, Carbone A, Carballo C, Zong J, Chen T, Lebaschi A et al (2016) The effect of purified human bone marrow-derived mesenchymal stem cells on rotator cuff tendon healing in an athymic rat. Arthroscopy 32:2435–2443CrossRefGoogle Scholar
  24. 24.
    Dyrna F, Buchmann S, Beitzel K, Imhoff AB (2016) Rotatorenmanschettenheilung Obere Extremität 11:3–9Google Scholar
  25. 25.
    El-Azab H, Buchmann S, Beitzel K, Waldt S, Imhoff AB (2010) Clinical and structural evaluation of arthroscopic double-row suture-bridge rotator cuff repair: early results of a novel technique. Knee Surg Sports Traumatol Arthrosc 18:1730–1737CrossRefGoogle Scholar
  26. 26.
    Ellman H (1987) Arthroscopic subacromial decompression: analysis of one- to three-year results. Arthroscopy 3:173–181CrossRefGoogle Scholar
  27. 27.
    Ficklscherer A, Serr M, Loitsch T, Niethammer TR, Lahner M, Pietschmann MF et al (2017) The influence of different footprint preparation techniques on tissue regeneration in rotator cuff repair in an animal model. Arch Med Sci 13:481–488CrossRefGoogle Scholar
  28. 28.
    Flury M, Rickenbacher D, Jung C, Schneider MM, Endell D, Audige L (2018) Porcine dermis patch augmentation of supraspinatus tendon repairs: a pilot study assessing tendon integrity and shoulder function 2 years after arthroscopic repair in patients aged 60 years or older. Arthroscopy 34:24–37CrossRefGoogle Scholar
  29. 29.
    Fuchs B, Weishaupt D, Zanetti M, Hodler J, Gerber C (1999) Fatty degeneration of the muscles of the rotator cuff: assessment by computed tomography versus magnetic resonance imaging. J Shoulder Elbow Surg 8:599–605CrossRefGoogle Scholar
  30. 30.
    Gerber C, Schneeberger AG, Beck M, Schlegel U (1994) Mechanical strength of repairs of the rotator cuff. J Bone Jt Surg Br 76:371–380CrossRefGoogle Scholar
  31. 31.
    Goutallier D, Postel JM, Bernageau J, Lavau L, Voisin MC (1995) Fatty infiltration of disrupted rotator cuff muscles. Rev Rhum Engl Ed 62:415–422Google Scholar
  32. 32.
    Gwinner C, Gerhardt C, Haneveld H, Scheibel M (2016) Two-staged application of PRP in arthroscopic rotator cuff repair: a matched-pair analysis. Arch Orthop Trauma Surg 136:1165–1171CrossRefGoogle Scholar
  33. 33.
    Harris MT, Butler DL, Boivin GP, Florer JB, Schantz EJ, Wenstrup RJ (2004) Mesenchymal stem cells used for rabbit tendon repair can form ectopic bone and express alkaline phosphatase activity in constructs. J Orthop Res 22:998–1003CrossRefGoogle Scholar
  34. 34.
    Hernigou P, Flouzat Lachaniette CH, Delambre J, Zilber S, Duffiet P, Chevallier N et al (2014) Biologic augmentation of rotator cuff repair with mesenchymal stem cells during arthroscopy improves healing and prevents further tears: a case-controlled study. Int Orthop 38:1811–1818CrossRefGoogle Scholar
  35. 35.
    Iannotti JP, Deutsch A, Green A, Rudicel S, Christensen J, Marraffino S et al (2013) Time to failure after rotator cuff repair: a prospective imaging study. J Bone Jt Surg Am 95:965–971CrossRefGoogle Scholar
  36. 36.
    Jensen PT, Lambertsen KL, Frich LH (2018) Assembly, maturation, and degradation of the supraspinatus enthesis. J Shoulder Elbow Surg 27:739–750CrossRefGoogle Scholar
  37. 37.
    Kuntz LA, Rossetti L, Kunold E, Schmitt A, von Eisenhart-Rothe R, Bausch AR et al (2018) Biomarkers for tissue engineering of the tendon-bone interface. PLoS One 13:e0189668CrossRefGoogle Scholar
  38. 38.
    Kwon J, Kim SH, Lee YH, Kim TI, Oh JH (2018) The rotator cuff healing index: a new scoring system to predict rotator cuff healing after surgical repair. Am J Sports Med 47:173–180CrossRefGoogle Scholar
  39. 39.
    Kyung HS, Kim SY, Oh CW, Kim SJ (2003) Tendon-to-bone tunnel healing in a rabbit model: the effect of periosteum augmentation at the tendon-to-bone interface. Knee Surg Sports Traumatol Arthrosc 11:9–15CrossRefGoogle Scholar
  40. 40.
    Lee KW, Lee JS, Kim YS, Shim YB, Jang JW, Lee KI (2016) Effective healing of chronic rotator cuff injury using recombinant bone morphogenetic protein-2 coated dermal patch in vivo. J Biomed Mater Res B Appl Biomater. Google Scholar
  41. 41.
    Li H, Jiang J, Wu Y, Chen S (2012) Potential mechanisms of a periosteum patch as an effective and favourable approach to enhance tendon-bone healing in the human body. Int Orthop 36:665–669CrossRefGoogle Scholar
  42. 42.
    Lippit SBHD, Matsen FA (1993) A practical tool for evaluating function: the simple shoulder test. In: Matsen FA, Fu FH, Hawkins RJ (eds) The shoulder: a balance of mobility and stability. American Academy of Orthopaedic Surgeons, Rosemont, pp 545–559Google Scholar
  43. 43.
    Liu Q, Yu Y, Reisdorf RL, Qi J, Lu CK, Berglund LJ et al (2018) Engineered tendon-fibrocartilage-bone composite and bone marrow-derived mesenchymal stem cell sheet augmentation promotes rotator cuff healing in a non-weight-bearing canine model. Biomaterials 192:189–198CrossRefGoogle Scholar
  44. 44.
    McMahon PJ, Prasad A, Francis KA (2014) What is the prevalence of senior-athlete rotator cuff injuries and are they associated with pain and dysfunction? Clin Orthop Relat Res 472:2427–2432CrossRefGoogle Scholar
  45. 45.
    Minagawa H, Yamamoto N, Abe H, Fukuda M, Seki N, Kikuchi K et al (2013) Prevalence of symptomatic and asymptomatic rotator cuff tears in the general population: from mass-screening in one village. J Orthop 10:8–12CrossRefGoogle Scholar
  46. 46.
    Murthi AM, Lankachandra M (2019) Technologies to augment rotator cuff repair. Orthop Clin North Am 50:103–108CrossRefGoogle Scholar
  47. 47.
    Papadopoulos P, Karataglis D, Boutsiadis A, Fotiadou A, Christoforidis J, Christodoulou A (2011) Functional outcome and structural integrity following mini-open repair of large and massive rotator cuff tears: a 3–5 year follow-up study. J Shoulder Elbow Surg 20:131–137CrossRefGoogle Scholar
  48. 48.
    Park JS, Park HJ, Kim SH, Oh JH (2015) Prognostic factors affecting rotator cuff healing after arthroscopic repair in small to medium-sized tears. Am J Sports Med 43:2386–2392CrossRefGoogle Scholar
  49. 49.
    Patte D (1990) Classification of rotator cuff lesions. Clin Orthop Relat Res 254:81–86Google Scholar
  50. 50.
    Pauly S, Gerhardt C, Scheibel M (2015) Sehnenheilung nach Rotatorenmanschettenrekonstruktion. Obere Extremität 10:17–23CrossRefGoogle Scholar
  51. 51.
    Pauzenberger L, Heuberer PR, Dyrna F, Obopilwe E, Kriegleder B, Anderl W et al (2018) Double-layer rotator cuff repair: anatomic reconstruction of the superior capsule and rotator cuff improves biomechanical properties in repairs of delaminated rotator cuff tears. Am J Sports Med 46:3165–3173CrossRefGoogle Scholar
  52. 52.
    Proctor CS (2014) Long-term successful arthroscopic repair of large and massive rotator cuff tears with a functional and degradable reinforcement device. J Shoulder Elbow Surg 23:1508–1513CrossRefGoogle Scholar
  53. 53.
    Ritsila V, Alhopuro S, Rintala A (1972) Bone formation with free periosteum. An experimental study. Scand J Plast Reconstr Surg 6:51–56CrossRefGoogle Scholar
  54. 54.
    Rothrauff BB, Smith CA, Ferrer GA, Novaretti JV, Pauyo T, Chao T et al (2018) The effect of adipose-derived stem cells on enthesis healing after repair of acute and chronic massive rotator cuff tears in rats. J Shoulder Elbow Surg. Google Scholar
  55. 55.
    Rui YF, Lui PP, Lee YW, Chan KM (2012) Higher BMP receptor expression and BMP-2-induced osteogenic differentiation in tendon-derived stem cells compared with bone-marrow-derived mesenchymal stem cells. Int Orthop 36:1099–1107CrossRefGoogle Scholar
  56. 56.
    Saraswat MK, Styles-Tripp F, Beaupre LA, Luciak-Corea C, Otto D, Lalani A et al (2015) Functional outcomes and health-related quality of life after surgical repair of full-thickness rotator cuff tears using a mini-open technique: a concise 10-year follow-up of a previous report. Am J Sports Med 43:2794–2799CrossRefGoogle Scholar
  57. 57.
    Scheibel M, Brown A, Woertler K, Imhoff AB (2007) Preliminary results after rotator cuff reconstruction augmented with an autologous periosteal flap. Knee Surg Sports Traumatol Arthrosc 15:305–314CrossRefGoogle Scholar
  58. 58.
    Sugaya H, Maeda K, Matsuki K, Moriishi J (2005) Functional and structural outcome after arthroscopic full-thickness rotator cuff repair: single-row versus dual-row fixation. Arthroscopy 21:1307–1316CrossRefGoogle Scholar
  59. 59.
    Thangarajah T, Pendegrass CJ, Shahbazi S, Lambert S, Alexander S, Blunn GW (2015) Augmentation of rotator cuff repair with soft tissue scaffolds. Orthop J Sports Med 3:2325967115587495CrossRefGoogle Scholar
  60. 60.
    Thomazeau H, Rolland Y, Lucas C, Duval JM, Langlais F (1996) Atrophy of the supraspinatus belly. Assessment by MRI in 55 patients with rotator cuff pathology. Acta Orthop Scand 67:264–268CrossRefGoogle Scholar
  61. 61.
    Yamamoto A, Takagishi K, Osawa T, Yanagawa T, Nakajima D, Shitara H et al (2010) Prevalence and risk factors of a rotator cuff tear in the general population. J Shoulder Elbow Surg 19:116–120CrossRefGoogle Scholar
  62. 62.
    Yoon JP, Lee CH, Jung JW, Lee HJ, Lee YS, Kim JY et al (2018) Sustained delivery of transforming growth factor beta1 by use of absorbable alginate scaffold enhances rotator cuff healing in a rabbit model. Am J Sports Med 46:1441–1450CrossRefGoogle Scholar
  63. 63.
    Youn I, Jones DG, Andrews PJ, Cook MP, Suh JK (2004) Periosteal augmentation of a tendon graft improves tendon healing in the bone tunnel. Clin Orthop Relat Res 419:223–231CrossRefGoogle Scholar
  64. 64.
    Zumstein MA, Jost B, Hempel J, Hodler J, Gerber C (2008) The clinical and structural long-term results of open repair of massive tears of the rotator cuff. J Bone Jt Surg Am 90:2423–2431CrossRefGoogle Scholar

Copyright information

© European Society of Sports Traumatology, Knee Surgery, Arthroscopy (ESSKA) 2019

Authors and Affiliations

  • C. Holwein
    • 1
    Email author
  • B. von Bibra
    • 1
  • P. M. Jungmann
    • 2
  • D. C. Karampinos
    • 3
  • K. Wörtler
    • 3
  • M. Scheibel
    • 4
  • A. B. Imhoff
    • 1
  • S. Buchmann
    • 5
  1. 1.Abteilung und Poliklinik für Sportorthopädie Klinikum rechts der Isar Technische Universität MünchenMunichGermany
  2. 2.Klinik für Neuroradiologie Universitätsspital ZürichZurichSwitzerland
  3. 3.Institut für diagnostische und interventionelle Radiologie Klinikum rechts der Isar Technische Universität MünchenMunichGermany
  4. 4.Centrum für Muskuloskeletale Chirurgie der Charité – Universitätsmedizin Berlin, Campus Virchow KlinikumBerlinGermany
  5. 5.OFZ Orthopädisches Fachzentrum WeilheimWeilheim in OberbayernGermany

Personalised recommendations