Ossifying tendinitis of the rotator cuff after arthroscopic excision of calcium deposits: report of two cases and literature review
© The Author(s) 2014
Received: 8 February 2014
Accepted: 23 June 2014
Published: 15 July 2014
Ossifying tendinitis (OT) is a type of heterotopic ossification, characterized by deposition of hydroxyapatite crystals in a histologic pattern of mature lamellar bone. It is usually associated with surgical intervention or trauma and is more commonly seen in Achilles or distal biceps tendons, and also in the gluteus maximus tendon. To our knowledge, there is no description of OT as a complication of calcifying tendinitis of the rotator cuff. In this report, we describe two cases in which the patients developed an OT of the supraspinatus after arthroscopic removal of calcium deposits. The related literature is reviewed.
KeywordsOssifying Calcifying Tendinitis Shoulder Arthroscopy
Subacromial calcium deposits and calcifications in the tendons of the rotator cuff (RC), with histologic presence of chondrocytes along tenocytes, were identified as a cause of scapulohumeral periarthritis in the early 1900s [1–3]. Later, the term calcifying tendinitis (CT) was coined, denoting an evolutionary process tending towards spontaneous healing . Prevalence of CT was reported to be 2.7 % in asymptomatic individuals and it seems to be more common in females between their fourth and sixth decades, and sedentary workers . Uhthoff and Sarkar  noted that CT evolves through a typical cycle in three distinct stages: pre-calcific, calcifying and post-calcific. The pre-calcific stage is characterized by metaplasia of tenocytes into chondrocytes that can be stimulated by multiple factors including hypoxia, microtrauma, disuse and hormonal action. The calcific stage can be divided into three phases: formation, resting and resorption; the process evolves from deposition of amorphous calcium phosphate followed by vascularisation to absorb the calcium deposits. The phase of resorption is associated with significant clinical pain experienced by the patient. The post-calcific stage marks collagenisation of the lesion by fibroblasts, thus ending the cycle of calcifying tendinitis.
It is usually associated with surgical intervention or trauma  and is more commonly seen in the Achilles tendon  or following repair of ruptured distal biceps . To our knowledge, there is no description of OT as a complication of calcifying tendinitis of the rotator cuff. In this report, we describe two cases in which patients developed an OT of the supraspinatus after arthroscopic removal of calcium deposits, and we review the literature.
In April 2005 the patient came to our outpatient office, complaining of severe pain and discomfort in the right shoulder for 1 year. After radiological and ultrasound (US) examination, he was diagnosed with calcific tendinitis of the rotator cuff and he underwent two cycles of extracorporeal shock wave (ESW) therapy. At 1 year follow-up he had not had any improvement in pain and shoulder function and therefore was advised to undergo shoulder arthroscopy.
After 1 year of moderate postoperative pain, the patient asked to be reassessed again due to severe disability during work and daily living activities Several attempts at conservative therapies (rehabilitation, laser therapy, NSAID, steroid injections) failed and he was therefore prescribed shoulder MRI that revealed slight changes in signal intensity (T1 weighted) of the supraspinatus insertion due to degenerative alterations of the tendon (Fig. 4d). A third arthroscopic approach in May 2009 showed a subacromial bursitis with fibrous adhesions and a complete tendon healing. We performed a S/A bursectomy, removal of adhesions and tendon stimulation with low radiofrequency (Fig. 5e, f).
The patient followed the standard postoperative program and he had slight pain for 3 years, especially during work activity. At the last FU examination in December 2013 (8 years) the CS was 87 and SST had 10/12 “yes” responses.
CT of the shoulder is a widespread clinical condition with a significant impact on patient’s quality of life. Although several treatments have been proposed, the best option to choose is still controversial [12–16]. Extracorporeal shock wave therapy (ESWT) has been described to be effective [13, 14], but a long-term follow-up study showed that about 20 % of the patients treated have required surgery . US-guided needling, irrigation and aspiration may reduce pain and stimulate calcium resorption , while a surgical approach is suggested in cases with persistent disabling symptoms for at least 6 months . Some case-series studies reported good results with partial removal of the calcific deposits, so as to preserve the integrity of the tendon [17, 18]. However, in cases with arthroscopic removal of large and deep calcific deposits, it is recommended to repair the defect with side-to-side sutures or anchors [16, 18]. Recurrence is a known complication following surgical excision of calcific deposits of the shoulder with an incidence reported between 16 % and 18 % , but to our knowledge, there is no description of recurrence in the form of OT. Tendon involvement by HO was found in 26.7 % of patients after shoulder surgery and 80 % of these occurred after RC repair and acromioplasty, but the presence of ossifications seemed to be of minor clinical impact [7, 8, 20, 21].
In a case series of 892 patients treated with acromioplasty and distal clavicle resection, Berg et al.  reported 5 % with ectopic bone formation, including sites like S/A space, acromio-clavicular joint, coraco-acromial ligament and coraco-clavicular ligament: around 3.2 % of them were symptomatic.
HO of the deltoid muscle  and supraspinatus tendon  has also been described following open RC repair. The first was managed with resection of pathologic bone and soft tissue contracture by open interval release and manipulation followed by radiation therapy; in the second case the authors did not perform any additional surgery but they described the association with axillary nerve palsy and they highlighted that there were several risk factors present, including two operations within 2 months, smoking and chronic pulmonary disease. In fact, it has been postulated that hypoxia may drive metaplasia in bone-forming cells in patients who are chronic smokers and continue smoking in the peri-operative period and in patients suffering from chronic pulmonary diseases [22, 23].
The mechanism of origin of bone metaplasia in the RC tendon with calcium deposits is unknown, but some aspects of this phenomenon can be interpreted through the findings already known to us. The presence of resident progenitor cells with multi-differentiation potential in the human tendon  and local release of bone morphogenic proteins (BMP) which helps in differentiation of pluripotent mesenchymal cells into osteoblasts [25, 26] has been noted after acromioplasty and in cases with degenerated cuff tissue; these biologic changes may thus induce ectopic bone formation [22, 27]. Ectopic chondrogenesis and ossification have been reported in the patellar calcific tendinopathy rat model and to a lesser extent, in the traumatic patellar tendon injury model . The authors detected BMP-2 protein in the chondrocyte-like cells and calcific deposits in both injury models but not in control samples, indicating that BMP-2 might be involved in the pathogenesis of ectopic chondrogenesis and ossification. HO is common after traumatic injuries requiring prolonged immobilization and rigorous passive physiotherapy  or can be associated with other specific rheumatic conditions . An additional predisposing factor for HO is an altered balance within the autonomic nervous system, as seen in brain, spinal cord or peripheral nerve injury . Finally, it can develop after minimally invasive surgery and arthroscopy, but the incidence is less common than after open shoulder surgery . The dilution of osteoinductive marrow elements with irrigation fluid and also its continuous washout may be implicated in its formation . We accurately investigated overall features of both our patients but we didn’t find any of the supposed risk factors which are implicated in HO. Both patients were non-smokers with no history of any chronic neurological or internal diseases, and surgeries were performed arthroscopically without pre- or postoperative nerve involvement. The patients followed a protocol of physiotherapy as standardized for all our cases of CT arthroscopically managed. No significant anthropometric difference was found comparing the two patients, nor did they have a family history of inflammatory osteoarthritis, connectivitis or other rheumatic or metabolic disorders; both were employed with no potential habits (smoking, alcohol, drugs, dietary behaviour) or work-related risk factors.
In both cases the RC was involved with severe pain and functional impairment that required an arthroscopic second look to ascertain the origin and the characteristics of the mass.
During the surgical procedure of case 1 we found a formation of hard consistency above and partly within the supraspinatus tendon at the same site the first calcific deposit was removed from; in case 2 we found similar macroscopic characteristics of the ossification, with a tendency to infiltrate the tendon. The histologic features showed in both cases areas of chondrometaplasia and ossification that were diagnosed as a particular form of OT, without supposing such a kind of evolution before the intraoperative assessment.
The ossifications found above and within the substance of the tendon may be the result of a transformation of mesenchymal cells to bone-forming cells in response to the surgical excision of the calcium deposit and suturing of the tendon during the arthroscopic procedure.
Our preference for complete, meticulous excision of the mass might help avoid further recurrence of the ossifying mass. The long-term follow-up of the two cases described in this study showed no clinical or radiological recurrence of the deposits. Although the surgical approach may have been the trigger event inducing the chondrometaplasia, we have not enough data to support this speculative hypothesis, nor can we rule out that the ossification and cartilaginous metaplasia could be the natural evolution of the case. The surgical findings described in this study led us to consider with caution arthroscopic excision of calcium deposits and to be meticulous during the subacromial debridement of calcific foci to minimize the risk of recurrence. We do believe that the description of these two rare cases of OT will be useful to include this condition as a further complication of CT and also to consider the shoulder as an additional potential site of OT.
Conflict of interest
Both patients provided informed consent to the publication of their clinical cases.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.
- Painter CF (1907) Subdeltoid bursa. Bost Med Surg J 156:345–349View ArticleGoogle Scholar
- Codman EA (1909) Bursitis subacromialis, or periarthritis of the shoulder joint. Publications of the Mass Gen Hospital in Boston 2:521–591Google Scholar
- Sandstrom C (1938) Peritendinitis calcarea: common disease of middle life: it’s diagnosis, pathology and treatment. Am J Roentgenol 40:1–21Google Scholar
- DeSeze S, Welfing J (1970) Calcifying tendinitis. Rheumatologie 22:45–50Google Scholar
- Bosworth B (1941) Calcium deposits in the shoulder and subacromial bursitis: a survey of 12,122 shoulders. JAMA 116:2477–2482View ArticleGoogle Scholar
- Uhthoff HK, Sarkar K, Maynard JA (1976) Calcifying tendinits: a new concept of its pathogenesis. Clin Orthop Relat Res 118:164–168PubMedGoogle Scholar
- Ozaki J, Kugai A, Tomita Y, Tamai S (1992) Tear of an ossified rotator cuff of the shoulder. A case report. Acta Orthop Scand 63:339–340PubMedView ArticleGoogle Scholar
- Erggelet C, Eggensperger G, Steinwachs M, Lahm A, Reichelt A (1999) Postoperative ossification of the shoulder. Incidence and clinical impact. Arch Orthop Trauma Surg 119:168–170PubMedView ArticleGoogle Scholar
- Ahmed SI, Burns TC, Landt C, Hayda R (2013) Heterotopic ossification in high-grade open fractures sustained in combat: risk factors and prevalence. J Orthop Trauma 27:162–169PubMedView ArticleGoogle Scholar
- Richards PJ, Braid JC, Carmont MR, Maffulli N (2008) Achilles tendon ossification: pathology, imaging and aetiology. Disabil Rehabil 30:1651–1665PubMedView ArticleGoogle Scholar
- Gallinet D, Dietsch E, Barbier-Brion B, Lerais JM, Obert L (2011) Suture anchor reinsertion of distal biceps rupture: clinical results and radiological assessment of tendon healing. Orthop Traumatol Surg Res 97:252–259PubMedView ArticleGoogle Scholar
- Krasny C, Enenkel M, Aigner N, Wlk M, Landsiedl F (2005) Ultrasound-guided needling combined with shock-wave therapy for the treatment of calcifying tendonitis of the shoulder. J Bone J Surg Br 87:501–517View ArticleGoogle Scholar
- Moretti B, Garofalo R, Genco S, Patella V, Mouhsine E (2005) Medium energy shock wave therapy in the treatment of rotator cuff calcifying tendonitis. Knee Surg Sports Traumatol Arthrosc 13:405–410PubMedView ArticleGoogle Scholar
- Daecke W, Kusnierczak D, Loew M (2002) Long-term effects of extracorporeal shockwave therapy in chronic calcific tendinitis of the shoulder. J Shoulder Elbow Surg 11:476–480PubMedView ArticleGoogle Scholar
- Sconfienza LM, Bandirali M, Serafini G, Lacelli F, Aliprandi A, Di Leo G et al (2012) Rotator cuff calcific tendinitis: does warm saline solution improve the short-term outcome of double-needle US-guided treatment? Radiology 262:560–566PubMedView ArticleGoogle Scholar
- Porcellini G, Paladini P, Campi F, Paganelli M (2004) Arthroscopic treatment of calcifying tendinitis of the shoulder: clinical and ultrasonographic follow-up findings at two to five years. J Shoulder Elbow Surg 13:503–508PubMedView ArticleGoogle Scholar
- Seil R, Litzenburger H, Kohn D, Rupp S (2006) Arthroscopic treatment of chronically painful calcifying tendinitis of the supraspinatus tendon. Arthroscopy 22:521–527PubMedView ArticleGoogle Scholar
- Yoo JC, Park WH, Koh KH, Kim SM (2010) Arthroscopic treatment of chronic calcific tendinitis with complete removal and rotator cuff tendon repair. Knee Surg Sports Traumatol Arthrosc 18:1694–1699PubMedView ArticleGoogle Scholar
- Wittenberg RH, Rubenthaler F, Wolk T et al (2001) Surgical or conservative treatment for chronic rotator cuff calcifying tendinitis — a matched pair analysis of 100 patients. Arch Orthop Trauma Surg 121:56–59PubMedView ArticleGoogle Scholar
- Matsumoto I, Ito Y, Tomo H, Nakao Y, Takaoka K (2005) Case reports: ossified mass of the rotator cuff tendon in the subacromial bursa. Clin Orthop Relat Res 437:247–250PubMedView ArticleGoogle Scholar
- Degreef I, Debeer P (2006) Heterotopic ossification of the supraspinatus tendon after rotator cuff repair: a case report. Clin Rheumatol 25:251–253PubMedView ArticleGoogle Scholar
- Berg EE, Ciullo JV (1995) Heterotopic ossification after acromioplasty and distal clavicle resection. J Shoulder Elbow Surg 4:188–193PubMedView ArticleGoogle Scholar
- Sanders BS, Wilcox RB 3rd, Higgins LD (2010) Heterotopic ossification of the deltoid muscle after arthroscopic rotator cuff repair. Am J Orthop (Belle Mead NJ) 39:e67–e71Google Scholar
- Salingcarnboriboon R, Yoshitake H, Tsuji K, Obinata M, Amagasa T, Nifuji A, Noda M (2003) Establishment of tendon derived cell lines exhibiting pluripotent mesenchymal stem cell-like property. Exp Cell Res 287:289–300PubMedView ArticleGoogle Scholar
- Buring K (1975) On the origin of cells in heterotopic bone formation. Clin Orthop Relat Res 110:293–302PubMedView ArticleGoogle Scholar
- Craven PL, Urist MR (1971) Osteogenesis by radioisotope labelled cell populations in implants of bone matrix under influence of ionising radiation. Clin Orthop Relat Res 76:231–233PubMedView ArticleGoogle Scholar
- Neuwirth J, Fuhrmann RA, Veit A, Aurich M, Stonans I, Trommer T, Hortschansky P, Chubinskaya S, Mollenhauer JA (2006) Expression of bioactive bone morphogenetic proteins in the subacromial bursa of patients with chronic degeneration of the rotator cuff. Arthritis Res Ther 8:R92PubMedPubMed CentralView ArticleGoogle Scholar
- Lui PP, Chan LS, Cheuk YC, Lee YW, Chan KM (2009) Expression of bone morphogenetic protein-2 in the chondrogenic and ossifying sites of calcific tendinopathy and traumatic tendon injury rat models. J Orthop Surg Res 21(4):27View ArticleGoogle Scholar
- Mader R, Buskila D, Verlaan JJ, Atzeni F, Olivieri I, Pappone N, Di Girolamo C et al (2013) Developing new classification criteria for diffuse idiopathic skeletal hyperostosis: back to square one. Rheumatology (Oxford) 52:326–330View ArticleGoogle Scholar
- Fuller DA, Mani US, Keenan MA (2013) Heterotopic ossification of the shoulder in patients with traumatic brain injury. J Shoulder Elbow Surg 22:52–56PubMedView ArticleGoogle Scholar
- Kircher J, Martinek V, Mittelmeier W (2007) Heterotopic ossification after minimally invasive rotator cuff repair. Arthroscopy 23:1359.e1–1359.e3View ArticleGoogle Scholar