Introduction

The proximal humerus is a common site of primary and metastatic tumours of bone [1, 2]. Advances in diagnostic imaging techniques and surgical interventions have allowed limb salvage in the treatment of bone tumours of the proximal humerus [2, 3]. However, functional reconstruction following tumour resection has been a surgical challenge because of surgical loss of functional soft tissues including shoulder joint capsule and rotator cuff tendons. The remaining rotator cuff tendons and capsule are usually functionless because their points of insertion on the humerus are resected. At present, the most commonly used functional reconstruction techniques following proximal humeral resection include osteoarticular allografts (OA) [4, 5], allograft-prosthesis composites (APC) [6, 7], and endoprosthesis (EP) reconstruction [2, 3, 8, 9]. Additional techniques such as Tikhoff-Linberg resection [10], fibular transplants [11] and shortening arthrodeses [12] were also used for shoulder construction. Of these commonly used techniques, EP reconstruction is considered more suitable for reconstruction of large bone defect after proximal humeral resection because of lower complication rates, higher implant survival and comparable functional results [13, 14]. Although the incidence of complications, such as infection, fracture and prosthesis loosening, is low, glenohumeral joint instability occurs in approximately 55 % of patients with EP reconstruction surgery [15].

To reduce the rate of joint instability and facilitate the remaining soft tissue reattachment, multiple biomaterials such as polyethylene terephthalate (PTT) tube [16] and expanded polytetrafluoroethylene (ePTFE) tube [17] have been used to reconstruct destroyed capsule and promote soft tissue reattachment in previous clinical practice. However, these biomaterials have small pore sizes, which may prevent ingrowth of surrounding soft tissues and subsequent biomaterials–soft tissue incorporation [18, 19]. In this study, a macroporous biomaterial, a polypropylene (PPP) mesh widely used in general surgery as a patch for the treatment of ventral hernia [20], was used to reconstruct shoulder joint capsule and promote soft tissues reattachment after tumour resection. We here describe (a) a detailed shoulder joint capsule reconstruction procedure using a PPP mesh, (b) functional outcomes of patients who underwent this procedure and (c) the complications associated with the use of the device.

Patients and methods

Clinical data

Eighteen patients (eight men, ten women; mean age, 29.8 years; range 18–67 years) who underwent endoprosthetic replacement of the proximal humerus and capsule reconstruction using PPP meshes between March 2005 and October 2010 were enrolled in this study. All patients underwent preoperative plain radiography (PR), computerized tomography (CT) and magnetic resonance imaging (MRI) and/or electrical capacitance tomography (ECT) bone scan. Patients with soft tissue sarcomas or bone tumours of the clavicle, scapula, or only the humeral diaphysis were excluded. This study included only patients who had a bone lesion of the proximal aspect of the humerus. The pre- and post-operative (two weeks after reconstruction procedure) pain severity was assessed according to a 10-cm visual analogue scale (VAS), and functional improvement at the time of final follow-up was assessed using the Musculoskeletal Tumour Society (MSTS) function score.

The pathological diagnoses of all patients were obtained by pre-operative needle biopsy. These diagnoses included osteosarcoma (six patients), chondrosarcoma (five patients), Ewing sarcoma (two patients), multiple myeloma (one patient), malignant fibrous histiocytoma (one patient), large B cell lymphoma (one patient), and metastatic bone tumours involving the humerus (breast cancer, two patients). According to the Malawer classification of shoulder girdle resections, all patients enrolled in this study had type IA or IB resection. The surgical stage [21] was as follows: two patients stage IA, three patients stage IB, seven patients stage IIA and six patients stage IIB (Table 1). Of these 18 patients, the endoprosthesis-PPP mesh composite was used as the initial reconstructive technique following primary resection of the tumour in 12 patients (12/18) and as a revision procedure in six patients (6/18) (four patients underwent pure endoprosthesis reconstruction, two patients underwent osteoarticular allografts reconstruction).

Table 1 Summary data for all patients
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To obtain a clear surgical margin and long-term survival prognosis, 13 patients (13/18, 72.2 %) with osteosarcoma, Ewing sarcoma, multiple myeloma, large B cell lymphoma, malignant fibrous histiocytoma and oligometastasis received pre-operative systemic neoadjuvant, adjuvant chemotherapy or chemotherapy. Two patients (2/18, 11.1 %) with Ewing sarcoma also received pre-operative adjuvant radiotherapy. Fifteen patients (15/18, 83.3 %; osteosarcoma, six patients; Ewing sarcoma, two patients; malignant fibrous histiocytoma, one patient; multiple myeloma, one patient; large B cell lymphoma, one patient; oligometastasis, two patients; chondrosarcoma, two patients) received postoperative chemotherapy. Although drug resistance often occurred in patients with chondrosarcoma, two patients received adjuvant chemotherapy according to the oncologist’s suggestion in this study (Table 1).

Materials

The proximal humerus endoprostheses were customized and produced (LDK, Co., Ltd) according to the pre-operative design based on PR diagnostic imaging and MR imaging. The nonabsorbable PPP mesh and nonabsorbable sutures used for anchoring mesh are from Johnson & Johnson, Ltd.

The PPP mesh (PROLENE® light mesh) (Ethicon, USA) is a synthetic nonabsorbable porous mesh which is constructed of knitted filaments of extruded polypropylene. In previous studies, these nonabsorbable meshes were often used to repair ventral hernia and fascial truck defects [22]. The synthetic porous mesh used in this study was 15 × 15 cm² and 0.5 mm thick, and can be cut into any desired shape or size according to the intra-operative planning.

Surgical technique

The study was approved and monitored by the Human Research Ethical Committee of our hospital. All patients were allowed to weigh the risks and benefits of endoprosthesis-PPP mesh composites reconstruction as a new method before signing informed consent.

All reconstruction surgeries were performed by an experienced orthopaedic oncologist (Z.W.S.), and the surgical procedures were performed through an anterior approach as described by Marulanda et al. [17] and Neer et al. [23]. After general anaesthesia, an incision was made from the palpable landmark of the coracoid process to the skin overlying the deltopectoral interval, and extended distally depending on the expected level of humeral resection. Soft tissue dissection was dependent on the presence or absence of tumour compromise, and the previous biopsy track and haematoma were excised in continuity with removed soft tissues. A jigsaw was used to make the osteotomy when the proposed level of humeral resection was identified. The remaining rotator cuff tendons and joint capsule were identified and tagged. For the patients who undergo type IA resection, protection of the axillary nerve is critical during the whole surgery. The resected specimens were sent for pathology analysis and confirmation of disease-free remaining bone.

A proper circular hole was prepared in the centre of the PPP mesh, and the whole edge of the central hole was reinforced by nonabsorbable suture (Fig. 1). As it shows in Fig. 2, the edge was then anchored and sutured to the remaining articular capsule and glenoid labrum of the glenohumeral joint. After proper location of the endoprosthesis, the endoprosthesis was cemented in place and wrapped by the free end of the PPP mesh (Figs. 3 and 4). Then the tagged rotator cuff tendons and surrounding soft tissues were reattached to the PPP sheath and fully covered the endoprosthesis. After successful hemostasis, the surgical incision was closed and large-bore suction catheter drainage was secured.

Fig. 1
figure 1

The polypropylene (PPP) mesh used for shoulder joint capsule reconstruction. A proper circular hole was prepared according to the dimension of the glenoid, and the whole edge of the central hole was reinforced by nonabsorbable suture

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Fig. 2
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Fixation of polypropylene (PPP) mesh. The reinforced edge was anchored and sutured to the remaining articular capsule and glenoid labrum of the glenohumeral joint

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Fig. 3
figure 3

Reconstruction of shoulder joint capsule. After proper location of the endoprosthesis, it was wrapped by the free end of polypropylene (PPP) mesh

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Fig. 4
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The formation of “polypropylene (PPP) mesh sheath”. The remaining rotator cuff tendons and surrounding soft tissues were sutured to the PPP sheath and covered the endoprosthesis

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Postoperative treatment

All patients received intravenous cephalosporins for the duration of the hospital stay (mean, five days; range three to eight days), and the surgical incisions were carefully monitored. The patients with postoperative pain received the treatment of non-steroidal anti-inflammatory drugs (NSAIDs). Most patients (15/18, 83.3 %) received postoperative chemotherapy or radiotherapy (details listed in Table 1). All patients in this study received the same function exercise program. To facilitate the repair of soft tissues, the reconstructive limb was maintained on an abduction splint for four to five weeks (Fig. 5). Once the abduction splint was removed, continuous passive movements, starting from a small range and gradually increasing to a larger range of motion, were suggested and active movements, such as abduction, flexion, extension, were also encouraged according to the different clinical situations.

Fig. 5
figure 5

A 38-year-old patient with the diagnosis of chondrosarcoma who underwent endoprosthesis-polypropylene (PPP) mesh composite reconstruction surgery. The reconstructive upper limb was maintained on an abduction splint

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Results

Two patients (one patient lost to follow-up and one patient with chondrosarcoma who died of the disease six months after the reconstruction procedure) were excluded from this study. The other 16 cases (16/18) were observed for 30–96 months with an average follow-up of 56 months. Most patients (15/16) experienced some alleviation of pain in two weeks after the reconstruction surgery (VAS, pre VS post; 7.8 ± 1.8 vs. 3.1 ± 1.3). The patient with postoperative pain (1/18) was an 18-year-old woman with a diagnosis of osteosarcoma. The symptom of pain disappeared after three weeks of treatment of NSAIDs and physical therapy. Ten patients (10/18) returned to their occupations within five months.

Functional assessments were performed at the time of final follow-up. The mean MSTS upper extremity functional outcome score was 20 (66.7 %, range, 16–27). Mean shoulder abduction was 36° (range, 18–125°) and mean shoulder flexion was 39° (range, 21–120°). The deltoid muscle, a critical muscle affecting the function and stability of reconstructive shoulder [17, 25], is often involved in the resection. As shown in Table 2, the patients with deltoid muscle resection (13/16, 81 %) had a significantly reduced range of motion in both abduction and flexion as compared with those in whom the deltoid muscle was reserved.

Table 2 Effect of deltoid muscle resection (partial/total) on shoulder joint functional outcomes
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Infection, periprosthetic fracture and shoulder dislocation were not observed in our study. Local recurrence occurred in one patient (1/16) with osteosarcoma, and the patient died of the disease one month after the last follow-up. Prosthesis loosening occurred in one patient (1/16) who often lifted heavy weights, and the patient had to undergo the revision surgery. In one patient (1/16) who underwent endoprosthesis-PPP mesh composite reconstruction as a revision surgery, the prosthetic humeral head moved upward a little three months after operation, and the “anterior subluxations” were not changed at the last follow-up (Table 3).

Table 3 Effect of EP and EP-PPP mesh composite reconstruction on shoulder stability
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Discussion

The shoulder joint has the largest range of motion in the human skeleton, which is closely related with its complex anatomy (including rotator cuff and joint capsule). Previous studies have stated that rotator cuff tendons and capsule are critical for stabilizing the shoulder joint [16, 17, 24]. Once these complex structures are destroyed, it is difficult to repair especially in patients who underwent proximal humeral resection. Advances in surgical interventions and metallic endoprosthesis have permitted orthopaedic oncologists to reconstruct large segments of diseased bone [2, 3, 8, 9, 13, 14]. However, the reattachment of remaining soft tissues after endoprosthesis reconstruction is a challenge because of poor metal–soft tissue adhesion. In the past, many strategies including osteoconductive scaffolds [25], coating of prosthesis with novel materials [26, 27] and predetermined suture sites embedded in the metallic prosthesis [28], have been used to promote soft tissue adhesion and ingrowth. All of these procedures have been associated with joint instability, recurrent dislocation and poor limb function [25–28]. With the development of biomaterials, surgeons have been attempting to reconstruct the destroyed capsule and improve the remaining soft tissue reattachment by biomaterial–soft tissue incorporation [16, 17]. In this study, we introduced a common and cheap biomaterial, a PPP mesh, to reconstruct capsule to reduce/prevent shoulder joint dislocation and instability, and evaluated the postoperative function level and elaborated complications associated with the reconstruction procedure.

Previous studies showed that glenohumeral joint instability and dislocation have a high recurrence rate in patients who underwent EP reconstruction [15, 29–31]. Bos et al. reported five of 18 patients (5/18) suffered dislocations that required revision surgery [30]. Ross et al. reported that 19 of 25 patients (19/25), treated with several different implants, suffered subluxations (16 cases) and dislocations (three cases) [31]. Moreover, five patients received EP reconstruction in our institution before the beginning of this study, and one of them (1/5) suffered dislocation and one (1/5) suffered subluxations (Table 3). Therefore, we postulated that use of an endoprosthesis-PPP mesh composite would decrease shoulder joint dislocation and strengthen its stability after tumour resection of proximal humerus, and we continued using the PPP mesh reconstruction in all patients after the first procedure was performed in March 2005.

In the past, several biomaterials, the PTT tube [16] and ePTFE tube [17], have been used to reconstruct destroyed joint capsules, which significantly reduces the rate of joint instability. Marulanda et al. reported that, of 16 patients treated with endoprosthesis reconstruction supplemented with a synthetic ePTFE tube, only one (1/16) experienced anterior subluxation of the shoulder [17]. Gosheger et al. reported that no cases (0/16) of subluxation or dislocation were observed in 16 patients with endoprosthesis reconstruction supplemented with a synthetic PTT tube [16]. In this series, we used a common and cheap biomaterial, PPP mesh, to reconstruct destroyed shoulder capsule and obtained similar clinical results. As shown in Table 3, only one patient (1/16) suffered anterior subluxations and no cases sustained dislocation. Recently, Ioannou et al. also reported nine of 21 patients (9/21) received the capsule reconstruction using PPP mesh and achieved stable shoulders [32]. Therefore, the PPP mesh may be an alternative for capsule reconstruction. In comparison to PTT and ePTFE tube, the PPP mesh has many potential advantages, such as larger pore size facilitating the reattachment of surrounding soft tissues, excellent plasticity and reasonable price.

In the present study, the mean MSTS upper extremity functional outcome score was 67 %. Mean active shoulder abduction and flexion were 36° and 39°, respectively. These patients in our series showed loss of a range of active motion when compared with that of 16 patients treated with endoprosthesis–ePTFE tube reconstruction in the study by Gosheger et al. [17]. The possible explain is that our patients experienced four to five weeks of abduction fixation on an abduction splint, while the patients in the study of Gosheger et al. began their shoulder passive motion during the hospital stay. Although the functional results are comparable, we think that the functional outcomes depend on many factors, such as different orthopaedic oncologists, tumour type, soft tissue involvement, pre- and post-operative therapy and different function exercise program.

Although these results support our primary hypothesis, this study is limited by the fact that it is a retrospective analysis, small sample and without a control group. All of these defects are associated with relatively rare proximal humerus reconstruction for tumours [13, 16, 17, 33]. Although our experience is very limited, the procedure offers some interesting information. The endoprosthesis reconstruction on the basis of nonabsorbable PPP mesh can significantly reduce the rate of glenohumeral joint instability and dislocation and improve patient’s quality of life.