An assessment of porcine dermal xenograft as an augmentation graft in the treatment of extensive rotator cuff tears

An assessment of porcine dermal xenograft as an augmentation graft in the treatment of extensive rotator cuff tears Sachin P. Badhe, MBBS, MS (Orthopaedics), MRCS,a Tom M. Lawrence, MBBS, MD, MSc, MRCS,b F. D. Smith, FRCR,c and P. G. Lunn, FRCS (Orthopaedics),d Derby and Nottingham, United Kingdom

Porcine dermal collagen (Zimmer Patch, formerly known as Permacol; Tissue Science Laboratories plc, Aldershot, Hampshire, UK) has been used for reinforcement of several human body tissues with success and has been shown to act as a durable, permanent tissue scaffold that assists healing. The purpose of this study was to determine the effectiveness of porcine dermal collagen as a tendon augmentation graft in the repair of extensive rotator cuff tears. This prospective study evaluated the clinical, ultrasound, and magnetic resonance imaging outcome 4.5 years (range, 3-5 years) after the treatment of extensive rotator cuff tears with porcine dermal collagen tendon augmentation grafting. The study group consisted of 10 patients (5 men, 5 women) with a mean age of 66 years (range, 46-80 years). Patients were evaluated clinically using the Constant score preoperatively, at 1 year, and at final follow-up when ultrasound and magnetic resonance imaging scans were performed to assess for graft and rotator cuff integrity. Average Constant scores improved from 41 preoperatively to 62 at final followup ( P ¼ .0003). Pain, abduction power, and range of motion significantly improved after surgery ( P < .05), and patient satisfaction levels were high. Imaging studies identified intact grafts in 8 patients and graft detachment in 2. No adverse side effects were reported during the study period. The use of porcine dermal collagen as an augmentation graft in the treatment of massive rotator cuff tears is safe and, in most patients, is associated with improved clinical outcome. Randomized trials are required to assess any benefit From the aDepartment of Trauma and Orthopaedic Surgery, Derbyshire Royal Hospital; bPrivate practice; and cDepartments of Radiology and dOrthopaedics, Derbyshire Royal Infirmary. Reprint requests: Sachin P Badhe, Department of Trauma and Orthopaedic Surgery, Derbyshire Royal Hospital, London Rd, Derby, DE1 2QY, UK (E-mail: [email protected]). Copyright ª 2008 by Journal of Shoulder and Elbow Surgery Board of Trustees. 1058-2746/2008/$34.00 doi:10.1016/j.jse.2007.08.005

over standard current surgical treatment regimens. (J Shoulder Elbow Surg 2008;17:35S-39S.)

T

he treatment of symptomatic extensive rotator cuff tears, defined as irreparable massive and large tears, presents a challenging problem in shoulder surgery. Traditional repair techniques are associated with high rupture rates due to excessive tension4 on the repair and the presence of degenerated tendon tissue, which has poor healing potential.13 Patients with failed repairs have been shown to have inferior clinical outcomes compared with those with intact repairs.7 These factors have led to attempts to reconstruct the rotator cuff with grafts, using synthetic materials16,19 or biologic tissues. Autograft biceps tendon,17 fascia lata,9 and allograft freeze dried rotator cuff,18 or patellar tendon14 have been attempted in the past with varied results. Recently, several commercially available tissue-engineered allografts and xenografts have been developed to augment rotator cuff repairs. Such implants should function to provide a stronger repair in the presence of poor quality tissue and act as a bridging scaffold upon which host healing may occur where there are deficiencies. Zimmer patch, formerly known as Permacol (Tissue Science Laboratories plc, Aldershot, Hampshire, UK), is a tough, flexible flat sheet of acellular, cross-linked, porcine dermal collagen and its constituent elastin fibers have been sterilized by gamma irradiation.6 Cross-linking provides resistance to collagenase enzymes that are responsible for the breakdown and resorption of implanted collagen.10 After implantation, the patch supports fibroblast infiltration and revascularization so that it gradually becomes incorporated into the surrounding tissue, providing strength and support while inhibiting wound contraction through scarring. It has been used successfully for the reconstruction of human soft connective tissue, where loss of dermis has occurred, and as a supporting tissue in numerous gynecologic, urologic, and general surgical procedures involving the treatment of abdominal wall defects, stress incontinence, and vaginal prolapse.1,3,11,15

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Figure 1 A, Before rotator cuff repair. B, Augmentation with porcine dermal collagen graft.

Zimmer patch is fully licensed in Europe and the United States for the reinforcement of rotator cuff repairs but, to our knowledge has not been assessed in a clinical study. The aim of this study was to assess prospectively the clinical and radiologic results in a group of patients with extensive rotator cuff tears treated operatively with a porcine dermal collagen augmented repair. MATERIALS AND METHODS This prospective study was set in a district general hospital and received Regional Ethics Committee approval. All patients provided informed consent for entry into the study. The study recruited 10 consecutive patients with extensive rotator cuff tear treated between January 2000 and December 2002. The diagnosis was by ultrasound scanning in 7 patients and by magnetic resonance imaging (MRI) in 3. The rotator cuff tears were at least 5 cm in size and involved both the supraspinatus and infraspinatus tendons. None of these patients had responded to a previous trial of nonoperative management, including physiotherapy and steroid injections. All were incapacitated mainly by pain, and decreased function was a secondary complaint. All patients were evaluated with preoperative and postoperative Constant and Murley scores and completed a shoulder questionnaire designed to assess satisfaction and return to activities of leisure and daily living. The study group consisted of 5 men and 5 women, with a mean age of 66 years (range 46-80 years). Operations were done on 6 right and 4 left shoulders, of which 8 were the dominant side. Two patients had previously undergone attempted, but failed, repairs on the ipsilateral shoulder, 1 with a Vicryl graft (Johnson & Johnson, UK) and the other using Panacryl (Ethicon) suture. The mean preoperative Constant score was 42.

Operative technique Patients were placed in the beach chair position and general or regional anesthesia was used. The shoulder was approached using either a bra-strap or superolateral inci-

sion. After careful detachment of the deltoid from the anterior acromion, open subacromial decompression was performed in all cases using an oscillating saw. The edges of the rotator cuff tear were identified, de´brided, and mobilization was attempted, confirming that primary repair was not possible without excessive tension due to tendon retraction. The porcine dermal collagen patch was then contoured to an appropriate size, corresponding to the remaining defect, and sutured with No 2 Ethibond suture (Ethicon, Johnson & Johnson, UK) using a modified Kessler technique to the retracted cuff edges. Soft tissue de´bridement was performed at the area of insertion of the rotator cuff on the humeral head, and an osseous groove was created. Two 2-mm drill holes were made in the groove to emerge on the lateral aspect of the greater tuberosity, allowing the passage of intraosseous No 2 Ethibond sutures. The sutures were tied to secure the patch into the groove under appropriate tension (Figure 1). To protect the repair postoperatively, the arm was maintained in a splint with 30 abduction and neutral rotation for 6 weeks, which was standard protocol for cuff repairs done at the time of the study. All patients were discharged home on the first postoperative day, with supervised passive range of motion exercises commenced immediately in an attempt to reduce capsular contractures. A wound evaluation was performed at 2 weeks. Supervised active movements were commenced at 6 weeks and increased at 3 months to strengthening exercises. Further follow-up occurred at 12 months, and a final review was made on average 4.5 years (range, 3-5 years) years after surgery. All patients completed a questionnaire, and single observer assessed Constant scores. Abduction strength was determined using the Nottingham myometer with the arm abducted and the patient seated. Ultrasound and MRI scans were performed at the final follow-up to assess the integrity of the graft and rotator cuff. All imaging studies were done and assessed by a senior musculoskeletal radiologist, who was blinded to the clinical results. The graft was considered to be intact when it was seen clearly at the insertion site over the greater tuberosity. Graft disruption was defined as an identifiable gap between the greater tuberosity and the graft.

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Table I Outcomes as assessed by Constant scores and imaging studies Constant scores Patient No

Age, y

Dominant limb

Operated limb

Follow-up, y

1 2 3 4 5 6 7 8 9 10 Mean

55 70 80 46 62 80 57 71 67 69 65.7

R R L R L L R R R R

L R L L L R R R R R

5 5 4 5 5 5 5 4.5 4 3

Pre-op

1-year

Final follow-up

Control shoulder

50 78 45 13 29 52 26 37 41 44 41.5

60 97 53 61 52 70 50 51 70 61 62.5

74 80 76 56 35 73 50 49 68 61 62.2

76 80 77 61 44 76 23 56 68 53 61.4

US scan

MRI

Intact Intact Intact Intact Disruption Intact Intact Intact Disruption Intact

Intact Intact Unable Intact Error Intact Intact Intact Disruption Intact

MRI, Magnetic resonance imaging; US, ultrasound.

Statistical analysis of preoperative and postoperative Constant scores was performed using the paired t test. A value of P < .05 was considered to be significant.

RESULTS No intraoperative or postoperative complications occurred. The mean Constant score improved significantly from 42 preoperatively to 63 at 1 year (P ¼ .0003; Table I). The trend was maintained at final follow-up at 3 to 5 years with a score of 62, which was comparable to the 61 score in the contralateral shoulder at final follow-up. All patients experienced significant pain relief. The mean preoperative pain score improved from 7 to 14 out of 15 at 1 year, which was the same at final followup (P ¼ .0003). Abduction power improved significantly from a preoperative mean of 6.3 kg to 10.3 kg at 1 year (P ¼ .05). It was noted to have decreased slightly to 9.8 kg at the final follow-up, but the difference was no longer significant (P ¼ .1). Range of motion significantly improved postoperatively at 1 year and at final follow-up in internal and external rotation and abduction. Forward flexion compared better with preoperative status, but this was not statistically significant. Mean active abduction was 89 , and mean passive abduction was 98 . The mean internal rotation was to T12. Mean active and passive external rotations with the arm at the side were 50 and 52 , respectively. The mean active external rotation with the abducted arm was 49 . Satisfaction levels were high after surgery on the basis of the questionnaire (Table II). All patients were able to perform daily activities of living, such as brushing their hair, and to return to leisure activities, such as playing golf. There was only 1 dissatisfied patient, who was pain free. However, despite an initial improvement in Constant score from 29 preoperatively

Table II Subscore values of Constant score assessment Subscores Constant score Activities of daily living Pain Strength, kg

Pre-op

Final follow-up

P

41.5 5.3

62.2 6.2

.0004 .3

6.8 6.3

14 9.8

.00003 .1

to 52 at 1 year, this subsequently fell to 35 at final follow-up, and graft failure was confirmed on both ultrasound and MRI scans. Ultrasound imaging at the final follow-up showed 8 of the 10 grafts were intact and 2 graft disruptions. Two patients could not complete MRI studies owing to claustrophobia. The MRI results of the remaining patients were comparable with those of the ultrasound scan (Figure 2). The other patient, with a demonstrated graft failure, had an improvement in Constant score from 41 preoperatively to 70 at 1 year postoperatively and 68 at the final follow-up. DISCUSSION Unreliable clinical results and high failure rates of repairs of extensive rotator cuff tears have stimulated interest in use of either synthetic or tissue grafts to augment surgical repair and facilitate tendon healing. Porcine dermal collagen patch offers an alternative for this purpose, but although it has been assessed for use in humans in the reconstruction of other tissues, to our knowledge there are no reports relating to rotator cuff repair. The results from this study suggest that repair augmented with porcine dermal collagen is an effective method in the treatment of chronic, extensive tears of

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Figure 2 A, A transverse section ultrasound scan shows the intact graft (arrow). B, A longitudinal section shows the intact graft (arrow)

rotator cuff. Only 2 of 10 patients were shown to have radiologic evidence of graft failure at 3 to 5 years after surgery. Constant scores improved significantly from 41 preoperatively to 62 at an average of 4.5 years. Pain scores, abduction strength, and range of motion also improved significantly, and satisfaction levels were high. There were no complications directly related to the use of the porcine dermal graft, and in particular, there was no evidence of tissue rejection. In contrast to our findings, other authors have demonstrated unfavorable rates of tendon healing, rupture rates, and clinical outcome scores with the use of a porcine small intestine submucosa (SIS) graft to augment massive rotator cuff repairs. Sclamberg et al20 found that 10 of 11 porcine SIS repairs had failed at 6 months postoperatively on MRI and recommended its use be discontinued. In a recent randomized controlled trial, Iannotti et al8 found a trend toward worse outcomes in a group augmented with porcine SIS grafts compared with a nonaugmented group. They suggested that the potential biologic value of the porcine SIS graft was lost owing to early resorption, leading to mechanical weakening and failure. In vitro mechanical tests have since demonstrated that dermal-based xenografts are not only stronger than mucosal products but also less liable to fail due to suture pull-out.2 The mechanical advantages of porcine dermal collagen patch over porcine SIS, which relate to the presence of collagen cross-linking, provide an explanation for the better results obtained in the current study. Furthermore, as evidenced by an absence of adverse clinical reactions in this series, porcine dermal collagen graft is nonallergenic, nontoxic, and does not elicit a foreign body response. It is, therefore, less likely to fail in the early postoperative

period. This is in contrast to porcine SIS, which has been shown to elicit inflammatory reactions requiring open de´bridement in up to 16% of rotator cuff repairs.12 The strengths of the current study include the mean duration of follow-up of 4.5 years, with a minimum of 3 years. We believe that this provides a long enough review period to consider the graft successful and surgery to be beneficial to the patient. The outcome measures, in the form of Constant scores and rotator cuff imaging with ultrasound and MRI, provide a prospective objective assessment. However, it became apparent during the study that the postoperative MRI was of limited diagnostic quality owing to poor patient tolerance in this relatively elderly cohort of patients, and additional measurements could not be performed because of the relative poor resolution. Therefore, ultrasound was used as an adjunct for interpretation. The imaging modalities used could only assess graft integrity. We believe that better quality preoperative and postoperative MR images, including arthrography, would have provided useful information about muscle fatty infiltration and bulk. The small number of patients in this study is a limitation. Furthermore, in the absence of a control group, it is uncertain how much the use of the porcine graft improved outcome. Improvements were most notable in relation to pain, and subacromial decompression may, in itself, have provided a significant contribution to pain relief as well as small secondary gains in strength and function. A randomized control trial with larger numbers is required to assess the effectiveness of porcine dermal collagen as an augmentation graft in the treatment of extensive rotator cuff tears. In addition, in vivo animal histologic and biomechanical

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studies, similar to those that have been performed for porcine SIS,5,21 would provide useful quantitative information about the efficacy of the graft to augment tendon healing and enhance mechanical strength. In conclusion, we believe that porcine dermal collagen is effective as an augmentation graft in the treatment of chronic extensive rotator cuff tears, providing excellent pain relief with a moderate improvement in active ranges of motion and strength. REFERENCES

1. Adedeji OA, Bailey CA, Varma JS. Porcine dermal collagen graft in abdominal-wall reconstruction. Br J Plast Surg 2002;55:85-6. 2. Barber FA, Herbert MA, Coons DA. Tendon augmentation grafts: biomechanical failure loads and failure patterns. Arthroscopy 2006;22:534-8. 3. Barrington JW, Dyer R, Bano F. Bladder augmentation using Pelvicol implant for intractable overactive bladder syndrome. Int Urogynecol J Pelvic Floor Dysfunct 2006;17:50-3. 4. Davidson PA, Rivenburgh DW. Rotator cuff repair tension as a determinant of functional outcome. J Shoulder Elbow Surg 2000;9: 502-6. 5. Dejardin LM, Arnoczky SP, Ewers BJ, et al. Tissue-engineered rotator cuff tendon using porcine small intestine submucosa. Histologic and mechanical evaluation in dogs. Am J Sports Med 2001;29: 175-84. 6. Harper C. Permacol: clinical experience with a new biomaterial. Hosp Med 2001;62:90-5. 7. Harryman DT 2nd, Mack LA, Wang KY, et al. Repairs of the rotator cuff. Correlation of functional results with integrity of the cuff. J Bone Joint Surg Am 1991;73:982-9. 8. Iannotti JP, Codsi MJ, Kwon YW, et al. Porcine small intestine submucosa augmentation of surgical repair of chronic two-tendon rotator cuff tears. A randomized, controlled trial. J Bone Joint Surg Am 2006;88:1238-44.

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9. Ito J, Morioka T. Surgical treatment for large and massive tears of the rotator cuff. Int Orthop 2003;27:228-31. 10. Jarman-Smith ML, Bodamyali T, Stevens C, et al. Porcine collagen crosslinking, degradation and its capability for fibroblast adhesion and proliferation. J Mater Sci Mater Med 2004;15:925-32. 11. Liyanage SH, Purohit GS, Frye JN, Giordano P. Anterior abdominal wall reconstruction with a Permacol implant. Br J Plast Surg 2005. 12. Malcarney HL, Bonar F, Murrell GA. Early inflammatory reaction after rotator cuff repair with a porcine small intestine submucosal implant: a report of 4 cases. Am J Sports Med 2005;33:907-11. 13. Matthews TJ, Hand GC, Rees JL, et al. Pathology of the torn rotator cuff tendon. Reduction in potential for repair as tear size increases. J Bone Joint Surg Br 2006;88:489-95. 14. Moore DR, Cain EL, Schwartz ML, Clancy WG Jr. Allograft reconstruction for massive, irreparable rotator cuff tears. Am J Sports Med 2006;34:392-6. 15. Moore RD, Miklos JR, Kohli N. Rectovaginal fistula repair using a porcine dermal graft. Obstet Gynecol 2004;104:1165-7. 16. Mura N, O’Driscoll SW, Zobitz ME, et al. Biomechanical effect of patch graft for large rotator cuff tears: a cadaver study. Clin Orthop Relat Res 2003:131-8. 17. Neviaser JS. Ruptures of the rotator cuff of the shoulder: new concepts in the diagnosis operative treatment of chronic ruptures. Arch Surg 1971;102: 483–85. 18. Neviaser JS, Neviaser RJ, Neviaser TJ. The repair of chronic massive ruptures of the rotator cuff of the shoulder by use of a freezedried rotator cuff. J Bone Joint Surg Am 1978;60:681-4. 19. Ozaki J, Fujimoto S, Masuhara K, et al. Reconstruction of chronic massive rotator cuff tears with synthetic materials. Clin Orthop Relat Res 1986:173-83. 20. Sclamberg SG, Tibone JE, Itamura JM, Kasraeian S. Six-month magnetic resonance imaging follow-up of large and massive rotator cuff repairs reinforced with porcine small intestinal submucosa. J Shoulder Elbow Surg 2004;13:538-41. 21. Zalavras CG, Gardocki R, Huang E, et al. Reconstruction of large rotator cuff tendon defects with porcine small intestinal submucosa in an animal model. J Shoulder Elbow Surg 2006;15:224-31.