Malignant tumors of the shoulder girdle are treated with wide local excision and limb salvage surgery because amputative procedures of the shoulder girdle result in a substantial functional impact on the patient. Although limb salvage surgery is the treatment of choice, it is technically challenging not only from an oncological perspective, but also from a reconstructive perspective. Currently, there is a paucity of data examining the long-term outcome of these procedures in terms of patient function and oncological outcome.
The authors have previously reported the short- and mid-term follow-up following limb salvage surgery at their institution showing patients had a satisfactory outcome in terms of pain, use of their limb, and acceptance of the procedure at a mean of 5 years postoperatively.1 The purpose of the current study was to provide an update of the previous series with a focus on only patients with a malignant tumor in terms of disease-specific survival to determine whether there are changes in patient function over time and the need for further reconstructive procedures.
Materials and Methods
Following institutional review board approval, the authors re-examined the medical records of the 57 patients undergoing surgical resection of a malignant or benign destructive bone tumor of the shoulder girdle. Four patients from the original study with a destructive giant cell tumor of the proximal humerus were removed. This cohort included 30 men and 23 women, with a mean age of 35 years (range, 5–71 years) at the time of resection. Limb salvage was performed in all cases.
All of the resections and reconstructions were performed by orthopedic oncology subspecialty surgeons. The resections were classified based on the modification of the Musculoskeletal Tumor Society (MSTS) system by Enneking et al.2 The tumor involved the scapula (n=14, 26%) and the proximal humerus (n=39, 74%). A majority (n=30, 57%) of tumors were considered “high” grade. Patients with documented metastatic disease at presentation (n=4, 8%) were removed from the disease-free survival analysis. Patients most commonly presented with a complaint of shoulder pain (n=50, 94%), with 7 (13%) patients having a pathologic fracture.
The surgical margin3 was described as wide negative in 39 (68%), marginal in 11 (19%), and contaminated in 3 (14%). Of the patients with humeral tumors, mean proximal humeral resection length was 14 cm (range, 0.5–24.5 cm). The most common pathology was chondrosarcoma (n=24, 45%).
To classify the level of resection, the shoulder girdle was divided into 5 sections.1 If the deltoid and rotator cuff were intact, then the resection was classified as an A; however, if they were disrupted, then it was classified as a B. An arthrodesis was performed if the deltoid and rotator cuff were resected.1 Reconstructive techniques following tumor resection included a functional spacer (n=17, 32%), endoprosthesis (n=12, 23%), none (n=9, 17%), arthrodesis (n=8, 15%), osteoarticular allograft (n=6, 11%), and pseudarthrosis (n=1, 2%).
Chemotherapy was administered to 26 (49%) patients within ±3 months of their procedure either preoperative (n=12, 23%), pre- and postoperative (n=12, 23%), or postoperative (n=2, 4%) based on tumor pathology. Preoperative radiation was used in 1 (2%) patient; postoperative in 2 (4%) patients; and pre- and postoperative in 1 (2%) patient.
Revision was defined as the removal and/or replacement of the proximal humeral component or allograft. Reoperation was defined as any surgical procedure performed on the shoulder girdle where the arthroplasty components or allograft were not removed or exchanged. Amputation of the limb was considered a failure of limb salvage surgery.
Accounting for All Patients
Postoperatively, patients were followed at regular intervals for local and systemic recurrence every 3 to 4 months for the first 2 years postoperatively, at 6-month intervals for postoperative years 2 to 5, and yearly for years 5 and beyond. Patients with an arthroplasty or functional spacer reconstruction were prospectively followed by the total joint registry over the course of the study at regular intervals through clinic visits or telephone/letter to the time of death, revision, tumor recurrence, or amputation.4
For the oncological outcomes, all surviving patients had achieved at least 2 years of clinical follow-up. Mean follow-up for the entire group of patients included the series was 23 years (range, 2–35 years). Mean time to death for all patients was 11 years (range, 6 weeks to 31 years). In the patient cohort, 9 patients have not returned to clinic or have been contacted through the registry for greater than 5 years. Of these 9 patients, 3 had not achieved 5 years of clinical follow-up. Mean clinical follow-up of these 3 patients was 3 years (range, 2–4 years). The additional 6 patients had all reached 5 years of oncologic follow-up, with a mean follow-up of this cohort of 13 years (range, 5–25 years).
To obtain the functional outcome measures, surviving patients were contacted by telephone and administered the modified MSTS5 and the Toronto Extremity Salvage Score (TESS).6 Of the 25 patients available to be administered the survey, 19 (76%) responded (Table 1). Mean follow-up of this group was 28 years (range, 24–35 years).
Long-term Outcome of Patients Undergoing Shoulder Girdle Resection
An unpaired Student's t test was used to assess continuous variables, with categorical variables compared with Fisher's exact test. Post hoc analysis of variance with Tukey honest significant difference was used to compare the mean MSTS rating and TESS score at the most recent time point. The Kaplan–Meier method was used to evaluate survival outcomes. Hazard regression analysis was performed to assess the risk of death from disease, disease recurrence, and implant or allograft failure. Statistical significance was set at P<.05.
During the course of the study, 21 (40%) patients died of all causes, with 11 (21%) dying from disease, as such the 5-, 10-, 20-, and 30-year disease-specific mortality rates were 87%, 84%, 79%, and 79%, respectively (Figure 1). Patients who developed metastatic disease (hazard ratio, 40.59; P<.01) or had a local tumor recurrence (hazard ratio, 11.68; P<.01) were at an increased risk of death from disease (Table 2). Likewise, younger patients (<55 years) (hazard ratio, 0.26; P=.03) had a reduced risk of death.
During the course of the series, 11 patients died of disease following shoulder girdle re-section, as such the 5-, 10-, 20-, and 30-year disease-specific mortality rates of patients were 87%, 84%, 79%, and 79%, respectively (top). Likewise, 9 patients developed disease recurrence, with 5-, 10-, 20-, and 30-year disease-free survival rates of 85%, 85%, 80%, and 80%, respectively (bottom).
Hazard Ratios for Long-term Death From Disease
For patients who presented with nonmetastatic disease (n=50, 94%), disease recurrence occurred in 9 (17%) patients, with a mean time to recurrence of 4 years (range, 2 months to 18 years). Tumor recurrence was classified as isolated local recurrence (n=1, 2%), isolated metastatic disease (n=4, 8%), and concurrent local and distant disease (n=4, 8%). Mean time to local disease recurrence and to metastatic disease was 3 years (range, 3 months to 14 years) and 5 years (range, 6 weeks to 18 years) postoperatively, respectively. The 5-, 10-, 20-, and 30-year disease-free survival rates were 85%, 85%, 80%, and 80%, respectively (Figure 1).
No analyzed factor was found to be significantly associated with local tumor recurrence (Table 3). Patients with local disease recurrence (hazard ratio, 19.94; P<.01) were at increased risk for the development of metastatic disease.
Factors Associated With Disease-Specific Survival in Patients With Primary Sarcomas of the Shoulder Girdle
Twelve (23%) patients underwent a revision of their reconstruction at a mean of 5 years postoperatively (range, 9 months to 22 years). Indications for revision included component loosening (n=4, 8%), fracture of the allograft (n=3, 6%), deep infection (n=2, 4%), and instability (n=2, 4%). The 5-, 10-, 20-, and 30-year revision-free survival rates were 79%, 74%, 74%, and 70%, respectively. No analyzed factor was found to be significantly associated with a revision procedure (Table 4). No difference in the rate of revision was found based on the different reconstructive techniques (P=.36).
Hazard Ratios for Revision Surgery
Reoperation and Postoperative Complications
Twenty (38%) patients underwent a reoperation for any cause during the course of the study at a mean of 4 years (range, 1 day to 22 years) postoperatively. The most common indication for reoperation was irrigation and debridement for a wound complication (n=5, 9%). Six (11%) patients underwent multiple reoperations, and in 2 (4%) patients, these complications led to a revision procedure. Four-quarter amputation was performed for local recurrence in 3 (6%) patients. The overall limb salvage rate was 94%.
Thirty-three (58%) patients sustained at least 1 postoperative complication. The most common complications were subluxation/instability (n=9, 16%) and allograft fracture (n=6, 11%). Subluxation/instability was treated with observation (n=7, 13%) and component removal and shoulder arthrodesis (n=2, 4%). Fractures were treated with revision (n=3, 6%) and observation (n=3, 6%). In addition to these complications, a deep postoperative infection occurred in 3 (6%) patients and resulted in component removal (n=2, 4%) and irrigation, debridement, and hardware removal (n=1, 2%).
At the completion of the previous study, the mean MSTS rating was 67% (range, 20%–97%).1 At long-term follow-up, the authors were able to collect functional outcome scores on 19 patients at a mean follow-up of 28 years (range, 24–32 years). The reconstruction of these patients included arthrodesis (n=5, 26%), endoprosthesis (n=5, 26%), osteoarticular allograft (n=4, 21%), functional spacer (n=4, 21%), and no reconstruction (n=1, 6%). Mean MSTS rating was 75% (range, 50%–97%), with 2 (11%) patients having the same MSTS rating, 9 (47%) with improvement their rating, and 7 (37%) with a decrease in their MSTS rating since the previous study. In addition to the MSTS rating, the mean TESS score was 85% (range, 63%–99%).
There was no difference (P=.98) comparing the mean MSTS rating between the patients with an endoprosthesis (76%; range, 50%–93%), arthrodesis (75%; range, 53%–90%), functional spacer (72%; range, 67%–73%), osteoarticular allograft (78%; range, 67%–97%), and no reconstruction (77%). Likewise, there was no difference (P=.60) in the mean TESS score between the patients with an endoprosthesis (86%; range, 63%–99%), arthrodesis (86%; range, 76%–96%), functional spacer (78%; range, 69%–86%), osteoarticular allograft (86%; range, 75%–94%), and no reconstruction (97%).
The shoulder girdle is a common site of primary bone sarcomas and metastatic disease. With advances in surgical techniques and adjuvant treatments, limb salvage has replaced an amputative procedure for many patients; however, the long-term outcome of the procedure is not well established. The results of this study show that patients who achieved at least 24 years of clinical follow-up have acceptable functional results, with a mean MSTS rating of 75% and TESS of 85%.
Multiple options remain for reconstruction of the shoulder girdle following resection including osteoarticular allografts, endoprosthesis, arthrodesis, allograft prosthetic composite, or a “flail” shoulder following a Tikhoff–Linberg type resection.1,2,7–12 The results of this study showed there was no difference in functional outcome based on the MSTS and TESS score between these techniques.
Kumar et al8 previously reported on the long-term (up to 20 years) outcome of patients with an endoprosthesis and showed that length of resection was significantly associated with outcome. In their series, the authors reported a mean MSTS rating of 79% and TESS score of 72%.8 Although not directly comparable, the current authors noted a similar MSTS rating (76%) but a higher TESS score (85%).
Getty and Peabody11 and Probyn et al12 noted mid-term MSTS ratings following osteoarticular allografts of 70% and 50%, respectively. Again, although the current authors were not able to directly compare patients, they noted superior outcome in terms of MSTS rating (mean, 78%). The current study highlights that although multiple treatment options exist, the treating surgeon should perform the best oncologic procedure for the patient, knowing the patient should have an acceptable functional outcome in the long-term regardless of reconstructive choice.
Although the results of the current series show the long-term outcome of shoulder reconstruction using these techniques is acceptable, newer forms of reconstruction for the proximal humerus exist that may improve the functional outcome of these patients.13–15 Advances in proximal humerus components that use a reverse shoulder component have been developed to reconstruct large bone defects of the proximal humerus. Because these reconstructions do not require a functional rotator cuff and are inherently stable to reduce proximal component migration, they may be able to reduce the incidence of complications related to poor shoulder function and instability. Even if the deltoid or axillary nerve is resected, local muscle transfers at the time of reconstruction can be used to compensate for the loss of these structures.16 Currently, the long-term outcome of these reconstructions is unknown; the early results of these reconstructions are promising.13–15
Complications following these complex reconstructive procedures are common; however, late complications were not, with 2 patients having a complication since the publication of the previous series. One patient had a periprosthetic fracture due to a fall 22 years following the index procedure leading to a revision. The remaining patient developed an ulcer over the surgical hardware and underwent an irrigation and debridement with partial hardware excision.
The incidence of late complications is relatively unknown following these reconstructions. Previous series examining the long-term outcome of shoulder reconstructions have not reported the time frame for complications.8 The results of the current series show some complications that are inherent to this type of oncological resection (namely instability) occur; however, late complications, including implant failure, are infrequent. Previous series have shown rates of subluxation up to 56% have been reported17–19; however, the use of synthetic mesh to reconstruct the joint capsule can potentially reduce this risk.20
Local recurrence following resection of tumors of the shoulder girdle has historically been high and is due to the intimate location of critical neurovascular structures that obligate a marginal resection to allow for limb salvage.21 In the current series, local recurrence occurred in 5 (9%) patients, with 4 of these patients also developing metastatic disease.
Although most of the local disease recurrences occurred within the first 2 years postoperatively, cases of late local recurrence remain a problem. Although the local recurrence rate is similar to studies examining sarcomas of the upper extremity,22 the current authors noted a significant risk of mortality (hazard ratio, 11.68; P<.01) in patients with a local recurrence. All patients who developed local recurrence, without metastatic disease, were alive at final follow-up, which is similar to the results of a study by Reddy et al23 of patients with osteosarcoma of the extremity. Highlighting the fact that patients are still curable even in the setting of local recurrence as long as these patients do not have concurrent distant disease.
Patient survival with sarcomas has improved related to adjuvant treatments and improved early detection.24,25 Patient age has been determined to be a factor in survival for osteosarcoma, with younger patients noted to have improved survival compared to patients older than 65 years.26 Tsuda et al26 noted the worse overall survival could be related to the finding that adjuvant chemotherapies were not as effective in older patients compared with younger patients. Although the patient cohort in the current series is not directly comparable, the current series highlights the overall worse survival for older patients with a sarcoma, which is likely multifactorial.
The results of this study should be considered in light of certain limitations. Due to the retrospective nature of the chart review, the authors were limited in the data they were able to collect and put constraint on the analysis they were able to perform. However, the prospective nature of the functional outcome reporting reduces the risk of recall bias. Although multiple surgeons were involved in the procedure, a subspecialty musculoskeletal oncology trained surgeon (F.H.S.) performed all resections. The patient population was heterogeneous in terms of disease pathology; likewise, the study population was small. This should be taken into consideration in terms of there being no difference in the functional outcome of the reconstructive techniques because this is likely related to the small group of patients. In addition, although the outcome measures used in the current series (MSTS93 and TESS) have shown validity for oncology patients,5,6,27,28 other measures of adult shoulder function could have potentially shown a difference in functional outcome.29 The follow-up of this study spanned a long period, and 4 patients had not reached at least 5 years of clinical follow-up. It is possible the outcome of these patients could substantially change the conclusions of this study.
Overall, the use of limb salvage surgery was associated with an acceptable means of local control and functional outcome following resection of a malignant bone tumor of the shoulder girdle. At long-term follow-up, patients should expect to maintain a functional limb, with some patients having continued functional improvement at a minimum of 24 years of follow-up.
- O'Connor MI, Sim FH, Chao EY. Limb salvage for neoplasms of the shoulder girdle: intermediate reconstructive and functional results. J Bone Joint Surg Am. 1996;78(12):1872–1888. doi:10.2106/00004623-199612000-00011 [CrossRef]8986665
- Enneking W, Dunham W, Gebhardt M, Malawar M, Pritchard D. A system for the classification of skeletal resections. Chir Organi Mov. 1990;75(suppl 1):217–240.2249538
- Enneking WF. A system of staging musculoskeletal neoplasms. Clin Orthop Relat Res. 1986;(204):9–24.3456859
- McGrory BJ, Morrey BF, Rand JA, Ilstrup DM. Correlation of patient questionnaire responses and physician history in grading clinical outcome following hip and knee arthroplasty: a prospective study of 201 joint arthroplasties. J Arthroplasty. 1996;11(1):47–57. doi:10.1016/S0883-5403(96)80160-4 [CrossRef]8676118
- Enneking WF, Dunham W, Gebhardt MC, Malawar M, Pritchard DJ. A system for the functional evaluation of reconstructive procedures after surgical treatment of tumors of the musculoskeletal system. Clin Orthop Relat Res. 1993;(286):241–246.8425352
- Davis AM, Wright JG, Williams JI, Bombardier C, Griffin A, Bell RS. Development of a measure of physical function for patients with bone and soft tissue sarcoma. Qual Life Res. 1996;5(5):508–516. doi:10.1007/BF00540024 [CrossRef]8973131
- Abdeen A, Hoang BH, Athanasian EA, Morris CD, Boland PJ, Healey JH. Allograft-prosthesis composite reconstruction of the proximal part of the humerus: functional outcome and survivorship. J Bone Joint Surg Am. 2009;91(10):2406–2415. doi:10.2106/JBJS.H.00815 [CrossRef]19797576
- Kumar D, Grimer RJ, Abudu A, Carter SR, Tillman RM. Endoprosthetic replacement of the proximal humerus: long-term results. J Bone Joint Surg Br. 2003;85(5):717–722. doi:10.1302/0301-620X.85B5.13838 [CrossRef]12892196
- Frassica FJ, Sim FH, Chao EY. Primary malignant bone tumors of the shoulder girdle: surgical technique of resection and reconstruction. Am Surg. 1987;53(5):264–269.3472479
- Gebhardt MC, Roth YF, Mankin HJ. Osteoarticular allografts for reconstruction in the proximal part of the humerus after excision of a musculoskeletal tumor. J Bone Joint Surg Am. 1990;72(3):334–345. doi:10.2106/00004623-199072030-00004 [CrossRef]2135632
- Getty PJ, Peabody TD. Complications and functional outcomes of reconstruction with an osteoarticular allograft after intraarticular resection of the proximal aspect of the humerus. J Bone Joint Surg Am. 1999;81(8):1138–1146. doi:10.2106/00004623-199908000-00009 [CrossRef]10466646
- Probyn LJ, Wunder JS, Bell RS, Griffin AM, Davis AM. A comparison of outcome of osteoarticular allograft reconstruction and shoulder arthrodesis following resection of primary tumours of the proximal humerus. Sarcoma. 1998;2(3–4):163–170. doi:10.1080/13577149877920 [CrossRef]
- Grosel TW, Plummer DR, Mayerson JL, Scharschmidt TJ, Barlow JD. Oncologic reconstruction of the proximal humerus with a reverse total shoulder arthroplasty megaprosthesis. J Surg Oncol. 2018;118(6):867–872. doi:10.1002/jso.25061 [CrossRef]30151889
- Sanchez-Sotelo J, Wagner ER, Sim FH, Houdek MT. Allograft-prosthetic composite reconstruction for massive proximal humeral bone loss in reverse shoulder arthroplasty. J Bone Joint Surg Am. 2017;99(24):2069–2076. doi:10.2106/JBJS.16.01495 [CrossRef]29257012
- Maclean S, Malik SS, Evans S, Gregory J, Jeys L. Reverse shoulder endoprosthesis for pathologic lesions of the proximal humerus: a minimum 3-year follow-up. J Shoulder Elbow Surg. 2017;26(11):1990–1994. doi:10.1016/j.jse.2017.04.005 [CrossRef]28684229
- Elhassan BT, Wagner ER, Werthel JD, Lehanneur M, Lee J. Outcome of reverse shoulder arthroplasty with pedicled pectoralis transfer in patients with deltoid paralysis. J Shoulder Elbow Surg. 2018;27(1):96–103. doi:10.1016/j.jse.2017.07.007 [CrossRef]
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- Mayilvahanan N, Paraskumar M, Sivaseelam A, Natarajan S. Custom mega-prosthetic replacement for proximal humeral tumours. Int Orthop. 2006;30(3):158–162. doi:10.1007/s00264-005-0029-z [CrossRef]16565840
- Cannon CP, Paraliticci GU, Lin PP, Lewis VO, Yasko AW. Functional outcome following endoprosthetic reconstruction of the proximal humerus. J Shoulder Elbow Surg. 2009;18(5):705–710. doi:10.1016/j.jse.2008.10.011 [CrossRef]19186077
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- Wright EH, Gwilym S, Gibbons CL, Critchley P, Giele HP. Functional and oncological outcomes after limb-salvage surgery for primary sarcomas of the upper limb. J Plast Reconstr Aesthet Surg. 2008;61(4):382–387. doi:10.1016/j.bjps.2007.01.080 [CrossRef]
- Reddy KI, Wafa H, Gaston CL, et al. Does amputation offer any survival benefit over limb salvage in osteosarcoma patients with poor chemonecrosis and close margins?Bone Joint J. 2015;97-B(1):115–120. doi:10.1302/0301-620X.97B1.33924 [CrossRef]25568424
- Wu J, Sun H, Li J, et al. Increased survival of patients aged 0–29 years with osteosarcoma: a period analysis, 1984–2013. Cancer Med. 2018;7(8):3652–3661. doi:10.1002/cam4.1659 [CrossRef]29992762
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- Tsuda Y, Ogura K, Shinoda Y, Kobayashi H, Tanaka S, Kawai A. The outcomes and prognostic factors in patients with osteosarcoma according to age: a Japanese nationwide study with focusing on the age differences. BMC Cancer. 2018;18(1):614. doi:10.1186/s12885-018-4487-2 [CrossRef]29855362
- Akiyama T, Uehara K, Ogura K, et al. Cross-cultural adaptation and validation of the Japanese version of the Toronto Extremity Salvage Score (TESS) for patients with malignant musculoskeletal tumors in the upper extremities. J Orthop Sci. 2017;22(1):127–132. doi:10.1016/j.jos.2016.09.012 [CrossRef]
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Long-term Outcome of Patients Undergoing Shoulder Girdle Resection
|Patient No.||Pathology||Stage||Reconstruction||Resection||Margin Status||Original MSTS Score||Final MSTS Score||TESS Score||Follow-up, y|
|8||Clear cell chondrosarcoma||IB||Endoprosthesis||S345B||Wide||70%||83%||99%||35|
|10||Ewing sarcoma||IIB||Functional spacer||S2345B||Wide||70%||67%||86%||28|
|16||Chondroblastic osteosarcoma||IIB||Functional spacer||S1234B||Wide||57%||73%||69%||27|
|17||Chondroblastic osteosarcoma||IIB||Osteoarticular allograft||S345A||Marginal||90%||73%||75%||27|
|18||Fibroblastic osteosarcoma||IIB||Functional spacer||S2345B||Wide||67%||73%||86%||26|
|19||Parosteal osteosarcoma||IB||Osteoarticular allograft||S345A||Wide||93%||73%||91%||25|
Hazard Ratios for Long-term Death From Disease
|Factor||Survival Hazard Ratio (95% Confidence Interval)||P|
|Metastatic disease||40.59 (9.79–275.91)a||<.01a|
|Local tumor recurrence||11.68 (2.86–44.78)a||<.01a|
|Humeral resection length ≥14 cm||5.33 (0.94–99.84)||.06|
|High-grade tumor||3.68 (0.92–24.42)||.06|
|Pathologic fracture||1.26 (0.19–5.06)||.76|
|Tumor necrosis ≥95%||0.89 (0.12–4.56)||.89|
|Age ≥55 y||0.26 (0.05–0.94)a||.03a|
Factors Associated With Disease-Specific Survival in Patients With Primary Sarcomas of the Shoulder Girdle
|Factor||Hazard Ratio (95% Confidence Interval)||P|
| High-grade tumor||3.73 (0.54–73.15)||.18|
| Resection length ≥14 cm||1.61 (0.15–34.68)||.69|
| Male||1.11 (0.18–8.44)||.90|
| Age ≥55 y||0.40 (0.05–2.44)||.31|
|Development of metastatic disease|
| Local recurrence||19.94 (4.31–103.26)a||<.01a|
| Resection length ≥14 cm||3.96 (0.63–76.01)||.15|
| High-grade tumor||2.79 (0.64–19.11)||.17|
| Male||2.20 (0.50–15.06)||.30|
| Pathologic fracture||1.68 (0.24–7.31)||.54|
| >90% tumor necrosis||0.78 (0.03–8.18)||.83|
| Age ≥55 y||0.35 (0.07–1.46)||.15|
Hazard Ratios for Revision Surgery
|Factor||Revision Hazard Ratio (95% Confidence Interval)||P|
|Resection length ≥14 cm||2.03 (0.63–7.62)||.23|
|High-grade tumor||1.35 (0.43–4.57)||.60|
|Age ≥55 y||0.36 (0.10–1.14)||.08|