BREAST SURGERY
Tissue Expander Complications Predict Permanent Implant Complications and Failure of Breast Reconstruction Joshua M. Adkinson, MD,* Nathan F. Miller, MD,Þ Sherrine M. Eid, MPH,þ Marshall G. Miles, DO,Þ and Robert X. Murphy, Jr, MD, MSÞ Background: Two-stage tissue expanderYbased breast reconstruction is the most commonly used reconstructive modality following mastectomy. We sought to determine if patients who experienced complications during the expansion phase were at increased risk for complications or reconstructive failure after the exchange procedure. Methods: A retrospective review of tissue expanderYbased breast reconstructions was performed from January 2007 through December 2011. Variables evaluated included age, presence of cancer, tobacco use, body mass index, comorbidities, use of acellular dermal matrix, chemotherapy, radiation, timing of reconstruction (delayed/immediate), intraoperative tissue expander fill, complications, and explantation or salvage of the reconstruction by means of debridement and closure or myocutaneous flap. Results: A total of 196 patients underwent mastectomy with 304 tissue expander reconstructions. Tobacco use (active and remote), hypertension, and radiation were associated with complications. Patients with a salvaged tissue expander complication were 3 times more likely to have a complication after placement of a permanent implant and 9 times more likely to fail permanent implant reconstruction (ie, require explantation). Conclusions: Women with complications after placement of a tissue expander are at significantly increased risk for both complications and reconstructive failure after placement of a permanent implant. Consideration for earlier autologous reconstruction as a salvage should be strongly considered in patients with a tissue expander complication, particularly in smokers and those undergoing radiation therapy. Key Words: tissue expander, complications, reconstruction, failure, breast cancer (Ann Plast Surg 2015;75: 24Y28)
METHODS
B
reast cancer is the most common malignancy in women, with an estimated 207,090 diagnoses in the United States in the year 2010 alone.1,2 As the population ages, the prevalence of breast cancer is also projected to rise.3Y5 Increasing diagnoses, patient knowledge of reconstructive options, and requests for prophylactic mastectomies3,6,7 have thus set the stage for a marked rise in the demand for concomitant breast reconstruction. Fortunately, multiple reconstructive options are available to women after mastectomy. Tissue expanderYbased reconstruction, however, continues to be the most commonly used technique,3,8,9 accounting for approximately 70% of all reconstructions in 2009.2,10Y12
Received May 17, 2013, and accepted for publication, after revision, December 27, 2013. From the *Department of Surgery, Section of Plastic Surgery, University of Michigan Health System, Ann Arbor, MI; and †Department of Surgery, Division of Plastic Surgery, and ‡Department of Community Health and Health Studies, Lehigh Valley Health Network, Allentown, PA. Conflicts of interest and sources of funding: none declared. Reprints: Nathan F. Miller, MD, Department of Surgery, Division of Plastic Surgery, Lehigh Valley Health Network, Cedar Crest & I-78, P.O. Box 689, Allentown, PA 18105-1556. E-mail: [email protected]. Copyright * 2014 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0148-7043/15/7501-0024 DOI: 10.1097/SAP.0000000000000142
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While typically performed in 2 stages,3,5,10 implant-based reconstruction is noted to have excellent cosmesis3 and is particularly useful in bilateral reconstruction, where symmetry is technically easier to achieve.5,8,10 The lack of a donor-site scar, less invasive nature, faster operative time, and shorter length of stay when compared to autologous approaches continue to make implant-based reconstruction an appealing option for both patients and surgeons.3,10,13 The frequency with which alloplastic techniques are used has allowed many authors to report on their experiences and complication rates. These rates vary widely, from a low of 2% to a high of 52% in some studies.2,6,9,14Y29 Smoking, obesity, hypertension, and age have been described as factors associated with high rates of complications after implant-based reconstructive efforts.10,30 Radiation is also associated with a significant increase in delayed healing, capsular contracture, implant malposition, implant extrusion, and infection after tissue expander reconstruction.3,31Y35 Among the many possible complications, however, infection is the most common after implant-based reconstruction.5,17,30 There are no data correlating tissue expander placement complications with outcomes after placement of a permanent implant. Are patients with complications during tissue expansion at higher risk for complications or failure after exchange to a permanent implant? To date, no studies have addressed the implications of salvaging an at-risk tissue expander. These data may be used during both the development of a best practice surgical algorithm and patient consultation regarding the risks of permanent implant-related complications and reconstructive failure.
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We performed an Institutional Review BoardYapproved retrospective review of patients undergoing 2-stage tissue expanderYbased breast reconstruction by 4 surgeons within our institution from January 2007 through December 2011. Patients were assessed for age at the time of surgery, presence of cancer, tobacco use, body mass index (BMI), hypertension, diabetes mellitus, placement of acellular dermal matrix, chemotherapy, radiation therapy, timing of reconstruction (delayed vs. immediate), and expander fill at time of procedure. Complications such as expander or permanent implant exposure or rupture, infection with or without the need for antibiotics, hematoma or seroma, capsular contracture, explantation or salvage of the reconstruction by means of debridement and closure or myocutaneous flap, and follow-up time were recorded. A multivariate logistic regression model was used to determine the likelihood of independent variables to contribute to a tissue expander complication, permanent implant complication, or both an expander and permanent implant complication. All analyses were performed using SPSS 15.0 (SPSS Inc., Chicago, IL). Alpha was set at 0.05 with a 95% confidence interval.
RESULTS The database identified 196 patients undergoing mastectomy, either unilateral or bilateral, with 304 tissue expanderYbased breast reconstructions. Of this cohort of patients, 175 patients underwent immediate reconstruction, while 21 patients underwent delayed reconstruction. One hundred ninety-one patients underwent reconstruction following Annals of Plastic Surgery
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mastectomy for cancer and 5 patients underwent prophylactic mastectomy. Of the 196 patients undergoing mastectomy, 166 patients underwent a second-stage exchange to a permanent implant, while 17 were awaiting exchange and 13 were explanted before implant exchange procedure without an attempt to replace the expander. Excluding those awaiting second-stage permanent implant placement (17 patients), 89.4% (160/179) successfully completed tissue-expander reconstruction. Mean follow-up time was 25.5 months (range 4.6Y63.7 months).
Overall Analysis of Risk Factors for Complications The mean age (51.86 T 10.55 compared to 50.96 T 11.15) and BMI (29.55 T 6.45 compared to 28.32 T 7.24) of those patients sustaining complications were higher, though these differences were not statistically significant (P = 0.578 and P = 0.600, respectively). A statistically significant difference was found for the likelihood of any complication in those patients with a history of hypertension (P = 0.035) and tobacco use (P = 0.001). A history of radiation therapy trended towards significance in univariate analysis (P = 0.098). No statistically significant difference was found with regard to a history of diabetes mellitus (P = 0.183), chemotherapy (P = 0.712), the use of acellular dermal matrix (P = 0.379), or intraoperative tissue expander fill volume (P = 0.994) (Table 1). A stepwise logistic regression was performed to evaluate the likelihood of complications at any point during the reconstructive timeline. Both active tobacco use and a remote history of tobacco use were shown to be associated with an increased risk for complications [OR = 3.709, 95% CI (1.434, 9.593) (P = 0.007) and OR = 2.423, 95% CI (1.129, 5.108) (P = 0.023), respectively]. Hypertension was also associated with a 2-fold increased risk for complications [OR = 2.030, 95% CI (1.069, 3.856) (P = 0.031)] (Table 2).
Complications After Tissue Expander Placement Of the 196 patients undergoing placement of a tissue expander, 54 patients (27.6%) had 72 complications. Infection comprised 54.2% of all complications after placement of a tissue expander. Other complications included flap necrosis, hematoma, seroma, capsular contracture, implant exposure, implant rupture, and nipple necrosis (Table 3).
Complications After Exchange Procedure Of the 166 patients undergoing second-stage exchange to permanent implant, 39 patients (23.5%) had 47 complications. Infection comprised 31.9% of all complications after the second-stage exchange procedure. Other complications included flap necrosis, hematoma, seroma, capsular contracture, implant exposure, and implant rupture (Table 3).
Procedures Performed for Complications Washout and debridement was the most commonly performed procedure for complications at any stage (n = 21 after the expander
Tissue Expander Complications
insertion and n = 11 after the exchange procedure). Explantation of a tissue expander was performed 15 times in 14 patients (1 patient underwent explantation twice). Myocutaneous f lap salvage was performed in 4 patients after placement of tissue expander [latissimus dorsi (LD) f lap = 2, transverse rectus abdominis myocutaneus (TRAM) f lap = 2] and in 2 patients (LD = 2) after the exchange procedure. Other procedures performed for complications included capsulectomy, tissue expander or permanent implant exchange, and evacuation of hematoma.
The Impact of Tissue Expander Complications on Exchange Procedure Complications and Reconstructive Failure Patients with salvaged tissue expander complications (ie, not explanted) were 3 times more likely to have complications after placement of a permanent implant [OR = 3.183, 95% CI (1.408, 7.198)] (P = 0.004) (Table 4). This patient cohort was also 9 times more likely to fail permanent implant reconstruction (explantation T f lap salvage) [OR = 9.034, 95% CI (1.579, 51.699)] (P = 0.003) (Table 5). We then sought to clarify why the 33 patients with tissue expander complications going on to the exchange procedure were at elevated risk for both implant complications and reconstructive failure. Of this subset, 14 patients sustained additional complications after the exchange procedure (19 patients completed reconstruction without further complication). Univariate analysis revealed that age, BMI, hypertension, diabetes mellitus, chemotherapy, acellular dermal matrix, and intraoperative tissue expander fill volume were not statistically associated with second-stage procedure complications in this patient subset. Tobacco use (P = 0.006) and radiation therapy (P = 0.004) were found to be statistically significantly associated with sustaining complications after both phases of reconstruction (Table 6).
DISCUSSION The literature is now replete with evidence describing the various risk factors for complications after tissue expanderYbased breast reconstruction. With the end goal of a durable, cosmetically appealing permanent implant reconstruction, all patients would ideally undergo a second operation to exchange the tissue expander for a permanent prosthesis. In this setting, we felt it useful to elucidate the determinants of complications after the second stage of reconstruction, particularly in those suffering complications after placement of tissue expanders. These data could then be used as an evidence-based foundation for patient counseling after a tissue expander complication as well as a guideline for possible conversion to autologous reconstruction. As is commonly known, complications of tissue expander reconstruction can be related to patient comorbidities,10,19 tobacco use,10,19,36 insult to the mastectomy flaps,22,37 reconstructive adjuncts
TABLE 1. Risk Factors for Complications During Reconstruction Characteristic Age, yr BMI HTN DM Smoker Chemotherapy Radiation Acellular dermal matrix Expander fill, mL
Complications (n = 79 Women)
No Complications (n = 117 Women)
P
51.86 T 10.55 29.55 T 6.45 30 (51.7%) 8 (57.1%) 33 (57.9%) 31 (38.8%) 29 (49.2%) 70 (39.3%) 205.13 T 109.95
50.96 T 11.15 28.32 T 7.24 28 (48.3%) 6 (42.9%) 24 (42.1%) 49 (61.3%) 30 (50.8%) 108 (60.7%) 188.38 T 111.69
0.578 0.600 0.035 0.183 0.001 0.712 0.098 0.379 0.994
BMI, body mass index; HTN, hypertension; DM, diabetes mellitus.
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Adkinson et al
TABLE 2. Logistic Regression of Risk Factors for Any Complication (P G 0.001)
Characteristic
N
P
Adjusted OR
95% Confidence Interval
SmokerVactive SmokerVremote Non-smoker HTN No HTN
22 35
0.007 0.023
58
0.031
3.709 2.423 1.0 2.030 1.0
1.434 9.593 1.129 5.108 Reference 1.069 3.856 Reference
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TABLE 4. Permanent Implant Complication After Tissue Expander Complication in Patients Undergoing Both Stages of Reconstruction Permanent Implant Complication
Expander complication
Yes No
Total
Yes
No
Total
14 (42.4%) 25 (18.8%) 39 (23.5%)
19 (57.6%) 108 (81.2%) 127 (76.5%)
33 (100%) 133 (100%) 166 (100%)
P = 0.004.
HTN, hypertension.
(ie, acellular dermal matrix),22,38,39 the prosthetic device,15,40 and/or neoadjuvant/adjuvant modalities for cancer treatment.33,41,42 In our series, complications occurred in 27.6% of patients after tissue expander placement and 23.5% of patients after exchange to a permanent implant. A smaller cohort of 14 patients (8.4%) suffered complications after both procedures. Age, BMI, diabetes mellitus, chemotherapy, use of acellular dermal matrix, and the volume of intraoperative tissue expander fill volume did not statistically correlate with an increased likelihood for complications at any point during the reconstructive timeline. Physiologically, tobacco use impairs both wound healing43,44 and flap survival45Y47 through a mechanism involving vasoconstriction, platelet adhesion, and a relative hypoxia secondary to carboxyhemoglobinemia.16,43,44 In multivariate analysis of all patients, tobacco use (both active and remote) was associated with an increased likelihood for complications. In fact, active tobacco use increased the risk of complications 3.7 times, while remote use increased the risk 2.4 times. Smoking is generally considered to be a risk factor for complications, particularly wound healing, after breast reconstruction.16,43,47 In a study by Goodwin et al,46 tobacco use led to an increased risk for overall complications, skin flap loss, and reconstructive failure. We noted a similar trend. Analysis of all patients after tissue expander placement also revealed that hypertension was associated with a 2-fold increased risk for complications. Hypertension is independently linked to both arterial rigidity and blood hyperviscosity48,49Vcharacteristics that would predispose to poor wound healing, flap necrosis, and infection. A similar relationship between the presence of hypertension and tissue expanderY related complications has been noted in a study by McCarthy et al in 1170 tissue expander-implant reconstructions.19 Radiation has repeatedly been shown to increase post-surgical complications in patients undergoing tissue expander reconstruction.10,31Y36,50,51 Though not statistically significant in initial univariate analysis of all patients, radiation therapy was determined to be associated with exchange procedure complications in those with a salvaged tissue expander complication. This discrepancy is likely explained by
the timing of radiation therapy, which typically occurs after placement of a tissue expander in our network, thus causing an ischemic insult to the surgical environment. Subsequent surgery in this compromised wound bed leads to an increased risk for complications. Consistent with previous studies,17,30,41 infection was the most common complication (54% of all complications after placement of tissue expander) and the most likely reason for explantation (73% of all explants). Further, complication rates were higher after the initial expander placement compared to the exchange procedure (27.6% vs. 23.5%). This trend has been noted previously17,23,52 and is attributable to the surgical insult of mastectomy flap elevation. The unique focus of this study has shown that patients with complications after expander insertion were 3 times more likely to have exchange procedure complications and 9 times more likely to fail implant-based reconstruction. This relationship was statistically linked to both tobacco use and radiation therapy. While studies have shown modest success in the setting of radiation,17,35,52Y56 this patient subset may be best served by immediate or delayed autologous techniques.3,57Y61 Importantly, hypertension was associated with tissue-expander placement complications, but did not contribute to the complications and failure after the exchange procedure. Spear et al62 have shown a high rate of success (92.3%) with repeat prosthetic reconstruction in those initially failing implant reconstruction as a result of infection or exposure (average BMI of 24.7 and 15% rate of radiation). Though these results are encouraging, our patients sustaining a complication differed significantly: average BMI of 29.55 and 26.7% rate of radiation (29 of 79 patients). In our patient population, we recommend early conversion to autologous techniques in tobacco users and radiated patients sustaining significant complications after tissue expander placement. By implementing this change in strategy, surgeons may mitigate the significant negative psychological impact on patients and prevent the potentially prolonged reconstructive timeline resulting from a failed implant reconstruction. As with any retrospective review, our study has several limitations, including the lack of standard documentation among surgeons and missing data points. During the study collection period, 17 women were still awaiting the exchange procedure; this subset was excluded
TABLE 3. Types of Complications After Each Stage of Surgery Complication Infection Flap necrosis Hematoma/seroma Capsular contracture Implant exposure Implant rupture Nipple necrosis Total complications
26
Expander Placement (n = 54 Women) 39 13 10 2 3 4 1 72
(54.2%) (18.1%) (13.9%) (2.8%) (4.2%) (5.6%) (1.4%) (100%)
Exchange Procedure (n = 39 Women) 15 6 6 13 4 3
(31.9%) (12.8%) (12.8%) (27.7%) (8.5%) (6.4%) V 47 (100%)
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TABLE 5. Failed Permanent Implant Reconstruction After Tissue Expander Complication in Patients Undergoing Both Stages of Reconstruction Failed Permanent Implant Reconstruction
Expander complication
Yes No
Total
Yes
No
Total
4 (12.1%) 2 (1.5%) 6 (3.6%)
29 (87.9%) 131 (98.5%) 160 (96.4%)
33 (100%) 133 (100%) 166 (100%)
P = 0.003.
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Tissue Expander Complications
TABLE 6. Univariate Analysis of 33 Patients With Expander Complications Undergoing Exchange Procedure Characteristic Age, yr BMI HTN DM Smoker Chemotherapy Radiation Acellular dermal matrix Expander fill, mL
Expander Complication Only (n = 19)
Expander and Exchange Procedure Complication (n = 14)
P
50.42 T 9.34 29.77 T 5.85 6 (13.3%) 2 (18.2%) 7 (17.5%) 3 (4.8%) 0 (0.0%) 18 (11.7%) 219.47 T 113.21
51.00 T 11.74 28.55 T 7.20 5 (11.1%) 0 (0.0%) 8 (20.0%) 8 (12.9%) 7 (17.5%) 13 (8.4%) 188.57 T 77.64
0.998 0.595 0.462 0.127 0.006 0.102 0.004 0.790 0.308
BMI, body mass index; HTN, hypertension; DM, diabetes mellitus.
from the final analysis. Additional considerations include the possibility of varied surgical techniques among the 4 surgeons included in the study and the exclusion of cancer staging. Further, only 5 of the 196 patients underwent prophylactic mastectomy in this series and, as such, the presence of cancer as a determinant of complications could not be assessed with any degree of statistical significance.
CONCLUSION Despite complications, approximately 90% of women successfully complete tissue expanderYbased breast reconstruction. However, women who experience complications during the expansion phase of breast reconstruction are at significantly increased risk for complications and reconstructive failure after placement of a permanent implant. The patient who experiences a complication during the expander phase should be closely followed, as this cohort has a much higher likelihood of failing implant-based breast reconstruction. As a result, we recommend early conversion to autologous reconstruction in patients with significant tissue expander complications, particularly in the setting of tobacco use and radiation therapy.
10. Serletti JM, Fosnot J, Nelson JA, et al. Breast reconstruction after breast cancer. Plast Reconstr Surg. 2011;127:124eY135e. 11. American Society of Plastic Surgeons. Report of the 2008 National Clearinghouse of Plastic Surgery Statistics. Available at: http://www.plasticsurgery.org/Media/ stats/2008-UScosmetic-reconstructive-plastic-surgery-minimally-invasivestatistics.pdf. Accessed July 1, 2009. 12. American Society of Plastic Surgeons. 2010 report of the 2009 statistics. National Clearinghouse of Plastic Surgery Statistics. Retained from: http:// www.plasticsurgery.org/Documents/Media/statistics/2009UScosmeticreconstructive plasticsurgeryminimally-invasive-statistics.pdf. 13. Spear SL, Mardini S, Ganz JC. Resource cost comparison of implant-based breast reconstruction versus TRAM flap breast reconstruction. Plast Reconstr Surg. 2003;112:101Y105. 14. Spear SL, Newman MK, Bedford MS, et al. A retrospective analysis of outcomes using three common methods for immediate breast reconstruction. Plast Reconstr Surg. 2008;122:340Y347. 15. O’Brien W, Hasselgren PO, Hummel R, et al. Comparison of postoperative wound complications and early cancer recurrence between patients undergoing mastectomy with or without immediate breast reconstruction. Am J Surg. 1993;166:1Y5. 16. Goodwin SJ, McCarthy CM, Pusic AL, et al. Complications in smokers after postmastectomy tissue expander/implant breast reconstruction. Ann Plast Surg. 2005;55:16Y20. 17. Cordeiro PG, McCarthy CM. A single surgeon’s 12-year experience with tissue expander/implant breast reconstruction: part I. A prospective analysis of early complications. Plast Reconstr Surg. 2006;118:825Y831.
ACKNOWLEDGMENT We would like to thank Jacqueline Grove, Medical Editor, Lehigh Valley Health Network, for her assistance with this manuscript.
18. McCarthy CM, Disa JJ, Pusic AL, et al. The effect of closed-suction drains on the incidence of local wound complications following tissue expander/implant reconstruction: a cohort study. Plast Reconstr Surg. 2007;119:2018Y2022.
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43. Krueger JK, Rohrich RJ. Clearing the smoke: the scientific rationale for tobacco abstention with plastic surgery. Plast Reconstr Surg. 2001;108:1063Y1073; discussion 1074Y1077. 44. Silverstein P. Smoking and wound healing. Am J Med. 1992;93:22SY24S. 45. Nolan J, Jenkins RA, Kurihara K, et al. The acute effects of cigarette smoke exposure on experimental skin flaps. Plast Reconstr Surg. 1985;75:544Y551. 46. Chang LD, Buncke G, Slezak S, et al. Cigarette smoking, plastic surgery and microsurgery. J Reconstr Microsurg. 1996;12:467Y474. 47. Spear SL, Ducic I, Cuoco F, et al. The effect of smoking on flap and donor-site complications in pedicled TRAM breast reconstruction. Plast Reconstr Surg. 2005;116:1873Y1880. 48. Levenson J, Simon AC, Cambien FA, et al. Cigarette smoking and hypertension. Factors independently associated with blood hyperviscosity and arterial rigidity. Arteriosclerosis. 1987;7:572Y577. 49. Tsuchida Y, Fukuda O, Kamata S. The correlation of skin blood flow with age, total cholesterol, hematocrit, blood pressure, and hemoglobin. Plast Reconstr Surg. 1991;88:844Y850. 50. Liu AS, Kao HK, Reish RG, et al. Postoperative complications in prosthesisbased breast reconstruction using acellular dermal matrix. Plast Reconstr Surg. 2011;127:1755Y1762. 51. Kronowitz SJ, Robb GL. Radiation therapy and breast reconstruction: a critical review of the literature. Plast Reconstr Surg. 2009;124:395Y408. 52. Miller AP, Falcone RE. Breast reconstruction: systemic factors influencing local complications. Ann Plast Surg. 1991;27:115Y120. 53. Paulhe P, Aubert JP, Magalon G. Forum on tissue expansion. Are tissue expansion and radiotherapy compatible? Apropos of a series of 50 consecutive breast reconstructions. Ann Chir Plast Esthet. 1993;38:54Y61. 54. Evans GR, Schusterman MA, Kroll SS, et al. Reconstruction and the radiated breast: is there a role for implants? Plast Reconstr Surg. 1995;96:1111Y1115. 55. Cordeiro PG, Pusic AL, Disa JJ, et al. Irradiation after immediate tissue expander/implant breast reconstruction: outcomes, complications, aesthetic results, and satisfaction among 156 patients. Plast Reconstr Surg. 2004;113: 877Y881. 56. Percec I, Bucky LP. Successful prosthetic breast reconstruction after radiation therapy. Ann Plast Surg. 2008;60:527Y531. 57. Vandeweyer E, Deraemaecker R, Nogaret JM, et al. Immediate breast reconstruction with implants and adjuvant chemotherapy: a good option? Acta Chir Belg. 2003;103:98Y101. 58. Krueger EA, Wilkins EG, Strawderman M, et al. Complications and patient satisfaction following expander/implant breast reconstruction with and without radiotherapy. Int J Radiat Oncol Biol Phys. 2001;49:713Y721. 59. Kroll SS, Schusterman MA, Reece GP, et al. Breast reconstruction with myocutaneous flaps in previously irradiated patients. Plast Reconstr Surg. 1994;93:460Y469; discussion 470Y471. 60. Taylor CW, Horgan K, Dodwell D. Oncological aspects of breast reconstruction. Breast. 2005;14:118Y130. 61. Corral CJ, Mustoe TA. Controversy in breast reconstruction. Surg Clin North Am. 1996;76:309Y326. 62. Spear SL, Masden D, Rao SS, et al. Long-term outcomes of failed prosthetic breast reconstruction. Ann Plast Surg. 2013;71:286Y291.
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Tissue Expander Complications Predict Permanent Implant Complications and Failure of Breast Reconstruction Joshua M. Adkinson, MD,* Nathan F. Miller, MD,Þ Sherrine M. Eid, MPH,þ Marshall G. Miles, DO,Þ and Robert X. Murphy, Jr, MD, MSÞ Background: Two-stage tissue expanderYbased breast reconstruction is the most commonly used reconstructive modality following mastectomy. We sought to determine if patients who experienced complications during the expansion phase were at increased risk for complications or reconstructive failure after the exchange procedure. Methods: A retrospective review of tissue expanderYbased breast reconstructions was performed from January 2007 through December 2011. Variables evaluated included age, presence of cancer, tobacco use, body mass index, comorbidities, use of acellular dermal matrix, chemotherapy, radiation, timing of reconstruction (delayed/immediate), intraoperative tissue expander fill, complications, and explantation or salvage of the reconstruction by means of debridement and closure or myocutaneous flap. Results: A total of 196 patients underwent mastectomy with 304 tissue expander reconstructions. Tobacco use (active and remote), hypertension, and radiation were associated with complications. Patients with a salvaged tissue expander complication were 3 times more likely to have a complication after placement of a permanent implant and 9 times more likely to fail permanent implant reconstruction (ie, require explantation). Conclusions: Women with complications after placement of a tissue expander are at significantly increased risk for both complications and reconstructive failure after placement of a permanent implant. Consideration for earlier autologous reconstruction as a salvage should be strongly considered in patients with a tissue expander complication, particularly in smokers and those undergoing radiation therapy. Key Words: tissue expander, complications, reconstruction, failure, breast cancer (Ann Plast Surg 2015;75: 24Y28)
METHODS
B
reast cancer is the most common malignancy in women, with an estimated 207,090 diagnoses in the United States in the year 2010 alone.1,2 As the population ages, the prevalence of breast cancer is also projected to rise.3Y5 Increasing diagnoses, patient knowledge of reconstructive options, and requests for prophylactic mastectomies3,6,7 have thus set the stage for a marked rise in the demand for concomitant breast reconstruction. Fortunately, multiple reconstructive options are available to women after mastectomy. Tissue expanderYbased reconstruction, however, continues to be the most commonly used technique,3,8,9 accounting for approximately 70% of all reconstructions in 2009.2,10Y12
Received May 17, 2013, and accepted for publication, after revision, December 27, 2013. From the *Department of Surgery, Section of Plastic Surgery, University of Michigan Health System, Ann Arbor, MI; and †Department of Surgery, Division of Plastic Surgery, and ‡Department of Community Health and Health Studies, Lehigh Valley Health Network, Allentown, PA. Conflicts of interest and sources of funding: none declared. Reprints: Nathan F. Miller, MD, Department of Surgery, Division of Plastic Surgery, Lehigh Valley Health Network, Cedar Crest & I-78, P.O. Box 689, Allentown, PA 18105-1556. E-mail: [email protected]. Copyright * 2014 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0148-7043/15/7501-0024 DOI: 10.1097/SAP.0000000000000142
24
While typically performed in 2 stages,3,5,10 implant-based reconstruction is noted to have excellent cosmesis3 and is particularly useful in bilateral reconstruction, where symmetry is technically easier to achieve.5,8,10 The lack of a donor-site scar, less invasive nature, faster operative time, and shorter length of stay when compared to autologous approaches continue to make implant-based reconstruction an appealing option for both patients and surgeons.3,10,13 The frequency with which alloplastic techniques are used has allowed many authors to report on their experiences and complication rates. These rates vary widely, from a low of 2% to a high of 52% in some studies.2,6,9,14Y29 Smoking, obesity, hypertension, and age have been described as factors associated with high rates of complications after implant-based reconstructive efforts.10,30 Radiation is also associated with a significant increase in delayed healing, capsular contracture, implant malposition, implant extrusion, and infection after tissue expander reconstruction.3,31Y35 Among the many possible complications, however, infection is the most common after implant-based reconstruction.5,17,30 There are no data correlating tissue expander placement complications with outcomes after placement of a permanent implant. Are patients with complications during tissue expansion at higher risk for complications or failure after exchange to a permanent implant? To date, no studies have addressed the implications of salvaging an at-risk tissue expander. These data may be used during both the development of a best practice surgical algorithm and patient consultation regarding the risks of permanent implant-related complications and reconstructive failure.
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We performed an Institutional Review BoardYapproved retrospective review of patients undergoing 2-stage tissue expanderYbased breast reconstruction by 4 surgeons within our institution from January 2007 through December 2011. Patients were assessed for age at the time of surgery, presence of cancer, tobacco use, body mass index (BMI), hypertension, diabetes mellitus, placement of acellular dermal matrix, chemotherapy, radiation therapy, timing of reconstruction (delayed vs. immediate), and expander fill at time of procedure. Complications such as expander or permanent implant exposure or rupture, infection with or without the need for antibiotics, hematoma or seroma, capsular contracture, explantation or salvage of the reconstruction by means of debridement and closure or myocutaneous flap, and follow-up time were recorded. A multivariate logistic regression model was used to determine the likelihood of independent variables to contribute to a tissue expander complication, permanent implant complication, or both an expander and permanent implant complication. All analyses were performed using SPSS 15.0 (SPSS Inc., Chicago, IL). Alpha was set at 0.05 with a 95% confidence interval.
RESULTS The database identified 196 patients undergoing mastectomy, either unilateral or bilateral, with 304 tissue expanderYbased breast reconstructions. Of this cohort of patients, 175 patients underwent immediate reconstruction, while 21 patients underwent delayed reconstruction. One hundred ninety-one patients underwent reconstruction following Annals of Plastic Surgery
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mastectomy for cancer and 5 patients underwent prophylactic mastectomy. Of the 196 patients undergoing mastectomy, 166 patients underwent a second-stage exchange to a permanent implant, while 17 were awaiting exchange and 13 were explanted before implant exchange procedure without an attempt to replace the expander. Excluding those awaiting second-stage permanent implant placement (17 patients), 89.4% (160/179) successfully completed tissue-expander reconstruction. Mean follow-up time was 25.5 months (range 4.6Y63.7 months).
Overall Analysis of Risk Factors for Complications The mean age (51.86 T 10.55 compared to 50.96 T 11.15) and BMI (29.55 T 6.45 compared to 28.32 T 7.24) of those patients sustaining complications were higher, though these differences were not statistically significant (P = 0.578 and P = 0.600, respectively). A statistically significant difference was found for the likelihood of any complication in those patients with a history of hypertension (P = 0.035) and tobacco use (P = 0.001). A history of radiation therapy trended towards significance in univariate analysis (P = 0.098). No statistically significant difference was found with regard to a history of diabetes mellitus (P = 0.183), chemotherapy (P = 0.712), the use of acellular dermal matrix (P = 0.379), or intraoperative tissue expander fill volume (P = 0.994) (Table 1). A stepwise logistic regression was performed to evaluate the likelihood of complications at any point during the reconstructive timeline. Both active tobacco use and a remote history of tobacco use were shown to be associated with an increased risk for complications [OR = 3.709, 95% CI (1.434, 9.593) (P = 0.007) and OR = 2.423, 95% CI (1.129, 5.108) (P = 0.023), respectively]. Hypertension was also associated with a 2-fold increased risk for complications [OR = 2.030, 95% CI (1.069, 3.856) (P = 0.031)] (Table 2).
Complications After Tissue Expander Placement Of the 196 patients undergoing placement of a tissue expander, 54 patients (27.6%) had 72 complications. Infection comprised 54.2% of all complications after placement of a tissue expander. Other complications included flap necrosis, hematoma, seroma, capsular contracture, implant exposure, implant rupture, and nipple necrosis (Table 3).
Complications After Exchange Procedure Of the 166 patients undergoing second-stage exchange to permanent implant, 39 patients (23.5%) had 47 complications. Infection comprised 31.9% of all complications after the second-stage exchange procedure. Other complications included flap necrosis, hematoma, seroma, capsular contracture, implant exposure, and implant rupture (Table 3).
Procedures Performed for Complications Washout and debridement was the most commonly performed procedure for complications at any stage (n = 21 after the expander
Tissue Expander Complications
insertion and n = 11 after the exchange procedure). Explantation of a tissue expander was performed 15 times in 14 patients (1 patient underwent explantation twice). Myocutaneous f lap salvage was performed in 4 patients after placement of tissue expander [latissimus dorsi (LD) f lap = 2, transverse rectus abdominis myocutaneus (TRAM) f lap = 2] and in 2 patients (LD = 2) after the exchange procedure. Other procedures performed for complications included capsulectomy, tissue expander or permanent implant exchange, and evacuation of hematoma.
The Impact of Tissue Expander Complications on Exchange Procedure Complications and Reconstructive Failure Patients with salvaged tissue expander complications (ie, not explanted) were 3 times more likely to have complications after placement of a permanent implant [OR = 3.183, 95% CI (1.408, 7.198)] (P = 0.004) (Table 4). This patient cohort was also 9 times more likely to fail permanent implant reconstruction (explantation T f lap salvage) [OR = 9.034, 95% CI (1.579, 51.699)] (P = 0.003) (Table 5). We then sought to clarify why the 33 patients with tissue expander complications going on to the exchange procedure were at elevated risk for both implant complications and reconstructive failure. Of this subset, 14 patients sustained additional complications after the exchange procedure (19 patients completed reconstruction without further complication). Univariate analysis revealed that age, BMI, hypertension, diabetes mellitus, chemotherapy, acellular dermal matrix, and intraoperative tissue expander fill volume were not statistically associated with second-stage procedure complications in this patient subset. Tobacco use (P = 0.006) and radiation therapy (P = 0.004) were found to be statistically significantly associated with sustaining complications after both phases of reconstruction (Table 6).
DISCUSSION The literature is now replete with evidence describing the various risk factors for complications after tissue expanderYbased breast reconstruction. With the end goal of a durable, cosmetically appealing permanent implant reconstruction, all patients would ideally undergo a second operation to exchange the tissue expander for a permanent prosthesis. In this setting, we felt it useful to elucidate the determinants of complications after the second stage of reconstruction, particularly in those suffering complications after placement of tissue expanders. These data could then be used as an evidence-based foundation for patient counseling after a tissue expander complication as well as a guideline for possible conversion to autologous reconstruction. As is commonly known, complications of tissue expander reconstruction can be related to patient comorbidities,10,19 tobacco use,10,19,36 insult to the mastectomy flaps,22,37 reconstructive adjuncts
TABLE 1. Risk Factors for Complications During Reconstruction Characteristic Age, yr BMI HTN DM Smoker Chemotherapy Radiation Acellular dermal matrix Expander fill, mL
Complications (n = 79 Women)
No Complications (n = 117 Women)
P
51.86 T 10.55 29.55 T 6.45 30 (51.7%) 8 (57.1%) 33 (57.9%) 31 (38.8%) 29 (49.2%) 70 (39.3%) 205.13 T 109.95
50.96 T 11.15 28.32 T 7.24 28 (48.3%) 6 (42.9%) 24 (42.1%) 49 (61.3%) 30 (50.8%) 108 (60.7%) 188.38 T 111.69
0.578 0.600 0.035 0.183 0.001 0.712 0.098 0.379 0.994
BMI, body mass index; HTN, hypertension; DM, diabetes mellitus.
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Annals of Plastic Surgery
Adkinson et al
TABLE 2. Logistic Regression of Risk Factors for Any Complication (P G 0.001)
Characteristic
N
P
Adjusted OR
95% Confidence Interval
SmokerVactive SmokerVremote Non-smoker HTN No HTN
22 35
0.007 0.023
58
0.031
3.709 2.423 1.0 2.030 1.0
1.434 9.593 1.129 5.108 Reference 1.069 3.856 Reference
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TABLE 4. Permanent Implant Complication After Tissue Expander Complication in Patients Undergoing Both Stages of Reconstruction Permanent Implant Complication
Expander complication
Yes No
Total
Yes
No
Total
14 (42.4%) 25 (18.8%) 39 (23.5%)
19 (57.6%) 108 (81.2%) 127 (76.5%)
33 (100%) 133 (100%) 166 (100%)
P = 0.004.
HTN, hypertension.
(ie, acellular dermal matrix),22,38,39 the prosthetic device,15,40 and/or neoadjuvant/adjuvant modalities for cancer treatment.33,41,42 In our series, complications occurred in 27.6% of patients after tissue expander placement and 23.5% of patients after exchange to a permanent implant. A smaller cohort of 14 patients (8.4%) suffered complications after both procedures. Age, BMI, diabetes mellitus, chemotherapy, use of acellular dermal matrix, and the volume of intraoperative tissue expander fill volume did not statistically correlate with an increased likelihood for complications at any point during the reconstructive timeline. Physiologically, tobacco use impairs both wound healing43,44 and flap survival45Y47 through a mechanism involving vasoconstriction, platelet adhesion, and a relative hypoxia secondary to carboxyhemoglobinemia.16,43,44 In multivariate analysis of all patients, tobacco use (both active and remote) was associated with an increased likelihood for complications. In fact, active tobacco use increased the risk of complications 3.7 times, while remote use increased the risk 2.4 times. Smoking is generally considered to be a risk factor for complications, particularly wound healing, after breast reconstruction.16,43,47 In a study by Goodwin et al,46 tobacco use led to an increased risk for overall complications, skin flap loss, and reconstructive failure. We noted a similar trend. Analysis of all patients after tissue expander placement also revealed that hypertension was associated with a 2-fold increased risk for complications. Hypertension is independently linked to both arterial rigidity and blood hyperviscosity48,49Vcharacteristics that would predispose to poor wound healing, flap necrosis, and infection. A similar relationship between the presence of hypertension and tissue expanderY related complications has been noted in a study by McCarthy et al in 1170 tissue expander-implant reconstructions.19 Radiation has repeatedly been shown to increase post-surgical complications in patients undergoing tissue expander reconstruction.10,31Y36,50,51 Though not statistically significant in initial univariate analysis of all patients, radiation therapy was determined to be associated with exchange procedure complications in those with a salvaged tissue expander complication. This discrepancy is likely explained by
the timing of radiation therapy, which typically occurs after placement of a tissue expander in our network, thus causing an ischemic insult to the surgical environment. Subsequent surgery in this compromised wound bed leads to an increased risk for complications. Consistent with previous studies,17,30,41 infection was the most common complication (54% of all complications after placement of tissue expander) and the most likely reason for explantation (73% of all explants). Further, complication rates were higher after the initial expander placement compared to the exchange procedure (27.6% vs. 23.5%). This trend has been noted previously17,23,52 and is attributable to the surgical insult of mastectomy flap elevation. The unique focus of this study has shown that patients with complications after expander insertion were 3 times more likely to have exchange procedure complications and 9 times more likely to fail implant-based reconstruction. This relationship was statistically linked to both tobacco use and radiation therapy. While studies have shown modest success in the setting of radiation,17,35,52Y56 this patient subset may be best served by immediate or delayed autologous techniques.3,57Y61 Importantly, hypertension was associated with tissue-expander placement complications, but did not contribute to the complications and failure after the exchange procedure. Spear et al62 have shown a high rate of success (92.3%) with repeat prosthetic reconstruction in those initially failing implant reconstruction as a result of infection or exposure (average BMI of 24.7 and 15% rate of radiation). Though these results are encouraging, our patients sustaining a complication differed significantly: average BMI of 29.55 and 26.7% rate of radiation (29 of 79 patients). In our patient population, we recommend early conversion to autologous techniques in tobacco users and radiated patients sustaining significant complications after tissue expander placement. By implementing this change in strategy, surgeons may mitigate the significant negative psychological impact on patients and prevent the potentially prolonged reconstructive timeline resulting from a failed implant reconstruction. As with any retrospective review, our study has several limitations, including the lack of standard documentation among surgeons and missing data points. During the study collection period, 17 women were still awaiting the exchange procedure; this subset was excluded
TABLE 3. Types of Complications After Each Stage of Surgery Complication Infection Flap necrosis Hematoma/seroma Capsular contracture Implant exposure Implant rupture Nipple necrosis Total complications
26
Expander Placement (n = 54 Women) 39 13 10 2 3 4 1 72
(54.2%) (18.1%) (13.9%) (2.8%) (4.2%) (5.6%) (1.4%) (100%)
Exchange Procedure (n = 39 Women) 15 6 6 13 4 3
(31.9%) (12.8%) (12.8%) (27.7%) (8.5%) (6.4%) V 47 (100%)
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TABLE 5. Failed Permanent Implant Reconstruction After Tissue Expander Complication in Patients Undergoing Both Stages of Reconstruction Failed Permanent Implant Reconstruction
Expander complication
Yes No
Total
Yes
No
Total
4 (12.1%) 2 (1.5%) 6 (3.6%)
29 (87.9%) 131 (98.5%) 160 (96.4%)
33 (100%) 133 (100%) 166 (100%)
P = 0.003.
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Tissue Expander Complications
TABLE 6. Univariate Analysis of 33 Patients With Expander Complications Undergoing Exchange Procedure Characteristic Age, yr BMI HTN DM Smoker Chemotherapy Radiation Acellular dermal matrix Expander fill, mL
Expander Complication Only (n = 19)
Expander and Exchange Procedure Complication (n = 14)
P
50.42 T 9.34 29.77 T 5.85 6 (13.3%) 2 (18.2%) 7 (17.5%) 3 (4.8%) 0 (0.0%) 18 (11.7%) 219.47 T 113.21
51.00 T 11.74 28.55 T 7.20 5 (11.1%) 0 (0.0%) 8 (20.0%) 8 (12.9%) 7 (17.5%) 13 (8.4%) 188.57 T 77.64
0.998 0.595 0.462 0.127 0.006 0.102 0.004 0.790 0.308
BMI, body mass index; HTN, hypertension; DM, diabetes mellitus.
from the final analysis. Additional considerations include the possibility of varied surgical techniques among the 4 surgeons included in the study and the exclusion of cancer staging. Further, only 5 of the 196 patients underwent prophylactic mastectomy in this series and, as such, the presence of cancer as a determinant of complications could not be assessed with any degree of statistical significance.
CONCLUSION Despite complications, approximately 90% of women successfully complete tissue expanderYbased breast reconstruction. However, women who experience complications during the expansion phase of breast reconstruction are at significantly increased risk for complications and reconstructive failure after placement of a permanent implant. The patient who experiences a complication during the expander phase should be closely followed, as this cohort has a much higher likelihood of failing implant-based breast reconstruction. As a result, we recommend early conversion to autologous reconstruction in patients with significant tissue expander complications, particularly in the setting of tobacco use and radiation therapy.
10. Serletti JM, Fosnot J, Nelson JA, et al. Breast reconstruction after breast cancer. Plast Reconstr Surg. 2011;127:124eY135e. 11. American Society of Plastic Surgeons. Report of the 2008 National Clearinghouse of Plastic Surgery Statistics. Available at: http://www.plasticsurgery.org/Media/ stats/2008-UScosmetic-reconstructive-plastic-surgery-minimally-invasivestatistics.pdf. Accessed July 1, 2009. 12. American Society of Plastic Surgeons. 2010 report of the 2009 statistics. National Clearinghouse of Plastic Surgery Statistics. Retained from: http:// www.plasticsurgery.org/Documents/Media/statistics/2009UScosmeticreconstructive plasticsurgeryminimally-invasive-statistics.pdf. 13. Spear SL, Mardini S, Ganz JC. Resource cost comparison of implant-based breast reconstruction versus TRAM flap breast reconstruction. Plast Reconstr Surg. 2003;112:101Y105. 14. Spear SL, Newman MK, Bedford MS, et al. A retrospective analysis of outcomes using three common methods for immediate breast reconstruction. Plast Reconstr Surg. 2008;122:340Y347. 15. O’Brien W, Hasselgren PO, Hummel R, et al. Comparison of postoperative wound complications and early cancer recurrence between patients undergoing mastectomy with or without immediate breast reconstruction. Am J Surg. 1993;166:1Y5. 16. Goodwin SJ, McCarthy CM, Pusic AL, et al. Complications in smokers after postmastectomy tissue expander/implant breast reconstruction. Ann Plast Surg. 2005;55:16Y20. 17. Cordeiro PG, McCarthy CM. A single surgeon’s 12-year experience with tissue expander/implant breast reconstruction: part I. A prospective analysis of early complications. Plast Reconstr Surg. 2006;118:825Y831.
ACKNOWLEDGMENT We would like to thank Jacqueline Grove, Medical Editor, Lehigh Valley Health Network, for her assistance with this manuscript.
18. McCarthy CM, Disa JJ, Pusic AL, et al. The effect of closed-suction drains on the incidence of local wound complications following tissue expander/implant reconstruction: a cohort study. Plast Reconstr Surg. 2007;119:2018Y2022.
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20. Preminger BA, McCarthy CM, Hu QY, et al. The influence of AlloDerm on expander dynamics and complications in the setting of immediate tissue expander/implant reconstruction: a matched-cohort study. Ann Plast Surg. 2008;60:510Y513. 21. Sbitany H, Sandeen SN, Amalfi AN, et al. Acellular dermis-assisted prosthetic breast reconstruction versus complete submuscular coverage: a head-to-head comparison of outcomes. Plast Reconstr Surg. 2009;124:1735Y1740. 22. Antony AK, McCarthy CM, Cordeiro PG, et al. Acellular human dermis implantation in 153 immediate two-stage tissue expander breast reconstructions: determining the incidence and significant predictors of complications. Plast Reconstr Surg. 2010;125:1606Y1614. 23. Alderman AK, Wilkins EG, Kim HM, et al. Complications in postmastectomy breast reconstruction: two-year results of the Michigan Breast Reconstruction Outcome Study. Plast Reconstr Surg. 2002;109:2265Y2274. 24. Pinsolle V, Grinfeder C, Mathoulin-Pelissier S, et al. Complications analysis of 266 immediate breast reconstructions. J Plast Reconstr Aesthet Surg. 2006;59:1017Y1024. 25. Woerdeman LA, Hage JJ, Smeulders MJ, et al. Skin-sparing mastectomy and immediate breast reconstruction by use of implants: an assessment of risk factors for complications and cancer control in 120 patients. Plast Reconstr Surg. 2006;118:321Y330. 26. Woerdeman LA, Hage J, Hofland MM, et al. A prospective assessment of surgical risk factors in 400 cases of skin-sparing mastectomy and immediate
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Annals of Plastic Surgery
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43. Krueger JK, Rohrich RJ. Clearing the smoke: the scientific rationale for tobacco abstention with plastic surgery. Plast Reconstr Surg. 2001;108:1063Y1073; discussion 1074Y1077. 44. Silverstein P. Smoking and wound healing. Am J Med. 1992;93:22SY24S. 45. Nolan J, Jenkins RA, Kurihara K, et al. The acute effects of cigarette smoke exposure on experimental skin flaps. Plast Reconstr Surg. 1985;75:544Y551. 46. Chang LD, Buncke G, Slezak S, et al. Cigarette smoking, plastic surgery and microsurgery. J Reconstr Microsurg. 1996;12:467Y474. 47. Spear SL, Ducic I, Cuoco F, et al. The effect of smoking on flap and donor-site complications in pedicled TRAM breast reconstruction. Plast Reconstr Surg. 2005;116:1873Y1880. 48. Levenson J, Simon AC, Cambien FA, et al. Cigarette smoking and hypertension. Factors independently associated with blood hyperviscosity and arterial rigidity. Arteriosclerosis. 1987;7:572Y577. 49. Tsuchida Y, Fukuda O, Kamata S. The correlation of skin blood flow with age, total cholesterol, hematocrit, blood pressure, and hemoglobin. Plast Reconstr Surg. 1991;88:844Y850. 50. Liu AS, Kao HK, Reish RG, et al. Postoperative complications in prosthesisbased breast reconstruction using acellular dermal matrix. Plast Reconstr Surg. 2011;127:1755Y1762. 51. Kronowitz SJ, Robb GL. Radiation therapy and breast reconstruction: a critical review of the literature. Plast Reconstr Surg. 2009;124:395Y408. 52. Miller AP, Falcone RE. Breast reconstruction: systemic factors influencing local complications. Ann Plast Surg. 1991;27:115Y120. 53. Paulhe P, Aubert JP, Magalon G. Forum on tissue expansion. Are tissue expansion and radiotherapy compatible? Apropos of a series of 50 consecutive breast reconstructions. Ann Chir Plast Esthet. 1993;38:54Y61. 54. Evans GR, Schusterman MA, Kroll SS, et al. Reconstruction and the radiated breast: is there a role for implants? Plast Reconstr Surg. 1995;96:1111Y1115. 55. Cordeiro PG, Pusic AL, Disa JJ, et al. Irradiation after immediate tissue expander/implant breast reconstruction: outcomes, complications, aesthetic results, and satisfaction among 156 patients. Plast Reconstr Surg. 2004;113: 877Y881. 56. Percec I, Bucky LP. Successful prosthetic breast reconstruction after radiation therapy. Ann Plast Surg. 2008;60:527Y531. 57. Vandeweyer E, Deraemaecker R, Nogaret JM, et al. Immediate breast reconstruction with implants and adjuvant chemotherapy: a good option? Acta Chir Belg. 2003;103:98Y101. 58. Krueger EA, Wilkins EG, Strawderman M, et al. Complications and patient satisfaction following expander/implant breast reconstruction with and without radiotherapy. Int J Radiat Oncol Biol Phys. 2001;49:713Y721. 59. Kroll SS, Schusterman MA, Reece GP, et al. Breast reconstruction with myocutaneous flaps in previously irradiated patients. Plast Reconstr Surg. 1994;93:460Y469; discussion 470Y471. 60. Taylor CW, Horgan K, Dodwell D. Oncological aspects of breast reconstruction. Breast. 2005;14:118Y130. 61. Corral CJ, Mustoe TA. Controversy in breast reconstruction. Surg Clin North Am. 1996;76:309Y326. 62. Spear SL, Masden D, Rao SS, et al. Long-term outcomes of failed prosthetic breast reconstruction. Ann Plast Surg. 2013;71:286Y291.
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