BREAST SURGERY
Evolving Trends in Autologous Breast Reconstruction Is the Deep Inferior Epigastric Artery Perforator Flap Taking Over? Irene Pien, BS, Sophia Caccavale, BS, Michael C. Cheung, MD, Parag Butala, MD, Duncan B. Hughes, MD, Cassandra Ligh, MD, Michael R. Zenn, MD, and Scott T. Hollenbeck, MD Background: Enthusiasm for the deep inferior epigastric artery perforator (DIEP) flap for autologous breast reconstruction has grown in recent years. However, this flap is not performed at all centers or by all plastic surgeons for breast reconstruction, and it is unclear whether practice patterns have measurably changed. This study aimed to (1) evaluate changing trends in breast flap use in the United States in recent years and (2) identify how these trends have affected charges and costs associated with autologous breast reconstruction. Methods: Patients undergoing autologous breast reconstruction [latissimus dorsi (LD), pedicled transverse rectus abdominus myocutaneous (pTRAM), free TRAM (fTRAM), and DIEP] were identified using the Healthcare Cost and Utilization Project Nationwide Inpatient Sample database (2009-2011). A total of 19,182 hospital discharges were reviewed. Patient demographics, hospital teaching center status, payer status, length of stay, total charges, and total costs per discharge were reviewed. Statistical analysis was performed using linear regression, t test, and analysis of variance models. Results: Between 2009 and 2011, the total number of discharges did not change significantly. Patient age distribution was similar for all flap groups. For individual flaps, there was a significant increase in DIEP flaps (P = 0.03), with a decreasing trend for other abdominal-based flaps. The patients receiving DIEP flap breast reconstruction were covered by private insurance at a higher rate than all other flap procedures (P = 0.03), whereas other potential cost determinants did not differ significantly between the groups. The mean charge per flap was $40,704 for LD, $51,933 for pTRAM, $69,909 for f TRAM, and $82,320 for DIEP. The mean cost per flap was $12,017 for LD, $15,538 for pTRAM, $20,756 for fTRAM, and $23,616 for DIEP. Conclusions: Between 2009 and 2011, the total amount of autologous breast reconstruction discharges was relatively stable, but the number of DIEP flaps increased significantly. Review of the Healthcare Cost and Utilization Project Nationwide Inpatient Sample data shows that, compared with LD, pTRAM, and f TRAM flaps, the DIEP flap is associated with higher charges and costs. Key Words: breast reconstruction, autologous breast reconstruction, economics of health care, health care use (Ann Plast Surg 2016;76: 489Y493)
T
hree hundred thousand women are diagnosed with invasive or in situ breast cancer annually in the United States.1 Nearly 36% of women with early-stage and 60% with late-stage breast cancer undergo therapeutic mastectomy2; furthermore, contralateral and bilateral prophylactic mastectomy rates continue to rise.3 The American Society of Plastic Surgery estimates that more than 91,000 patients underwent breast reconstructive procedures in 2012,4 with implantbased techniques remaining the most commonly used modality for
Received June 13, 2014, and accepted for publication, after revision, July 23, 2014. From the Division of Plastic and Reconstructive Surgery, Duke University Health System, Durham, NC. Conflicts of interest and sources of funding: none declared. Reprints: Scott T. Hollenbeck, MD, Duke University Medical Center, Box 3945, Durham, NC 27710. E-mail: [email protected]. Copyright * 2014 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0148-7043/16/7605-0489 DOI: 10.1097/SAP.0000000000000339
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breast reconstruction. Autologous techniques still account for 20% of breast reconstruction, which has remained unchanged during the past 10 years.4Y6 The 4 most commonly used options for autologous breast reconstruction include the latissimus dorsi (LD) flap, the pedicled transverse rectus abdominus myocutaneous (pTRAM) flap, the free or muscle-sparing free TRAM (f TRAM) flap, and the deep inferior epigastric artery perforator (DIEP) flap. The DIEP flap was first described by Allen and Treece7 in 1994 as an alternative method for breast reconstruction. By eliminating muscle harvest, this perforator flap has the theoretical benefit of decreased donor site morbidity compared with pTRAM and f TRAM flaps.8Y11 The popularity of this flap has grown in recent years, in part because of the increase in surgeons trained in this technique. Patients, too, have become increasingly aware about the potential differences in specific autologous breast reconstruction techniques and seek the best results with the least amount of recovery and long-term disability.12 The aims of this study were to evaluate the use of these 4 flaps and to determine whether the popularity of the DIEP flap with patients has translated into a greater percentage of DIEP flaps performed over time. With increasing focus placed on health care costs and optimization of health care delivery, analyzing the potential differences in economic burden of breast reconstruction techniques both in the United States and elsewhere is becoming a critical issue.13Y15 The secondary goal was to assess whether changes in flap selection has had an effect on the charges and costs associated with autologous breast reconstruction in the United States.
PATIENTS AND METHODS Patient data were extracted from the Healthcare Cost and Utilization Project (HCUP) Nationwide Inpatient Sample (NIS) database for review. This is the largest all-payer inpatient database in the United States and captures a 20% sample of all hospital discharges. This sample is routinely used to estimate national statistics in health care use.16 Specific procedures may be queried as ‘‘primary’’ or ‘‘all-listed’’ procedures. Patients undergoing autologous breast reconstruction were defined using the International Classification of Diseases, Ninth Revision (ICD-9) procedure codes. Beginning in 2009, the HCUP NIS divided autologous breast reconstruction into individual flap types; TRAM flaps were further subspecified as pTRAM, f TRAM, and DIEP flaps. Inclusion criteria for the study were patients who underwent procedures using LD (ICD-9 85.71), pTRAM (85.72), f TRAM (85.73), and DIEP (85.74) flaps listed as the primary procedure between 2009 and 2011. This included patients undergoing both immediate and delayed reconstructions but excluded patients whose flap procedure was not listed as the primary procedure. Between 2009 and 2011, a total of 19,182 records were identified for the study. The study assessment included patient age, hospital teaching status, insurance status, costs, and charges. Patient age is reported categorically by the HCUP NIS in bins comprising 1 to 17, 18 to 44, 45 to 64, and 65 to 84 years old. Teaching status for a hospital is defined as either teaching or nonteaching. For a hospital to be considered a teaching hospital, it must have residency training approval designated by the www.annalsplasticsurgery.com
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Accreditation Council for Graduate Medical Education, be a member of the Council of Teaching Hospitals, or have a ratio of resident trainees to beds of 0.25 or higher.16 Insurance status is defined as the expected primary payer and includes Medicare, Medicaid, private insurance, uninsured, or other. Charges are reported by the NIS as those charges provided by the hospital except for professional fees and noncovered charges.16 The HCUP NIS reports costs by converting total charges to costs using cost-charge ratios based on hospital accounting reports from the Centers for Medicare and Medicaid Services.16 Statistical analysis was performed using JMP Pro software (SAS Institute, Cary, NC) functions for Student t test, analysis of variance (ANOVA), and regression analyses.17
RESULTS Data from 19,182 breast flap reconstructions were analyzed for 2009 through 2011. The most common age group represented was the 45- to 64-year-old category, and this was true for all 4 flaps (Table 1). A higher percentage of DIEP flap patients were 18 to 44 years old (31.2%) than other flap types; however, this was not statistically significant. For the 65- to 84-year-old category, LD flaps were performed more frequently than abdominal flaps, although the exact percentages of flaps performed for this 65-to-84 bin cannot be determined from HCUP data because of the low numbers of procedures in this age category. The total number of flap procedures occurring annually did not change significantly per year: 6249 in 2009, 6552 in 2010, and 6381 in 2011. The trend in numbers of specific flap procedures performed during the 3-year study period was variable (Fig. 1). Overall, LD flaps were performed more commonly than other flaps. The number of LD flap procedures performed did not change significantly during the 3 years studied (R2 G 0.001, P = 0.99). The number of pTRAM procedures decreased, but this change was not significant (NS) (R2 = 0.808, P = 0.29). The number of f TRAM procedures decreased significantly (R2 = 0.999, P = 0.02), and the number of DIEP procedures increased significantly (R2 = 0.997, P = 0.03). For determinants of costs and use, there was a significant difference among the 4 flap procedure types in regard to hospital teaching status, patient insurance status, and length of stay (ANOVA, P G 0.05) (Table 2). Specifically, a greater percentage of DIEP procedures (82.9%) were performed in teaching hospitals in comparison with LD procedures (61.5%, P G 0.05). In addition, a significantly higher percentage of DIEP procedures were performed on patients with private insurance than f TRAM, pTRAM, and LD procedures (80.2% vs 71.4% vs 67.6% vs 67.4%, respectively; P G 0.05). The length of stay for DIEP procedures was significantly greater than that for LD procedures (4.6 vs 2.5 days; P G 0.05) but did not differ from that for pTRAM or f TRAM flaps (NS). The 3-year mean charges per flap procedure were highly variable (ANOVA, P G 0.05) (Fig. 2A). The mean charges for the DIEP procedures ($82,320) were significantly greater than the mean charges for LD ($40,704, P = 0.004) and pTRAM ($51,933, P = 0.01) flaps. During the study period, the mean charge per flap did not change significantly TABLE 1. Distribution of Age Among Patients Receiving Autologous Breast Reconstructions (2009Y2011) Age Group
LD
pTRAM
fTRAM
DIEP
Overall P
18Y44 45Y64 65Y84
24.3 (3.1) 65.7 (6.3) 10.0 (1.6)
21.7 (3.6) 68.4 (8.1) *
29.1 (5.4) 67.8 (10.3) *
31.2 (7.7) 68.8 (14.2) *
0.89 0.92 *
Data are expressed as estimates of national mean (SEM) percentage, as calculated by HCUPnet. *Incomplete HCUPnet data.
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FIGURE 1. Autologous breast reconstruction by flap type, 2009 to 2011. The total number of flaps performed as primary procedure on a yearly basis is shown for each flap type. Data are expressed as estimates of total US procedures + SEM, as provided by HCUPnet. *Regression analysis (ANOVA of bivariate fit by year; P G 0.05).
between years (Fig. 2B). The 3-year mean costs per flap procedure were also highly variable (ANOVA, P G 0.001) (Fig. 3A). The mean costs for the DIEP flap ($23,616) were significantly greater than the mean costs for the 3 other flaps, LD ($12,017, P = 0.003), pTRAM ($15,538, P = 0.012), and f TRAM ($20,756, P = 0.017). The mean costs per flap did not change significantly between years in the study period (Fig. 3B).
DISCUSSION Since its description in the 1990s, enthusiasm for the musclepreserving DIEP flap over conventional TRAM flaps has steadily grown among patients and surgeons alike. The literature is replete with reports of decreased abdominal wall morbidity and quicker recovery with patients undergoing DIEP flap procedures relative to traditional pTRAM and f TRAM flaps.8Y11,18 The public has become more aware of these potential benefits, and surgeons seeking to capture patients can be readily found marketing this approach. Until recently, it has been difficult to quantify the impact that the DIEP flap has had on autologous breast flap reconstruction. Now, data from the HCUP NIS demonstrate that national trends in flap selection for autologous breast reconstruction are indeed changing to favor the DIEP flap over the pTRAM and f TRAM flaps. These data also highlight the financial ramifications associated with this change and allow identification of potential areas for cost savings in the future. Surprisingly, the number of LD flap reconstructions has not changed during the 3-year study period. In fact, LD flaps were performed more commonly than any other flap studied. However, the HCUP NIS data identify several distinct differences for LD flap patients relative to DIEP flap patients. Specifically, LD flaps were performed significantly less frequently at teaching hospitals (62%) and significantly less frequently on private insurance patients (67%) than were DIEP flaps (83% and 80%, respectively). On the basis of the HCUP NIS data, it is difficult to determine what drives this difference, but clearly, LD flaps remain an alternative to abdominal-based flaps and seem unaffected by the increasing popularity of DIEP flaps, particularly in nonacademic centers. This corroborates the findings based on a survey of nearly 500 practicing American Society of Plastic Surgery plastic surgeons, which showed a significantly higher percentage of DIEP procedures performed by those in academic settings versus solo practice.19 It is well established that increases in surgical complexity are often associated with an increase in costs. This has recently been shown by Albornoz et al,15 using the NIS data to evaluate the economic impact of * 2014 Wolters Kluwer Health, Inc. All rights reserved.
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Is the DIEP Flap Taking Over?
TABLE 2. Available Determinants of Charges and Costs Mean (SEM) percentage of procedures performed in teaching hospitals Mean (SEM) percentage of patients receiving procedures covered by private insurance Mean (SEM) length of stay, d
LD
pTRAM
fTRAM
DIEP
Overall P
61.5 (7.3)* 67.4 (6.96)* 2.5 (0.3)*
70.2 (10.2) 67.6 (8.8)* 4.0 (0.2)
72.7 (15.1) 71.4 (12.2)* 4.7 (0.1)
82.9 (18.0) 80.2 (18.4)* 4.6 (0.2)
0.034† 0.013† 0.013†
*Student t test (DIEP vs LD, P G 0.05). †ANOVA between f lap types, P G 0.05.
recent trends in immediate autologous breast reconstruction. In that study, although procedures were not categorized by specific flap type, the authors did find increased costs associated with complex microsurgical reconstructions. Importantly, the HCUP NIS data do not reflect the potential long-term cost savings of flap reconstruction or the decreased disability associated with microsurgical flap reconstruction. To truly compare cost, one should compare the entire cost of reconstruction during a lifetime. It is unfair to compare the hospital admission costs of DIEP flap reconstruction with a 1-time admission for tissue expander placement or implant exchange or capsulotomy. One could certainly view the increased charges and costs associated with microsurgical breast reconstruction as a longterm investment because the technique avoids the repeated operations
often required for implant-related complications over time.20Y23 Indeed, others have demonstrated this cost-effectiveness for autologous reconstruction compared with implant reconstruction during the long-term.24 Operating room and perioperative efficiencies have become a focal point for autologous breast flap costs and potential savings. Some authors suggest that cost savings could be gained by performing these complex procedures only at high-volume centers, which have decreased hospital charges both in the setting of reconstruction complications and without, a finding recently identified by Albornoz et al15 in regard to immediate autologous breast reconstruction. One of the interesting findings of this study is insurance coverage trends for patients undergoing DIEP f laps; these patients
FIGURE 2. A, Mean charges per flap (2009Y2011). The mean charges for each flap procedure are expressed as US dollars + SEM, as calculated by HCUPnet. ANOVA between the 4 flaps, P G 0.05. *Student t test, LD versus DIEP, P = 0.004. **Student t test, pTRAM versus DIEP, P = 0.01. B, Trend in annual mean charges per flap (2009Y2011). The mean charges for each flap procedure are expressed as US dollars + SEM, as calculated by HCUPnet. Regression analysis (ANOVA of bivariate fit within each flap type; NS). * 2014 Wolters Kluwer Health, Inc. All rights reserved.
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FIGURE 3. A, Mean cost per flap from 2009 to 2011. The mean costs for each procedure are expressed as US dollars + SEM, as calculated by HCUPnet. ANOVA between the 4 flaps, P G 0.001. *Student t test, LD versus DIEP, P = 0.003. **Student t test, pTRAM versus DIEP, P = 0.012. ***Student t test, fTRAM versus DIEP, P = 0.017. B, Trend in annual mean costs per flap (2009Y2011). The mean costs for each flap procedure are expressed as US dollars + SEM, as calculated by HCUPnet. Regression analysis (ANOVA of bivariate fit within each flap type; NS).
were covered significantly more by private insurance compared with other f laps. Rates of postmastectomy breast reconstruction, too, are affected by patient insurance status,25 but it is perhaps surprising that the type of reconstruction the patient receives is correlated with insurance status. It should be noted that, if more than 1 payer is listed for a hospital discharge, only the first-listed payer is reported in the HCUP NIS for classifying insurance status; this may overestimate or underestimate insurance coverage for this cohort.16 Nonetheless, the reason for this finding is unclear, although one might argue that patients with private insurance are savvier when it comes to health care consumption. Patients with private health insurance use the Internet for health information more frequently than those with other types of insurance coverage,26 so it is conceivable that they might be more aware of and seek out surgeons who advertise DIEP f lap services. It is also possible that surgeons offer DIEP f laps at a higher rate to those who are privately insured, feeling that the time and effort associated with perforator breast f lap reconstruction will be reimbursed higher. It may not be financially viable to offer such lengthy and resource-heavy procedures to payers such as Medicaid, where surgeons can actually lose money on the procedure. 492
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It is clear from the HCUP NIS data that DIEP f lap breast reconstruction is associated with higher charges and costs compared with all other f laps examined. It should be noted that ‘‘charges’’ are somewhat arbitrary and often have no clear relationship with costs and actual reimbursement but do serve as a metric of perceived value. Still, these findings could be a ref lection of the relatively longer operative times of the procedure or special equipment required.27,28 The length of stay did not differ significantly from pTRAM and f TRAM f laps, making major complications as a determinant of charges and costs unlikely. Review of the literature reveals studies that have reported both shortened18,29 and lengthened30 hospital stays with DIEP f lap reconstruction, so this seems more experience and volume related rather than actual procedural differences. There is a learning curve for any new f lap, and perforator f lap dissection is certainly more complex and time consuming than myocutaneous f lap dissection.27,31 As previously stated, NIS charges and costs do not account for professional fees, so any additional billing associated with performing a DIEP f lap does not explain these findings. A number of limitations to this study should be considered. From the data available, it cannot be determined whether patients have * 2014 Wolters Kluwer Health, Inc. All rights reserved.
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undergone unilateral or bilateral reconstructions. It is possible that more DIEP flap patients have had bilateral reconstructions in comparison with pTRAM flap patients and that this is a determinant of cost that has not been assessed. In addition, the current ICD-9 procedure codes do not distinguish a full muscle harvest f TRAM from a muscle-sparing f TRAM flap, so it is difficult to know how these cases were coded. The coding of DIEP flaps is presumed to be consistent with the accepted definition for DIEP flaps as a complete muscle-preserving flap,32 but this cannot be determined precisely and is dependent on the preferences of the coder. One additional aspect of charges and costs that these data raise is the potential differences among hospital types (teaching vs nonteaching, low- vs high-volume centers). This is a complex question given the potential differences that exist between patients typically treated at major academic centers versus community hospitals. A number of studies have shown improved outcomes for certain procedures at high-volume centers,33Y35 and we suspect that breast flap surgery is similar. However, this concept remains to be determined for this subset of procedures and is the subject of our ongoing research. Finally, the HCUP NIS data used in this study are inclusive of only f laps listed as the ‘‘primary’’ procedure. Thus, it is quite possible that the procedures included in this study are more likely to represent delayed breast reconstructions because mastectomy is often considered the primary procedure in immediate reconstruction cases. However, this is not always the case because some institutions list the reconstruction procedure as the primary procedure on the basis of relative value units weighting. At the present time, the HCUP NIS data are not complete when searching for DIEP f laps coded as an all-listed procedure.
SUMMARY Review of the HCUP NIS data on autologous breast reconstruction illustrates that the use of the DIEP f lap is increasing and replacing the use of other free abdominal f laps, although pTRAM f laps remained stable. Overall, the rate of autologous breast reconstruction also remained relatively stable. Latissimus dorsi f laps are the most common procedure performed annually for autologous breast reconstruction, but DIEP f laps are rapidly approaching similar numbers. Further economic analysis will be required to see whether the increased costs and charges associated with the DIEP f lap can be sustained moving forward in a constrained health care environment. REFERENCES 1. American Cancer Society. Breast Cancer Facts & Figures 2013Y2014. Atlanta, GA: American Cancer Society Inc; 2013. 2. Siegel R, DeSantis C, Virgo K, et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin. 2012;62:220Y241. 3. Pesce CE, Liederbach E, Czechura T, et al. Changing surgical trends in young patients with early stage breast cancer, 2003-2010: a report from the National Cancer Data Base. J Am Coll Surg. 2014;219:19Y28. 4. American Society of Plastic Surgeons. 2012 Plastic Surgery Statistics Report. Arlington Heights, IL: American Society of Plastic Surgeons; 2013. 5. Cemal Y, Albornoz CR, Disa JJ, et al. A paradigm shift in U.S. breast reconstruction: part 2. The influence of changing mastectomy patterns on reconstructive rate and method. Plast Reconstr Surg. 2013;131:320eY326e. 6. Albornoz CR, Bach PB, Mehrara BJ, et al. A paradigm shift in U.S. breast reconstruction: increasing implant rates. Plast Reconstr Surg. 2013;131:15Y23. 7. Allen RJ, Treece P. Deep inferior epigastric perforator flap for breast reconstruction. Ann Plast Surg. 1994;32:32Y38. 8. Egeberg A, Rasmussen MK, Sorensen JA. Comparing the donor-site morbidity using DIEP, SIEA or MS-TRAM flaps for breast reconstructive surgery: a meta-analysis. J Plast Reconstr Aesthet Surg. 2012;65:1474Y1480. 9. Chang EI, Chang EI, Soto-Miranda MA, et al. Comprehensive analysis of donor-site morbidity in abdominally based free flap breast reconstruction. Plast Reconstr Surg. 2013;132:1383Y1391. 10. Bottero L, Lefaucheur JP, Fadhul S, et al. Electromyographic assessment of rectus abdominis muscle function after deep inferior epigastric perforator flap surgery. Plast Reconstr Surg. 2004;113:156Y161.
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11. Man LX, Selber JC, Serletti JM. Abdominal wall following free TRAM or DIEP flap reconstruction: a meta-analysis and critical review. Plast Reconstr Surg. 2009;124:752Y764. 12. Duggal CS, Metcalfe D, Sackeyfio R, et al. Patient motivations for choosing postmastectomy breast reconstruction. Ann Plast Surg. 2013;70:574Y580. 13. Damen TH, Wei W, Mureau MA, et al. Medium-term cost analysis of breast reconstructions in a single Dutch centre: a comparison of implants, implants preceded by tissue expansion, LD transpositions and DIEP flaps. J Plast Reconstr Aesthet Surg. 2011;64:1043Y1053. 14. Israeli R, Funk S, Reaven NL. Comparative analysis of 18-month outcomes and costs of breast reconstruction flap procedures. Plast Reconstr Surg. 2014;133:471Y479. 15. Albornoz CR, Cordeiro PG, Mehrara BJ, et al. Economic implications of recent trends in U.S. immediate autologous breast reconstruction. Plast Reconstr Surg. 2014;133:463Y470. 16. HCUP Nationwide Inpatient Sample (NIS). Healthcare Cost and Utilization Project (HCUP). 2007Y2009. Rockville, MD: Agency for Healthcare Research and Quality. Available at: http://www.hcup-us.ahrq.gov/nisoverview.jsp Accessed March 24, 2014. 17. JMP Pro. Version 11.0. Cary, NC: SAS Institute Inc; 1989Y2007. 18. Garvey PB, Buchel EW, Pockaj BA, et al. DIEP and pedicled TRAM flaps: a comparison of outcomes. Plast Reconstr Surg. 2006;117:1711Y1721. 19. Gurunluoglu R, Gurunluoglu A, Williams SA, et al. Current trends in breast reconstruction: survey of American Society of Plastic Surgeons 2010. Ann Plast Surg. 2013;70:103Y110. 20. Fischer JP, Wes AM, Nelson JA, et al. Propensity-matched, longitudinal outcomes analysis of complications and cost comparing abdominal free flaps and implant-based breast reconstruction. J Am Coll Surg. 2014;219:303Y312. 21. Woerdeman LA, Hage JJ, Hofland MM, et al. A prospective assessment of surgical risk factors in 400 cases of skin-sparing mastectomy and immediate breast reconstruction with implants to establish selection criteria. Plast Reconstr Surg. 2007;119:455Y463. 22. Baschnagel AM, Shah C, Wilkinson JB, et al. Failure rate and cosmesis of immediate tissue expander/implant breast reconstruction after postmastectomy irradiation. Clin Breast Cancer. 2012;12:428Y432. 23. Fischer JP, Nelson JA, Cleveland E, et al. Breast reconstruction modality outcome study: a comparison of expander/implants and free flaps in select patients. Plast Reconstr Surg. 2013;131:928Y934. 24. Grover R, Padula WV, Van Vliet M, et al. Comparing five alternative methods of breast reconstruction surgery: a cost-effectiveness analysis. Plast Reconstr Surg. 2013;132:709eY723e. 25. Coburn N, Fulton J, Pearlman DN, et al. Treatment variation by insurance status for breast cancer patients. Breast J. 2008;14:128Y134. 26. Cohen RA, Adams PF. Use of the Internet for Health Information: United States, 2009. Washington, DC: NCHS Data Brief: US Department of Health and Human Services; 2011. 27. Hofer SO, Damen TH, Mureau MA, et al. A critical review of perioperative complications in 175 free deep inferior epigastric perforator flap breast reconstructions. Ann Plast Surg. 2007;59:137Y142. 28. Kroll SS, Reece GP, Miller MJ, et al. Comparison of cost for DIEP and free TRAM flap breast reconstructions. Plast Reconstr Surg. 2001;107:1413Y1416; discussion 1417Y1418. 29. Kroll SS, Sharma S, Koutz C, et al. Postoperative morphine requirements of free TRAM and DIEP flaps. Plast Reconstr Surg. 2001;107:338Y341. 30. Chevray PM. Breast reconstruction with superficial inferior epigastric artery flaps: a prospective comparison with TRAM and DIEP flaps. Plast Reconstr Surg. 2004;114:1077Y1083. 31. Busic V, Das-Gupta R, Mesic H, et al. The deep inferior epigastric perforator flap for breast reconstruction, the learning curve explored. J Plast Reconstr Aesthet Surg. 2006;59:580Y584. 32. Hallock GG. Muscle perforator flaps: the name game. Ann Plast Surg. 2003;51: 630Y632. 33. Halm EA. Is volume related to outcome in health care? A systematic review and methodologic critique of the literature. Ann Intern Med. 2002;137:511. 34. Finlayson EV, Goodney PP, Birkmeyer JD. Hospital volume and operative mortality in cancer surgery: a national study. Arch Surg. 2003;138:721Y725; discussion 726. 35. Birkmeyer JD, Stukel TA, Siewers AE, et al. Surgeon volume and operative mortality in the United States. N Engl J Med. 2003;349:2117Y2127.
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493
Evolving Trends in Autologous Breast Reconstruction Is the Deep Inferior Epigastric Artery Perforator Flap Taking Over? Irene Pien, BS, Sophia Caccavale, BS, Michael C. Cheung, MD, Parag Butala, MD, Duncan B. Hughes, MD, Cassandra Ligh, MD, Michael R. Zenn, MD, and Scott T. Hollenbeck, MD Background: Enthusiasm for the deep inferior epigastric artery perforator (DIEP) flap for autologous breast reconstruction has grown in recent years. However, this flap is not performed at all centers or by all plastic surgeons for breast reconstruction, and it is unclear whether practice patterns have measurably changed. This study aimed to (1) evaluate changing trends in breast flap use in the United States in recent years and (2) identify how these trends have affected charges and costs associated with autologous breast reconstruction. Methods: Patients undergoing autologous breast reconstruction [latissimus dorsi (LD), pedicled transverse rectus abdominus myocutaneous (pTRAM), free TRAM (fTRAM), and DIEP] were identified using the Healthcare Cost and Utilization Project Nationwide Inpatient Sample database (2009-2011). A total of 19,182 hospital discharges were reviewed. Patient demographics, hospital teaching center status, payer status, length of stay, total charges, and total costs per discharge were reviewed. Statistical analysis was performed using linear regression, t test, and analysis of variance models. Results: Between 2009 and 2011, the total number of discharges did not change significantly. Patient age distribution was similar for all flap groups. For individual flaps, there was a significant increase in DIEP flaps (P = 0.03), with a decreasing trend for other abdominal-based flaps. The patients receiving DIEP flap breast reconstruction were covered by private insurance at a higher rate than all other flap procedures (P = 0.03), whereas other potential cost determinants did not differ significantly between the groups. The mean charge per flap was $40,704 for LD, $51,933 for pTRAM, $69,909 for f TRAM, and $82,320 for DIEP. The mean cost per flap was $12,017 for LD, $15,538 for pTRAM, $20,756 for fTRAM, and $23,616 for DIEP. Conclusions: Between 2009 and 2011, the total amount of autologous breast reconstruction discharges was relatively stable, but the number of DIEP flaps increased significantly. Review of the Healthcare Cost and Utilization Project Nationwide Inpatient Sample data shows that, compared with LD, pTRAM, and f TRAM flaps, the DIEP flap is associated with higher charges and costs. Key Words: breast reconstruction, autologous breast reconstruction, economics of health care, health care use (Ann Plast Surg 2016;76: 489Y493)
T
hree hundred thousand women are diagnosed with invasive or in situ breast cancer annually in the United States.1 Nearly 36% of women with early-stage and 60% with late-stage breast cancer undergo therapeutic mastectomy2; furthermore, contralateral and bilateral prophylactic mastectomy rates continue to rise.3 The American Society of Plastic Surgery estimates that more than 91,000 patients underwent breast reconstructive procedures in 2012,4 with implantbased techniques remaining the most commonly used modality for
Received June 13, 2014, and accepted for publication, after revision, July 23, 2014. From the Division of Plastic and Reconstructive Surgery, Duke University Health System, Durham, NC. Conflicts of interest and sources of funding: none declared. Reprints: Scott T. Hollenbeck, MD, Duke University Medical Center, Box 3945, Durham, NC 27710. E-mail: [email protected]. Copyright * 2014 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0148-7043/16/7605-0489 DOI: 10.1097/SAP.0000000000000339
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breast reconstruction. Autologous techniques still account for 20% of breast reconstruction, which has remained unchanged during the past 10 years.4Y6 The 4 most commonly used options for autologous breast reconstruction include the latissimus dorsi (LD) flap, the pedicled transverse rectus abdominus myocutaneous (pTRAM) flap, the free or muscle-sparing free TRAM (f TRAM) flap, and the deep inferior epigastric artery perforator (DIEP) flap. The DIEP flap was first described by Allen and Treece7 in 1994 as an alternative method for breast reconstruction. By eliminating muscle harvest, this perforator flap has the theoretical benefit of decreased donor site morbidity compared with pTRAM and f TRAM flaps.8Y11 The popularity of this flap has grown in recent years, in part because of the increase in surgeons trained in this technique. Patients, too, have become increasingly aware about the potential differences in specific autologous breast reconstruction techniques and seek the best results with the least amount of recovery and long-term disability.12 The aims of this study were to evaluate the use of these 4 flaps and to determine whether the popularity of the DIEP flap with patients has translated into a greater percentage of DIEP flaps performed over time. With increasing focus placed on health care costs and optimization of health care delivery, analyzing the potential differences in economic burden of breast reconstruction techniques both in the United States and elsewhere is becoming a critical issue.13Y15 The secondary goal was to assess whether changes in flap selection has had an effect on the charges and costs associated with autologous breast reconstruction in the United States.
PATIENTS AND METHODS Patient data were extracted from the Healthcare Cost and Utilization Project (HCUP) Nationwide Inpatient Sample (NIS) database for review. This is the largest all-payer inpatient database in the United States and captures a 20% sample of all hospital discharges. This sample is routinely used to estimate national statistics in health care use.16 Specific procedures may be queried as ‘‘primary’’ or ‘‘all-listed’’ procedures. Patients undergoing autologous breast reconstruction were defined using the International Classification of Diseases, Ninth Revision (ICD-9) procedure codes. Beginning in 2009, the HCUP NIS divided autologous breast reconstruction into individual flap types; TRAM flaps were further subspecified as pTRAM, f TRAM, and DIEP flaps. Inclusion criteria for the study were patients who underwent procedures using LD (ICD-9 85.71), pTRAM (85.72), f TRAM (85.73), and DIEP (85.74) flaps listed as the primary procedure between 2009 and 2011. This included patients undergoing both immediate and delayed reconstructions but excluded patients whose flap procedure was not listed as the primary procedure. Between 2009 and 2011, a total of 19,182 records were identified for the study. The study assessment included patient age, hospital teaching status, insurance status, costs, and charges. Patient age is reported categorically by the HCUP NIS in bins comprising 1 to 17, 18 to 44, 45 to 64, and 65 to 84 years old. Teaching status for a hospital is defined as either teaching or nonteaching. For a hospital to be considered a teaching hospital, it must have residency training approval designated by the www.annalsplasticsurgery.com
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Accreditation Council for Graduate Medical Education, be a member of the Council of Teaching Hospitals, or have a ratio of resident trainees to beds of 0.25 or higher.16 Insurance status is defined as the expected primary payer and includes Medicare, Medicaid, private insurance, uninsured, or other. Charges are reported by the NIS as those charges provided by the hospital except for professional fees and noncovered charges.16 The HCUP NIS reports costs by converting total charges to costs using cost-charge ratios based on hospital accounting reports from the Centers for Medicare and Medicaid Services.16 Statistical analysis was performed using JMP Pro software (SAS Institute, Cary, NC) functions for Student t test, analysis of variance (ANOVA), and regression analyses.17
RESULTS Data from 19,182 breast flap reconstructions were analyzed for 2009 through 2011. The most common age group represented was the 45- to 64-year-old category, and this was true for all 4 flaps (Table 1). A higher percentage of DIEP flap patients were 18 to 44 years old (31.2%) than other flap types; however, this was not statistically significant. For the 65- to 84-year-old category, LD flaps were performed more frequently than abdominal flaps, although the exact percentages of flaps performed for this 65-to-84 bin cannot be determined from HCUP data because of the low numbers of procedures in this age category. The total number of flap procedures occurring annually did not change significantly per year: 6249 in 2009, 6552 in 2010, and 6381 in 2011. The trend in numbers of specific flap procedures performed during the 3-year study period was variable (Fig. 1). Overall, LD flaps were performed more commonly than other flaps. The number of LD flap procedures performed did not change significantly during the 3 years studied (R2 G 0.001, P = 0.99). The number of pTRAM procedures decreased, but this change was not significant (NS) (R2 = 0.808, P = 0.29). The number of f TRAM procedures decreased significantly (R2 = 0.999, P = 0.02), and the number of DIEP procedures increased significantly (R2 = 0.997, P = 0.03). For determinants of costs and use, there was a significant difference among the 4 flap procedure types in regard to hospital teaching status, patient insurance status, and length of stay (ANOVA, P G 0.05) (Table 2). Specifically, a greater percentage of DIEP procedures (82.9%) were performed in teaching hospitals in comparison with LD procedures (61.5%, P G 0.05). In addition, a significantly higher percentage of DIEP procedures were performed on patients with private insurance than f TRAM, pTRAM, and LD procedures (80.2% vs 71.4% vs 67.6% vs 67.4%, respectively; P G 0.05). The length of stay for DIEP procedures was significantly greater than that for LD procedures (4.6 vs 2.5 days; P G 0.05) but did not differ from that for pTRAM or f TRAM flaps (NS). The 3-year mean charges per flap procedure were highly variable (ANOVA, P G 0.05) (Fig. 2A). The mean charges for the DIEP procedures ($82,320) were significantly greater than the mean charges for LD ($40,704, P = 0.004) and pTRAM ($51,933, P = 0.01) flaps. During the study period, the mean charge per flap did not change significantly TABLE 1. Distribution of Age Among Patients Receiving Autologous Breast Reconstructions (2009Y2011) Age Group
LD
pTRAM
fTRAM
DIEP
Overall P
18Y44 45Y64 65Y84
24.3 (3.1) 65.7 (6.3) 10.0 (1.6)
21.7 (3.6) 68.4 (8.1) *
29.1 (5.4) 67.8 (10.3) *
31.2 (7.7) 68.8 (14.2) *
0.89 0.92 *
Data are expressed as estimates of national mean (SEM) percentage, as calculated by HCUPnet. *Incomplete HCUPnet data.
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FIGURE 1. Autologous breast reconstruction by flap type, 2009 to 2011. The total number of flaps performed as primary procedure on a yearly basis is shown for each flap type. Data are expressed as estimates of total US procedures + SEM, as provided by HCUPnet. *Regression analysis (ANOVA of bivariate fit by year; P G 0.05).
between years (Fig. 2B). The 3-year mean costs per flap procedure were also highly variable (ANOVA, P G 0.001) (Fig. 3A). The mean costs for the DIEP flap ($23,616) were significantly greater than the mean costs for the 3 other flaps, LD ($12,017, P = 0.003), pTRAM ($15,538, P = 0.012), and f TRAM ($20,756, P = 0.017). The mean costs per flap did not change significantly between years in the study period (Fig. 3B).
DISCUSSION Since its description in the 1990s, enthusiasm for the musclepreserving DIEP flap over conventional TRAM flaps has steadily grown among patients and surgeons alike. The literature is replete with reports of decreased abdominal wall morbidity and quicker recovery with patients undergoing DIEP flap procedures relative to traditional pTRAM and f TRAM flaps.8Y11,18 The public has become more aware of these potential benefits, and surgeons seeking to capture patients can be readily found marketing this approach. Until recently, it has been difficult to quantify the impact that the DIEP flap has had on autologous breast flap reconstruction. Now, data from the HCUP NIS demonstrate that national trends in flap selection for autologous breast reconstruction are indeed changing to favor the DIEP flap over the pTRAM and f TRAM flaps. These data also highlight the financial ramifications associated with this change and allow identification of potential areas for cost savings in the future. Surprisingly, the number of LD flap reconstructions has not changed during the 3-year study period. In fact, LD flaps were performed more commonly than any other flap studied. However, the HCUP NIS data identify several distinct differences for LD flap patients relative to DIEP flap patients. Specifically, LD flaps were performed significantly less frequently at teaching hospitals (62%) and significantly less frequently on private insurance patients (67%) than were DIEP flaps (83% and 80%, respectively). On the basis of the HCUP NIS data, it is difficult to determine what drives this difference, but clearly, LD flaps remain an alternative to abdominal-based flaps and seem unaffected by the increasing popularity of DIEP flaps, particularly in nonacademic centers. This corroborates the findings based on a survey of nearly 500 practicing American Society of Plastic Surgery plastic surgeons, which showed a significantly higher percentage of DIEP procedures performed by those in academic settings versus solo practice.19 It is well established that increases in surgical complexity are often associated with an increase in costs. This has recently been shown by Albornoz et al,15 using the NIS data to evaluate the economic impact of * 2014 Wolters Kluwer Health, Inc. All rights reserved.
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Is the DIEP Flap Taking Over?
TABLE 2. Available Determinants of Charges and Costs Mean (SEM) percentage of procedures performed in teaching hospitals Mean (SEM) percentage of patients receiving procedures covered by private insurance Mean (SEM) length of stay, d
LD
pTRAM
fTRAM
DIEP
Overall P
61.5 (7.3)* 67.4 (6.96)* 2.5 (0.3)*
70.2 (10.2) 67.6 (8.8)* 4.0 (0.2)
72.7 (15.1) 71.4 (12.2)* 4.7 (0.1)
82.9 (18.0) 80.2 (18.4)* 4.6 (0.2)
0.034† 0.013† 0.013†
*Student t test (DIEP vs LD, P G 0.05). †ANOVA between f lap types, P G 0.05.
recent trends in immediate autologous breast reconstruction. In that study, although procedures were not categorized by specific flap type, the authors did find increased costs associated with complex microsurgical reconstructions. Importantly, the HCUP NIS data do not reflect the potential long-term cost savings of flap reconstruction or the decreased disability associated with microsurgical flap reconstruction. To truly compare cost, one should compare the entire cost of reconstruction during a lifetime. It is unfair to compare the hospital admission costs of DIEP flap reconstruction with a 1-time admission for tissue expander placement or implant exchange or capsulotomy. One could certainly view the increased charges and costs associated with microsurgical breast reconstruction as a longterm investment because the technique avoids the repeated operations
often required for implant-related complications over time.20Y23 Indeed, others have demonstrated this cost-effectiveness for autologous reconstruction compared with implant reconstruction during the long-term.24 Operating room and perioperative efficiencies have become a focal point for autologous breast flap costs and potential savings. Some authors suggest that cost savings could be gained by performing these complex procedures only at high-volume centers, which have decreased hospital charges both in the setting of reconstruction complications and without, a finding recently identified by Albornoz et al15 in regard to immediate autologous breast reconstruction. One of the interesting findings of this study is insurance coverage trends for patients undergoing DIEP f laps; these patients
FIGURE 2. A, Mean charges per flap (2009Y2011). The mean charges for each flap procedure are expressed as US dollars + SEM, as calculated by HCUPnet. ANOVA between the 4 flaps, P G 0.05. *Student t test, LD versus DIEP, P = 0.004. **Student t test, pTRAM versus DIEP, P = 0.01. B, Trend in annual mean charges per flap (2009Y2011). The mean charges for each flap procedure are expressed as US dollars + SEM, as calculated by HCUPnet. Regression analysis (ANOVA of bivariate fit within each flap type; NS). * 2014 Wolters Kluwer Health, Inc. All rights reserved.
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FIGURE 3. A, Mean cost per flap from 2009 to 2011. The mean costs for each procedure are expressed as US dollars + SEM, as calculated by HCUPnet. ANOVA between the 4 flaps, P G 0.001. *Student t test, LD versus DIEP, P = 0.003. **Student t test, pTRAM versus DIEP, P = 0.012. ***Student t test, fTRAM versus DIEP, P = 0.017. B, Trend in annual mean costs per flap (2009Y2011). The mean costs for each flap procedure are expressed as US dollars + SEM, as calculated by HCUPnet. Regression analysis (ANOVA of bivariate fit within each flap type; NS).
were covered significantly more by private insurance compared with other f laps. Rates of postmastectomy breast reconstruction, too, are affected by patient insurance status,25 but it is perhaps surprising that the type of reconstruction the patient receives is correlated with insurance status. It should be noted that, if more than 1 payer is listed for a hospital discharge, only the first-listed payer is reported in the HCUP NIS for classifying insurance status; this may overestimate or underestimate insurance coverage for this cohort.16 Nonetheless, the reason for this finding is unclear, although one might argue that patients with private insurance are savvier when it comes to health care consumption. Patients with private health insurance use the Internet for health information more frequently than those with other types of insurance coverage,26 so it is conceivable that they might be more aware of and seek out surgeons who advertise DIEP f lap services. It is also possible that surgeons offer DIEP f laps at a higher rate to those who are privately insured, feeling that the time and effort associated with perforator breast f lap reconstruction will be reimbursed higher. It may not be financially viable to offer such lengthy and resource-heavy procedures to payers such as Medicaid, where surgeons can actually lose money on the procedure. 492
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It is clear from the HCUP NIS data that DIEP f lap breast reconstruction is associated with higher charges and costs compared with all other f laps examined. It should be noted that ‘‘charges’’ are somewhat arbitrary and often have no clear relationship with costs and actual reimbursement but do serve as a metric of perceived value. Still, these findings could be a ref lection of the relatively longer operative times of the procedure or special equipment required.27,28 The length of stay did not differ significantly from pTRAM and f TRAM f laps, making major complications as a determinant of charges and costs unlikely. Review of the literature reveals studies that have reported both shortened18,29 and lengthened30 hospital stays with DIEP f lap reconstruction, so this seems more experience and volume related rather than actual procedural differences. There is a learning curve for any new f lap, and perforator f lap dissection is certainly more complex and time consuming than myocutaneous f lap dissection.27,31 As previously stated, NIS charges and costs do not account for professional fees, so any additional billing associated with performing a DIEP f lap does not explain these findings. A number of limitations to this study should be considered. From the data available, it cannot be determined whether patients have * 2014 Wolters Kluwer Health, Inc. All rights reserved.
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undergone unilateral or bilateral reconstructions. It is possible that more DIEP flap patients have had bilateral reconstructions in comparison with pTRAM flap patients and that this is a determinant of cost that has not been assessed. In addition, the current ICD-9 procedure codes do not distinguish a full muscle harvest f TRAM from a muscle-sparing f TRAM flap, so it is difficult to know how these cases were coded. The coding of DIEP flaps is presumed to be consistent with the accepted definition for DIEP flaps as a complete muscle-preserving flap,32 but this cannot be determined precisely and is dependent on the preferences of the coder. One additional aspect of charges and costs that these data raise is the potential differences among hospital types (teaching vs nonteaching, low- vs high-volume centers). This is a complex question given the potential differences that exist between patients typically treated at major academic centers versus community hospitals. A number of studies have shown improved outcomes for certain procedures at high-volume centers,33Y35 and we suspect that breast flap surgery is similar. However, this concept remains to be determined for this subset of procedures and is the subject of our ongoing research. Finally, the HCUP NIS data used in this study are inclusive of only f laps listed as the ‘‘primary’’ procedure. Thus, it is quite possible that the procedures included in this study are more likely to represent delayed breast reconstructions because mastectomy is often considered the primary procedure in immediate reconstruction cases. However, this is not always the case because some institutions list the reconstruction procedure as the primary procedure on the basis of relative value units weighting. At the present time, the HCUP NIS data are not complete when searching for DIEP f laps coded as an all-listed procedure.
SUMMARY Review of the HCUP NIS data on autologous breast reconstruction illustrates that the use of the DIEP f lap is increasing and replacing the use of other free abdominal f laps, although pTRAM f laps remained stable. Overall, the rate of autologous breast reconstruction also remained relatively stable. Latissimus dorsi f laps are the most common procedure performed annually for autologous breast reconstruction, but DIEP f laps are rapidly approaching similar numbers. Further economic analysis will be required to see whether the increased costs and charges associated with the DIEP f lap can be sustained moving forward in a constrained health care environment. REFERENCES 1. American Cancer Society. Breast Cancer Facts & Figures 2013Y2014. Atlanta, GA: American Cancer Society Inc; 2013. 2. Siegel R, DeSantis C, Virgo K, et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin. 2012;62:220Y241. 3. Pesce CE, Liederbach E, Czechura T, et al. Changing surgical trends in young patients with early stage breast cancer, 2003-2010: a report from the National Cancer Data Base. J Am Coll Surg. 2014;219:19Y28. 4. American Society of Plastic Surgeons. 2012 Plastic Surgery Statistics Report. Arlington Heights, IL: American Society of Plastic Surgeons; 2013. 5. Cemal Y, Albornoz CR, Disa JJ, et al. A paradigm shift in U.S. breast reconstruction: part 2. The influence of changing mastectomy patterns on reconstructive rate and method. Plast Reconstr Surg. 2013;131:320eY326e. 6. Albornoz CR, Bach PB, Mehrara BJ, et al. A paradigm shift in U.S. breast reconstruction: increasing implant rates. Plast Reconstr Surg. 2013;131:15Y23. 7. Allen RJ, Treece P. Deep inferior epigastric perforator flap for breast reconstruction. Ann Plast Surg. 1994;32:32Y38. 8. Egeberg A, Rasmussen MK, Sorensen JA. Comparing the donor-site morbidity using DIEP, SIEA or MS-TRAM flaps for breast reconstructive surgery: a meta-analysis. J Plast Reconstr Aesthet Surg. 2012;65:1474Y1480. 9. Chang EI, Chang EI, Soto-Miranda MA, et al. Comprehensive analysis of donor-site morbidity in abdominally based free flap breast reconstruction. Plast Reconstr Surg. 2013;132:1383Y1391. 10. Bottero L, Lefaucheur JP, Fadhul S, et al. Electromyographic assessment of rectus abdominis muscle function after deep inferior epigastric perforator flap surgery. Plast Reconstr Surg. 2004;113:156Y161.
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11. Man LX, Selber JC, Serletti JM. Abdominal wall following free TRAM or DIEP flap reconstruction: a meta-analysis and critical review. Plast Reconstr Surg. 2009;124:752Y764. 12. Duggal CS, Metcalfe D, Sackeyfio R, et al. Patient motivations for choosing postmastectomy breast reconstruction. Ann Plast Surg. 2013;70:574Y580. 13. Damen TH, Wei W, Mureau MA, et al. Medium-term cost analysis of breast reconstructions in a single Dutch centre: a comparison of implants, implants preceded by tissue expansion, LD transpositions and DIEP flaps. J Plast Reconstr Aesthet Surg. 2011;64:1043Y1053. 14. Israeli R, Funk S, Reaven NL. Comparative analysis of 18-month outcomes and costs of breast reconstruction flap procedures. Plast Reconstr Surg. 2014;133:471Y479. 15. Albornoz CR, Cordeiro PG, Mehrara BJ, et al. Economic implications of recent trends in U.S. immediate autologous breast reconstruction. Plast Reconstr Surg. 2014;133:463Y470. 16. HCUP Nationwide Inpatient Sample (NIS). Healthcare Cost and Utilization Project (HCUP). 2007Y2009. Rockville, MD: Agency for Healthcare Research and Quality. Available at: http://www.hcup-us.ahrq.gov/nisoverview.jsp Accessed March 24, 2014. 17. JMP Pro. Version 11.0. Cary, NC: SAS Institute Inc; 1989Y2007. 18. Garvey PB, Buchel EW, Pockaj BA, et al. DIEP and pedicled TRAM flaps: a comparison of outcomes. Plast Reconstr Surg. 2006;117:1711Y1721. 19. Gurunluoglu R, Gurunluoglu A, Williams SA, et al. Current trends in breast reconstruction: survey of American Society of Plastic Surgeons 2010. Ann Plast Surg. 2013;70:103Y110. 20. Fischer JP, Wes AM, Nelson JA, et al. Propensity-matched, longitudinal outcomes analysis of complications and cost comparing abdominal free flaps and implant-based breast reconstruction. J Am Coll Surg. 2014;219:303Y312. 21. Woerdeman LA, Hage JJ, Hofland MM, et al. A prospective assessment of surgical risk factors in 400 cases of skin-sparing mastectomy and immediate breast reconstruction with implants to establish selection criteria. Plast Reconstr Surg. 2007;119:455Y463. 22. Baschnagel AM, Shah C, Wilkinson JB, et al. Failure rate and cosmesis of immediate tissue expander/implant breast reconstruction after postmastectomy irradiation. Clin Breast Cancer. 2012;12:428Y432. 23. Fischer JP, Nelson JA, Cleveland E, et al. Breast reconstruction modality outcome study: a comparison of expander/implants and free flaps in select patients. Plast Reconstr Surg. 2013;131:928Y934. 24. Grover R, Padula WV, Van Vliet M, et al. Comparing five alternative methods of breast reconstruction surgery: a cost-effectiveness analysis. Plast Reconstr Surg. 2013;132:709eY723e. 25. Coburn N, Fulton J, Pearlman DN, et al. Treatment variation by insurance status for breast cancer patients. Breast J. 2008;14:128Y134. 26. Cohen RA, Adams PF. Use of the Internet for Health Information: United States, 2009. Washington, DC: NCHS Data Brief: US Department of Health and Human Services; 2011. 27. Hofer SO, Damen TH, Mureau MA, et al. A critical review of perioperative complications in 175 free deep inferior epigastric perforator flap breast reconstructions. Ann Plast Surg. 2007;59:137Y142. 28. Kroll SS, Reece GP, Miller MJ, et al. Comparison of cost for DIEP and free TRAM flap breast reconstructions. Plast Reconstr Surg. 2001;107:1413Y1416; discussion 1417Y1418. 29. Kroll SS, Sharma S, Koutz C, et al. Postoperative morphine requirements of free TRAM and DIEP flaps. Plast Reconstr Surg. 2001;107:338Y341. 30. Chevray PM. Breast reconstruction with superficial inferior epigastric artery flaps: a prospective comparison with TRAM and DIEP flaps. Plast Reconstr Surg. 2004;114:1077Y1083. 31. Busic V, Das-Gupta R, Mesic H, et al. The deep inferior epigastric perforator flap for breast reconstruction, the learning curve explored. J Plast Reconstr Aesthet Surg. 2006;59:580Y584. 32. Hallock GG. Muscle perforator flaps: the name game. Ann Plast Surg. 2003;51: 630Y632. 33. Halm EA. Is volume related to outcome in health care? A systematic review and methodologic critique of the literature. Ann Intern Med. 2002;137:511. 34. Finlayson EV, Goodney PP, Birkmeyer JD. Hospital volume and operative mortality in cancer surgery: a national study. Arch Surg. 2003;138:721Y725; discussion 726. 35. Birkmeyer JD, Stukel TA, Siewers AE, et al. Surgeon volume and operative mortality in the United States. N Engl J Med. 2003;349:2117Y2127.
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