THE AXILLARY VERSUS INTERNAL MAMMARY RECIPIENT VESSEL SITES FOR BREAST RECONSTRUCTION WITH DIEP FLAPS: A RETROSPECTIVE STUDY OF 256 CONSECUTIVE CASES FABIO SANTANELLI
DI
POMPEO, M.D., Ph.D.,* BENEDETTO LONGO, M.D., Ph.D., MICHAIL SOROTOS, M.D., MARCO
PAGNONI, M.D., and ROSARIA LAPORTA, M.D.
The aim of this study is to present our experience on the use of various recipient sites for deep inferior epigastric perforator (DIEP) flap breast reconstruction and compare them by means of objective data. Two hundred fifty six DIEP flap breast reconstructions, performed between March 2004 and May 2011, were retrospectively analyzed. Only unilateral reconstructions were included in the study and divided into three groups depending on the recipient site choice: internal mammary vessels (IMV) (n 5 52), thoracodorsal vessels (TDV) (n 5 109), and circumflex scapular vessels (CSV) (n 5 95). Clinical records of each patient were reviewed to acquire relevant data such as operative time, postoperative complications, and use of a second vein anastomosis. CSV group showed a statistically significant lower operative time (4.92 6 0.54 hours) compared to TDV (5.67 6 1.01 hours) and IMV groups (6.75 6 1.09 hours) (P < 0.001). Second vein anastomosis was performed in 84 cases (88.1%) of CSV, in 85 cases (77.9%) of TDV, and in 18 cases (35.1%) of IMV groups (P < 0.001). No significant differences were observed among groups regarding risk factors and complications (P > 0.05). The axillary vessels seem to be the ideal recipient site because of reduced operative time and increased possibility to perform a second vein anastomosis. Among them, CSV can be safely used due to following advantages: easy dissection, larger vessel caliber, and optimal flap insetting. C 2014 Wiley Periodicals, Inc. Microsurgery Moreover, their location does not expose them completely to radiotherapy consequences. V 00:000–000, 2014.
Autologous tissue is considered the gold standard by many authors for breast reconstruction and among free flaps the deep inferior epigastric perforator (DIEP) flap and the superficial inferior epigastric artery (SIEA) flap are the most popular choices.1–3 Selection of adequate recipient vessels is one of the keys for success in free tissue transfer. Initially, the most common recipient vessels were those of the axillary system, including the thoracodorsal and the circumflex scapular pedicle, as first described by Holmstr€om in 1979.4 The use of the internal mammary vessels (IMV), described in 1980 by Harashina, has been recommended as the first choice for breast microsurgical reconstruction since 1996, while IMV perforators were described in 2001 and have been routinely proposed since 2007.5–8 Progress in the field of oncology including the skin sparing mastectomy (SSM),9,10 the evolution in the surgical management of the lymphatic axillary system of women with breast cancer (sentinel lymph node), and recent studies on the perforator flap flow led us to reconsider the circumflex scapular vessels (CSV) for microvascular breast reconstruction.11–13 Currently, in the absence of a widely accepted algorithm, choice of recipient Plastic Surgery Unit, Sant’Andrea Hospital, School of Medicine and Psychology, “Sapienza” University of Rome, Rome, Italy *Correspondence to: Fabio Santanelli di Pompeo, M.D., Ph.D., Plastic Surgery Unit, c/o Azienda Ospedaliera Sant’Andrea, Via di Grottarossa 10351039, 00189 Rome, Italy. E-mail: [email protected] Received 30 September 2013; Revision accepted 10 April 2014; Accepted 11 April 2014 Published online 00 Month 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/micr.22266 Ó 2014 Wiley Periodicals, Inc.
vessels in free flap breast reconstruction is based on surgeon’s experience. The aim of this study is to present our experience on the use of the various recipient sites for DIEP flap breast reconstruction and compare them by means of objective data. PATIENTS AND METHODS
A retrospective analysis of 256 consecutive breast reconstructions with the DIEP flap performed by the senior author (FS) between March 2004 and May 2011 was performed. Patients undergoing unilateral reconstruction were included and they were divided into three groups depending on the recipient site choice: IMV (n 5 52), thoracodorsal vessels (TDV) (n 5 109), and CSV (n 5 95). All patients received preoperative computerized-tomography angiography to evaluate the flap perforators’ pattern and, as other studies confirm, proved helpful in identifying the ideal perforator.14 On the other hand, we did not perform any radiologic study for the recipient vessels. The following risk factors were evaluated: patient’s age, body mass index (BMI), and personal history of smoking, radiotherapy, or chemotherapy.15 Clinical records of each patient were reviewed to acquire relevant data such as operative time, postoperative complications, and use of a second vein anastomosis. In all procedures, the deep inferior epigastric vessels were dissected down to their origin from the external iliac vessels to obtain as long pedicle as possible and when present the superficial inferior epigastric vein was harvested down to its origin. All IMV were exposed after removal of a portion of the
2
Santanelli di Pompeo et al. Table 1. Patient Related Risk Factors Incidence Among Groups
No. of patients Age (years) (mean 6 SD) BMI (kg/m2) (mean 6 SD) Smoking history (cases/%) Preoperative radiotherapy (cases/%) Preoperative chemotherapy (cases/%)
IMV
TDV
CSV
P-value
52 53.06 6 9.02 29.3 6 3.01 7 (13.4%) 4 (7.7%) 6 (11.5%)
109 50.12 6 9.95 28.7 6 3.81 17 (15.6%) 10 (9.2%) 17 (15.5%)
95 51.99 6 9.80 28.5 6 3.01 17 (17.8%) 8 (8.4%) 12 (12.6%)
0.902 0.783 0.773 0.949 0.730
IMV: internal mammary vessels group; TDV: thoracodorsal vessels group; CSV: circumflex scapular vessels group.
Table 2. Number of Perforators Selected and Divided by Groups No. of perforators 4 3 2 1
IMV
TDV
CSV
0 8 28 16
3 20 71 15
1 15 53 26
IMV: internal mammary vessels group; TDV: thoracodorsal vessels group; CSV: circumflex scapular vessels group.
Table 3. Complications Incidence Among Groups Complication (cases/%) Hematoma Seroma Partial flap necrosis Total flap necrosis Arterial Thrombosis Venous Thrombosis
IMV
CSV
TDV
P-value
1 (1.9%) 1 (1.9%) 8 (15.3%) 1 (1.9%) 0 (0%) 1 (1.9%)
2 (2.1%) 2 (2.1%) 8 (7.6%) 0 (0%) 1 (1.05%) 1 (1.05%)
1 (0.9%) 1 (0.9%) 16 (14.6%) 0 (0%) 0 (0%) 1 (0.9%)
0.408 0.427 0.232 0.487 0.512 0.342
IMV: internal mammary vessels group; TDV: thoracodorsal vessels group; CSV: circumflex scapular vessels group.
third rib, while TDV and CSV were prepared through the previous mastectomy access or by a new “T” incision in the axillary fold, during axillary node dissection in immediate reconstructions or separately in delayed ones, as described in literature.6,16–19 The Chi-squared tests were used for the continuous variable (operative time) and the evaluation of the risk factors. The Kruskal Wallis and Bonferroni tests analyzed categorical variables such as the incidence of complications and the use of second vein anastomosis. A P-value 0.05 was considered significant. RESULTS
The three groups were homogeneous regarding the patient’s age and the other risk factors (Table 1) (P > 0.05). Seven (13.4%) patients had a smoking history, 4 (7.7%) had received neoadjuvant radiotherapy, and 6 (11.5%) neoadjuvant chemotherapy in the IMV compared to 17 (15.6%) with a smoking history, 10 (9.2%) that had received preoperative radiotherapy, and 17 (15.5%) preoperative chemotherapy in the TDV Microsurgery DOI 10.1002/micr
group. In the CSV group, 17 (17.8%) patients were smokers, 8 (8.4%) had undergone preoperative radiotherapy, and 12 (12.6%) preoperative chemotherapy. Table 2 summarizes the number of perforators selected and divided by groups. CSV group showed a statistically significant lower operative time (4.92 6 0.54 hours) compared to TDV (5.67 6 1.01 hours) and IMV groups (6.75 6 1.09 hours) (P < 0.001). Second vein anastomosis was performed in 84 cases (88.1%) of CSV, in 85 cases (77.9%) of TDV, and in 18 cases (35.1%) of IMV groups (P < 0.001). From the data, the second vein anastomosis was always available in TDV and CSV groups and considered unnecessary by the surgeon in selected cases, while in IMV group was not done because of the unmatched caliber in 28 of 34 cases and in 6 was considered unnecessary by the surgeon. No significant differences were observed among groups regarding complications (Table 3) (P > 0.05). More specifically in IMV group 8 (15.3%) flaps suffered partial necrosis, compared to 16 (14.6%) in TDV and 8 (7.6%) in CSV. One (1.9%) hematoma and one (1.9%) seroma were seen in IMV group, compared to 1 (0.9%) hematoma and 1 (0.9%) seroma in TDV and 2 (2.1%) hematomas and 2 (2.1%) seromas in CSV group. One (1.9%) venous thrombosis was observed in IMV group, one (0.9%) in TDV, and one (1.05%) in CSV group. One (1.9%) total flap necrosis was encountered in the IMV group and one (1.05%) arterial thrombosis was seen in the CSV group. DISCUSSION
The choice of recipient vessels is one of the key points for microvascular breast reconstruction because flap perfusion and operative time depend on their reliability and surgical site. Both IMV and TDV are usually easy to expose, of suitable caliber, permit an end-to-end anastomosis, and have demonstrated success in this setting. The choice is largely up to the reconstructive surgeon and usually based on comfort level and experience, flow characteristics, chest topography, and patient comorbidities. Currently, the recent trend in literature advocates
Recipient Vessel Sites
the use of IMV as recipient artery and vein of choice.11,16–18,20 Nevertheless, some authors note unpredictable quality and inconsistency of the internal mammary veins diameter at the level of the fourth rib often necessitating vein grafts.21 Time for vessels’ dissection and exposure in immediate reconstruction represents another issue in favor of the axillary vessels, that is, the preparation of these vessels contemporaneously with the axillary lymphadenectomy or sentinel lymph node biopsy by the general surgeon while the access to the IMV adds an extra “step” to the surgical procedure. Moran et al.,20 in a prospective study reported no difference in operative times between IMV and TDV, while in our report CSV group showed a statistically significant lower operative time compared to TDV and IMV groups (P < 0.001). The analysis of the evolution, in time, of recipient site selection showed an inversion of the trend between TDV and CSV and a continuous decrease of the IMV. CSV and TDV are both located in the axilla; the latter are more superficial and anterior, which is supposed to make dissection faster than the deeper and posteriorly located CSV. Our results could be possibly explained by a combination of a greater fraction of immediate reconstructions, with a greater use of CSV more recently in the senior author experience and learning-curve which lead to shorter operative times. Previous reports have demonstrated that the bigger is the flap the greater is its flow rate and consequently the higher its venous drainage needs to be.12,22 Therefore, adding veins in parallel and choosing larger diameter veins are the two main factors that increase drainage from the flap reducing risk of venous congestion. There is no doubt that both axillary or IMV as recipients for a DIEP flap have sufficient negative vein pressure and drainage, but when the IMV are used the possibility of obtaining two veins of adequate size and length is lower than that offered by the TDV and CSV.21,22 At the axillary site, veins of different caliber are available for proper matching and even a very large vein anastomosis, including both satellites veins, can be performed if the DIEP pedicle is harvested to its iliac vessel source after satellites veins confluence. The need for a second vein with IMV system could occasionally force surgeons to use both ends of the sectioned mammary vein giving to the flap a primary antegrade and an accessory retrograde venous drainage.23 It should be noted that a recent study by Mackey et al. has identified a proportion of IMV that appear to have valves between the commonly used 2nd or 3rd rib-spaces, and the next draining side branch.24 Moreover, the two IMV stumps are usually very short with thin walls that make their lumen easily collapsing which together with the continuous respiratory movements affects microscope focus rendering the anastomosis difficult to perform. Some authors even suggest the
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preoperative study of IMV with computed tomography angiography to detect eventual anatomic variations.25 The above mentioned conditions may extend the IMV operative time or encourage the surgeon to perform anastomosis of only one vein, excluding superficial vein drainage and risking an insufficient venous outflow and therefore increasing the risk of postoperative complications. Most common complication in DIEP flap transfer is partial necrosis and although it most often depends on the vein outflow it can be presumed that arterial inflow might play a role.20,26–28 The use of IMV carries several risks and can lead to various complications such as pneumothorax, impaired vascularity of the sternum, parasternal or intercostal hernia, and intercostal neuralgia. Recently, it has also been reported a case of intraoperative cardiac tamponade and fatal bleeding related to IMV use.29 Finally, the use of IMV for breast reconstruction renders them unavailable for aorto-coronary bypass and an informed consent needs to be signed by the patient acknowledging this fact.30,31 The argument that anastomosis to IMV ensures a better aesthetic result due to a more medial position of the flap can be valid only for those flaps that have a short pedicle such as the free transverse rectus abdominis myocutaneous (TRAM) flap or the sparing muscle free TRAM flap.32 This assumption is not applicable to the DIEP flap because its pedicle if it is dissected down to the iliac vessels can easily reach the axilla, especially by using 2–3 cm long CSV as recipients. We believe that the use of IMV site may facilitate kinking of veins because of their course at 90 from the intercostal space. Moreover, the DIEP pedicle cannot be shortened too much to keep a proper caliber congruity, and its extra-length need to be locally redistributed to avoid twisting. By using the axilla, recipient and pedicle vessels are positioned on the same plane running inferiorly along the lateral breast pole, and the eventual pedicle extra-length can be easily distributed on a longer distance. In this study, the number of perforators selected in each groups was dictated by vein caliber, independently from the recipient vessels site. When more than one perforator was captured, pedicle length could be reduced but not clinically significant as it was always dissected and severed to its origin, requiring routine stretching to avoid redundancy and vein kinking. The use of CSV may overcome the problems traditionally related to the use of TDV, i.e. avoids the sacrifice of the entire TDV pedicle to assure the vitality of a myocutaneous latissimus dorsi flap, useful for secondary salvage reconstructive procedure. Furthermore, despite the possibility of accidental TDV damage by the general surgeon during lymph node dissection or of radiotherapy injury in patients presenting for delayed reconstruction this is almost impossible for CSV due to their anatomical location.18,33 Being in the omotricipital space these Microsurgery DOI 10.1002/micr
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Santanelli di Pompeo et al.
vessels are not embedded in scar tissue and their lumen is never reduced or weakened.18,19 Even difficulties in positioning the operating table by two operators can be overcome, either raising up CSV once they have been isolated, or slightly releasing the pectoralis major muscle. In our experience when SSM with axillary lymph node dissection is planned, it can be totally handled through the periareolar access and a 4 cm 3 4 cm Tshaped incision in the axilla is used for CSV exposure and anastomosis. When a nipple-sparing mastectomy (NSM) with axillary lymph node dissection is required, both can be totally mastered via an infero-lateral incision, and CSV exposure and anastomosis can be performed through an axillary T-shaped access. In all cases, the axillary access often used for sentinel node dissection too, if properly positioned in the hairy skin area, remains well hidden and rarely visible with a negligible cosmetic result. In our experience, exposure of IMV and performance of anastomosis during SSM and NSM is hard and demanding due to limited access because of the mastectomy flap and DIEP flap bulkiness. Furthermore, in NSM substantial medial extension of the infero-lateral or emiperiareolar access is required to visualize the anastomotic area, which may harm proper mastectomy flap perfusion. Recently, the use of new recipient vessels was suggested in breast microsurgery.5–8,34,35 IMV perforators result as a brilliant idea that avoids many of the complications related to the use of IMV, but unfortunately perforator presence is dependent on anatomical variability and its preservation from the general surgeon. Recent study shows that in immediate reconstruction these perforators are present in 93.5% but only usable in 37.2% of the cases, their presence decreases to 12.9% in delayed reconstruction.34 Tan et al. even proposed Multi Detector computed Tomography Angiography, as non-invasive imaging method, for investigating the anatomic characteristics of IMV and its perforators before planning the operation.36 These data, combined with the difficulty of finding a second vein, make the use of IMV perforator a random, unplanned, intraoperative finding. The absence of a proper and careful preoperative planning may often result in an unjustified increased operative time and/or surgical errors. Although our results are limited by a retrospective study design, the sample size of 256 consecutive breast reconstructions including only a specific type of flap performed by a single surgeon makes the groups more homogeneous and could be considered reliable indicators of a good statistical design. It is obvious that each surgeon has different training and different learning curve leading to different results than ours. This study can contribute to enhance the developing literature about this issue and could be helpful to carry out further studies from multiple surgeons to draw totally reliable conclusions. Microsurgery DOI 10.1002/micr
CONCLUSIONS
Our study has demonstrated that the choice of the recipient site for DIEP flap breast reconstruction does not influence the incidence of complications. The axillary vessels seem to reduce the operative time and offer the possibility to perform a second vein anastomosis. Among the axillary vessels, we believe that CSV can be safely used as recipient vessels due to the following advantages: easier dissection compared to the one for the IMV because of their anatomical characteristics; greater and more constant caliber than the IMV perforator vessels; optimal flap insetting due to the pedicle’s length when dissected until its origin. Moreover, their location in the posterior axillary region does not expose them completely to the consequences of radiotherapy. Finally, their use does not influence the choice of alternative flaps such as latissimus dorsi flap.
REFERENCES 1. Granzow JW, Levine JL, Chiu ES, Allen RJ. Breast reconstruction using perforator flaps. J Surg Oncol 2006;94:441–454. 2. Healy C, Allen RJ Sr. The evolution of perforator flap breast reconstruction: Twenty years after the first DIEP flap. J Reconstr Microsurg 2014;30:121–125. 3. Santanelli F, Longo B, Angelini M, Laporta R, Paolini G. Prospective computerized analyses of sensibility in breast reconstruction with non-reinnervated DIEP flap. Plast Reconstr Surg 2011;127: 1790–1795. 4. Holmstr€ om H. The free abdominoplasty flap and its use in breast reconstruction. An experimental study and clinical case report. Scand J Plast Reconstr Surg 1979;13:423–427. 5. Harashina T, Imai T, Nakajima H, Fujino T. Breast reconstruction with microsurgical free composite tissue transplantation. Br J Plast Surg 1980;33:30–37. 6. Dupin CL, Allen RJ, Glass CA, Bunch R. The internal mammary artery and vein as a recipient site for free-flap breast reconstruction: A report of 110 consecutive cases. Plast Reconstr Surg 1996;98: 685–689; discussion 690–692. 7. Guzzetti T, Thione A. Successful breast reconstruction with a perforator to deep inferior epigastric perforator flap. Ann Plast Surg 2001; 46:641–643. 8. Saint-Cyr M, Chang DW, Robb GL, Chevray PM. Internal mammary perforator recipient vessels for breast reconstruction using free TRAM, DIEP, and SIEA flaps. Plast Reconstr Surg 2007;120:1769– 1773. 9. Mosahebi A, Ramakrishnan V, Gittos M, Collier J. Aesthetic outcome of different techniques of reconstruction following nippleareola-preserving envelope mastectomy with immediate reconstruction. Plast Reconstr Surg 2007;119:796–803. 10. Santanelli F, Paolini G, Campanale A, Longo B, Amanti C. The “Type V” skin-sparing mastectomy for upper quadrant skin resections. Ann Plast Surg 2010;65:135–139. 11. Banwell M, Trotter D, Ramakrishnan V. The thoracodorsal artery and vein as recipient vessels for microsurgical breast reconstruction. Ann Plast Surg 2012;68:542–543. 12. Rubino C, Ramakrishnan V, Figus A, Bulla A, Coscia V, Cavazzuti MA. Flap size/flow rate relationship in perforator flaps and its importance in DIEAP flap drainage. J Plast Reconstr Aesthet Surg 2009;62:1666–1670. 13. Lorenzetti F, Suominen S, Tukiainen E, Kuokkanen H, Suominen E, Vuola J, Asko-Seljavaara S. Evaluation of blood flow in free microvascular flaps. J Reconstr Microsurg 2001;17:163–167.
Recipient Vessel Sites 14. Teunis T, van Voss MR, Kon M, van Maurik JF. CT-angiography prior to DIEP flap breast reconstruction: A systematic review and meta-analysis. Microsurgery 2013;33:496–502. 15. Santanelli F, Longo B, Sorotos M, Farcomeni A, Paolini G. Flap survival of skin-sparing mastectomy type IV: A retrospective cohort study of 75 consecutive cases. Ann Surg Oncol 2013;20:981–989. 16. Serletti JM, Moran SL, Orlando GS, Fox I. Thoracodorsal vessels as recipient vessels for the free TRAM flap in delayed breast reconstruction. Plast Reconstr Surg 1999;104:1649–1655. 17. Robb GL. Thoracodorsal vessels as a recipient site. Clin Plast Surg 1998;25:207–211. 18. Lantieri LA, Mitrofanoff M, Rimareix F, Gaston E, Raulo Y, Baruch JP. Use of circumflex scapular vessels as a recipient pedicle for autologous breast reconstruction: A report of 40 consecutive cases. Plast Reconstr Surg 1999;104:2049–2053. 19. Dabernig J, Ong KO, McGowan R, Wiberg M, Payne AP, Hart AM. The anatomic and radiologic basis of the circumflex scapular artery perforator flap. Ann Plast Surg 2010; 64:784–788. 20. Moran SL, Nava G, Behnam AB, Serletti JM. An outcome analysis comparing the thoracodorsal and internal mammary vessels as recipient sites for microvascular breast reconstruction: A prospective study of 100 patients. Plast Reconstr Surg 2003;111:1876–1882. 21. Lorenzetti F, Kuokkanen H, von Smitten K, Asko-Seljavaara S. Intraoperative evaluation of blood flow in the internal mammary or thoracodorsal artery as a recipient vessel for a free TRAM flap. Ann Plast Surg 2001;46:590–593. 22. Arnez ZM, Valdatta L, Tyler MP, Planinsek F. Anatomy of the internal mammary veins and their use in free TRAM flap breast reconstruction. Br J Plast Surg 1995;48:540–545. 23. Kerr-Valentic MA, Gottlieb LJ, Agarwal JP. The retrograde limb of the internal mammary vein: An additional outflow option in DIEP flap breast reconstruction. Plast Reconstr Surg 2009;124:717–721. 24. Mackey SP, Ramsey KW. Exploring the myth of the valveless internal mammary vein—A cadaveric study. J Plast Reconstr Aesthet Surg 2011;64:1174–1179. 25. Rozen WM, Alonso-Burgos A, Murray AC, Whitaker IS. Is there a need for preoperative imaging of the internal mammary recipient site for autologous breast reconstruction? Ann Plast Surg 2013;70: 111–115.
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26. Blondeel PN, Arnstein M, Verstraete K, Depuydt K, Van Landuyt KH, Monstrey SJ, Kroll SS. Venous congestion and blood flow in free transverse rectus abdominis myocutaneous and deep inferior epigastric perforator flaps. Plast Reconstr Surg 2000;106:1295–1299. 27. Blondeel PN. One hundred free DIEP flap breast reconstructions: A personal experience. Br J Plast Surg 1999;52:104–111. 28. Santanelli F, Longo B, Cagli B, Pugliese P, Sorotos M, Paolini G. Predictive and protective factors for partial necrosis in DIEP flap breast reconstruction: Does nulliparity bias flap viability? Ann Plast Surg 2013, Jul 11. 29. Pratt GF, Faris JG, Lethbridge M, Teh LG. Breast reconstruction with a free DIEP (TRAM) flap complicated by cardiac tamponade and arrest: A case report. J Plast Reconstr Aesthet Surg 2009;62: e73–e75. 30. Nahabedian MY. The internal mammary artery and vein as recipient vessels for microvascular breast reconstruction: are we burning a future bridge? Ann Plast Surg 2004;53:311–316. 31. Al-Benna S, Steinstraesser L, Patani N. Free flap breast reconstruction consent forms should warn against the potential loss of the internal thoracic artery for coronary artery bypass grafting. Plast Reconstr Surg 2012;129:867e–868e. 32. Majumder S, Batchelor AG. Internal mammary vessels as recipients for free TRAM breast reconstruction: Aesthetic and functional considerations. Br J Plast Surg 1999;52:286–289. 33. Laporta R, Longo B, Pagnoni M, Catta F, Garbarino GM, Santanelli F. Accidental injury of the latissimus dorsi flap pedicle during axillae dissection: Types and reconstruction algorithm. Microsurgery 2014;34:5–9. 34. Munhoz AM. Internal mammary perforator recipient vessels for breast reconstruction using free TRAM, DIEP, and SIEA flaps. Plast Reconstr Surg 2008;122:315–316. 35. Santanelli F, Longo B, Laporta R, Pagnoni M, Cavalieri E. The use of the Serratus Anterior muscle vascular pedicle as recipient site in DIEP flap transfer for breast reconstruction. J Plast Reconstr Surg 2014;67:456–460. 36. Tan O, Yuce I, Aydin OE, Kantarci M. A radioanatomic study of the internal mammary artery and its perforators using multidetector computed tomography angiography. Microsurgery 2014;34:277–288.
Microsurgery DOI 10.1002/micr
DI
POMPEO, M.D., Ph.D.,* BENEDETTO LONGO, M.D., Ph.D., MICHAIL SOROTOS, M.D., MARCO
PAGNONI, M.D., and ROSARIA LAPORTA, M.D.
The aim of this study is to present our experience on the use of various recipient sites for deep inferior epigastric perforator (DIEP) flap breast reconstruction and compare them by means of objective data. Two hundred fifty six DIEP flap breast reconstructions, performed between March 2004 and May 2011, were retrospectively analyzed. Only unilateral reconstructions were included in the study and divided into three groups depending on the recipient site choice: internal mammary vessels (IMV) (n 5 52), thoracodorsal vessels (TDV) (n 5 109), and circumflex scapular vessels (CSV) (n 5 95). Clinical records of each patient were reviewed to acquire relevant data such as operative time, postoperative complications, and use of a second vein anastomosis. CSV group showed a statistically significant lower operative time (4.92 6 0.54 hours) compared to TDV (5.67 6 1.01 hours) and IMV groups (6.75 6 1.09 hours) (P < 0.001). Second vein anastomosis was performed in 84 cases (88.1%) of CSV, in 85 cases (77.9%) of TDV, and in 18 cases (35.1%) of IMV groups (P < 0.001). No significant differences were observed among groups regarding risk factors and complications (P > 0.05). The axillary vessels seem to be the ideal recipient site because of reduced operative time and increased possibility to perform a second vein anastomosis. Among them, CSV can be safely used due to following advantages: easy dissection, larger vessel caliber, and optimal flap insetting. C 2014 Wiley Periodicals, Inc. Microsurgery Moreover, their location does not expose them completely to radiotherapy consequences. V 00:000–000, 2014.
Autologous tissue is considered the gold standard by many authors for breast reconstruction and among free flaps the deep inferior epigastric perforator (DIEP) flap and the superficial inferior epigastric artery (SIEA) flap are the most popular choices.1–3 Selection of adequate recipient vessels is one of the keys for success in free tissue transfer. Initially, the most common recipient vessels were those of the axillary system, including the thoracodorsal and the circumflex scapular pedicle, as first described by Holmstr€om in 1979.4 The use of the internal mammary vessels (IMV), described in 1980 by Harashina, has been recommended as the first choice for breast microsurgical reconstruction since 1996, while IMV perforators were described in 2001 and have been routinely proposed since 2007.5–8 Progress in the field of oncology including the skin sparing mastectomy (SSM),9,10 the evolution in the surgical management of the lymphatic axillary system of women with breast cancer (sentinel lymph node), and recent studies on the perforator flap flow led us to reconsider the circumflex scapular vessels (CSV) for microvascular breast reconstruction.11–13 Currently, in the absence of a widely accepted algorithm, choice of recipient Plastic Surgery Unit, Sant’Andrea Hospital, School of Medicine and Psychology, “Sapienza” University of Rome, Rome, Italy *Correspondence to: Fabio Santanelli di Pompeo, M.D., Ph.D., Plastic Surgery Unit, c/o Azienda Ospedaliera Sant’Andrea, Via di Grottarossa 10351039, 00189 Rome, Italy. E-mail: [email protected] Received 30 September 2013; Revision accepted 10 April 2014; Accepted 11 April 2014 Published online 00 Month 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/micr.22266 Ó 2014 Wiley Periodicals, Inc.
vessels in free flap breast reconstruction is based on surgeon’s experience. The aim of this study is to present our experience on the use of the various recipient sites for DIEP flap breast reconstruction and compare them by means of objective data. PATIENTS AND METHODS
A retrospective analysis of 256 consecutive breast reconstructions with the DIEP flap performed by the senior author (FS) between March 2004 and May 2011 was performed. Patients undergoing unilateral reconstruction were included and they were divided into three groups depending on the recipient site choice: IMV (n 5 52), thoracodorsal vessels (TDV) (n 5 109), and CSV (n 5 95). All patients received preoperative computerized-tomography angiography to evaluate the flap perforators’ pattern and, as other studies confirm, proved helpful in identifying the ideal perforator.14 On the other hand, we did not perform any radiologic study for the recipient vessels. The following risk factors were evaluated: patient’s age, body mass index (BMI), and personal history of smoking, radiotherapy, or chemotherapy.15 Clinical records of each patient were reviewed to acquire relevant data such as operative time, postoperative complications, and use of a second vein anastomosis. In all procedures, the deep inferior epigastric vessels were dissected down to their origin from the external iliac vessels to obtain as long pedicle as possible and when present the superficial inferior epigastric vein was harvested down to its origin. All IMV were exposed after removal of a portion of the
2
Santanelli di Pompeo et al. Table 1. Patient Related Risk Factors Incidence Among Groups
No. of patients Age (years) (mean 6 SD) BMI (kg/m2) (mean 6 SD) Smoking history (cases/%) Preoperative radiotherapy (cases/%) Preoperative chemotherapy (cases/%)
IMV
TDV
CSV
P-value
52 53.06 6 9.02 29.3 6 3.01 7 (13.4%) 4 (7.7%) 6 (11.5%)
109 50.12 6 9.95 28.7 6 3.81 17 (15.6%) 10 (9.2%) 17 (15.5%)
95 51.99 6 9.80 28.5 6 3.01 17 (17.8%) 8 (8.4%) 12 (12.6%)
0.902 0.783 0.773 0.949 0.730
IMV: internal mammary vessels group; TDV: thoracodorsal vessels group; CSV: circumflex scapular vessels group.
Table 2. Number of Perforators Selected and Divided by Groups No. of perforators 4 3 2 1
IMV
TDV
CSV
0 8 28 16
3 20 71 15
1 15 53 26
IMV: internal mammary vessels group; TDV: thoracodorsal vessels group; CSV: circumflex scapular vessels group.
Table 3. Complications Incidence Among Groups Complication (cases/%) Hematoma Seroma Partial flap necrosis Total flap necrosis Arterial Thrombosis Venous Thrombosis
IMV
CSV
TDV
P-value
1 (1.9%) 1 (1.9%) 8 (15.3%) 1 (1.9%) 0 (0%) 1 (1.9%)
2 (2.1%) 2 (2.1%) 8 (7.6%) 0 (0%) 1 (1.05%) 1 (1.05%)
1 (0.9%) 1 (0.9%) 16 (14.6%) 0 (0%) 0 (0%) 1 (0.9%)
0.408 0.427 0.232 0.487 0.512 0.342
IMV: internal mammary vessels group; TDV: thoracodorsal vessels group; CSV: circumflex scapular vessels group.
third rib, while TDV and CSV were prepared through the previous mastectomy access or by a new “T” incision in the axillary fold, during axillary node dissection in immediate reconstructions or separately in delayed ones, as described in literature.6,16–19 The Chi-squared tests were used for the continuous variable (operative time) and the evaluation of the risk factors. The Kruskal Wallis and Bonferroni tests analyzed categorical variables such as the incidence of complications and the use of second vein anastomosis. A P-value 0.05 was considered significant. RESULTS
The three groups were homogeneous regarding the patient’s age and the other risk factors (Table 1) (P > 0.05). Seven (13.4%) patients had a smoking history, 4 (7.7%) had received neoadjuvant radiotherapy, and 6 (11.5%) neoadjuvant chemotherapy in the IMV compared to 17 (15.6%) with a smoking history, 10 (9.2%) that had received preoperative radiotherapy, and 17 (15.5%) preoperative chemotherapy in the TDV Microsurgery DOI 10.1002/micr
group. In the CSV group, 17 (17.8%) patients were smokers, 8 (8.4%) had undergone preoperative radiotherapy, and 12 (12.6%) preoperative chemotherapy. Table 2 summarizes the number of perforators selected and divided by groups. CSV group showed a statistically significant lower operative time (4.92 6 0.54 hours) compared to TDV (5.67 6 1.01 hours) and IMV groups (6.75 6 1.09 hours) (P < 0.001). Second vein anastomosis was performed in 84 cases (88.1%) of CSV, in 85 cases (77.9%) of TDV, and in 18 cases (35.1%) of IMV groups (P < 0.001). From the data, the second vein anastomosis was always available in TDV and CSV groups and considered unnecessary by the surgeon in selected cases, while in IMV group was not done because of the unmatched caliber in 28 of 34 cases and in 6 was considered unnecessary by the surgeon. No significant differences were observed among groups regarding complications (Table 3) (P > 0.05). More specifically in IMV group 8 (15.3%) flaps suffered partial necrosis, compared to 16 (14.6%) in TDV and 8 (7.6%) in CSV. One (1.9%) hematoma and one (1.9%) seroma were seen in IMV group, compared to 1 (0.9%) hematoma and 1 (0.9%) seroma in TDV and 2 (2.1%) hematomas and 2 (2.1%) seromas in CSV group. One (1.9%) venous thrombosis was observed in IMV group, one (0.9%) in TDV, and one (1.05%) in CSV group. One (1.9%) total flap necrosis was encountered in the IMV group and one (1.05%) arterial thrombosis was seen in the CSV group. DISCUSSION
The choice of recipient vessels is one of the key points for microvascular breast reconstruction because flap perfusion and operative time depend on their reliability and surgical site. Both IMV and TDV are usually easy to expose, of suitable caliber, permit an end-to-end anastomosis, and have demonstrated success in this setting. The choice is largely up to the reconstructive surgeon and usually based on comfort level and experience, flow characteristics, chest topography, and patient comorbidities. Currently, the recent trend in literature advocates
Recipient Vessel Sites
the use of IMV as recipient artery and vein of choice.11,16–18,20 Nevertheless, some authors note unpredictable quality and inconsistency of the internal mammary veins diameter at the level of the fourth rib often necessitating vein grafts.21 Time for vessels’ dissection and exposure in immediate reconstruction represents another issue in favor of the axillary vessels, that is, the preparation of these vessels contemporaneously with the axillary lymphadenectomy or sentinel lymph node biopsy by the general surgeon while the access to the IMV adds an extra “step” to the surgical procedure. Moran et al.,20 in a prospective study reported no difference in operative times between IMV and TDV, while in our report CSV group showed a statistically significant lower operative time compared to TDV and IMV groups (P < 0.001). The analysis of the evolution, in time, of recipient site selection showed an inversion of the trend between TDV and CSV and a continuous decrease of the IMV. CSV and TDV are both located in the axilla; the latter are more superficial and anterior, which is supposed to make dissection faster than the deeper and posteriorly located CSV. Our results could be possibly explained by a combination of a greater fraction of immediate reconstructions, with a greater use of CSV more recently in the senior author experience and learning-curve which lead to shorter operative times. Previous reports have demonstrated that the bigger is the flap the greater is its flow rate and consequently the higher its venous drainage needs to be.12,22 Therefore, adding veins in parallel and choosing larger diameter veins are the two main factors that increase drainage from the flap reducing risk of venous congestion. There is no doubt that both axillary or IMV as recipients for a DIEP flap have sufficient negative vein pressure and drainage, but when the IMV are used the possibility of obtaining two veins of adequate size and length is lower than that offered by the TDV and CSV.21,22 At the axillary site, veins of different caliber are available for proper matching and even a very large vein anastomosis, including both satellites veins, can be performed if the DIEP pedicle is harvested to its iliac vessel source after satellites veins confluence. The need for a second vein with IMV system could occasionally force surgeons to use both ends of the sectioned mammary vein giving to the flap a primary antegrade and an accessory retrograde venous drainage.23 It should be noted that a recent study by Mackey et al. has identified a proportion of IMV that appear to have valves between the commonly used 2nd or 3rd rib-spaces, and the next draining side branch.24 Moreover, the two IMV stumps are usually very short with thin walls that make their lumen easily collapsing which together with the continuous respiratory movements affects microscope focus rendering the anastomosis difficult to perform. Some authors even suggest the
3
preoperative study of IMV with computed tomography angiography to detect eventual anatomic variations.25 The above mentioned conditions may extend the IMV operative time or encourage the surgeon to perform anastomosis of only one vein, excluding superficial vein drainage and risking an insufficient venous outflow and therefore increasing the risk of postoperative complications. Most common complication in DIEP flap transfer is partial necrosis and although it most often depends on the vein outflow it can be presumed that arterial inflow might play a role.20,26–28 The use of IMV carries several risks and can lead to various complications such as pneumothorax, impaired vascularity of the sternum, parasternal or intercostal hernia, and intercostal neuralgia. Recently, it has also been reported a case of intraoperative cardiac tamponade and fatal bleeding related to IMV use.29 Finally, the use of IMV for breast reconstruction renders them unavailable for aorto-coronary bypass and an informed consent needs to be signed by the patient acknowledging this fact.30,31 The argument that anastomosis to IMV ensures a better aesthetic result due to a more medial position of the flap can be valid only for those flaps that have a short pedicle such as the free transverse rectus abdominis myocutaneous (TRAM) flap or the sparing muscle free TRAM flap.32 This assumption is not applicable to the DIEP flap because its pedicle if it is dissected down to the iliac vessels can easily reach the axilla, especially by using 2–3 cm long CSV as recipients. We believe that the use of IMV site may facilitate kinking of veins because of their course at 90 from the intercostal space. Moreover, the DIEP pedicle cannot be shortened too much to keep a proper caliber congruity, and its extra-length need to be locally redistributed to avoid twisting. By using the axilla, recipient and pedicle vessels are positioned on the same plane running inferiorly along the lateral breast pole, and the eventual pedicle extra-length can be easily distributed on a longer distance. In this study, the number of perforators selected in each groups was dictated by vein caliber, independently from the recipient vessels site. When more than one perforator was captured, pedicle length could be reduced but not clinically significant as it was always dissected and severed to its origin, requiring routine stretching to avoid redundancy and vein kinking. The use of CSV may overcome the problems traditionally related to the use of TDV, i.e. avoids the sacrifice of the entire TDV pedicle to assure the vitality of a myocutaneous latissimus dorsi flap, useful for secondary salvage reconstructive procedure. Furthermore, despite the possibility of accidental TDV damage by the general surgeon during lymph node dissection or of radiotherapy injury in patients presenting for delayed reconstruction this is almost impossible for CSV due to their anatomical location.18,33 Being in the omotricipital space these Microsurgery DOI 10.1002/micr
4
Santanelli di Pompeo et al.
vessels are not embedded in scar tissue and their lumen is never reduced or weakened.18,19 Even difficulties in positioning the operating table by two operators can be overcome, either raising up CSV once they have been isolated, or slightly releasing the pectoralis major muscle. In our experience when SSM with axillary lymph node dissection is planned, it can be totally handled through the periareolar access and a 4 cm 3 4 cm Tshaped incision in the axilla is used for CSV exposure and anastomosis. When a nipple-sparing mastectomy (NSM) with axillary lymph node dissection is required, both can be totally mastered via an infero-lateral incision, and CSV exposure and anastomosis can be performed through an axillary T-shaped access. In all cases, the axillary access often used for sentinel node dissection too, if properly positioned in the hairy skin area, remains well hidden and rarely visible with a negligible cosmetic result. In our experience, exposure of IMV and performance of anastomosis during SSM and NSM is hard and demanding due to limited access because of the mastectomy flap and DIEP flap bulkiness. Furthermore, in NSM substantial medial extension of the infero-lateral or emiperiareolar access is required to visualize the anastomotic area, which may harm proper mastectomy flap perfusion. Recently, the use of new recipient vessels was suggested in breast microsurgery.5–8,34,35 IMV perforators result as a brilliant idea that avoids many of the complications related to the use of IMV, but unfortunately perforator presence is dependent on anatomical variability and its preservation from the general surgeon. Recent study shows that in immediate reconstruction these perforators are present in 93.5% but only usable in 37.2% of the cases, their presence decreases to 12.9% in delayed reconstruction.34 Tan et al. even proposed Multi Detector computed Tomography Angiography, as non-invasive imaging method, for investigating the anatomic characteristics of IMV and its perforators before planning the operation.36 These data, combined with the difficulty of finding a second vein, make the use of IMV perforator a random, unplanned, intraoperative finding. The absence of a proper and careful preoperative planning may often result in an unjustified increased operative time and/or surgical errors. Although our results are limited by a retrospective study design, the sample size of 256 consecutive breast reconstructions including only a specific type of flap performed by a single surgeon makes the groups more homogeneous and could be considered reliable indicators of a good statistical design. It is obvious that each surgeon has different training and different learning curve leading to different results than ours. This study can contribute to enhance the developing literature about this issue and could be helpful to carry out further studies from multiple surgeons to draw totally reliable conclusions. Microsurgery DOI 10.1002/micr
CONCLUSIONS
Our study has demonstrated that the choice of the recipient site for DIEP flap breast reconstruction does not influence the incidence of complications. The axillary vessels seem to reduce the operative time and offer the possibility to perform a second vein anastomosis. Among the axillary vessels, we believe that CSV can be safely used as recipient vessels due to the following advantages: easier dissection compared to the one for the IMV because of their anatomical characteristics; greater and more constant caliber than the IMV perforator vessels; optimal flap insetting due to the pedicle’s length when dissected until its origin. Moreover, their location in the posterior axillary region does not expose them completely to the consequences of radiotherapy. Finally, their use does not influence the choice of alternative flaps such as latissimus dorsi flap.
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Microsurgery DOI 10.1002/micr
