Advantages and disadvantages of using the internal thoracic artery perforators as recipient vessels in autologous breast reconstruction—a narrative review
Review Article

Advantages and disadvantages of using the internal thoracic artery perforators as recipient vessels in autologous breast reconstruction—a narrative review

Suzanne M. Beecher^

Department of Plastic & Reconstructive Surgery, Mater Misericordiae Hospital, Dublin, Ireland

^ORCID: 0000-0001-6489-3424.

Correspondence to: Suzanne M. Beecher. Department of Plastic & Reconstructive Surgery, Mater Misericordiae Hospital, Dublin, Ireland. Email: suzub@hotmail.com.

Abstract: The rates of breast reconstruction after mastectomy are rising each year. Autologous breast reconstruction using free tissue transfer is considered the gold standard reconstruction, especially with recent controversy surrounding breast implant-associated anaplastic large cell lymphoma (BIA-ALCL). During free tissue transfer, the flap vessels must be anastomosed to recipient vessels on the chest wall. There are multiple options of recipient vessels during microvascular breast reconstruction. Most commonly, the thoracodorsal vessels or the internal thoracic vessels [also known as the internal mammary (IM) vessels] are used as the recipient vessels for microvascular anastomosis of the free tissue transfer. Other second-line options include the thoracoacromial axis and the lateral thoracic vessels. The use of perforators of the internal thoracic vessels for free flap anastomosis during autologous breast reconstruction has been in use for almost twenty years. They are generally favoured over use of thoracodorsal vessels as they result in medialisation of the flap. In recent years, the use of perforators of the internal thoracic vessels has become popular. Great debate surrounds whether or not they should be used as recipient vessels as opposed to the conventional main vessels. In this article, we discuss the advantages and disadvantages of both techniques to guide the choice of reconstructive microsurgeons.

Keywords: Internal mammary perforators (IM perforators); internal thoracic artery (ITA); breast reconstruction; microvascular reconstruction


Received: 20 April 2020; Accepted: 08 January 2021; Published: 30 June 2021.

doi: 10.21037/abs-20-50


Introduction

The rates of breast reconstruction are rising internationally. Breast reconstruction has been shown to have psychological benefits for patients. Autologous reconstruction is becoming very popular as it uses the patient’s own tissue. It is also a better option compared to prosthetic implants if adjuvant radiotherapy is required.

During autologous breast reconstruction, a flap of tissue is transferred from elsewhere in the body, from sites such as the abdomen or the thigh. The vessels require anastomosis to native vessels in the region of the breast. The recipient vessels for anastomosis are usually the thoracodorsal or the internal thoracic vessels [also known as the internal mammary (IM) vessels]. Other secondary options, though rarely used, include the thoracoacromial and the lateral thoracic vessels (1). In recent years, the use of perforators of the internal thoracic vessels has become popular. Great debate surrounds whether or not they should be used as recipient vessels as opposed to the conventional main vessels. In this article, we discuss the advantages and disadvantages of the recipient vessels in microvascular breast reconstruction. A review of the literature was performed, with relevant articles obtained from SCOPUS and Medline. We present the following article in accordance with the Narrative Review reporting checklist (available at http://dx.doi.org/10.21037/abs-20-50).


Thoracodorsal vessels

The thoracodorsal were previously the vessels of choice. The thoracodorsal vessels however are potentially damaged during axillary clearances. Even if still present, during delayed breast reconstruction, there is often a significant amount of scarring in the region of the axilla due to prior surgery or radiotherapy, which may make dissection of the thoracodorsal axis technically difficult (2). When using the thoracodorsal vessels, a longer vascular pedicle is required on the free flap. There may also be a reduction of tissue available to reconstruct volume in the medial aspect of the breast due to the flap being placed laterally in the breast (2). With the advent of sentinel node biopsy, axillary node clearances are not always required. Because of this, there has been a decline in the use of the thoracodorsal axis as it is generally not exposed, as would’ve been the case when patients underwent node clearances (3). Also, if the thoracodorsal vessels are used at the time of sentinel node biopsy, if a subsequent axillary node clearance is required, the pedicle may be potentially compromised (4).


Internal thoracic vessels

The use of the internal thoracic axis as the recipient vessel was first described by Harashina et al. in 1980 (5). The internal thoracic vessels have the advantage of being a good size match to the flap pedicle, and also the site is more accessible for performing microsurgery (6). The average diameter of the internal thoracic artery (ITA) is 3.6 mm and the average size of the vein is also 3.6 mm (7). At the third intercostal (IC) space, the vessels are consistently of adequate caliber for anastomosis (8). Using the internal thoracic vessels also allows for easier positioning of the flap, and also there is a lower risk of avulsion injury and shoulder stiffness due to shoulder immobilisation when using the thoracodorsal axis for flap anastomosis. A shorter pedicle is required to optimally position the flap on the chest wall (9). Its use may also preserve the thoracodorsal vessels for use for a secondary latissimus dorsi flap in the case of flap failure (10). The internal thoracic arteries bilaterally are good size matches for the deep inferior epigastric artery, as is the right internal thoracic vein. The left internal thoracic vein however, is often much smaller than the deep inferior epigastric vein, which may lead to vessel size mismatch during microsurgical anastomosis (3). The thoracodorsal and internal thoracic vessels when used as recipients for free flap anastomosis have a similar rate of complications, however, use of the internal thoracic vessels may be associated with a higher rate of nipple necrosis in immediate nipple-sparing reconstruction (11).

The ITA is a branch of the subclavian artery. It passes inferiorly and 1–2 cm lateral to the sternal border, dividing into its terminal branches at the level of the sixth rib. Its terminal branches are the superior epigastric artery and the musculophrenic artery. In addition to these terminal branches, the ITA gives off medial and lateral branches. The medial branches give supply to the area surrounding the sternum. The lateral branches include the anterior IC arteries, which supply the ribcage, with two branches to each IC space. The branches at the lower IC spaces are larger, with the largest being in the 5th and 6th IC spaces (7). Laterally there are also branches to pectoralis major. Also, arising from the lateral border of the ITA, the anterior ICs or the muscular branches are cutaneous perforators that supply the skin. The ITA gives blood supply to approximately 60% of the breast parenchyma (12). The cutaneous vascular territory of the ITA extends from the midline medially to the mid-clavicular line, two to three centimeters lateral to the nipple laterally. Cranially, it extends to the inferior border of the clavicle. The caudal border of the skin territory supplied can vary between the ninth rib to the umbilicus (7).

There are however disadvantages to using internal thoracic vessels for free flap anastomosis. In order to anastomose the free flap pedicle to the internal thoracic vessels, a section of cartilage is often removed in order to gain access to the vessels. There are multiple methods to remove the rib, but often the methods described by Haddock et al is employed, with removal of the cartilage piecemeal with a rongeur until the posterior perichondrium is exposed (13). Rib resection can be quite painful, and resection of cartilage and surgery in this area may result in chronic IC neuralgia (14). Pain can result in post-operative atelectasis due to a reduction in deep breathing (15). Another potential disadvantage of cartilage or rib resection is that it may result in a contour deformity on the chest wall (10,16). This may require fat grafting to correct (17). One benefit to rib resection is that the cartilage can be banked and subsequently used during nipple reconstruction to give the nipple support (Figure 1) (18).

Figure 1 Costal cartilage banking and use in nipple reconstruction.

Of note, there is however a rib sparing technique that can be performed that prevents a contour deformity and results in less pain. This involves elevating an area of the IC muscle in the second or third IC space (9,10). The second IC space is the largest IC space (19). This may not be feasible in the presence of a bifid rib (20). In the case of the patient who has had previous radiotherapy however, the segment of ITA that is behind the rib has less damage due to the radiotherapy, which may be more reliable for anastomosis (21). In dissecting out the ITA vessels a pneumothorax may also occur (22). Another, more disadvantageous sequelae are that using the internal thoracic vessels for free flap anastomosis would mean the vessels would be removed as a potential donor for coronary artery bypass grafting. Radiotherapy is a common adjunct to treatment of breast cancer. These patients are at higher risk for coronary artery disease due the effects of radiotherapy on the cardiac vasculature. This may mean this cohort of patients may need coronary artery bypass grafting in the future (23). The ITA is the vessel of choice for surgeons performing bypass grafting (24). Sacrifice of this vessel may also lead to complications in sternal wound closure during cardiothoracic surgery (25). Performing an end to side anastomosis from the flap to the ITA, the vessel can be potentially preserved for future bypass grafting (26). End to side vessel anastomosis is not associated with an increased risk of flap associated complications, however it may lead to increased flap ischaemia time and increased costs associated with the procedure (27). Anastomosing the free flap pedicle at the 4th or 5th IC space can also preserve the ITA for future bypass grafting (28). The ITA, with a segment of the DIEP pedicle could also be used for coronary artery bypass grafting (28).


Internal thoracic perforators

The use of a perforator of the ITA for free flap anastomosis during autologous breast reconstruction was first described by Guzzetti et al. in 2001 (29). Perforator flaps have become increasingly popular compared to musculocutaneous flaps as they significantly reduce donor site morbidity. By moving from main vessel to the use of perforators when choosing the recipient vessels, morbidity can also be reduced. Using perforators from the internal thoracic removes the need for resection a segment of cartilage. This reduces exposure and vessel preparation time and thus the duration of the operation. It also reduces the amount of post-operative pain (30). The vessels are then also still available for potential future coronary artery bypass grafting. The anastomosis may also be technically easier as the excursion of the vessels due to respiratory movements and the beating heart is dampened compared to the ITA, which is in closer proximity to the lung and there is more room to perform the anastomosis (2,29). The arterial or venous anastomosis can be performed conventionally by suturing. They can also be successfully performed using a coupler device (15). This can reduce flap ischaemia times. The tunica media of the ITA perforators are less affected by atherosclerotic degenerative change when compared to the main ITA vessels (31). This may make the vessels more reliable for anastomosis. The use of perforators in comparison to the main IM vessels is not associated with increased flap site complications (32).

ITA perforators are always present. They are the main perforators for the deltopectoral flap (30). Up to 91% of people have perforators greater than 1mm in the first or second IC space (33). ITA perforators can be easily identified using a Doppler (2). Duplex ultrasonography and CT angiography may also be useful in identifying adequate perforators (33-35). The most common location of perforators is in the parasternal area, where the perforators arise directly from the ITA. Usually, extensive intra-muscular dissection is not required as most perforators are superficial to pectoralis major (36). If there has been previous breast surgery, they are still preserved at the level of the second IC space, as this is out of the field of mastectomy and from previous radiotherapy (6). These cutaneous perforators can vary in size, however generally a “principle perforator” exists. This can vary in location, most commonly found in the 2nd IC space, but is always present in the 1st 4 IC spaces (7,37). The majority of perforators are found between 0.5 and 3 cm from the sternum. The largest perforators are found in the second IC space (38). The diameter of perforators from the ITA is on average 1.14 mm for the artery and 1.7 mm for the vein (2,8,38).

The main issue with using ITA perforators is the caliber of the vessels. It can be technically demanding as the vessels can be small (30). This is particularly true for the thin walled perforating veins (32). The quantity of blood flow to the flap may be of concern with small diameter recipients. There may also be vessel size mismatch between the flap pedicle and the recipient vessels (2). A concomitant vein may not always be present with the perforating artery (8). An adequate recipient perforator may only be present in 27% to 63% of patients (6,32,39,40). The lower perforators may also have been sacrificed at the time of mastectomy. Preservation of perforators may be achieved in collaboration with the breast surgeon at the time of oncological resection of the breast (2,8). Also, with increased familiarity and experience with identifying and performing perforator anastomosis, the rate of successfully identifying a suitable perforator can improve (40). There is also concern that sacrifice of the perforators may compromise the mastectomy skin flaps, which may lead to skin necrosis, however it has been shown that skin necrosis rates are comparable between the use of the main vessels and perforators (32). The use of perforators may also not be suitable if a perforator flap with a short pedicle is used, such as the superior gluteal artery flap, as the pedicle may not reach the second or third IC space when the flap is placed at the desired position (40).


Conclusions

In conclusion, the main internal thoracic vessels are still the most commonly used vessels for free flap anastomosis during autologous breast reconstruction as the internal thoracic perforators vary in caliber. We would recommend assessing for the presence of adequate size perforators at the time of reconstruction, as the use of these can negate morbidity associated with the resection of ribs or cartilage. Attempts to localize perforators are certainly justified in order to preserve the IM vessels for future potential bypass grafting. If adequate vessels are present, these should be the microsurgeon’s preferred option. In the absence of adequate perforating vessels, the main internal thoracic vessels should be used.


Acknowledgments

Funding: None.


Footnote

Reporting Checklist: The author has completed the Narrative Review reporting checklist. Available at http://dx.doi.org/10.21037/abs-20-50

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Conflicts of Interest: The author has completed the ICMJE uniform disclosure form (available at http://dx.doi.org/10.21037/abs-20-50). The author has no conflicts of interest to declare.

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References

  1. Lopez CE, Caicedo JJ, Pizano A, et al. Breast Reconstruction with a Lateral Breast Free Flap: A New Application of Breast-sharing. Plast Reconstr Surg Glob Open 2020;8:e2701 [Crossref] [PubMed]
  2. Park MC, Lee JH, Chung J, et al. Use of internal mammary vessel perforator as a recipient vessel for free TRAM breast reconstruction. Ann Plast Surg 2003;50:132-7. [Crossref] [PubMed]
  3. Saint-Cyr M, Youssef A, Bae HW, et al. Changing trends in recipient vessel selection for microvascular autologous breast reconstruction: An analysis of 1483 consecutive cases. Plast Reconstr Surg 2007;119:1993-2000. [Crossref] [PubMed]
  4. Curtis MS, Arslanian B, Colakoglu S, et al. Immediate microsurgical breast reconstruction and simultaneous sentinel lymph node dissection: Issues with node positivity and recipient vessel selection. J Reconstr Microsurg 2011;27:445-8. [Crossref] [PubMed]
  5. Harashina T, Imai T, Nakajima H, et al. Breast reconstruction with microsurgical free composite tissue transplantation. Br J Plast Surg 1980;33:30-7. [Crossref] [PubMed]
  6. Haywood RM, Raurell A, Perks AGB, et al. Autologous free tissue breast reconstruction using the internal mammary perforators as recipient vessels. Br J Plast Surg 2003;56:689-91. [Crossref] [PubMed]
  7. Palmer JH, Ian Taylor G. The vascular territories of the anterior chest wall. Br J Plast Surg 1986;39:287-99. [Crossref] [PubMed]
  8. Munhoz AM, Ishida LH, Montag E, et al. Perforator flap breast reconstruction using internal mammary perforator branches as a recipient site: An anatomical and clinical analysis. Plast Reconstr Surg 2004;114:62-8. [Crossref] [PubMed]
  9. Sacks JM, Chang DW. Rib-sparing internal mammary vessel harvest for microvascular breast reconstruction in 100 consecutive cases. Plast Reconstr Surg 2009;123:1403-7. [Crossref] [PubMed]
  10. Parrett BM, Caterson SA, Tobias AM, et al. The rib-sparing technique for internal mammary vessel exposure in microsurgical breast reconstruction. Ann Plast Surg 2008;60:241-3. [Crossref] [PubMed]
  11. Yang SJ, Eom JS, Lee TJ, et al. Recipient vessel selection in immediate breast reconstruction with free abdominal tissue transfer after nipple-sparing mastectomy. Arch Plast Surg 2012;39:216-21. [Crossref] [PubMed]
  12. Gonyon DL Jr, Zenn MR, Milano CA, et al. Breast necrosis following use of the internal mammary artery for coronary artery bypass. Ann Plast Surg 2005;54:88-91. [Crossref] [PubMed]
  13. Haddock NT, Teotia SS. Five Steps to Internal Mammary Vessel Preparation in Less than 15 Minutes. Plast Reconstr Surg 2017;140:884-6. [Crossref] [PubMed]
  14. Conacher ID, Doig JC, Rivas L, et al. Intercostal neuralgia associated with internal mammary artery grafting. Anaesthesia 1993;48:1070-1. [Crossref] [PubMed]
  15. Rad AN, Flores JI, Rosson GD. Free DIEP and SIEA breast reconstruction to internal mammary intercostal perforating vessels with arterial microanastomosis using a mechanical coupling device. Microsurgery 2008;28:407-11. [Crossref] [PubMed]
  16. Schwabegger AH, Gschnitzer C, Ninkovic MM. Contour deformity at the internal mammary recipient site. Br J Plast Surg 1999;52:674. [Crossref] [PubMed]
  17. Weichman KE, Broer PN, Tanna N, et al. The role of autologous fat grafting in secondary microsurgical breast reconstruction. Ann Plast Surg 2013;71:24-30. [Crossref] [PubMed]
  18. Mori H, Uemura N, Okazaki M. Nipple reconstruction with banked costal cartilage after vertical-type skin-sparing mastectomy and deep inferior epigastric artery perforator flap. Breast Cancer 2015;22:95-7. [Crossref] [PubMed]
  19. Tuinder S, Dikmans R, Schipper RJ, et al. Anatomical evaluation of the internal mammary vessels based on magnetic resonance imaging (MRI). J Plast Reconstr Aesthet Surg 2012;65:1363-7. [Crossref] [PubMed]
  20. Molina AR, Mellington AJ, Jones ME. A case of bifid third rib encountered during DIEP flap breast reconstruction. J Plast Reconstr Aesthet Surg 2011;64:e101-2. [Crossref] [PubMed]
  21. Chaput B, Garrido I, Chavoin JP, et al. Rib-sparing and internal mammary artery-preserving microsurgical breast reconstruction with the free DIEP flap. Plast Reconstr Surg 2013;132:868e-870e. [Crossref] [PubMed]
  22. Dupin CL, Allen RJ, Glass CA, et al. 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;98:685-9; discussion 690-2. [Crossref] [PubMed]
  23. Gyenes G, Rutqvist LE, Liedberg A, et al. Long-term cardiac morbidity and mortality in a randomized trial of pre- and postoperative radiation therapy versus surgery alone in primary breast cancer. Radiother Oncol 1998;48:185-90. [Crossref] [PubMed]
  24. Canver CC. Conduit options in coronary artery bypass surgery. Chest 1995;108:1150-5. [Crossref] [PubMed]
  25. Ståhle E, Tammelin A, Bergström R, et al. Sternal wound complications - Incidence, microbiology and risk factors. Eur J Cardiothorac Surg 1997;11:1146-53. [Crossref] [PubMed]
  26. Hemphill AF, De Jesus RA, McElhaney N, et al. End-to-side anastomosis to the internal mammary artery in free flap breast reconstruction: Preserving the internal mammary artery for coronary artery bypass grafting. Plast Reconstr Surg 2008;122:149e-150e. [Crossref] [PubMed]
  27. Apostolides JG, Magarakis M, Rosson GD. Preserving the internal mammary artery: End-to-side microvascular arterial anastomosis for DIEP and SIEA flap breast reconstruction. Plast Reconstr Surg 2011;128:225e-232e. [Crossref] [PubMed]
  28. Rozen WM, Ye X, Guio-Aguilar PL, et al. Autologous microsurgical breast reconstruction and coronary artery bypass grafting: An anatomical study and clinical implications. Breast Cancer Res Treat 2012;134:181-98. [Crossref] [PubMed]
  29. Guzzetti T, Thione A. Successful breast reconstruction with a perforator to deep inferior epigastric perforator flap. Ann Plast Surg 2001;46:641-3. [Crossref] [PubMed]
  30. Hamdi M, Blondeel P, Van Landuyt K, et al. Algorithm in choosing recipient vessels for perforator free flap in breast reconstruction: The role of the internal mammary perforators. Br J Plast Surg 2004;57:258-65. [Crossref] [PubMed]
  31. Munhoz AM, Ishida LH, Montag E, et al. Internal mammary perforator vessels as recipient site for microsurgical breast reconstruction: A comparative histomorphometric analysis and incidence of degenerative vascular changes. Microsurgery 2014;34:217-23. [Crossref] [PubMed]
  32. Saint-Cyr M, Chang DW, Robb GL, et al. Internal mammary perforator recipient vessels for breast reconstruction using free TRAM, DIEP, and SIEA flaps. Plast Reconstr Surg 2007;120:1769-73. [Crossref] [PubMed]
  33. Murray ACA, Rozen WM, Alonso-Burgos A, et al. The anatomy and variations of the internal thoracic (internal mammary) artery and implications in autologous breast reconstruction: Clinical anatomical study and literature review. Surg Radiol Anat 2012;34:159-65. [Crossref] [PubMed]
  34. Abou-Gamrah S, Abdel-Monem K, Elshahat A, et al. Role of color duplex sonography in pre-operative internal mammary artery perforators assessment for breast reconstruction using contralateral lower pole flap. Egyptian Journal of Radiology and Nuclear Medicine 2012;43:85-92. [Crossref]
  35. Kim H, Lim SY, Pyon JK, et al. Preoperative computed tomographic angiography of both donor and recipient sites for microsurgical breast reconstruction. Plast Reconstr Surg 2012;130:11e-20e. [Crossref] [PubMed]
  36. Halim AS, Alwi AA. Internal mammary perforators as recipient vessels for deep inferior Epigastric perforator and muscle-sparing free transverse Rectus abdominis musculocutaneous flap breast reconstruction in an asian population. Ann Plast Surg 2014;73:170-3. [Crossref] [PubMed]
  37. Manchot C. Die Hautarterien des menschlichen Körpers. Vogel; 1889.
  38. Rosson GD, Holton LH, Silverman RP, et al. Internal mammary perforators: A cadaver study. J Reconstr Microsurg 2005;21:239-42. [Crossref] [PubMed]
  39. Munhoz AM. Internal mammary perforator recipient vessels for breast reconstruction using free tram, diep, and siea flaps. Plast Reconstr Surg 2008;122:315-6. [Crossref] [PubMed]
  40. Follmar KE, Prucz RB, Manahan MA, et al. Internal mammary intercostal perforators instead of the true internal mammary vessels as the recipient vessels for breast reconstruction. Plast Reconstr Surg 2011;127:34-40. [Crossref] [PubMed]
doi: 10.21037/abs-20-50
Cite this article as: Beecher SM. Advantages and disadvantages of using the internal thoracic artery perforators as recipient vessels in autologous breast reconstruction—a narrative review. Ann Breast Surg 2021;5:16.