Although the abdominal wall donor site has BREAST

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Avoiding Denervation of Rectus Abdominis in DIEP Flap Harvest II: An Intraoperative

Assessment of the Nerves to Rectus

Warren M. Rozen, M.B.B.S., B.Med.Sc.

Mark W. Ashton, M.B.B.S., M.D.

Birgitte J. Kiil, M.B.B.S.

Damien Grinsell, M.B.B.S., F.R.A.C.S.

Sugitha Seneviratne, M.B.B.S., F.R.A.C.S.

Russell J. Corlett, M.B.B.S., F.R.A.C.S.

G. Ian Taylor, M.B.B.S., M.D.

Parkville, Victoria, Australia

Background: The deep inferior epigastric artery perforator (DIEP) flap aims to reduce donor-site morbidity by minimizing rectus muscle damage; however, damage to motor nerves during perforator dissection may denervate rectus muscle. Although cadaveric research has demonstrated that individual nerves do not arise from single spinal cord segments and are not distributed segmentally, the functional distribution of individual nerves remains unknown. Using intraoperative nerve stimulation, the current study describes the motor distribution of individual nerves supplying the rectus abdominis, providing a guide to nerve dissection during DIEP flap harvest.

Methods: Twenty rectus abdominis muscles in 17 patients undergoing reconstructive surgery involving rectus abdominis (DIEP, transverse rectus abdominis musculocutaneous, or vertical rectus abdominis musculocutaneous flaps) underwent intraoperative stimulation of nerves innervating the infraumbilical segment of the rectus. Nerve course and extent of rectus muscle contraction were recorded.

Results: In each case, three to seven nerves entered the infraumbilical segment of the rectus abdominis. Small nerves (type 1) innervated small longitudinal strips of rectus muscle, rather than transverse strips as previously described.

There was significant overlap between adjacent type 1 nerves. In 18 of 20 cases, a single large nerve (type 2) at the level of the arcuate line supplied the entire width and length of rectus muscle.

Conclusions: Nerves innervating the rectus abdominis are at risk during DIEP flap harvest. Small, type 1 nerves have overlapping innervation from adjacent nerves and may be sacrificed without functional detriment. However, large type 2 nerves at the level of the arcuate line innervate the entire width of rectus muscle without adjacent overlap and may contribute to donor-site morbidity if sacrificed. (Plast. Reconstr. Surg. 122: 1321, 2008.)

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lthough the abdominal wall donor site has become increasingly used for autologous breast reconstruction, complications based on abdominal wall morbidity still arise. The deep inferior epigastric artery perforator (DIEP) flap is a modification of the surgical technique that aims to reduce donor-site morbidity by minimizing damage to rectus abdominis muscle fibers. De- spite a reduction in rectus muscle sacrifice, donor- site morbidity is still a recognized complication of the procedure.^1–10In fact, recent studies compar-

ing the muscle-sparing transverse rectus abdominis musculocutaneous (TRAM) with the DIEP flap have suggested that there may be no significant improvement in abdominal wall morbidity with a reduction in the amount of muscle sacrificed, with one suggested cause being denervation of rectus abdominis muscle by nerve damage during the raising of the flap.^11–13

The nerves that innervate the rectus abdominis arise from the thoracolumbar spinal nerves and traverse the anterolateral abdominal wall to

From the Jack Brockhoff Reconstructive Plastic Surgery Re- search Unit, Department of Anatomy and Cell Biology, Uni- versity of Melbourne.

Received for publication February 14, 2008; accepted April 10, 2008.

Disclosure: The authors declare that there is no source of financial or other support, or any financial or professional relationships that may pose a com- peting interest.

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enter the rectus sheath.^{14 –17} They then enter the posterolateral surface of the rectus abdominis. In a move to consider the implications of sacrificing individual nerves within the rectus sheath, we em- barked on a cadaveric study that was able to ex- plore the course of these nerves.¹⁸ Of particular note in the findings of this research was the extensive branching of segmental spinal nerves, both within the neurovascular plane of the anterolateral abdominal wall and within the rectus sheath.

This suggested that individual nerves identified within the rectus sheath do not arise from single spinal cord segments, and may not denervate segmental myotomes if damaged.

Although cadaveric research has demonstrated that individual nerves are not distributed segmentally, the functional distribution of individual nerves remains unknown. As a function of the extensive branching of these nerves, the segmental origins and functional roles of these nerves have not been in- vestigated. The current report is a clinical study using intraoperative nerve stimulation in patients undergoing lower abdominal flap surgery. The motor distribution of individual nerves supplying the rectus abdominis is thus explored, ultimately aiming to suggest guidelines for the dissection of nerves and perforators during DIEP flap harvest.

PATIENTS AND METHODS

The study design was a prospective cohort study of consecutive patients undergoing reconstructive surgery involving rectus abdominis (DIEP flaps, TRAM flaps, or vertical rectus abdominis musculocutaneous flaps). This included 15 women and two men, all between the ages of 35 to 90 years, with no extremes of body habitus. Patients were recruited through a single institution and institu- tional ethics approval was obtained.

Seventeen patients (20 rectus abdominis muscles) were included in the study, of which there were nine unilateral DIEP flaps, three bilateral DIEP flaps, one pedicled TRAM flap, and four vertical rectus abdominis musculocutaneous flaps. All patients were between 40 and 60 years of age, and spanned a wide range of body habitus. All nerve stimulation findings were recorded by one of the first two authors (W.M.R., M.W.A.) in all cases.

Nerve Stimulation Technique

During each operation, careful dissection of the nerves entering the lateral part of the rectus abdominis muscle was undertaken, with identifi- cation of the nerves supplying the infraumbilical part of the rectus abdominis achieved in all cases

(Fig. 1). The number of nerves within the operative field, the location of nerves, and the course of each nerve identified were all recorded.

On localization, intraoperative nerve stimulation of each nerve was undertaken with the use of a surgical nerve locator (Vari-Stim III Surgical Nerve Locator; Medtronic Xomed, Inc., Jackson- ville, Fla.). The nerve stimulator used was a battery- powered, single-use device, with adjustable current settings and a subdermal needle as the grounding (anode) electrode (Fig. 2). Intraoperative nerve stimulation for nerve localization has been used for many years, with the current device shown to be safe and effective for clinical use.^19,20In all cases, a setting of 0.5 mA was used, with a “current flow” light en- abling confirmation of current flow.

Nerve stimulation enabled the dual function of confirming the structures identified as nerves and quantifying the motor distribution of innervation of each nerve identified by documenting the extent of rectus abdominis muscle contraction during stimulation. This was achieved by marking the muscle at regular intervals and observing the intervals that shortened (contracted muscle) and those that lengthened (stretched muscle). Trans- verse segments contracting were identified by observing visually contracting muscle fibers. The nerve stimulation findings and the observational results were recorded in a blinded fashion, with quantitative

Fig. 1. Intraoperative photograph demonstrating the identifi- cation of a segmental nerve (N) innervating the rectus abdominis (RA). The relationship to the deep inferior epigastric artery (DIEA) pedicle and perforators (P) is shown.

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results compiled for presentation in tables, and qual- itative data presented descriptively.

RESULTS Number of Nerves

In 20 hemiabdominal walls (17 patients), 75 nerves were identified as entering the infraumbilical segment of the rectus abdominis. There were no differences in findings between the sexes or for other attributes. In each hemiabdominal wall, three to five nerves were identified within the infraumbilical part of the rectus sheath as encroaching on the rectus abdominis from its lateral border (Fig. 1).

The number of nerves seen below the umbilicus per hemiabdomen, for both the cadaveric and the clinical studies, is shown in Table 1. The observed differences between these studies are consistent with the differences in observational techniques between the cadaveric and clinical studies. In the clinical study, the infraumbilical part of the rectus sheath only underwent a limited exploration in each case, such as was viable within the limits of the operation.

As such, the uppermost and lowermost portions of this field were not explored routinely, with the pres- ence of one nerve above and one nerve below the plane of dissection (two nerves per hemiabdomen) expected to be present. The majority of specimens demonstrated innervation by three to four infraum-

bilical nerves, and when the error margin of two nerves is included, these findings correlate closely with the findings of our cadaveric study.¹⁸Of note, the nerves identified in the current clinical study were of variable size, with the majority of nerves (57 of 75) being less 0.5 mm in diameter and a small number (18 of 75) being of significantly larger diameter (0.5 mm or more).

Distribution of Nerves

On stimulation of these individual nerves, the rectus abdominis muscle was seen to contract to variable longitudinal and transverse extents. The width of rectus abdominis contraction was classified as less than one-quarter of its width, one-quarter or more but less than three-quarters, or three-quarters or more of the width (otherwise classified as the full transverse extent). The majority of nerves (41 of 75) contracted less than one fourth of the width; 16 contracted one fourth or more, but less than three fourths; 18 contracted three fourths or more.

The nerves that innervated the full width of the rectus muscle were all found to be large (0.5 mm or more in diameter). These nerves were present in 18 of 20 hemiabdominal walls, and we have called them type 2 nerves, as they appear to be morphologically and functionally different from the smaller type 1 nerves. Figure 3 presents a schematic of the nerves identified. The anatomical basis for this difference is discussed below.

In addition, four clinical cases of DIEP flap harvest required the sacrifice of nerves that inter-

Fig. 2. Photograph of the surgical nerve locator (Vari-Stim III Sur- gical Nerve Locator).

Table 1. Number of Nerves Supplying the

Infraumbilical Segment of the Rectus Abdominis in Our Previous 20 Cadaveric Specimen Dissections and in the Current 20 Intraoperative Clinical Cases No. of

Infraumbilical Nerves

No. of Cadaveric

Specimens (%) No. of Clinical Cases (%)

3 — 8/20 (40)

4 3/20 (15) 9/20 (45)

5 11/20 (55) 3/20 (15)

6 5/20 (25) —

7 1/20 (5) —

Fig. 3. Schematic diagram demonstrating the general path of segmental nerves innervating the infraumbilical part of the rectus abdominis. The segment of rectus abdominis between the umbilicus (U) and the pubic symphysis (PS) is commonly inner- vated by three to five small, type 1 nerves (N1) and one large, type 2 nerve (N2) at the level of the arcuate line (AL).

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fered with the dissection of the vascular pedicle.

These were all type 1 nerves. After transection of these nerves, stimulation of the remaining nerves (including a type 2 nerve in each of the four cases) resulted in complete functionality of the rectus abdominis muscle, so that no segment had been denervated. In contrast, there were segments of rectus muscle that could not be stimulated by any nerve identified other than the type 2 nerve.

The longitudinal distribution of each nerve was also recorded. All type 2 nerves innervated the entire caudocranial extent of the infraumbilical rectus muscle. Type 1 nerves had variable heights of distribution, varying from 50 percent of the height of rectus exposed to 100 percent. None of the nerves supplied less than 50 percent of this height.

DISCUSSION

The DIEP flap has become popularized for breast reconstruction, as it can minimize the sacrifice of rectus abdominis muscle fibers during dissection of the vascular pedicle. Where a single perforator or multiple aligned perforators can be used in the supply to the flap, the rectus abdominis muscle can be spared entirely. Despite this, abdominal wall weakness, lower abdominal bulge, and abdominal wall herniation are all ongoing complications of the DIEP flap.3–5,7,11–13,21The sacrifice of some muscle where multiple perforators are used is likely to contribute to these outcomes²²; however, it is unlikely to be the major contributor to the abdominal wall sequelae complicating this flap.

In addition to the sacrifice of rectus muscle, other factors contributing to these abdominal wall complications have been suggested, and all are likely to contribute to varying degrees. The denervation of rectus abdominis muscle,14,15,23,24 in- adequate closure of the anterior rectus sheath,^25,26 and attenuation and/or laxity of the anterior rectus sheath^3–5have all been demonstrated as having some influence. Our previous anatomical studies demonstrated an intimate relationship between the nerve supply to the rectus abdominis and the vascular supply used in the raising of a DIEP flap.¹⁸ The nerves supplying the rectus abdominis were shown to form a plexus around the main trunk and the most lateral branch of the deep inferior epigastric artery, with motor nerves entering the rectus abdominis with lateral row perforators, placing them at risk during flap harvest. These findings suggested that the denervation of rectus abdominis was a significant consideration in the cause of abdominal wall complications following DIEP flap harvest.

The anatomical basis for denervation, initi- ated in our cadaveric research, has been further explored and validated in the current functional study. Using nerve stimulation, the functional distribution of the nerves within the rectus sheath has been demonstrated. The majority of nerves within the rectus sheath are small, type 1 nerves, which supply only narrow strips of rectus muscle and have no functional sequelae if divided. However, in most cases, there is a large type 2 nerve at the level of the arcuate line that is functionally important and innervated the entire width of rectus muscle. If divided, denervated segments of rectus abdominis muscle may remain, resulting in abdominal wall complications.

The current study also demonstrated some important anatomical findings. Much of the anatomical literature, based on early anatomical work, describes the innervation of the rectus abdominis by segmental nerves supplying transverse sections of the rectus abdominis muscle.^27,28Although sub- sequent studies have broadened this concept by describing extensive branching of the nerves innervating the anterior abdominal wall, the concept of transverse, segmental myotomes innervated by single nerves still exists.15,17,29,30 The current findings demonstrated that individual nerves do not supply transverse segments of rectus muscle but rather supply extensive longitudinal strips of varying transverse widths. Although this does not preclude the possibility of single spinal cord segments innervating transverse myotomes, it does negate the perception of the role of individual nerves. In addition, there is clearly a functional and morphologic difference between the type 1 and type 2 nerves identified. Type 2 nerves do innervate the entire width of the rectus abdominis muscle and may indeed constitute the bulk of fibers from a single spinal cord segment (likely to be the T12 distribution). Type 1 nerves are not segmental in origin and likely contain mixed fibers from multiple adjacent spinal cord segments.

With an increasing emphasis on operative re- finements as a move to decreasing donor-site morbidity, the current study provides important guidelines to aid in achieving this end. Despite the move to diminishing muscle sacrifice in raising an abdominal wall flap, sacrifice of the innervation of the rectus abdominis may well play an even more important role in abdominal wall function than muscle preservation. The role of the lower type 2 nerves is of particular importance and may further explain why muscle-sparing type 0 and 1 TRAM flaps do show increasing donor-site complications,

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whereas muscle sparing type 2 TRAM flaps are comparable to DIEP flaps.

CONCLUSIONS

The nerves innervating the rectus abdominis muscle are at risk during the raising of a DIEP flap, with damage to these nerves potentially denerva- ting rectus abdominis muscle. This may contribute to donor-site complications such as abdominal wall weakness, bulge, and herniation. Small, type 1 nerves innervate small longitudinal strips of muscle that have overlapping innervation from adjacent nerves and may be sacrificed without functional detriment. However, a large type 2 nerve is frequently identifiable at the level of the arcuate line that innervates the entire width of rectus muscle without adjacent overlap and may contribute to donor-site morbidity if sacrificed.

Warren M. Rozen, M.B.B.S., B.Med.Sc.

Jack Brockhoff Reconstructive Plastic Surgery Research Unit Department of Anatomy and Cell Biology University of Melbourne Parkville, Victoria, Australia warrenrozen@hotmail.com

REFERENCES

1. Blondeel, N., Vanderstraeten, G. G., Monstrey, S. J., et al. The donor site morbidity of free DIEP flaps and free TRAM flaps for breast reconstruction. Br. J. Plast. Surg. 50: 322, 1997.

2. Futter, C. M., Webster, M. H., Hagen, S., et al. A retrospective comparison of abdominal muscle strength following breast reconstruction with a free TRAM or DIEP flap. Br. J. Plast.

Surg. 53: 578, 2000.

3. Nahabedian, M. Y. Secondary operations of the anterior abdominal wall following microvascular breast reconstruc- tion with the TRAM and DIEP flaps. Plast. Reconstr. Surg. 120:

365, 2007.

4. Nahabedian, M. Y., Dooley, W., Singh, N., and Manson, P. N.

Contour abnormalities of the abdomen after breast reconstruction with abdominal flaps: The role of muscle preser- vation. Plast. Reconstr. Surg. 109: 91, 2002.

5. Nahabedian, M. Y., and Momen, B. Lower abdominal bulge after deep inferior epigastric perforator flap (DIEP) breast reconstruction. Ann. Plast. Surg. 54: 124, 2005.

6. Nahabedian, M. Y., Momen, B., Galdino, G., and Manson, P.

N. Breast reconstruction with the free TRAM or DIEP flap:

Patient selection, choice of flap, and outcome. Plast. Reconstr.

Surg. 110: 466, 2002.

7. Nahabedian, M. Y., Tsangaris, T., and Momen, B. Breast reconstruction with the DIEP flap or the muscle-sparing (MS-2) free TRAM flap: Is there a difference? Plast. Reconstr.

Surg. 115: 436, 2005.

8. Zhong, T., Lao, A., Werstein, M. S., Downey, D. B., and Evans, H. B. High-frequency ultrasound: A useful tool for evaluating the abdominal wall following free TRAM and DIEP flap surgery. Plast. Reconstr. Surg. 117: 1113, 2006.

9. Allen, R. J. DIEP versus TRAM for breast reconstruction.

Plast. Reconstr. Surg. 111: 2478, 2003.

10. Allen, R. J. Comparison of the costs of DIEP and TRAM flaps.

Plast. Reconstr. Surg. 108: 2165, 2001.

11. Bajaj, A. K., Chevray, P. M., and Chang, D. W. Comparison of donor site complications and functional outcomes in free muscle-sparing TRAM flap and free DIEP flap breast recon- struction. Plast. Reconstr. Surg. 117: 737, 2006.

12. Chen, C. M., Halvorson, E. G., Disa, J. J., et al. Immediate postoperative complications in DIEP versus free/muscle- sparing TRAM flaps. Plast. Reconstr. Surg. 120: 1477, 2007.

13. Schaverien, M. V., Perks, A. G. B., and McCulley, S. J. Com- parison of outcomes and donor-site morbidity in unilateral free TRAM versus DIEP flap breast reconstruction. J. Plast.

Reconstr. Aesthet. Surg. 60: 1219, 2007.

14. Duchateau, J., Declety, A., and Lejour, M. Innervation of the rectus abdominis muscle: Implications for rectus flaps. Plast.

Reconstr. Surg. 82: 223, 1988.

15. Hammond, D. C., Larson, D. L., Severinac, R. N., and Mar- cias, M. Rectus abdominis muscle innervation: Implications for TRAM flap elevation. Plast. Reconstr. Surg. 96: 105, 1995.

16. Moon, H. K., and Taylor, G. I. The vascular anatomy of rectus abdominis musculocutaneous flaps based on the deep su- perior epigastric system. Plast. Reconstr. Surg. 82: 815, 1988.

17. Yap, L. H., Whiten, S. C., Forster, A., and Stevenson, J. H. The anatomical and neurophysiological basis of the sensate free TRAM and DIEP flaps. Br. J. Plast. Surg. 55: 35, 2002.

18. Rozen, W. M., Ashton, M. W., Murray, A. C. A., and Taylor, G. I. Avoiding denervation of rectus abdominis during DIEP flap harvest: The importance of medial row perforators. Plast.

Reconstr. Surg. 122: 710, 2008.

19. Van Beek, A., Hubble, B., Kinkead, L., Torros, S., and Suchy, H. Clinical use of nerve stimulation and recording tech- niques. Plast. Reconstr. Surg. 71: 225, 1983.

20. Page, C., Laude, M., Legars, D., Foulon, P., and Strunski, V.

The external laryngeal nerve: Surgical and anatomic con- siderations. Report of 50 total thyroidectomies. Surg. Radiol.

Anat. 26: 182, 2004.

21. Nahabedian, M. Y., and Manson, P. N. Contour abnormalities of the abdomen after transverse rectus abdominis mus- cle flap breast reconstruction: A multifactorial analysis. Plast.

Reconstr. Surg. 109: 81, 2002.

22. Rozen, W. M., Ashton, M. W., Pan, W. R., and Taylor, G. I.

Raising perforator flaps for breast reconstruction: The in- tramuscular anatomy of the DIEA. Plast. Reconstr. Surg. 120:

1443, 2007.

23. Bottero, L., Lefaucheur, J. P., Fadhul, S., Raulo, Y., Collins, E. D., and Lantieri, L. Electromyographic assessment of rectus abdominis muscle function after deep inferior epigastric perforator flap surgery. Plast. Reconstr. Surg. 113: 156, 2004.

24. Galli, A., Adami, M., Berrino, P., Leone, S., and Santi, P.

Long-term evaluation of the abdominal wall competence after total and selective harvesting of the rectus abdominis muscle. Ann. Plast. Surg. 28: 409, 1992.

25. Hartrampf, C. R. J. Abdominal wall competence in trans- verse abdominal island flap operations. Ann. Plast. Surg.

12: 139, 1984.

26. Kroll, S. S., and Marchi, M. Comparison of strategies for preventing abdominal-wall weakness after TRAM flap breast reconstruction. Plast. Reconstr. Surg. 89: 1045, 1992.

27. Davies, F., Gladstone, R. J., and Stibbe, E. P. The anatomy of the intercostal nerves. J. Anat. 66: 323, 1931.

28. Walmsley, T. The costal musculature. J. Anat. Physiol. 50: 165, 1916.

29. Monkhouse, W. S., and Khalique, A. Variations in the com- position of the human rectus sheath: A study of the anterior abdominal wall. J. Anat. 145: 61, 1986.

30. Tansatit, T., Chokrungvaranont, P., Sanguansit, P., and Wanidchaphloi, S. Neurovascular anatomy of the deep inferior epigastric perforator flap for breast reconstruction.

J. Med. Assoc. Thai. 89: 1630, 2006.