World J. Surg. 26, 1088 –1093, 2002 DOI: 10.1007/s00268-002-6277-9

WORLD Journal of

SURGERY © 2002 by the Socie´te´ Internationale de Chirurgie

Indications and Complications of Latissimus Dorsi Myocutaneous Flaps in Oncologic Breast Surgery J. Apffelstaedt, M.D. Breast Clinic, Department of Surgery, University of Stellenbosch, PO Box 19063, Tygerberg 7505, Cape Town, South Africa Published Online: June 20, 2002 Abstract. The use of the latissimus dorsi myocutaneous flap (LDMF) in reconstructive breast surgery is well documented. Few reports exist of its use in oncologic breast surgery. This series describes indications and complications of the LDMF in locally advanced cancer. The records of 83 patients were analysed for age and sex, menstrual status, stage, indication, margins of resection, chemotherapy, radiotherapy, complications, and survival. The indication was to cover defects caused by resection of locally advanced breast cancer (67 cases), recurrent breast cancer (13 cases), radiation damage (2 cases), and surgical complications (1 case). The mean age of the patients was 50.2 years; 52% were postmenopausal. The flaps had mean diameters of 32 by 14 cm. The donor site was skin grafted. Clear margins were achieved in 83%. At the LDMF insertion site, wound infection required drainage in 1 case; flap necrosis required reintervention in 7 cases. In 2 cases a second skin graft was done for the LDMF donor site. The proportions of wound infections and incomplete skin graft take were significantly greater in patients receiving preoperative cyclophosphamide/methotrexate/5-fluorouracil (CMF) versus cyclophosphamide/doxorubicin/5-fluorouracil (CAF) chemotherapy (p < 0.001 and p < 0.05, respectively). The late complication rate was 7.2%. The mean follow-up is 40.0 months. The complication rates for CMF versus CAF chemotherapy suggest an adverse effect of methotrexate, which warrants further investigation. The use of the LDMF made wide resection of locally advanced lesions and radionecrosis possible; major complications were rare. LDMF has its place in the armamentarium of the surgeon who regularly sees locally advanced breast cancer.

Tansini was the first to describe the technique of the latissimus dorsi myocutaneous flap (LDMF) closure in oncologic breast surgery in 1896 [1]. The technique was little used in the following seven decades until rediscovered by Olivari in 1976 [2]. Mühlbauer and Olbrich [3] and Schneider et al. [4] described the flap for breast reconstruction. Since then, a number of authors [5–15] have described indications, technique, and complications for the LDMF in reconstructive breast surgery. In contrast to reconstructive surgery, the patient who needs a LDMF for wound cover after mastectomy usually has locally advanced disease, requires a larger flap, aggressive preoperative or postoperative chemotherapy, and radiotherapy. The purpose of this paper is to describe the indications for and the short-term and Correspondence to: J. Apffelstaedt, M.D., Head, Neck, Breast and Sarcoma Clinic, University of Stellenbosch, PO Box 19063, Tygerberg 7505, South Africa, e-mail: [email protected]

long-term complications of the LDMF under the conditions of advanced local disease.

Materials and Methods In our prospective breast cancer database, patients were identified who had a LDMF performed for wound cover. The records were analyzed for age and sex, menstrual status, stage according to the TNM classification of malignant tumors [16], indication for LDMF wound cover, margins of resection, type and number of cycles of preoperative chemotherapy, preoperative and postoperative radiotherapy dosages and fields, indication for the procedure, early and late complications, and survival. Some patients received preoperative induction chemotherapy consisting of cyclophosphamide [500 mg/m2], doxorubicin [50 mg/ m2], and 5-fluorouracil [500 mg/m2] (CAF), or cyclophosphamide [500 mg/m2], methotrexate [35 mg/m2], and 5-fluorouracil [500 mg/m2] (CMF) three-weekly up to maximum response as part of a protocol for the treatment of locally advanced breast cancer. The last cycle was given at least 3 weeks preoperatively. White cell and platelet counts were allowed to normalize. Preoperative radiotherapy was terminated at least 3 months before surgery. Mastectomies were performed with complete axillary clearance according to the technique described by Dao and Patel [17]. For mastectomies and resections of local recurrences, skin incisions were designed to include all tumor clinically, and wherever there was suspicion of infiltration of the pectoralis major or serratus anterior muscle, these muscles were sacrificed. The ensuing defect was measured and a LDMF raised according to the technique described by Olivari [2]. The flap was then sutured into place. The large size of the flaps made split-thickness skin grafting of the flap donor site necessary in all cases. Postoperative radiotherapy was started at the earliest 4 weeks after surgery. Sources were Co 60 or a 6 MV linear accelerator. Chest wall irradiation was administered by medial and lateral tangential fields at a 50 Gy central dose in 25 fractions; supraclavicular and sternal fields were treated up to a total of 50 Gy in daily doses of 2 Gy at 2cm. Complications were defined as follows:

Apffelstaedt: Latissimus Dorsi Flaps

1089

Table 1. Initial staging of breast cancer. Indication for LDMF Primary treatment Local recurrence

Radiation necrosis Surgical complications

Stage at initial diagnosis of breast cancer

n

II B III A III B In situ II A II B III A III B Unknowna II B III A In situ

1 2 64 1 2 1 1 6 2 1 1 1

LDMF: latissimus dorsi myocutaneous flap. Initial treatment elsewhere.

a

Table 2. Preoperative chemotherapy. Preoperative chemotherapy regime

Wound Number of Average number of infection Necrosis patients cycles per patient (n) (n)

No chemotherapy 30 CAF 39 CMF 14

0 3.5 4.1

5 2* 7*

3 7** 4**

C: cyclophosphamide; A: doxorubicin; F: 5-fluorouracil; M: methotrexate. *p ⬍ 0.001; **not significant.

● ● ●

●

Infection: any cellulitis or abscess at the flap insertion site requiring either administration of antibiotics or drainage. Necrosis: any skin or combined skin and muscle loss at the flap insertion site. Incomplete skin graft take: necessity to apply dressings to the skin graft site beyond 4 weeks postoperatively or defects requiring regrafting. Long-term complication: any event at any of the three wound sites that required treatment.

Because of small sample sizes, tests for statistical significance were performed applying Fisher’s exact test as described by Agresti [18].

The elliptic flaps had a mean longitudinal diameter of 32 cm and a mean transverse diameter of 14 cm. Histopathologic evaluation revealed clear margins in 69 cases (83%) and resection through tumor in 14 cases (17%). The flap insertion site was the site of the following complications: infection in 14 cases, 13 of which resolved with administration of antibiotics alone; 1 case required formal abscess drainage. In 7 cases, marginal necrosis of the flap was observed, not requiring any specific therapy. In a further 7 cases the necrosis required intervention as detailed in Table 3. Complications at the flap insertion site with respect to preoperative treatment are given in Tables 2 and 4. The proportion of wound infections was significantly greater in the group of patients receiving preoperative CMF versus CAF chemotherapy (p ⬍ 0.001). The proportion of wound margin necrosis in these two groups was not significantly different. The flap donor site skin graft took completely in 57 cases; minor defects made prolonged dressing necessary in 24 cases, and 2 cases required a second skin graft. Partial skin graft failure occurred in 8 of 30 patients who did not receive preoperative chemotherapy, in 9 of 39 patients who received CAF chemotherapy, and in 8 of 14 patients who received CMF chemotherapy. The proportion of incomplete skin graft take was significantly higher in the group of patients that had CMF chemotherapy versus CAF chemotherapy (p ⬍ 0.05). No complications occurred at the skin graft donor site. None of the patients died within 30 days of the operation. Only in one case did complications retard postoperative treatment. Postoperatively, patients received radiotherapy to the chest wall, supraclavicular and sternal fields. Dosage was 20 Gy, 30 Gy, and 43 Gy each in one patient and 50 Gy in 64 patients. Sixteen patients did not receive postoperative radiotherapy. Six patients developed complications more than 30 days postoperatively for a late complication rate of 7.2%. These are summarized in Table 5. Ultimately, a complete, permanent epithelial cover was achieved for the chest wall in 80 patients (96%); in one patient the wound did not heal before her death 7 months postoperatively; 2 others suffered ulcerating local recurrence 6 and 3 months before death; they had had 15 and 18 months of complete epithelial cover. Twelve further patients suffered a local recurrence that remained well controlled until their death. The mean follow-up of the entire group is 40.0 months. Twenty-four of the patients are alive with no evidence of disease, 5 are alive with evidence of disease, 41 have died of their disease, 5 died of other causes, and 8 are lost to follow-up.

Results From January 1987 to December 1995, of a total of 3007 new cases of breast cancer seen, 83 patients had a LDMF to cover defects caused by the resection of locally advanced breast cancer (67 cases), resection of locally recurrent breast cancer (13 cases), resection of radiation damage (2 cases) after radical irradiation of locally advanced breast cancer, and surgical complications (1 case). The initial staging of breast cancer in respect of the indication for the procedure is reflected in Table 1. The patients’ mean age was 50.2 years (range: 28 to 86 years). Two patients were men. Forty-three of the women were postmenopausal. Details of preoperative chemotherapy are given in Table 2. Sixty-eight patients did not have radiotherapy prior to mastectomy. Two patients had 20 Gy, one patient had 30 Gy, 9 patients had 50 Gy, and 1 patient each had 56, 60, and 70 Gy radiotherapy to the breast before mastectomy.

Discussion Even with aggressive multimodality treatment, most patients with locally advanced breast cancer will die of their disease within 10 years [19 –21]. The survival for patients with local recurrence also is limited [22–26]. For these patients, local control becomes the most important treatment goal. Radiotherapy for advanced lesions requires high dosages to achieve local control, increasing the complication rate [27–29]. Recurrences after breast conservation preclude the use of tumouricidal dosages of radiotherapy because the field has already been irradiated. Some authors have reported good results in the management of locally advanced breast cancer by regimens that rely on radiotherapy to provide local control [30 –34]. Many authors have found an improvement in local control rates and—in some series—survival if surgery is included in the man-

1090

World J. Surg. Vol. 26, No. 9, September 2002

Table 3. Management of flap necrosis. Case

Defect sizea

Management

Time to epithelialize

Comments

1 2 3

Minor Minor 50% of flap

4 months 4 weeks 2 months

4 5

Minor Minor

— — Despite technical adequacy of both procedures and exhaustive search for medical reasons for flap failure, no reason identified — —

6

Minor

Debridement only Debridement ⫹ skin graft Redo with TRAM flap Also 50% necrosis Finally skin graft Debridement ⫹ skin graft Debridement and immediate closure Debridement onlyb

7 months

7

Minor

Debridement onlyb

6 months

6 weeks 2 weeks

Combined with infected local recurrence; patient died of progressive disease with ulcer present Combined with infection

a b

Minor: ⬍ 10% of flap surface. Debridement carried out at bedside under local anesthesia.

Table 4. Flap insertion site complications for preoperative radiotherapy. Preoperative radiotherapy

Number of patients

Wound infection (n)

Necrosis (n)

No Yes

68 15

10* 4*

10* 4*

*Not significant.

agement [19 –21, 25, 35– 42]. Reviewers recommend its inclusion in the treatment of locally advanced breast cancer [19, 43– 45]. The use of the LDMF for wound cover allows for wide resection of big, otherwise unresectable lesions [46]. Olivari initially described the flap for cover of radiation damage on the chest wall [2]. This indication has become rare with the use of modern radiation techniques and better definition of the indications for radiotherapy in locally advanced breast cancer [2, 46 – 48]. No report was found where the flap has been used for wound cover after extensive wound margin necrosis after mastectomy for locally advanced breast cancer. This should also be a rare indication. The wound complication rate after chemotherapy in this series compares to the findings of Broadwater et al. [48] and Danforth et al. [49] for mastectomies without myocutaneous flaps, except for the much higher complication rate for CMF pretreated patients in the present series (Table 6). The introduction of a myocutaneous flap after mastectomy following chemotherapy does not seem to increase the complication rate. The significantly higher complication rate at the flap insertion site and the flap donor site for patients who received CMF versus CAF chemotherapy suggests an adverse effect of methotrexate. This finding may be explained by differences in the two groups as the treatment was not randomized; e.g., the average age of patients in the CMF group was 10 years higher than in the CAF group. The difference, however, remains so striking as to warrant further investigation. Only 5 of the patients had both chemotherapy and radiotherapy preoperatively, and therefore no conclusions concerning the combined effects of radiotherapy and chemotherapy on the complication rate can be drawn. No other series in the English literature was found detailing the complications of LDMF cover after mastectomy for locally advanced breast cancer. Therefore complication rates are compared with the rates reported for LDMF breast reconstruction. In the available series [7, 8, 11, 50], the complication rates are lower than

in the present series (Table 7). This may be due in part to the performance of most of the reconstructions as a separate intervention months to years after the mastectomy. A further explanation may be the larger size of the flaps in the present series. The flaps extended to the pelvic rim, necessitating division of perforating branches from the intercostal and lumbar arteries during mobilization. This may compromise the perfusion of the distal third of the flap [51, 52] and predispose to marginal flap necrosis and infection. The flap insertion site communicates freely with the flap donor site, which in our series was covered with a splitthickness skin graft, allowing free drainage and preventing the accumulation of a seroma. The insertion of the flap may also introduce an alternative pathway for lymphatic drainage around the parts of the axilla that have been dissected. In a large series of LDMFs for chest wall radionecrosis, Rouanet et al. [47] found a 23% early complication rate without specifying the individual complications; 15% of the patients in that series required secondary surgery, versus 8.4% in our series. The large size of the flaps made primary closure of the donor site at the back impossible. Skin grafting to cover the defect introduced its own complications. The base of the recipient site on the back consists largely of fascia and fatty tissue. Furthermore, the proximal part of the site takes part in the movements of the shoulder girdle, making immobilization of the graft on the recipient surface impossible. Under these circumstances incomplete graft take is to be expected [53, 54]. An unexpected finding was the appreciable rate of long-term complications. The long-term complications reported in series of LDMF breast reconstructions [7, 8, 10, 11] are related to the use of prosthetic implants. Most of the patients in these series did not have any radiotherapy. Kroll et al. [9] reported a higher complication rate for reconstructions with latissimus dorsi flaps after radiotherapy versus nonirradiated patients. No differentiation of early and late complications was made, however. The late complication rate of 7% in Rouanet’s series [47] compares to that of the present series (7.2%), and in both series most late complications are of an infective nature. Probably, these are rather a consequence of radiotherapy than an intrinsic problem of the flap. A detailed functional evaluation of the latissimus dorsi donor site was reported by Russell et al. [55]. They found subtle deficits in shoulder function in most patients. Only one patient in our series complained about limited range of motion of her shoulder joint. Other techniques used for wound cover after resection of locally

Apffelstaedt: Latissimus Dorsi Flaps

1091

Table 5. Late complications. Time after operation (months) 3 6 6 6 6 15

Complication

Management

Time to epithelialize completely

Abscess Abscess Abscess Fibrosis of flap pedicle Sinus in scar

Drainage Drainage Drainage ⫹ skin graft Physiotherapy

2 months 2 months 4 months —

Conservative

3 years

Granuloma in scar

Excision

2 weeks

Comment — — Diabetic patient Limits elevation of arm above 90 degrees Diabetic patient; refused operative revision —

Table 6. Reported complication rates of mastectomy after chemotherapy. Series

Preoperative chemotherapy

Number of patients

Infection rate (%)

Necrosis rate (%)

Seroma rate (%)

Danforth et al. [33] Broadwater et al. [29] Present series

CAMFPT CAF CAF CMF

54 106 39 14

2 7 5 50

15 11 18 29

9 15 0 0

P: prednisone; T: tamoxifen. Table 7. Complication rates for breast reconstruction with LDMF.

Series

n

Infection rate (%)

De Mey et al. [6] Moore et al. [9] Hokin et al. [10] Olivari [39] Present series

150 170 55 74 83

3.3 5 ND 8.0 17

Necrosis rate (%)

Seroma/ hematoma rate (%)

4 3.6 20 5.4 17

8.6 9.6 3.6 5.3 0

ND: not described.

advanced lesions and radiation damage are transposed omentum with skin graft, fasciocutaneous flaps, transverse rectus abdominis musculocutaneous (TRAM) flap and breast flap [2, 43, 44, 46, 47, 56]. In contrast to the TRAM flap in particular, which is the other commonly used musculocutaneous flap in breast surgery, the availability of the latissimus dorsi flap is not limited by prior abdominal surgery; it is technically less demanding, more reliable with less long-term donor site morbidity [7, 10, 47]. In the practice of this author, which is located in developing country where there are long distances between medical centers, 30% of patients still present with stage III breast cancer. Many of our rural patients do not have the means to afford the regular trips required for neoadjuvant chemotherapy and need complete therapy of their disease during one single stay. Also, while the majority of patients who receive induction chemotherapy respond to allow for modified radical mastectomy to be performed, there is a significant minority, in our experience about 10% of patients, who neither respond well nor progress during induction chemotherapy. In these patients and patients with isolated local recurrence, the use of the latissimus dorsi myocutaneous flap made wide resection of advanced lesions possible. Major complications were rare. Its technique is simple and has its place in the armamentarium of the surgeon who regularly sees locally advanced breast cancer. Résumé. L’utilisation du lambeau myocutané du grand dorsal (LMGD) dans la chirurgie reconstructrice du sein est bien documentée. Il existe

quelques publications concernant son utilisation en chirurgie oncologique du sein. Cette série décrit les indications et les complications de l’utilisation du LMGD dans les cancers avancés mais localisés du sein. Les dossiers de 83 patients ont été analysés en ce qui concerne l’âge et le sexe, l’état menstruel, le stade, l’indication, les marges de résection, la chimiothérapie, la radiothérapie, les complications et la survie. Les indications du lambeau comprenaient la couverture après résection du cancer du sein avancé localisé (67 cas), du cancer du sein récidivé (13 cas), des lésions secondaires à l’irradiation (2 cas) et des complications chirurgicales (1 cas). L’âge moyen des patients était de 50.2 ans; 52% étaient en période post menstruelle. En moyenne, les lambeaux mesuraient 32 par 14 cm. On a toujours greffé le site donneur par une greffe de peau. On a réalisé des marges non envahies dans 83% des cas. On a observé un cas d’infection au niveau de l’insertion du LMGD qui a nécessité un drainage; la nécrose du lambeau a nécessité une réintervention dans sept cas. Dans deux cas, une deuxième greffe de peau a été réalisée au site donneur. La proportion de l’infection de la plaie et les greffes incomplètes de peau a été significativement plus élevée chez les patients recevant une chimiothérapie CMF (Cyclophosphamide, méthotrexate, 5-fluorouracile) en préopératoire par rapport à celles recevant une chimiothérapie CAF (Cyclophosphamide, doxorbicine, 5fluorouracile) (p < 0.001 et p < 0.05, respectivement). Des complications tardives ont été observées chez 7.2% des patientes. Le suivi moyen a été de 40.0 mois. Le taux de complications de la CMF plus élevée que pour la CAF suggère un effet indésirable pour le méthotrexate, ce qui mérite de plus amples investigations. L’utilisation du LMGD rend possible une résection large des lésions localement avancées et des lésions secondaires à la radionécrose; les complications majeures ont été rares. Cette thérapeutique a sa place dans l’arsénal thérapeutique du chirurgien qui voit souvent des cas de cancer du sein localement avancé. Resumen. El uso del colgajo miocutáneo de dorsal ancho, latissimus dorsi (CMLD), en la cirugía reconstructiva del seno está bien documentado, aunque son escasos los informes sobre su utilización en cirugía oncológica mamaria. El presente artículo describe nuestra serie de casos, con sus indicaciones y complicaciones en pacientes con cáncer localmente avanzado. Se analizaron las historias clínicas de 83 pacientes, en cuanto a edad y género, estado menstrual, estadio, indicación, márgenes de resección, quimioterapia, radioterapia, complicaciones y supervivencia. La indicación fue cubrir los defectos consecuentes a la resección de cáncer de seno localmente avanzado (67 casos), cáncer mamario recurrente (13 casos), daño por irradiación (2 casos) y complicaciones quirúrgicas (1 caso). La edad promedio en el grupo de pacientes fue 50.2 años; 52% de las pacientes eran postmenopáusicas. Los colgajos tuvieron diámetros promedio de 32 por 14 cm. El sitio donante fue cubierto con trasplante de piel. Se registraron márgenes libres en 83% de los casos. En un caso se

1092 requirió drenaje del sitio de inserción del CMLD por infección de la herida; en 7 casos se requirió reintervención; en 2 casos se practicó un segundo injerto de piel en el sitio donante del CMLD. Las tasas de infección y de falla parcial del injerto fueron significativamente mayores en las pacientes que recibieron quimioterapia preoperatoria con CMF versus CAF (p < 0.001 y p < 0.05, respectivamente). La tasa de complicaciones a largo plazo fue 7.2%. El seguimiento promedio fue de 40.0 meses. Las tasas de complicaciones de CMF versus CAF sugieren un efecto adverso del metrotrexato, lo cual merece investigación. El uso del CMLD ha hecho factible la resección amplia de cánceres localmente avanzados y de regiones de radionecrosis. El CMLD posee un lugar definido en el armamentario del cirujano que trata cánceres mamarios localmente avanzados.

Acknowledgments Thanks to Dr. Theunis J.v.W. Kotze, B.Sc., Chief Statistician at the Center for Statistical Consultation, Department of Statistics, University of Stellenbosch, Stellenbosch, South Africa, for statistical supervision in the preparation of the manuscript. References 1. Tansini I. Nuovo processo per l’amputazione della mamella per cancre. Riforma Med. Napoli 1896;12:3 2. Olivari N. The latissimus flap. Br. J. Plast. Surg. 1976;29:126 –128 3. Mühlbauer W, Olbrich R. The latissimus dorsi myocutaneous flap for breast reconstruction. Chir. Plast. 1977;4:27 4. Schneider WJ, Hill HL, Brown RG. Latissimus dorsi myocutaneous flap for breast reconstruction. Br. J. Plast. Surg. 1977;30:277 5. Berrino P, Campora E, Leone S, et al. Correction of type II breast deformities following conservative cancer surgery. Plast. Reconstr. Surg. 1992;90:846 – 853 6. Bostwick J, Scheflan M. The latissimus dorsi musculocutaneous flap: a one-stage breast reconstruction. Clin. Plast. Surg. 1980;7:71–78 7. DeMey A, Lejour M, Declety A, et al. Late results and current indications of latissimus dorsi breast reconstructions. Br. J. Plast. Surg. 1991;44:1 8. Hokin JA, Silfverskiold KL. Breast reconstruction without an implant: results and complications using an extended latissimus dorsi flap. Plast. Reconstr. Surg. 1987;79:58 – 66 9. Kroll SS, Schustermann MA, Reece GP, et al. Breast reconstruction with myocutaneous flaps in previously irradiated patients. Plast. Reconstr. Surg. 1994;93:460 10. Kroll SS, Baldwin B. A comparison of outcomes using three different methods of breast reconstruction. Plast. Reconstr. Surg. 1992;90:455– 462 11. Moore TS, Farrell LD. Latissimus dorsi myocutaneous flap for breast reconstruction: long-term results. Plast. Reconstr. Surg. 1992;89:666 – 672 12. Noone RB, Murphy JB, Spear SL, et al. A 6-year experience with immediate reconstruction after mastectomy for cancer. Plast. Reconstr. Surg. 1985;76:258 –269 13. Pendergast W, Bostwick J, Jurkiewicz JM. The subcutaneous mastectomy cripple: surgical rehabilitation with the latissimus dorsi flap. Plast. Reconstr. Surg. 1980;66:554 14. Slavin SA. Improving the latissimus dorsi myocutaneous flap with tissue expansion. Plast. Reconstr. Surg. 1994;93:811– 824 15. Zoetmulder FA, Borger JH, Rutgers EJ, et al. Breast conserving therapy in patients with relatively large (T2, T3) breast cancers by preoperative irradiation and myocutaneous LD flap reconstruction. A new technique in breast conservation. Eur. J. Cancer 1993;29A:957– 961 16. Hermanek P, Sobin LH. TNM Classification of Malignant Tumours. International Union Against Cancer, 4th Edition,. Berlin, SpringerVerlag, 1987:93–99 17. Dao TL, Patel J. Modified Radical Mastectomy. Boston, Little Brown & Company, 1984:257–264 18. Agresti A. Inference for 2-Way Contingency Tables. New York, John Wiley, 1992:36 –78

World J. Surg. Vol. 26, No. 9, September 2002 19. Borgen PI. Management of locally advanced breast cancer. World J. Surg. 1994;18:81– 86 20. Graham MV, Perez CA, Kuske RR, et al. Locally advanced (noninflammatory) carcinoma of the breast: results and comparison of various treatment modalities. Int. J. Radiat. Oncol. Biol. Phys. 1991;21: 311–318 21. Swain SM. Selection of therapy for stage III breast cancer. Surg. Clin. North Am. 1990;70:1061–1080 22. Chen KK, Montague ED, Oswald MJ. Results of irradiation in the treatment of locoregional breast cancer recurrence. Cancer 1985;56: 1269 –1273 23. Gilliland MD, Barton RM, Copeland EM. The implications of local recurrence of breast cancer as the first site of therapeutic failure. Ann. Surg. 1983;197:284 –287 24. Haffty BG, Goldberg NB, Fischer D, et al. Conservative surgery and radiation therapy in breast carcinoma: local recurrence and prognostic implications. Int. J. Radiat. Oncol. Biol. Phys. 1989;17:727–732 25. Osborne MP, Simmons RM. Salvage surgery for recurrence after breast conservation. World J. Surg. 1994;18:93–97 26. Toonkel LM, Fix I, Jacobson LH, et al. The significance of local recurrence of carcinoma of the breast. Int. J. Radiat. Oncol. Biol. Phys. 1983;9:33–39 27. Puthawala AA, Syed AM, Sheikh KM, et al. Combined external and interstitial irradiation in the treatment of stage III breast cancer. Radiology 1984;153:813– 816 28. Sheldon T, Hayes DF, Cady B, et al. Primary radiation therapy for locally advanced breast cancer. Cancer 1987;60:1219 –1225 29. Spanos-WJ J, Montague ED, Fletcher GH. Late complications of radiation only for advanced breast cancer. Int. J. Radiat. Oncol. Biol. Phys. 1980;6:1473–1476 30. Borger JH, van-Tienhoven G, Passchier DH, et al. Primary radiotherapy of breast cancer: treatment results in locally advanced breast cancer and in operable patients selected by positive axillary apex biopsy. Radiother. Oncol. 1992;25:1–11 31. Weshler Z, Brufman G, Sulkes A, et al. Radiation therapy for locally advanced breast cancer: prognostic factors and complication rate. Eur. J. Surg. Oncol. 1990;16:430 – 435 32. Ahern V, Barraclough B, Bosch C, et al. Locally advanced breast cancer: defining an optimum treatment regimen. Int. J. Radiat. Oncol. Biol. Phys. 1994;28:867– 875 33. Bartelink H, Rubens RD, van-der-Schueren E, et al. Hormonal therapy prolongs survival in irradiated locally advanced breast cancer: A European Organization for Research and Treatment of Cancer Randomized Phase III Trial. J. Clin. Oncol. 1997;15:207–215 34. Koning C, Hart G. Long-term follow-up of a randomized trial on adjuvant chemotherapy and hormonal therapy in locally advanced breast cancer. Int. J. Radiat. Oncol. Biol. Phys. 1998;41:397– 400 35. Toonkel LM, Fix I, Jacobson LH, et al. Locally advanced breast carcinoma: results with combined regional therapy. Int. J. Radiat. Oncol. Biol. Phys. 1986;12:1583–1587 36. Pierce LJ, Lippman M, Ben-Baruch N, et al. The effect of systemic therapy on local-regional control in locally advanced breast cancer. Int. J. Radiat. Oncol. Biol. Phys. 1992;23:949 –960 37. Martijn H, Caspers RJ, Welvaart K, et al. Locally advanced breast cancer: radiotherapy alone versus surgery and radiotherapy. Radiother. Oncol. 1989;16:23–29 38. Lopez MJ, Andriole DP, Kraybill WG, et al. Multimodal therapy in locally advanced breast carcinoma. Am. J. Surg. 1990;160:669 – 674 39. Ames FC, Balch CM. Management of local and regional recurrence after mastectomy or breast-conserving treatment. Surg. Clin. North Am. 1990;70:1115–1124 40. Hathaway CL, Rand RP, Moe R, et al. Salvage surgery for locally advanced and locally recurrent breast cancer. Arch. Surg. 1994;129: 582–587 41. McKenna-RJ J, McMurtrey MJ, Larson DL, et al. A perspective on chest wall resection in patients with breast cancer. Ann. Thorac. Surg. 1984;38:482– 487 42. Perloff M, Lesnick GJ, Korzun A, et al. Combination chemotherapy with mastectomy or radiotherapy for stage III breast carcinoma: a Cancer and Leukemia Group B study. J. Clin. Oncol. 1988;6:261–269 43. Hortobagyi GN, Buzdar AU, Strom EA, et al. Primary chemotherapy for early and advanced breast cancer. Cancer Lett. 1995;90:103–109

Apffelstaedt: Latissimus Dorsi Flaps 44. Perez EA, Foo ML, Fulmer JT. Management of locally advanced breast cancer. Oncology (Huntingt) 1997;11(Suppl 9):9 –17 45. Hunt KK, Ames FC, Singletary SE, et al. Locally advanced noninflammatory breast cancer. Surg. Clin. North Am. 1996;76:393– 410 46. Amelung S, Kufer C. [Myocutaneous latissimus dorsi flaps for covering defects in local recurrences of breast cancers or radiation ulcers] Myokutane Latissimus-dorsi-Lappen zur Defektdeckung bei Mammakarzinom-Lokalrezidiven oder Strahlenulzera. Geburtshilfe. Frauenheilkd. 1988;48:326 –330 47. Rouanet P, Fabre JM, Tica V, et al. Chest wall reconstruction for radionecrosis after breast carcinoma therapy. Ann. Plast. Surg. 1995; 34:465– 470 48. Broadwater JR, Edwards MJ, Kuglen C, et al. Mastectomy following preoperative chemotherapy. Strict operative criteria control operative morbidity [see comments]. Ann. Surg. 1991;213:126 –129 49. Danforth J, Lippman ME, McDonald H, et al. Effect of preoperative chemotherapy on mastectomy for locally advanced breast cancer. Am. Surg. 1990;56:6 –11 50. Olivari N (1989) The latissimus dorsi flap and breast reconstruction.

1093

51. 52.

53. 54. 55. 56.

In Bohmert HH, Leis HP Jr., Jackson IT, editors. Breast Cancer: Conservative and Reconstructive Surgery. New York, Thieme Medical Publishers Inc., pp 253–260 El-Maasarany SH, Sharaf E, Moustafa F, et al. Anatomical basis of latissimus dorsi myocutaneous flap: clinical applications. Surg. Radiol. Anat. 1989;11:197–203 Cormack GC. Thoracodorsal artery–latissimus dorsi musculocutaneous flap. In Cormack GC, Lamberty BGH, editors, The Arterial Anatomy of Skin Flaps, 2nd edition, New York, Churchill Livingstone, 1994;473– 477 Johnson TM, Ratner D, Nelson BR. Soft tissue reconstruction with skin grafting. J. Am. Acad. Dermatol. 1992;27:151–165 Branham GH, Thomas JR. Skin grafts. Otolaryngol. Clin. North Am. 1990;23:889 – 897 Russell RC, Pribaz J, Zook EG, et al. Functional evaluation of latissimus dorsi donor site. Plast. Reconstr. Surg. 1986;78:336 –344 Olivari N. Use of thirty latissimus dorsi flaps. Plast. Reconstr. Surg. 1979;64:654 – 661