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Thrombosis of the internal mammary artery during delayed autologous breast reconstruction - A manifestation of occult residual cancer

March 2016
JPRAS Open 8(C)

DOI:10.1016/j.jpra.2016.02.001

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The Royal Marsden NHS Foundation Trust

A prothombotic state may be a manifestation of malignancy, either primary or recurrent. In this report we present a case of thrombosis of the internal mammary artery during delayed autologous breast reconstruction occurring in association with, and as a possible manifestation of, occult recurrent breast cancer. We discuss salvage of the microsurgical anastomosis using a vein graft and microvascular anastomotic coupler device.

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Case report

Thrombosis of the internal mammary artery during delayed

autologous breast reconstruction: A manifestation of occult

residual cancer

Alexandra Bucknor

, Mobinulla Syed

, Gerald Gui

, Stuart James

Department of Plastic and Reconstructive Surgery, Charing Cross Hospital, Fulham Palace Road, London W6 8RF, UK

Department of Plastic and Reconstructive Surgery, The Royal Marsden Hospital, Fulham Road, London SW3 6JJ, UK

Breast Surgery, The Royal Marsden Hospital, Fulham Road, London SW3 6JJ, UK

article info

Article history:

Received 22 October 2015

Accepted 9 February 2016

Available online 2 March 2016

Keywords:

Autologous breast reconstruction

Internal mammary thrombosis

Breast cancer recurrence

Anastomotic coupler

Heparin

abstract

A prothombotic state may be a manifestation of malignancy, either

primary or recurrent. In this report we present a case of throm-

bosis of the internal mammary artery during delayed autologous

breast reconstruction occurring in association with, and as a

possible manifestation of, occult recurrent breast cancer. We

discuss salvage of the microsurgical anastomosis using a vein graft

and microvascular anastomotic coupler device.

Association of Plastic, Reconstructive and Aesthetic Surgeons. This

is an open access article under the CC BY-NC-ND license (http://

creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

Thrombosis is well documented in association with malignancy, with a number of theories pro-

posed accounting for this phenomenon. Mechanisms include direct activation of the coagulation

cascade by tumour cells, or indirectly, through production of pro-coagulant factors or inhibition of anti-

coagulant factors.

The pattern of early recurrence is variable and is governed by complex interplay

between tumour factors and patient factors. Peri-operative factors, including the trauma of surgery

itself, may also inﬂuence the pattern of recurrence.

*Corresponding author. Tel.: þ44 20 3311 1234.

E-mail address: alexandrabucknor@gmail.com (A. Bucknor).

Contents lists available at ScienceDirect

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journal homepage: http://www.journals.elsevier.com/

jpras-open

http://dx.doi.org/10.1016/j.jpra.2016.02.001

Surgeons. This is an openaccess article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

JPRAS Open 8 (2016) 6e8

There has been a recent report alluding to the possibility of reactivation of quiescent micro-

metastasis lying within internal mammary (IM) nodal territory at the time of delayed breast recon-

struction, leading to recurrence.

IM vessels have long been recognised as useful recipient sites for vascular anastomosis in autolo-

gous breast reconstruction.

The safety proﬁle is equal to that of the previously favoured thoracodorsal

vessels with the added advantage of relative ease of dissection in delayed reconstruction, particularly

where axillary node clearance or radiotherapy has been performed.

We present a case of intra-operative IM artery thrombosis following microsurgical anastomosis that

seemed to have occurred as a result of activation of local tissue factors, which may have increased the

propensity for thrombosis. We go on to discuss further intra-operative and post-operative manage-

ment of such a challenging situation.

Case report

A 32-year old woman, without signiﬁcant past medical history, presented with a lump in the left

breast and was diagnosed with a 4 cm, grade two invasive ductal carcinoma in 2012, with no evidence

of metastatic disease. The patient was treated with neoadjuvant chemotherapy with 5- Flourouracil,

epirubicin, cyclophosphamide and docetaxel; to which she had a good response. She underwent a left

skin-sparing mastectomy and axillary clearance, with three out of 14 lymph nodes involved, followed

by insertion of a submuscular, expandable implant-based reconstruction. 6 mm of local, residual cancer

was found and she was treated with radiotherapy and tamoxifen.

In 2014, the patient underwent implant removal and a delayed left breast reconstruction with a

deep inferior epigastric perforator (DIEP) free ﬂap.

During the reconstruction, only a few minutes after a technically sound anastomosis performed

under a microscope with 9/0 nylon sutures, IM arterial thrombosis was noted. On exploration, there

were streaks of thrombi extending from each of the sutures of the arterial anastomosis. In order to

remove the areas of the vessel with thrombus and the precipitating activated endothelium, approxi-

mately 2 cm of the IM artery was resected and further thrombosis necessitated that an interpositional

vein graft was harvested to redo the anastomosis. A venous coupler device was used to anastomose the

vein graft to IM artery and the graft to the ﬂap vessels. The patient was given an intraoperative bolus of

5000 IU of intravenous heparin and subsequently maintained on a heparin infusion to achieve an

activated partial prothrombin time (APPT) ratio of three for the next ﬁve days. She was then discharged

with a month's course of aspirin, 75 mg once-daily; the ﬂap remains healthy at most recent check, one

year and eight months post-operatively.

The section of the IM artery that was resected was sent for histopathology in view of the intra-

operative ﬁndings. Immunostaining demonstrated a small nest and cords of atypical cells within the

ﬁbrous tissue and perineural space; these cells were positive for CAM5.2 and ER, conﬁrming the

presence of metastatic adenocarcinoma, consistent with a breast primary.

A post-operative PET scan was negative, but an MRI suggested suspicious lesions in the liver with a

possibility of recurrence. The patient was put on Letrozole and underwent radiofrequency ablation for

the liver lesions. One year and ten months later, she remains well and is under four-monthly

surveillance.

Discussion

Microvascular autologous breast reconstruction is of well-established importance in the operative

management of breast cancer. The safety proﬁle of breast reconstruction with regard to cancer

recurrence has been well established, with studies reporting similar or lower recurrence rates in pa-

tients undergoing reconstruction, when comparing them to those who did not.

Wojciech et al

re-

ported on a patient who, one year post-delayed DIEP ﬂap reconstruction, presented with an

erythematous rash as a manifestation of recurrence, where cutaneous lymphatics may have been the

route of spread. Shariff et al

identiﬁed a woman found to have two separate recurrences of breast

cancer after a delayed latissimus dorsi ﬂap reconstruction, involving the ﬂap and its underlying

A. Bucknor et al. / JPRAS Open 8 (2016) 6e87

musculature. A case series reported on three women who developed recurrence after delayed recon-

struction, one of whom had been disease-free for fourteen years.

In our patient with previously undetected quiescent micrometastases, local production of pro-

coagulant factors within the IM vessels, combined with the surgical trauma of IM vessel harvest may

have triggered the observed, rapid thrombosis. Streaks of thrombi extending like wisps from each

suture and coalescing in the vessel are uncommon enever encountered previously in our senior au-

thor's practice eand might reﬂect the highly hypercoagulable state.

The use of heparin prophylaxis against vascular thrombosis during free ﬂap surgery should be

balanced against the inherent risks. Heparin inhibits the coagulation cascade by binding to antithrombin

III, and platelet aggregation is impaired; given that platelet aggregation underlies arterial thrombosis, it

is an effective means of preventing arterial thrombosis. However, there is an increased risk of bleeding,

subsequent haematoma formation and compromised ﬂap perfusion. Currently, no clear consensus exists

on the type, timing and duration of anticoagulation used in ﬂap surgery; however, in this instance it may

have contributed to maintaining a patent anastomosis and preventing ﬂap failure.

The microvascular coupler reduces the risk of thrombosis by negating the need for foreign (suture)

material within the vascular lumen. A study on 1000 venous anastomoses performed with the coupler

in autologous breast reconstruction found much reduced thrombosis rates when compared with su-

tured equivalents, 0.6% and 2.8%, respectively.

Conclusion

Internal mammary vessels remain the preferred recipient vessels during autologous microvascular

breast reconstruction at our institution. This case demonstrates how unprecedented on-table IM artery

thrombosis may be successfully managed with the microvascular anastomotic coupler and prolonged

heparinisation, securing a patent anastomosis despite a prothrombotic environment.

In addition, it reinforces the need for a high index of suspicion where severe thrombotic tendencies

are seen; histopathological and immunohistochemical investigations should be undertaken fromintra-

operative specimens to rule out occult disease.

Conﬂicts of interest

None.

Funding

None.

Ethical approval

Not applicable.

References

1. Lip Gregor YH, Chin Bernard SP, Blann Andrew D. Cancer and the prothrombotic state. Lancet Oncol. 2002;3:27e34.

2. Rosich-Medina Anais, Wang Susan, Erel Erten, Malata Charles M. Internal mammary recipient site breast cancer recurrence

following delayed microvascular breast reconstruction. EPlasty. 2013;13:24e30.

3. Saint-Cyr Michel, Youssef Adel, Bae Hyung Woon, Robb Geoffrey L, Chang David W. Changing trends in recipient vessel

selection for microvascular autologous breast reconstruction: an analysis of 1483 consecutive cases. Plast Reconstr Surg Glob

Open. 2007;119:1993e2000, 2007.

4. Lindford Andrew J, Siponen Elina T, Jahkola Tiina A, Leidenius Marjut HK. Effect of delayed autologous breast reconstruction

on breast cancer recurrence and survival. World J Surg. 2013;37:2872e2882.

5. Przylecki Wojciech H, Chan Rodney K, Carty Matthew J, Caterson Stephanie A. Metastatic breast cancer after delayed deep

inferior epigastric perforator ﬂap reconstruction. Ann Plast Surg. 2011;63:233e234.

6. Hazarika Shariff A, Cassell Oliver, Grifﬁths Carl. Breast cancer recurrence following delayed reconstruction detected within

the latissimus dorsi ﬂap and locoregional tissue. Plast Reconstr Surg Glob Open. 20 06;117:2096e2097.

7. Jandali Shareef, Wu Liza C, Vega Stephen J, Kovach Stephen J, Serletti Joseph M. 1000 consecutive venous anastomoses using

the microvascular anastomotic coupler in breast reconstruction. Plast Reconstr Surg Glob Open. 2010;125:792e798.

A. Bucknor et al. / JPRAS Open 8 (2016) 6e88

Chest wall reconstruction in recurrent breast carcinoma – a case report

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Introduction Complex chest wall reconstruction after an oncological resection requires a multidisciplinary approach with the aim of curative resection. Aim The complexity of such reconstruction is challenged by prior reconstructions that limit the options for free tissue transfer and recipient vessels for microsurgical anastomoses. Case study We present a case of an immunocompromised patient with prior breast reconstruction for left breast carcinoma with a pedicled lattisimus dorsi flap who presents with a recurrence to the latissimus dorsi flap requiring a more extensive oncological resection. Results and discussion This resulted in a large chest wall defect that is reconstructed with plating and an anterolateral thigh fasciocutaneous free flap for soft tissue coverage. Conclusions The radical resection allows for excellent overall survival and better quality of life.

Risk Assessment and Anesthesia Classification in Breast Cancer Surgery

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Nov 2018

Background: There are various factors affecting the effectiveness of the treatment of breast cancer patients. Although the disease pathology, along with surgery and other therapeutic modalities, plays the principal role in patient outcomes, anesthesia still plays an important role in the success of treatment. This study was designed to show the effects of anesthetic plans on risk classification and assessment in breast cancer surgeries. Methods: Two hundred sixty patients receiving different types of breast cancer surgery for therapeutic and reconstructive purposes were enrolled in this study. They were divided into three groups according to the anesthesia risk assessment. Group 1 consisted of low-risk patients (ASA I) who received small surgeries such as lumpectomy. Patients with intermediate risk of anesthesia (ASA II) or those who underwent breast cancer and axillary surgery with overnight admission (ASA I or II) were considered as group 2. Group 3 comprised the patients with higher risk for anesthesia (ASA class III) regardless of the surgery type or those in any ASA class who were about to undergo advanced and prolonged surgeries such as breast reconstruction with free or pedicle flaps. Results: Two hundred sixty-eight surgical interventions were done in 260 patients. There were 106, 107, and 47 patients in groups 1, 2, and 3, respectively. In group 1, five patients out of 106 were admitted in the hospital for 24 hours after surgery and the remaining 101 patients were discharged from the hospital in a few hours after the operation when they were fully conscious and could tolerate the diet completely. All 107 patients in group 2 were admitted in the hospital for a few days after the operation, though the vast majority of them (98 patients) discharged from the hospital the day after surgery. In the last group, 6 out of 47 patients showed the signs of surgical complications such as partial flap ischemia in the postoperative period, mostly after TRAM or DIEP flap breast reconstruction surgery. Conclusion: The findings of this study support the idea that breast surgeries can be done in an ambulatory situation with no considerable risk. In contrast, all medical and anesthetic considerations should be taken into account in more complex surgeries, especially when they are applied in high-risk patients.

Internal Mammary Recipient Site Breast Cancer Recurrence Following Delayed Microvascular Breast Reconstruction

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Jan 2013

Objective: The internal mammary vessels are a popular recipient site for microsurgical anastomoses of free flap breast reconstructions. We, however, observed 3 patients undergoing internal mammary vessel delayed free flap breast reconstruction that subsequently developed tumor recurrence at this site. We reviewed their characteristics to determine whether there was a correlation between delayed microsurgical reconstruction and local recurrence. Methods: A retrospective review of a single surgeon's delayed free flap breast reconstructions using the internal mammary vessels was conducted over a 7-year period to identify the time intervals between mastectomy and delayed breast reconstruction and between delayed breast reconstruction and recurrence. Results: Three patients developed local recurrence at the site of the microvascular anastomoses following delayed breast reconstruction. All patients had been disease-free following mastectomy. The median time interval between mastectomy and delayed breast reconstruction was 28 months (range = 20-120 months) while that between delayed breast reconstruction and local recurrence was 7 months (range = 4-10 months). Two patients died from metastatic disease, 36 and 72 months following their local recurrence. One patient remains alive 44 months after reconstruction. Conclusions: Local tumor recurrence at the internal mammary vessel dissection site following delayed breast reconstruction raises the question whether these 2 events may be related. Specifically, could internal mammary vessel dissection undertaken for delayed microsurgical reconstruction predispose to recurrence in the internal mammary lymph nodes? Further research is needed to ascertain whether delayed breast reconstruction increases the risk of local recurrence in this patient group.

Effect of Delayed Autologous Breast Reconstruction on Breast Cancer Recurrence and Survival

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WORLD J SURG

The goal of the present study was to evaluate the impact of delayed autologous breast reconstruction on disease relapse in breast cancer patients treated with mastectomy. The study was based on 503 consecutive patients younger than 70 years of age who underwent mastectomy between January 2000 and December 2003. Overall, 391 (78 %) received mastectomy alone and 112 (22 %) underwent a delayed breast reconstruction. The median time from mastectomy to delayed breast reconstruction was 34 months. The median duration of follow-up was 102 months. There were no locoregional recurrences (LRR) in patients who underwent delayed reconstruction (0.0 %); 21 LRR developed in patients treated with mastectomy only (5.4 %), P = 0.011. Distant metastases occurred less frequently in the reconstruction group (12.5 %) than in the patients who underwent mastectomy alone (21.5 %); P = 0.0343. The 8-year breast cancer specific survival in the reconstruction group was 98.2 and 85.7 % for the mastectomy only group, P = 0.000. Delayed autologous breast reconstruction does not appear to adversely influence disease progression when compared to patients treated with mastectomy only.

Metastatic Breast Cancer After Delayed Deep Inferior Epigastric Perforator Flap Reconstruction

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ANN PLAS SURG

Locoregional breast cancer recurrence is a relatively rare event, occurring more frequently in patients diagnosed with more advanced stages of cancer and those with inflammatory features. While typical signs of recurrence after reconstruction include the development of a mass in the native skin or deep chest wall, oncologic relapse may also rarely be heralded by subtle cutaneous changes. This article describes a patient with inflammatory breast cancer who underwent neoadjuvant chemotherapy, mastectomy, radiation therapy, and hormonal therapy followed by delayed reconstruction with a deep inferior epigastric artery perforator flap and subsequently presented with a recurrence manifest as a localized rash over the upper abdomen. Surgeons who perform breast reconstruction should be attuned to both common and uncommon recurrence symptoms, as they may be the first to diagnose recrudescent disease.

1000 Consecutive Venous Anastomoses Using the Microvascular Anastomotic Coupler in Breast Reconstruction Reply

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Mar 2010

Microvascular anastomosis is one of the more critical aspects of free flap surgery. A safe, effective, and expedient method for venous anastomosis minimizes flap ischemia time, is easier on the surgical team, and saves costly operating room time. The authors report on their experience using the Synovis microvascular anastomotic coupling device in 1000 consecutive venous anastomoses in free flap breast reconstruction. The authors retrospectively reviewed 1000 consecutive venous anastomoses that were performed using the microvascular anastomotic coupler between July of 2002 and July of 2008. Data were obtained on flap type, recipient vessel, coupler size, incidence of venous thrombosis, timing of venous thrombosis, and morbidity as a result of venous thrombosis. All anastomoses were performed in an end-to-end fashion. There were 460 unilateral cases and 270 bilateral cases of breast reconstruction. Flap types included muscle-sparing free transverse rectus abdominis myocutaneous, deep inferior epigastric perforator, superficial inferior epigastric artery, superior gluteal artery perforator, and inferior gluteal artery perforator. The vast majority of the recipient vessels were the internal mammary or thoracodorsal vessels. Most of the couplers that were used were either 3 or 2.5 mm in diameter. Overall, there were six instances of venous thrombosis (rate of 0.6 percent). There were no total flap losses due to venous thrombosis in this series, although two patients had partial flap necrosis. The patency rate for venous anastomoses performed with the microvascular coupler is excellent when compared with standard suture techniques and has the advantage of overall easier application.

Cancer and the prothrombotic state

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Feb 2002
LANCET ONCOL

Thrombosis is a frequent complication of cancer, so it follows that the presence of a tumour confers a prothrombotic state. Indeed, in patients with cancer, each of the three components of Virchow's triad that predispose for thrombus formation have abnormalities, thus fulfilling the requirement for a prothrombotic or hypercoagulable state. The many signs and symptoms of the prothrombotic state in cancer range from asymptomatic basic abnormal coagulation tests to massive clinical thromboembolism, when the patient may be gravely ill. Many procoagulant factors, such as tissue factor and cancer procoagulant, are secreted by or are expressed at the cell surface of many tumours. Platelet turnover and activity are also increased. Damaged endothelium and abnormalities of blood flow in cancer also seem to play a part, as does abnormal tumour angiogenesis. Some studies have even suggested that these abnormalities may be related to long-term prognosis and treatment. We briefly describe the various clinical manifestations of thrombosis in cancer and discuss the evidence for the existence of a prothrombotic or hypercoagulable state associated with this disease. Further work is needed to examine the mechanisms leading to the prothrombotic state in cancer, the potential prognostic and treatment implications, and the possible value of quantifying indices of hypercoagulability in clinical practice.

Breast Cancer Recurrence following Delayed Reconstruction Detected within the Latissimus Dorsi Flap and Locoregional Tissue

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Changing Trends in Recipient Vessel Selection for Microvascular Autologous Breast Reconstruction: An Analysis of 1483 Consecutive Cases

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Jul 2007

Over the years, the authors' preferred recipient vessels for microvascular autologous breast reconstruction have changed from the thoracodorsal to the internal mammary vessels. From 1994 to 2004, 1483 microvascular autologous breast reconstructions were performed in 1168 patients at the authors' institution. Potential factors involved in the selection of the recipient vessels were evaluated and compared between the thoracodorsal and internal mammary groups. Rates of recipient vessel unusability and flap-related complications were also analyzed and compared between the two groups. The mean patient age was 48 years, and the mean follow-up time was 1.5 years. The vessel conversion rate was 2.8 percent for the thoracodorsal group and 1.9 percent for the internal mammary group. Preoperative radiotherapy and previous axillary node dissection were significantly associated with thoracodorsal vessel conversion (odds ratios, 4.7 and 2.6, respectively). The overall flap-related complication rate (12.6 percent versus 8.6 percent) and specific flap-related complications, including flap loss (2.6 percent versus 3.8 percent), vessel thrombosis (3.7 percent versus 5.0 percent), fat necrosis (4.5 percent versus 2.6 percent), infection (0.7 percent versus 0.7 percent), and hematoma (1.6 percent versus 1.9 percent), were comparable between the two groups, but the flap seroma rate was significantly higher in the thoracodorsal group (4.0 percent versus 0.7 percent; odds ratio, 4.2). In the authors' experience, use of internal mammary vessels is safe, with low rates of vessel conversion and flap-related complications.