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Long term study into surgical re-exploration of the ‘free flap in difficulty’
Journal of Plastic, Reconstructive & Aesthetic Surgery (2010) 63, 1080e1086
Long term study into surgical re-exploration of the ‘free flap in difficulty’* R.I.S. Winterton a,b,*, R.M. Pinder a,b, A.N. Morritt b, S.L. Knight a,b, A.G. Batchelor b, M.I. Liddington a,b, S.P. Kay a,b a b
Leeds General Infirmary, Leeds Teaching Hospital NHS Trust, Great George Street, Leeds LS1 3EX, UK St James’s University Hospital, Leeds Teaching Hospitals NHS Trust, Beckett Street, Leeds LS9 7TF, UK
Received 13 November 2008; accepted 20 May 2009
KEYWORDS Free flap; Re-exploration; Re-intervention; Salvage; Microsurgery
Summary Background: Free tissue transfers must survive in order to achieve their surgical goals. There is little consensus about managing the ‘failing’ free flap, and practice is often guided by anecdote. Material and methods: We have prospectively collected data about all free flaps performed within our department between 1985 and 2008 (2569 flaps). We identified 327 flaps which were re-explored a total of 369 times. We analysed these flaps with regard to indication for re-exploration, operative findings and outcome. Results: Thirteen percent (327) of free flaps were re-explored. Of these, 291 (83%) had a successful outcome. Successful re-explorations took place at a mean 19 h post-op and unsuccessful re-explorations at a mean 56 h post-op. Clinical diagnosis prior to re-exploration was confirmed operatively in 91% of cases. Conclusion: We have considered the factors that allowed us to achieve the salvage rates described over a prolonged period, and identified two key areas. Firstly, we favour a model for free flap monitoring with clinical judgement at its core. Secondly, we feel the facility to recover patients post-operatively in a specialised, warmed environment, and return them to theatre quickly should the need arise, is essential. These two simple, yet institutionally determined factors are vital for maintaining excellent success rates. ª 2009 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved.
* Previously presented: This work was presented as an oral presentation at the BAPRAS Winter Meeting 2006 (The Royal College of Surgeons of England, London) and was awarded the 2006 York Medical Technologies/Heinz Waldrich Microsurgical Prize for best Oral Presentation Regarding Microsurgery. * Corresponding author. 43 Wike Ridge Avenue, Leeds LS17 9NL, UK. Tel.: þ44 7771 801 220. E-mail address: [email protected] (R.I.S. Winterton).
Since free tissue transfer was first described in animals in 1959,1 the technique has grown to be extremely powerful in the field of reconstructive surgery. Free tissue transfer allows selection of the most appropriate tissue for the purpose of reconstruction, thus facilitating high quality reconstruction whilst minimising donor morbidity.
1748-6815/$ - see front matter ª 2009 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.bjps.2009.05.029
Long term study into surgical re-exploration Free tissue transfer surgery has a specific set of complications related to anastomotic failure. Failure of the arterial anastomosis leads to ischaemia and flap necrosis. Failure of the venous anastomosis also results in necrosis, heralded by congestion and bleeding. When an anastomosis occludes, unless the problem is rectified, the flap will not survive. We have examined free flaps that have returned to theatre for surgical re-exploration during the post-operative period. We have examined the timing and outcomes of such procedures, and the accuracy of clinical diagnosis of why the flap is failing. Specifically we have posed, and answered, the following questions: 1. Can we predict which free flaps will require re-exploration? 2. Are we good at recognising, and responding to, the failing flap? 3. Can we predict which re-explorations will be successful?
Methods Data collection and analysis Details regarding microsurgical free tissue transfers have been collected in a Microsoft Accessª Database since the first free flap was performed in Leeds in 1985. Key information held on the database includes: patient demographics, pre-morbid health status, social habits, medications indication for free tissue transfer, anatomical region to be reconstructed operative date, grade of surgeon, total time anaesthetised flap type, recipient vessels, anastomosis type, warm ischaemia time use of vein graft, whether the microsurgery was uncomplicated whether the patient was anticoagulated postoperatively DT (core versus peripheral temperature), measures of patient haemodynamic status, diuretic/blood transfusion requirement whether the flap was re-explored surgically and details of any re-exploration the microsurgical outcome of the free tissue transfer Warm ischaemia time (WIT) is measured as the time from when the artery was clamped during flap harvest, to when flow in both vessels was re-established permanently. When a flap required re-exploration, the pre-operative clinical diagnosis and intra-operative findings of the cause of the compromise was recorded, along with the timing of the re-exploration. The database also records whether one or other of the anastomoses needed to be revised during the initial surgery. Statistical analysis was performed with the collaboration of the Clinical trials Research Unit at the University of Leeds. The statistical package that was used was SPSS v15.
1081 Statistical tests employed include the chi-square test, ANOVA and logistic regression analysis.
Clinical environment All cases were performed with a theatre team consisting of anaesthetist, scrub nurses, and operating department practitioners trained in microsurgical equipment and techniques. Under general anaesthesia invasive monitoring was placed (central venous and arterial lines) and regional anaesthesia was administered if applicable (brachial plexus or caudal blockade). Surgery was carried out in a warmed theatre (27 C) and additional direct warming measures used to maintain core body temperature at 38 C. The desired centraleperipheral temperature difference (6T) was <1 C during the procedure and subsequent high dependency unit care. Flaps were raised, inset and anastomosed by the same surgical team. Loupe magnification was employed for raising flaps, and microscope magnification (6e15) for anastomoses. Heparinised Hartman’s solution (5000 units heparin/500 mls Hartman’s) irrigation was used during microsurgery. Topical Verapamil Hydrochloride (0.125 mg/ml, SecuronIV, Abbott Laboratories Ltd.) and warm saline packs were applied following clamp release. Surgical drains were used routinely where appropriate, and the choice of type of drain left to the preference of the individual surgeon. Drains were not routinely used in paediatric cases. All patients were taken to the high dependency unit immediately post-operatively, and remained there routinely for 48 h under the care of experienced nursing staff. It is a tenet of our post-operative management that monitoring the patient is as, or more important than monitoring the flap, since an anastomosis that is patent at the end of the procedure will remain so unless there is a systemic or mechanical change in circumstances. Both invasive and noninvasive methods are used to monitor the haemodynamic and respiratory status of the patient (BP, pulse, CVP, urine output, DT, respiratory rate, O2 saturation and ABG). Pain score is recorded and effective analgesia administered. This allows us to avoid the pernicious vasospastic stimuli of pain, fear, cold and hypovolaemia, which is important as we believe that maintenance of a hyper-dynamic circulatory state is important for optimal flap perfusion in the post-operative period. The flap is also monitored, with parameters inspected and recorded every 15 min for 2 h, every 30 min for the next 4 h, and then every hour until 48 h have passed. Parameters were further recorded every 2 h for the next 48 h and every 4 h until discharge from hospital. The temperature, turgor, colour and capillary refill of the flap were monitored in every case and Doppler flow ultrasound and pin-prick testing used only if required. We do not routinely use any of the more complex flap monitoring techniques available. Buried flaps are monitored with Doppler ultrasound alone, and no skin paddles were left externalised unless indicated from a reconstruction perspective. Intra-oral flaps are monitored in the same way as other flaps, as permitted by the available access. When the patient was fit to return to the ward (after a minimum of 48 h) they were transferred to a warmed side room, and monitoring continued there. The more invasive
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devices were removed, but flap monitoring continued at time points according to the protocol.
Results Between 1985 and 2008, 2569 flaps have been performed in 2196 patients. 57% of patients were male and 43% female. The age of patients at the time of surgery ranges from three months to eighty-nine years (Figure 1) with a mean of 37.6 years. 64% of flaps were performed in non-smokers, 27% in smokers and 9% in ex-smokers. The indications for free flap reconstruction in this series were varied (Figure 2), and the flaps employed were as diverse as the indications (Table 1). Of the 2569 flaps undertaken, 327 were re-explored, 38 on two occasions and two were re-explored for a third time. This represents a re-exploration rate of 12.7%. The success rate in flaps that were not re-explored was 97.9% and in those that were re-explored was 82.5%. Overall success rate for all free tissue transfers performed by all surgeons was 95.3%. In 1.8% of flaps, the flap failed but was not explored in the early post-operative period. In over half of these cases, a difficult initial procedure lead to all reasonable options to salvage the flap being exhausted before recourse to a reexploration procedure. Other reasons for failure without re-exploration include occasions where the patients were not medically fit for a second operation, and in a small number of cases where failure occurred late (after discharge, of transfer to another ward) the flap was not felt to be salvageable and therefore simply debrided, rather than re-explored per se.
Pre-operative predictors of re-exploration Several factors thought to be pre-operative predictors of re-exploration proved, on statistical analysis, to have no predictive power. These factors include smoking status, type of flap, site of flap and indication for reconstruction. The only individual factor which was statistically significant in predicting risk of re-exploration was patient age at time of surgery (Figure 3). Mean age of those patients whose flaps were re-explored was 43.2 years and the mean age in those not re-explored was 36.8 years (P < 0.001). Flaps performed in children under 16 years had a re-exploration rate of 6.7% compared to 16.6% in those over 16 years of
Figure 1
Number of free flaps performed by age group.
Figure 2
Indication for free tissue transfer.
age (P < 0.001). Logistic regression analysis also shows that age has a significant effect on overall success rate of free tissue transfer (P < 0.05) with younger patients having a significantly higher success rate than older patients. We looked at whether muscle containing flaps were less likely to be salvaged than those not containing muscle, given that muscle is particularly sensitive to ischaemia. Though there is a suggestion of muscle containing flaps having a lower re-exploration success rate, this does not reach a statistically significant level (Table 2).
Intra-operative predictors of re-exploration When investigating intra-operative factors which may predict re-exploration, no individual factor reaches the level of statistical significance. This includes factors that Table 1
Number of flaps performed by name
Flap name
Number performed
2nd toe ALT DCIA DIEP Fibula Gracillis Groin Jejunum Lateral arm Latissimus dorsi Parascapular Pec minor RAFF Rectus abdominis Scapular Serratus anterior Testis Toe wrap TRAM VRAM Ulnar nerve Miscellaneous
300 31 30 42 42 136 192 110 252 498 12 35 194 163 33 14 16 35 317 20 21 76
Long term study into surgical re-exploration
Figure 3
1083
Risk of flap re-exploration by age group.
might suggest microsurgical difficulty such as gauge of suture used or whether an anastomosis had to be revised during the primary procedure. Warm ischaemia time (WIT) is the factor which most closely approaches statistical significance, with the mean WIT in flaps which were not re-explored being 71.4 min compared to 75.4 min in those that were re-explored (P < 0.036).
Re-exploration data The clinical diagnosis that lead to re-exploration, and the intra-operative findings were divided into ‘haematoma’, ‘arterial problem’, ‘venous problem’, or ‘miscellaneous other problem’. If haematoma was felt to be secondary to venous congestion then the indication was classified as ‘venous problem’. The relative frequency of each indication for re-exploration can be seen in Figure 4. The preoperative diagnosis was confirmed operatively in 91.3% of cases. Negative re-explorations took place in nine cases (2.8% of all re-explorations, or 0.4% of all flaps performed) where no problem was identified, and the flap went on to survive. Most re-explorations (82.4%) were performed during the first 24 h post-op. This is perhaps to be expected, as we know a large proportion of re-explorations are performed for haematoma, which is usually an early surgical complication. However this pattern is maintained when anastomotic problems are isolated, with 84.8% of those reexplorations also taking place during the first 24 h. 43% of all re-explorations took place within the first 6 h post-op and by the end of the 5th day, 96.9% of all re-explorations had taken place. The timing of flap re-exploration can be shown to be a significant predictor of re-exploration success. Successful re-explorations took place a mean 19.4 h post-op (SE 2.5 h) compared to the mean time at which an unsuccessful
Figure 4
Indications for re-exploration.
re-exploration took place, 56.1 h post-op (SE 10.5 h). This is highly significant (P < 0.001). Timing is also a predictor of re-exploration if anastomosis problems are looked at in isolation. The mean post-op time of successful re-exploration, in those flaps with arterial or venous problems, is 13.0 h (SE 20.7 h) compared to 42.7 h (SE 24.5 h) for unsuccessful re-explorations. Again this is highly statistically significant, P < 0.001. Indication for the re-exploration is also predictive of reexploration success (Figure 5). The group re-explored for haematoma do significantly better than all other groups either individually or together (P < 0.001 for each comparison). The success rate for flaps re-explored for haematoma is 97.8% compared to a success rate of 97.9% in flaps which were not re-explored at all. If logistic regression is applied to the data it can be shown that both timing and indication for re-exploration act as independent predictors of re-exploration, and do not confound one another (P < 0.001). Apart from the timing and indication for re-exploration, no other recorded factor can be used to predict the outcome of a particular re-exploration at a statistically significant level.
Anticoagulation Patients were routinely given DVT prophylaxis post-operatively, and protocols for this have changed over the years.
Table 2 Success rates of re-exploration of flaps containing muscle versus flaps containing no muscle Outcome
Flap containing muscle Flap containing no muscle
Success
Failure
79.4% 85.2%
20.6% 14.8%
Figure 5 Indication for re-exploration as a predictor of successful outcome.
1084 Our unit has no formalised policy with regard to postoperative administration of dextran/heparin/clexane/ prostacyclin/aspirin etc. The decision has always been left to the preference of the individual surgeon. The overall rate of use of an agent other than routine DVT prophylactic anticoagulation is 7.4%. In flaps not re-explored this is 7.1%, and is 9.1% in the group of flaps which were re-explored. This is not statistically significant. In this series thrombolytic agents have not been used as we feel that the risk profile is too great for the uncertain clinical benefits that may be achieved by utilising such agents in the presence of anastomotic problems discovered at re-exploration.2
Discussion Ours is the largest of several large series of free flaps presented in the literature.3e8 Studies in the past have evaluated flap selection,9,10 monitoring,11,12 salvage8,13 and outcome.13,14 The aims of this study were to evaluate whether any factors predict the need for salvage surgery, evaluate our protocols of post-operative monitoring and comment upon how we managed surgical re-exploration and whether any factors could be used to predict outcome of re-exploration. We present a heterogeneous group of patients having a wide range of free flaps over a prolonged period. Eleven surgeons have performed more than 10 free tissue transfers in our unit, and there is no significant difference in reexploration rates or overall success rates between surgeons (P < 0.01). This is despite the fact that the database includes some surgeons who have only performed their first few free tissue transfers, and some surgeons have performed many hundreds of free tissue transfers over 20 years. This supports our hypothesis that free tissue transfer outcome is strongly related to the microsurgical culture and facilities of an institution, and is contrary to the findings in other studies.15 Our overall success rate of 95.3% is consistent with other large series of free tissue transfers.4e6,8
Pre-operative predictors of re-exploration Our data show that when taken in isolation, only patient age is seen to be significantly different in flaps that are reexplored compared to those not re-explored. We saw that children under 16 years had a re-exploration rate of 6.7%, and adults over 16 years had a re-exploration rate of 16.6%. Although small vessel anastomoses can be technically demanding, vessels in children are very healthy, some aspects of children’s physiology resist vascular occlusion, and children are inherently resilient towards physiological insults. These important patient factors are responsible for the lower expectation of a requirement for surgical re-exploration.
Intra-operative predictors of re-exploration The intra-operative data revealed no factor was able to predict the need for surgical re-exploration. It was perhaps a little surprising that WIT and intra-operative revision of the anastomosis had no predictive power, but if we
R.I.S. Winterton et al. consider these measures of microsurgical difficulty, then the same phenomenon has been reported previously.16 However demanding the microsurgery should be, we would ordinarily expect the surgeon to obtain satisfactory flow at the conclusion of the operation, and it follows that if satisfactory flow is achieved some other, independent problem must arise to compromise the flap. It would therefore be straightforward to conclude that more demanding microsurgery does not result in a higher re-exploration rate, but of course it is not quite so simple. The most technically challenging cases are unlikely to be undertaken by the least experienced surgeons, and therefore within an effective unit, complexity of case is a variable that is controlled, and we suspect this is why measures of microsurgical complexity do not predict the need for reexploration, and also why there is no statistical difference in re-exploration rates between experienced and inexperienced surgeons.
Re-exploration data Free flaps are usually monitored closely in the early postoperative period, but there is no generally accepted protocol for such monitoring.17,18 Conventional techniques include clinical observation, Doppler ultrasound, and temperature measurement.19e21 A myriad of sophisticated techniques are also available to the microsurgeon to assist in flap monitoring, including laser Doppler flow monitoring,22 tissue oxygen tension measurement,23 infra-red spectroscopy,24 microdialysis,25,26 nuclear isotope monitoring,27 implantable Doppler flow measurement12,28 and photoplethysmography.29 However, invasive monitoring techniques add to the cost of surgery and may cause further patient distress.30 We favour a clinical model of flap monitoring with simple technological adjuncts, relying on experienced individuals monitoring regularly for subtle changes. This series demonstrates that excellent success rates can be achieved both overall and within the subgroup of re-explored free flaps using such a protocol, echoing the findings of an earlier study.31 Our clinical diagnosis of the failing free flap, and underlying cause, is also good, with the correct diagnosis being made pre-operatively in over 90% of re-explorations. The development that is likely to be most widely used over the coming years is the implantable Doppler probe.12 With free tissue transfer becoming more common practice in the functional setting, buried free flaps are increasingly used. This is a specific example of where the patient can be effectively monitored, but the flap cannot.11 In this environment a device to confirm the presence of blood flow may prove to be a useful adjunct along with skin32 or other33 islands which are externalised to allow monitoring.34
Timing of re-exploration We have observed that most flaps are re-explored during the first 24 h post-op. This peak in re-explorations during the first 24 h has also been reported elsewhere.6,8,35e38 As the first 24 h is most critical for diagnosing a compromised flap, it follows that flap monitoring should be at its most frequent during this time. Looking more closely, the first 6 h
Long term study into surgical re-exploration post-op encompasses the most re-explorations. These observations support our flap monitoring protocol where monitoring is most frequent during the first 6 h and continues with at least hourly observations until 48 h have passed. Another way of looking at these data is to see that successful re-explorations take place much earlier in the post-operative time course than unsuccessful re-explorations. It is important to note that this finding persists even when haematoma (as the indication for re-exploration) is removed from the data. Indeed when anastomotic problems (as the indication for re-exploration) are looked at in isolation, the difference between timing of successful (13.0 h, SE 20.7) and unsuccessful (42.7 h, SE 24.5) re-explorations is stark. There may be more than one explanation for this phenomenon.39 During the first 48 h post-op, the flap and patient are monitored very closely in an HDU setting. Any changes in either the flap or patient will therefore be recognised quickly, so minimising flap ischaemia time if re-exploration is required. Also, if anastomotic thrombus is detected early, it has less time to develop and propagate, and reexploration has a greater chance of clearing thrombus from the flap. Both of these factors influence flap survival.35,40 As a consequence of these observations we advocate surgical exploration as soon as a problem is suspected, rather than known. An aggressive (early and with a low threshold) re-exploration policy is accepted as being vital for a high overall success rate.19,20,41 Although negative reexplorations may be deemed inappropriate, we take the view that a small number (0.4% of all flaps performed) is acceptable if overall re-exploration success rates are high, since many flaps will not be salvaged if re-exploration is delayed until the indication is absolute. Focussing on the fact that the timing of re-exploration is so important,8 we considered the factors that have allowed us to achieve excellent salvage rates over a prolonged period. Firstly, the fact that for a long time our HDU was located very close to, and on the same floor as the operating theatres allowed patients to be returned to theatre for re-exploration very quickly. A recent large study showed a median time of 5 h between diagnosing a problem and returning the patient to theatre 7 which we were fortunate to circumvent given how important timely re-exploration has been shown to be in this and other studies.42 Secondly, the fact that we have 24-h access to a specialised microsurgical theatre team means the experienced practitioners can be called upon for any microsurgical intervention at any time. These observations lend weight to our proposal that free tissue transfer success rates are related to institutional organisation as much as individual surgical competency.
Summary Our data shows that excellent success rates for free tissue transfer can be achieved over a long period using a model of flap monitoring with experienced human judgement at its core. Where there is doubt regarding the condition of a flap, we advocate urgent assertive surgical intervention. This is the variable that the surgeon can control, and is the factor shown to have the biggest impact on outcome.
1085 When a flap is explored for haematoma, success rate should be the same as flaps which are not re-explored at all. When the reason for exploration is anastomotic failure, then four out of five flaps can reasonably be salvaged. The failing free flap need not fail if intervention is timely and well judged. An experienced and organised surgical unit is vital for outcomes to be maintained across a department.
Acknowledgements We would like to thank Phil McShane for his great help and patience in the preparation of the statistics for this paper.
Conflict of interest None.
Funding None.
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1086 13. Yajima H, Tamai S, Mizumoto S, et al. Vascular complications of vascularized composite tissue transfer: outcome and salvage techniques. Microsurgery 1993;14:473e8. 14. Wei FC, Demirkan F, Chen HC, et al. The outcome of failed free flaps in head and neck and extremity reconstruction: what is next in the reconstructive ladder? Plast Reconstr Surg 2001; 108:1154e60 [discussion 61e2]. 15. Chaivanichsiri P. Influence of recipient vessels on free tissue transplantation of the extremities. Plast Reconstr Surg 1999; 104:970e5. 16. Shaw WW, Ko CY, Ahn CY, et al. Safe ischemia time in free-flap surgery: a clinical study of contact-surface cooling. J Reconstr Microsurg 1996;12:421e4. 17. Jallali N, Ridha H, Butler PE. Postoperative monitoring of free flaps in UK plastic surgery units. Microsurgery 2005;25:469e72. 18. Whitaker IS, Gulati V, Ross GL, et al. Variations in the postoperative management of free tissue transfers to the head and neck in the United Kingdom. Br J Oral Maxillofac Surg 2007;45:16e8. 19. Kay S, Coady M. The role of microsurgery and free tissue transfer in the reconstruction of the paediatric upper extremity. Ann Acad Med Singap 1995;24:113e23. 20. Kay SP, Wiberg M. Toe to hand transfer in children. Part 1: technical aspects. J Hand Surg [Br] 1996;21:723e34. 21. Serletti JM, Schingo Jr VA, Deuber MA, et al. Free tissue transfer in pediatric patients. Ann Plast Surg 1996;36:561e8. 22. Heller L, Levin LS, Klitzman B. Laser Doppler flowmeter monitoring of free-tissue transfers: blood flow in normal and complicated cases. Plast Reconstr Surg 2001;107:1739e45. 23. Hirigoyen MB, Blackwell KE, Zhang WX, et al. Continuous tissue oxygen tension measurement as a monitor of free-flap viability. Plast Reconstr Surg 1997;99:763e73. 24. Irwin MS, Thorniley MS, Dore CJ, et al. Near infra-red spectroscopy: a non-invasive monitor of perfusion and oxygenation within the microcirculation of limbs and flaps. Br J Plast Surg 1995;48:14e22. 25. Udesen A, Lontoft E, Kristensen SR. Monitoring of free TRAM flaps with microdialysis. J Reconstr Microsurg 2000;16:101e6. 26. Jyranki J, Suominen S, Vuola J, et al. Microdialysis in clinical practice: monitoring intraoral free flaps. Ann Plast Surg 2006; 56:387e93. 27. Top H, Sarikaya A, Aygit AC, et al. Review of monitoring free muscle flap transfers in reconstructive surgery: role of 99mTc sestamibi scintigraphy. Nucl Med Commun 2006;27:91e8.
R.I.S. Winterton et al. 28. Pryor SG, Moore EJ, Kasperbauer JL. Implantable Doppler flow system: experience with 24 microvascular free-flap operations. Otolaryngol Head Neck Surg 2006;135:714e8. 29. Futran ND, Stack Jr BC, Hollenbeak C, et al. Green light photoplethysmography monitoring of free flaps. Arch Otolaryngol Head Neck Surg 2000;126:659e62. 30. Wilson R, Yates A. Paediatric microvascular surgery: anaesthetic experience of 27 toe to hand transfers. Paediatr Anaesth 1993;3:209e15. 31. Jones I, Kelly M, Percival N. Clinical monitoring of free flaps in the UK. Br J Plast Surg 1999;52:78e9. 32. Pellini R, Pichi B, Ruggieri M, et al. Venous flow-through flap as an external monitor for buried radial forearm free flap in head and neck reconstruction. J Plast Reconstr Aesthet Surg 2006; 59:1217e21. 33. Yang JC, Kuo YR, Hsieh CH, et al. The use of radial vessel stump in free radial forearm flap as flap monitor in head and neck reconstruction. Ann Plast Surg 2007;59:378e81. 34. Yuen JC. Techniques of external monitoring of buried free flaps. Ann Plast Surg 2005;55:460e5. 35. Brown JS, Devine JC, Magennis P, et al. Factors that influence the outcome of salvage in free tissue transfer. Br J Oral Maxillofac Surg 2003;41:16e20. 36. Devine JC, Potter LA, Magennis P, et al. Flap monitoring after head and neck reconstruction: evaluating an observation protocol. J Wound Care 2001;10:525e9. 37. Hui KC, Zhang F, Shaw WW, et al. Assessment of the patency of microvascular venous anastomosis. J Reconstr Microsurg 2002; 18:111e4. 38. Zeebregts C, Acosta R, Bolander L, et al. Clinical experience with non-penetrating vascular clips in free-flap reconstructions. Br J Plast Surg 2002;55:105e10. 39. Salgado CJ, Smith A, Kim S, et al. Effects of late loss of arterial inflow on free flap survival. J Reconstr Microsurg 2002;18: 579e84. 40. Kerrigan CL, Wizman P, Hjortdal VE, et al. Global flap ischemia: a comparison of arterial versus venous etiology. Plast Reconstr Surg 1994;93:1485e95 [discussion 96e7]. 41. Devaraj VS, Kay SP, Batchelor AG, et al. Microvascular surgery in children. Br J Plast Surg 1991;44:276e80. 42. Hidalgo DA, Jones CS. The role of emergent exploration in freetissue transfer: a review of 150 consecutive cases. Plast Reconstr Surg 1990;86:492e8 [discussion 99e501].
Long term study into surgical re-exploration of the ‘free flap in difficulty’* R.I.S. Winterton a,b,*, R.M. Pinder a,b, A.N. Morritt b, S.L. Knight a,b, A.G. Batchelor b, M.I. Liddington a,b, S.P. Kay a,b a b
Leeds General Infirmary, Leeds Teaching Hospital NHS Trust, Great George Street, Leeds LS1 3EX, UK St James’s University Hospital, Leeds Teaching Hospitals NHS Trust, Beckett Street, Leeds LS9 7TF, UK
Received 13 November 2008; accepted 20 May 2009
KEYWORDS Free flap; Re-exploration; Re-intervention; Salvage; Microsurgery
Summary Background: Free tissue transfers must survive in order to achieve their surgical goals. There is little consensus about managing the ‘failing’ free flap, and practice is often guided by anecdote. Material and methods: We have prospectively collected data about all free flaps performed within our department between 1985 and 2008 (2569 flaps). We identified 327 flaps which were re-explored a total of 369 times. We analysed these flaps with regard to indication for re-exploration, operative findings and outcome. Results: Thirteen percent (327) of free flaps were re-explored. Of these, 291 (83%) had a successful outcome. Successful re-explorations took place at a mean 19 h post-op and unsuccessful re-explorations at a mean 56 h post-op. Clinical diagnosis prior to re-exploration was confirmed operatively in 91% of cases. Conclusion: We have considered the factors that allowed us to achieve the salvage rates described over a prolonged period, and identified two key areas. Firstly, we favour a model for free flap monitoring with clinical judgement at its core. Secondly, we feel the facility to recover patients post-operatively in a specialised, warmed environment, and return them to theatre quickly should the need arise, is essential. These two simple, yet institutionally determined factors are vital for maintaining excellent success rates. ª 2009 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved.
* Previously presented: This work was presented as an oral presentation at the BAPRAS Winter Meeting 2006 (The Royal College of Surgeons of England, London) and was awarded the 2006 York Medical Technologies/Heinz Waldrich Microsurgical Prize for best Oral Presentation Regarding Microsurgery. * Corresponding author. 43 Wike Ridge Avenue, Leeds LS17 9NL, UK. Tel.: þ44 7771 801 220. E-mail address: [email protected] (R.I.S. Winterton).
Since free tissue transfer was first described in animals in 1959,1 the technique has grown to be extremely powerful in the field of reconstructive surgery. Free tissue transfer allows selection of the most appropriate tissue for the purpose of reconstruction, thus facilitating high quality reconstruction whilst minimising donor morbidity.
1748-6815/$ - see front matter ª 2009 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.bjps.2009.05.029
Long term study into surgical re-exploration Free tissue transfer surgery has a specific set of complications related to anastomotic failure. Failure of the arterial anastomosis leads to ischaemia and flap necrosis. Failure of the venous anastomosis also results in necrosis, heralded by congestion and bleeding. When an anastomosis occludes, unless the problem is rectified, the flap will not survive. We have examined free flaps that have returned to theatre for surgical re-exploration during the post-operative period. We have examined the timing and outcomes of such procedures, and the accuracy of clinical diagnosis of why the flap is failing. Specifically we have posed, and answered, the following questions: 1. Can we predict which free flaps will require re-exploration? 2. Are we good at recognising, and responding to, the failing flap? 3. Can we predict which re-explorations will be successful?
Methods Data collection and analysis Details regarding microsurgical free tissue transfers have been collected in a Microsoft Accessª Database since the first free flap was performed in Leeds in 1985. Key information held on the database includes: patient demographics, pre-morbid health status, social habits, medications indication for free tissue transfer, anatomical region to be reconstructed operative date, grade of surgeon, total time anaesthetised flap type, recipient vessels, anastomosis type, warm ischaemia time use of vein graft, whether the microsurgery was uncomplicated whether the patient was anticoagulated postoperatively DT (core versus peripheral temperature), measures of patient haemodynamic status, diuretic/blood transfusion requirement whether the flap was re-explored surgically and details of any re-exploration the microsurgical outcome of the free tissue transfer Warm ischaemia time (WIT) is measured as the time from when the artery was clamped during flap harvest, to when flow in both vessels was re-established permanently. When a flap required re-exploration, the pre-operative clinical diagnosis and intra-operative findings of the cause of the compromise was recorded, along with the timing of the re-exploration. The database also records whether one or other of the anastomoses needed to be revised during the initial surgery. Statistical analysis was performed with the collaboration of the Clinical trials Research Unit at the University of Leeds. The statistical package that was used was SPSS v15.
1081 Statistical tests employed include the chi-square test, ANOVA and logistic regression analysis.
Clinical environment All cases were performed with a theatre team consisting of anaesthetist, scrub nurses, and operating department practitioners trained in microsurgical equipment and techniques. Under general anaesthesia invasive monitoring was placed (central venous and arterial lines) and regional anaesthesia was administered if applicable (brachial plexus or caudal blockade). Surgery was carried out in a warmed theatre (27 C) and additional direct warming measures used to maintain core body temperature at 38 C. The desired centraleperipheral temperature difference (6T) was <1 C during the procedure and subsequent high dependency unit care. Flaps were raised, inset and anastomosed by the same surgical team. Loupe magnification was employed for raising flaps, and microscope magnification (6e15) for anastomoses. Heparinised Hartman’s solution (5000 units heparin/500 mls Hartman’s) irrigation was used during microsurgery. Topical Verapamil Hydrochloride (0.125 mg/ml, SecuronIV, Abbott Laboratories Ltd.) and warm saline packs were applied following clamp release. Surgical drains were used routinely where appropriate, and the choice of type of drain left to the preference of the individual surgeon. Drains were not routinely used in paediatric cases. All patients were taken to the high dependency unit immediately post-operatively, and remained there routinely for 48 h under the care of experienced nursing staff. It is a tenet of our post-operative management that monitoring the patient is as, or more important than monitoring the flap, since an anastomosis that is patent at the end of the procedure will remain so unless there is a systemic or mechanical change in circumstances. Both invasive and noninvasive methods are used to monitor the haemodynamic and respiratory status of the patient (BP, pulse, CVP, urine output, DT, respiratory rate, O2 saturation and ABG). Pain score is recorded and effective analgesia administered. This allows us to avoid the pernicious vasospastic stimuli of pain, fear, cold and hypovolaemia, which is important as we believe that maintenance of a hyper-dynamic circulatory state is important for optimal flap perfusion in the post-operative period. The flap is also monitored, with parameters inspected and recorded every 15 min for 2 h, every 30 min for the next 4 h, and then every hour until 48 h have passed. Parameters were further recorded every 2 h for the next 48 h and every 4 h until discharge from hospital. The temperature, turgor, colour and capillary refill of the flap were monitored in every case and Doppler flow ultrasound and pin-prick testing used only if required. We do not routinely use any of the more complex flap monitoring techniques available. Buried flaps are monitored with Doppler ultrasound alone, and no skin paddles were left externalised unless indicated from a reconstruction perspective. Intra-oral flaps are monitored in the same way as other flaps, as permitted by the available access. When the patient was fit to return to the ward (after a minimum of 48 h) they were transferred to a warmed side room, and monitoring continued there. The more invasive
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devices were removed, but flap monitoring continued at time points according to the protocol.
Results Between 1985 and 2008, 2569 flaps have been performed in 2196 patients. 57% of patients were male and 43% female. The age of patients at the time of surgery ranges from three months to eighty-nine years (Figure 1) with a mean of 37.6 years. 64% of flaps were performed in non-smokers, 27% in smokers and 9% in ex-smokers. The indications for free flap reconstruction in this series were varied (Figure 2), and the flaps employed were as diverse as the indications (Table 1). Of the 2569 flaps undertaken, 327 were re-explored, 38 on two occasions and two were re-explored for a third time. This represents a re-exploration rate of 12.7%. The success rate in flaps that were not re-explored was 97.9% and in those that were re-explored was 82.5%. Overall success rate for all free tissue transfers performed by all surgeons was 95.3%. In 1.8% of flaps, the flap failed but was not explored in the early post-operative period. In over half of these cases, a difficult initial procedure lead to all reasonable options to salvage the flap being exhausted before recourse to a reexploration procedure. Other reasons for failure without re-exploration include occasions where the patients were not medically fit for a second operation, and in a small number of cases where failure occurred late (after discharge, of transfer to another ward) the flap was not felt to be salvageable and therefore simply debrided, rather than re-explored per se.
Pre-operative predictors of re-exploration Several factors thought to be pre-operative predictors of re-exploration proved, on statistical analysis, to have no predictive power. These factors include smoking status, type of flap, site of flap and indication for reconstruction. The only individual factor which was statistically significant in predicting risk of re-exploration was patient age at time of surgery (Figure 3). Mean age of those patients whose flaps were re-explored was 43.2 years and the mean age in those not re-explored was 36.8 years (P < 0.001). Flaps performed in children under 16 years had a re-exploration rate of 6.7% compared to 16.6% in those over 16 years of
Figure 1
Number of free flaps performed by age group.
Figure 2
Indication for free tissue transfer.
age (P < 0.001). Logistic regression analysis also shows that age has a significant effect on overall success rate of free tissue transfer (P < 0.05) with younger patients having a significantly higher success rate than older patients. We looked at whether muscle containing flaps were less likely to be salvaged than those not containing muscle, given that muscle is particularly sensitive to ischaemia. Though there is a suggestion of muscle containing flaps having a lower re-exploration success rate, this does not reach a statistically significant level (Table 2).
Intra-operative predictors of re-exploration When investigating intra-operative factors which may predict re-exploration, no individual factor reaches the level of statistical significance. This includes factors that Table 1
Number of flaps performed by name
Flap name
Number performed
2nd toe ALT DCIA DIEP Fibula Gracillis Groin Jejunum Lateral arm Latissimus dorsi Parascapular Pec minor RAFF Rectus abdominis Scapular Serratus anterior Testis Toe wrap TRAM VRAM Ulnar nerve Miscellaneous
300 31 30 42 42 136 192 110 252 498 12 35 194 163 33 14 16 35 317 20 21 76
Long term study into surgical re-exploration
Figure 3
1083
Risk of flap re-exploration by age group.
might suggest microsurgical difficulty such as gauge of suture used or whether an anastomosis had to be revised during the primary procedure. Warm ischaemia time (WIT) is the factor which most closely approaches statistical significance, with the mean WIT in flaps which were not re-explored being 71.4 min compared to 75.4 min in those that were re-explored (P < 0.036).
Re-exploration data The clinical diagnosis that lead to re-exploration, and the intra-operative findings were divided into ‘haematoma’, ‘arterial problem’, ‘venous problem’, or ‘miscellaneous other problem’. If haematoma was felt to be secondary to venous congestion then the indication was classified as ‘venous problem’. The relative frequency of each indication for re-exploration can be seen in Figure 4. The preoperative diagnosis was confirmed operatively in 91.3% of cases. Negative re-explorations took place in nine cases (2.8% of all re-explorations, or 0.4% of all flaps performed) where no problem was identified, and the flap went on to survive. Most re-explorations (82.4%) were performed during the first 24 h post-op. This is perhaps to be expected, as we know a large proportion of re-explorations are performed for haematoma, which is usually an early surgical complication. However this pattern is maintained when anastomotic problems are isolated, with 84.8% of those reexplorations also taking place during the first 24 h. 43% of all re-explorations took place within the first 6 h post-op and by the end of the 5th day, 96.9% of all re-explorations had taken place. The timing of flap re-exploration can be shown to be a significant predictor of re-exploration success. Successful re-explorations took place a mean 19.4 h post-op (SE 2.5 h) compared to the mean time at which an unsuccessful
Figure 4
Indications for re-exploration.
re-exploration took place, 56.1 h post-op (SE 10.5 h). This is highly significant (P < 0.001). Timing is also a predictor of re-exploration if anastomosis problems are looked at in isolation. The mean post-op time of successful re-exploration, in those flaps with arterial or venous problems, is 13.0 h (SE 20.7 h) compared to 42.7 h (SE 24.5 h) for unsuccessful re-explorations. Again this is highly statistically significant, P < 0.001. Indication for the re-exploration is also predictive of reexploration success (Figure 5). The group re-explored for haematoma do significantly better than all other groups either individually or together (P < 0.001 for each comparison). The success rate for flaps re-explored for haematoma is 97.8% compared to a success rate of 97.9% in flaps which were not re-explored at all. If logistic regression is applied to the data it can be shown that both timing and indication for re-exploration act as independent predictors of re-exploration, and do not confound one another (P < 0.001). Apart from the timing and indication for re-exploration, no other recorded factor can be used to predict the outcome of a particular re-exploration at a statistically significant level.
Anticoagulation Patients were routinely given DVT prophylaxis post-operatively, and protocols for this have changed over the years.
Table 2 Success rates of re-exploration of flaps containing muscle versus flaps containing no muscle Outcome
Flap containing muscle Flap containing no muscle
Success
Failure
79.4% 85.2%
20.6% 14.8%
Figure 5 Indication for re-exploration as a predictor of successful outcome.
1084 Our unit has no formalised policy with regard to postoperative administration of dextran/heparin/clexane/ prostacyclin/aspirin etc. The decision has always been left to the preference of the individual surgeon. The overall rate of use of an agent other than routine DVT prophylactic anticoagulation is 7.4%. In flaps not re-explored this is 7.1%, and is 9.1% in the group of flaps which were re-explored. This is not statistically significant. In this series thrombolytic agents have not been used as we feel that the risk profile is too great for the uncertain clinical benefits that may be achieved by utilising such agents in the presence of anastomotic problems discovered at re-exploration.2
Discussion Ours is the largest of several large series of free flaps presented in the literature.3e8 Studies in the past have evaluated flap selection,9,10 monitoring,11,12 salvage8,13 and outcome.13,14 The aims of this study were to evaluate whether any factors predict the need for salvage surgery, evaluate our protocols of post-operative monitoring and comment upon how we managed surgical re-exploration and whether any factors could be used to predict outcome of re-exploration. We present a heterogeneous group of patients having a wide range of free flaps over a prolonged period. Eleven surgeons have performed more than 10 free tissue transfers in our unit, and there is no significant difference in reexploration rates or overall success rates between surgeons (P < 0.01). This is despite the fact that the database includes some surgeons who have only performed their first few free tissue transfers, and some surgeons have performed many hundreds of free tissue transfers over 20 years. This supports our hypothesis that free tissue transfer outcome is strongly related to the microsurgical culture and facilities of an institution, and is contrary to the findings in other studies.15 Our overall success rate of 95.3% is consistent with other large series of free tissue transfers.4e6,8
Pre-operative predictors of re-exploration Our data show that when taken in isolation, only patient age is seen to be significantly different in flaps that are reexplored compared to those not re-explored. We saw that children under 16 years had a re-exploration rate of 6.7%, and adults over 16 years had a re-exploration rate of 16.6%. Although small vessel anastomoses can be technically demanding, vessels in children are very healthy, some aspects of children’s physiology resist vascular occlusion, and children are inherently resilient towards physiological insults. These important patient factors are responsible for the lower expectation of a requirement for surgical re-exploration.
Intra-operative predictors of re-exploration The intra-operative data revealed no factor was able to predict the need for surgical re-exploration. It was perhaps a little surprising that WIT and intra-operative revision of the anastomosis had no predictive power, but if we
R.I.S. Winterton et al. consider these measures of microsurgical difficulty, then the same phenomenon has been reported previously.16 However demanding the microsurgery should be, we would ordinarily expect the surgeon to obtain satisfactory flow at the conclusion of the operation, and it follows that if satisfactory flow is achieved some other, independent problem must arise to compromise the flap. It would therefore be straightforward to conclude that more demanding microsurgery does not result in a higher re-exploration rate, but of course it is not quite so simple. The most technically challenging cases are unlikely to be undertaken by the least experienced surgeons, and therefore within an effective unit, complexity of case is a variable that is controlled, and we suspect this is why measures of microsurgical complexity do not predict the need for reexploration, and also why there is no statistical difference in re-exploration rates between experienced and inexperienced surgeons.
Re-exploration data Free flaps are usually monitored closely in the early postoperative period, but there is no generally accepted protocol for such monitoring.17,18 Conventional techniques include clinical observation, Doppler ultrasound, and temperature measurement.19e21 A myriad of sophisticated techniques are also available to the microsurgeon to assist in flap monitoring, including laser Doppler flow monitoring,22 tissue oxygen tension measurement,23 infra-red spectroscopy,24 microdialysis,25,26 nuclear isotope monitoring,27 implantable Doppler flow measurement12,28 and photoplethysmography.29 However, invasive monitoring techniques add to the cost of surgery and may cause further patient distress.30 We favour a clinical model of flap monitoring with simple technological adjuncts, relying on experienced individuals monitoring regularly for subtle changes. This series demonstrates that excellent success rates can be achieved both overall and within the subgroup of re-explored free flaps using such a protocol, echoing the findings of an earlier study.31 Our clinical diagnosis of the failing free flap, and underlying cause, is also good, with the correct diagnosis being made pre-operatively in over 90% of re-explorations. The development that is likely to be most widely used over the coming years is the implantable Doppler probe.12 With free tissue transfer becoming more common practice in the functional setting, buried free flaps are increasingly used. This is a specific example of where the patient can be effectively monitored, but the flap cannot.11 In this environment a device to confirm the presence of blood flow may prove to be a useful adjunct along with skin32 or other33 islands which are externalised to allow monitoring.34
Timing of re-exploration We have observed that most flaps are re-explored during the first 24 h post-op. This peak in re-explorations during the first 24 h has also been reported elsewhere.6,8,35e38 As the first 24 h is most critical for diagnosing a compromised flap, it follows that flap monitoring should be at its most frequent during this time. Looking more closely, the first 6 h
Long term study into surgical re-exploration post-op encompasses the most re-explorations. These observations support our flap monitoring protocol where monitoring is most frequent during the first 6 h and continues with at least hourly observations until 48 h have passed. Another way of looking at these data is to see that successful re-explorations take place much earlier in the post-operative time course than unsuccessful re-explorations. It is important to note that this finding persists even when haematoma (as the indication for re-exploration) is removed from the data. Indeed when anastomotic problems (as the indication for re-exploration) are looked at in isolation, the difference between timing of successful (13.0 h, SE 20.7) and unsuccessful (42.7 h, SE 24.5) re-explorations is stark. There may be more than one explanation for this phenomenon.39 During the first 48 h post-op, the flap and patient are monitored very closely in an HDU setting. Any changes in either the flap or patient will therefore be recognised quickly, so minimising flap ischaemia time if re-exploration is required. Also, if anastomotic thrombus is detected early, it has less time to develop and propagate, and reexploration has a greater chance of clearing thrombus from the flap. Both of these factors influence flap survival.35,40 As a consequence of these observations we advocate surgical exploration as soon as a problem is suspected, rather than known. An aggressive (early and with a low threshold) re-exploration policy is accepted as being vital for a high overall success rate.19,20,41 Although negative reexplorations may be deemed inappropriate, we take the view that a small number (0.4% of all flaps performed) is acceptable if overall re-exploration success rates are high, since many flaps will not be salvaged if re-exploration is delayed until the indication is absolute. Focussing on the fact that the timing of re-exploration is so important,8 we considered the factors that have allowed us to achieve excellent salvage rates over a prolonged period. Firstly, the fact that for a long time our HDU was located very close to, and on the same floor as the operating theatres allowed patients to be returned to theatre for re-exploration very quickly. A recent large study showed a median time of 5 h between diagnosing a problem and returning the patient to theatre 7 which we were fortunate to circumvent given how important timely re-exploration has been shown to be in this and other studies.42 Secondly, the fact that we have 24-h access to a specialised microsurgical theatre team means the experienced practitioners can be called upon for any microsurgical intervention at any time. These observations lend weight to our proposal that free tissue transfer success rates are related to institutional organisation as much as individual surgical competency.
Summary Our data shows that excellent success rates for free tissue transfer can be achieved over a long period using a model of flap monitoring with experienced human judgement at its core. Where there is doubt regarding the condition of a flap, we advocate urgent assertive surgical intervention. This is the variable that the surgeon can control, and is the factor shown to have the biggest impact on outcome.
1085 When a flap is explored for haematoma, success rate should be the same as flaps which are not re-explored at all. When the reason for exploration is anastomotic failure, then four out of five flaps can reasonably be salvaged. The failing free flap need not fail if intervention is timely and well judged. An experienced and organised surgical unit is vital for outcomes to be maintained across a department.
Acknowledgements We would like to thank Phil McShane for his great help and patience in the preparation of the statistics for this paper.
Conflict of interest None.
Funding None.
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1086 13. Yajima H, Tamai S, Mizumoto S, et al. Vascular complications of vascularized composite tissue transfer: outcome and salvage techniques. Microsurgery 1993;14:473e8. 14. Wei FC, Demirkan F, Chen HC, et al. The outcome of failed free flaps in head and neck and extremity reconstruction: what is next in the reconstructive ladder? Plast Reconstr Surg 2001; 108:1154e60 [discussion 61e2]. 15. Chaivanichsiri P. Influence of recipient vessels on free tissue transplantation of the extremities. Plast Reconstr Surg 1999; 104:970e5. 16. Shaw WW, Ko CY, Ahn CY, et al. Safe ischemia time in free-flap surgery: a clinical study of contact-surface cooling. J Reconstr Microsurg 1996;12:421e4. 17. Jallali N, Ridha H, Butler PE. Postoperative monitoring of free flaps in UK plastic surgery units. Microsurgery 2005;25:469e72. 18. Whitaker IS, Gulati V, Ross GL, et al. Variations in the postoperative management of free tissue transfers to the head and neck in the United Kingdom. Br J Oral Maxillofac Surg 2007;45:16e8. 19. Kay S, Coady M. The role of microsurgery and free tissue transfer in the reconstruction of the paediatric upper extremity. Ann Acad Med Singap 1995;24:113e23. 20. Kay SP, Wiberg M. Toe to hand transfer in children. Part 1: technical aspects. J Hand Surg [Br] 1996;21:723e34. 21. Serletti JM, Schingo Jr VA, Deuber MA, et al. Free tissue transfer in pediatric patients. Ann Plast Surg 1996;36:561e8. 22. Heller L, Levin LS, Klitzman B. Laser Doppler flowmeter monitoring of free-tissue transfers: blood flow in normal and complicated cases. Plast Reconstr Surg 2001;107:1739e45. 23. Hirigoyen MB, Blackwell KE, Zhang WX, et al. Continuous tissue oxygen tension measurement as a monitor of free-flap viability. Plast Reconstr Surg 1997;99:763e73. 24. Irwin MS, Thorniley MS, Dore CJ, et al. Near infra-red spectroscopy: a non-invasive monitor of perfusion and oxygenation within the microcirculation of limbs and flaps. Br J Plast Surg 1995;48:14e22. 25. Udesen A, Lontoft E, Kristensen SR. Monitoring of free TRAM flaps with microdialysis. J Reconstr Microsurg 2000;16:101e6. 26. Jyranki J, Suominen S, Vuola J, et al. Microdialysis in clinical practice: monitoring intraoral free flaps. Ann Plast Surg 2006; 56:387e93. 27. Top H, Sarikaya A, Aygit AC, et al. Review of monitoring free muscle flap transfers in reconstructive surgery: role of 99mTc sestamibi scintigraphy. Nucl Med Commun 2006;27:91e8.
R.I.S. Winterton et al. 28. Pryor SG, Moore EJ, Kasperbauer JL. Implantable Doppler flow system: experience with 24 microvascular free-flap operations. Otolaryngol Head Neck Surg 2006;135:714e8. 29. Futran ND, Stack Jr BC, Hollenbeak C, et al. Green light photoplethysmography monitoring of free flaps. Arch Otolaryngol Head Neck Surg 2000;126:659e62. 30. Wilson R, Yates A. Paediatric microvascular surgery: anaesthetic experience of 27 toe to hand transfers. Paediatr Anaesth 1993;3:209e15. 31. Jones I, Kelly M, Percival N. Clinical monitoring of free flaps in the UK. Br J Plast Surg 1999;52:78e9. 32. Pellini R, Pichi B, Ruggieri M, et al. Venous flow-through flap as an external monitor for buried radial forearm free flap in head and neck reconstruction. J Plast Reconstr Aesthet Surg 2006; 59:1217e21. 33. Yang JC, Kuo YR, Hsieh CH, et al. The use of radial vessel stump in free radial forearm flap as flap monitor in head and neck reconstruction. Ann Plast Surg 2007;59:378e81. 34. Yuen JC. Techniques of external monitoring of buried free flaps. Ann Plast Surg 2005;55:460e5. 35. Brown JS, Devine JC, Magennis P, et al. Factors that influence the outcome of salvage in free tissue transfer. Br J Oral Maxillofac Surg 2003;41:16e20. 36. Devine JC, Potter LA, Magennis P, et al. Flap monitoring after head and neck reconstruction: evaluating an observation protocol. J Wound Care 2001;10:525e9. 37. Hui KC, Zhang F, Shaw WW, et al. Assessment of the patency of microvascular venous anastomosis. J Reconstr Microsurg 2002; 18:111e4. 38. Zeebregts C, Acosta R, Bolander L, et al. Clinical experience with non-penetrating vascular clips in free-flap reconstructions. Br J Plast Surg 2002;55:105e10. 39. Salgado CJ, Smith A, Kim S, et al. Effects of late loss of arterial inflow on free flap survival. J Reconstr Microsurg 2002;18: 579e84. 40. Kerrigan CL, Wizman P, Hjortdal VE, et al. Global flap ischemia: a comparison of arterial versus venous etiology. Plast Reconstr Surg 1994;93:1485e95 [discussion 96e7]. 41. Devaraj VS, Kay SP, Batchelor AG, et al. Microvascular surgery in children. Br J Plast Surg 1991;44:276e80. 42. Hidalgo DA, Jones CS. The role of emergent exploration in freetissue transfer: a review of 150 consecutive cases. Plast Reconstr Surg 1990;86:492e8 [discussion 99e501].