Further study of hemodynamics in the distal end of multi-territory perforator flap_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

CAO Zilong ,  LIU Liqiang

No.1 Department of Scar and Wound Treatment, Plastic Surgery Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100144, P. R. China;

Corresponding author：

LIU Liqiang, Email: liuliqiang@psh.pumc.edu.cn

Keywords：

Multi-territory perforator flap; perforasome; choke vessel zone; arterial super-charge; venous super-drainage

DOI：

10.7507/1002-1892.202208113

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize and discuss the key factors affecting the hemodynamics in the distal end of the multi-territory perforator flap, so as to provide a theoretical basis for the follow-up research and clinical application in this field. Methods The related recent literature about multi-territory perforator flaps was extensively reviewed, and the concepts and researches of perforasome, choke vessel zone, arterial super-charge, and venous super-drainage were summarized. Results The multi-territory perforator flap is composed of multiple perforasomes, and there are different types of vascular anastomosis in the choke vessel zones, which have important impacts on the hemodynamics of the flap. In order to ensure the survival of the multi-territory perforator flap, arterial super-charge and venous super-drainage are mainly used in clinical practice. However, no consensus has been reached on the choice of the two techniques. The different distribution of blood vessels in the flap, the number of perforasomes, and the type of vascular anastomosis may be the main reasons for the different results. Conclusion The location, diameter, and axial characteristics of perforators, the number of perforasomes, and the type of vascular anastomosis are the key factors affecting the hemodynamics of the multi-territory perforator flaps, which should be paid attention to in preoperative design and surgical procedure.

Citation： CAO Zilong, LIU Liqiang. Further study of hemodynamics in the distal end of multi-territory perforator flap. Chinese Journal of Reparative and Reconstructive Surgery, 2022, 36(12): 1534-1541. doi: 10.7507/1002-1892.202208113 Copy

1.	Taylor GI, Palmer JH. The vascular territories (angiosomes) of the body: experimental study and clinical applications. Br J Plast Surg, 1987, 40(2): 113-141.
2.	Koshima I, Soeda S. Inferior epigastric artery skin flaps without rectus abdominis muscle. Br J Plast Surg, 1989, 42(6): 645-648.
3.	Low OW, Sebastin SJ, Cheah AEJ. A review of pedicled perforator flaps for reconstruction of the soft tissue defects of the leg and foot. Indian J Plast Surg, 2019, 52(1): 26-36.
4.	Blondeel PN, Van Landuyt KH, Monstrey SJ, et al. The “Gent” consensus on perforator flap terminology: preliminary definitions. Plast Reconstr Surg, 2003, 112(5): 1378-1383.
5.	Saint-Cyr M, Wong C, Schaverien M, et al. The perforasome theory: vascular anatomy and clinical implications. Plast Reconstr Surg, 2009, 124(5): 1529-1544.
6.	Wolff KD. Perforator flaps: the next step in the reconstructive ladder? Br J Oral Maxillofac Surg, 2015, 53(9): 787-795.
7.	赵海福, 方柏荣. choke血管血流动力学及血管重构的研究进展. 中华整形外科杂志, 2022, 38(1): 109-114.
8.	唐茂林, 刘元波. 轴型皮瓣与血管体区及穿支体区的内在联系. 中华整形外科杂志, 2019, 35(9): 847-853.
9.	Tutor EG, Auba C, Benito A, et al. Easy venous superdrainage in DIEP flap breast reconstruction through the intercostal branch. J Reconstr Microsurg, 2002, 18(7): 595-598.
10.	Ayestaray B, Yonekura K, Motomura H, et al. A comparative study between deep inferior epigastric artery perforator and thoracoacromial venous supercharged deep inferior epigastric artery perforator flaps. Ann Plast Surg, 2016, 76(1): 78-82.
11.	Lee KT, Mun GH. Benefits of superdrainage using SIEV in DIEP flap breast reconstruction: A systematic review and meta-analysis. Microsurgery, 2017, 37(1): 75-83.
12.	Cao Z, Liu L, Fan J, et al. Different transfer forms of the expanded forehead flap pedicled with superficial temporal vessels to treat chin and submental scar deformities. J Craniofac Surg, 2022, 33(4): 1066-1070.
13.	Gan C, Fan J, Liu L, et al. Reconstruction of large unilateral hemi-facial scar contractures with supercharged expanded forehead flaps based on the anterofrontal superficial temporal vessels. J Plast Reconstr Aesthet Surg, 2013, 66(11): 1470-1476.
14.	Vinh VQ, Van Anh T, Gia Tiên N, et al. Reconstruction of neck and face scar contractures using occipito-cervico-dorsal supercharged “super-thin flaps”: A retrospective analysis of 82 cases in Vietnam. Burns, 2018, 44(2): 462-467.
15.	Herlin C, Bekara F, Bertheuil N, et al. Venous supercharging reduces complications and improves outcomes of distally based sural flaps. J Reconstr Microsurg, 2017, 33(5): 343-351.
16.	McGregor IA, Morgan G. Axial and random pattern flaps. Br J Plast Surg, 1973, 26(3): 202-213.
17.	Cormack GC, Lamberty BG. Cadaver studies of correlation between vessel size and anatomical territory of cutaneous supply. Br J Plast Surg, 1986, 39(3): 300-306.
18.	Chubb DP, Taylor GI, Ashton MW. True and ‘choke’ anastomoses between perforator angiosomes: part Ⅱ. dynamic thermographic identification. Plast Reconstr Surg, 2013, 132(6): 1457-1464.
19.	Cormack GC, Lamberty BG. A classification of fascio-cutaneous flaps according to their patterns of vascularisation. Br J Plast Surg, 1984, 37(1): 80-87.
20.	Taylor GI, Chubb DP, Ashton MW. True and ‘choke’ anastomoses between perforator angiosomes: part i. anatomical location. Plast Reconstr Surg, 2013, 132(6): 1447-1456.
21.	Fang F, Liu M, Xiao J, et al. Arterial supercharging is more beneficial to flap survival due to quadruple dilation of venules. J Surg Res, 2020, 247: 490-498.
22.	Gascoigne AC, Taylor GI, Corlett RJ, et al. Increasing perfusion pressure does not distend perforators or anastomoses but reveals arteriovenous shuntings. Plast Reconstr Surg Glob Open, 2020, 8(6): e2857. doi: 10.1097/GOX.0000000000002857.
23.	Luo X, Zhao B, Chu T, et al. Improvement of multiterritory perforator flap survival supported by a hybrid perfusion mode: A novel strategy and literature review. J Tissue Viability, 2021, 30(2): 276-281.
24.	牙祖蒙, 陈宗基. 跨区反流轴型皮瓣成活机理的实验研究. 中华整形外科杂志, 2002, 18(4): 197-199.
25.	Taylor GI, Gianoutsos MP, Morris SF. The neurovascular territories of the skin and muscles: anatomic study and clinical implications. Plast Reconstr Surg, 1994, 94(1): 1-36.
26.	Teo TC. The propeller flap concept. Clin Plast Surg, 2010, 37(4): 615-626.
27.	Taylor GI, Corlett RJ, Dhar SC, et al. The anatomical (angiosome) and clinical territories of cutaneous perforating arteries: development of the concept and designing safe flaps. Plast Reconstr Surg, 2011, 127(4): 1447-1459.
28.	Nakamura Y, Takanari K, Nakamura R, et al. Correlation between blood flow, tissue volume and microvessel density in the flap. Nagoya J Med Sci, 2020, 82(2): 291-300.
29.	Dusseldorp JR, Pennington DG. Quantifying blood flow in the DIEP flap: An ultrasonographic study. Plast Reconstr Surg Glob Open, 2014, 2(10): e228. doi: 10.1097/GOX.0000000000000191.
30.	Tao Y, Hu S, Lui KW, et al. Quantitative regression analysis of the cutaneous vascular territories in a rat model. Surg Radiol Anat, 2011, 33(9): 789-799.
31.	Tao Y, Ding M, Wang A, et al. Basic perforator flap hemodynamic mathematical model. Plast Reconstr Surg Glob Open, 2016, 4(5): e714. doi: 10.1097/GOX.0000000000000689.
32.	Nakada T, Kwee IL, Igarashi H, et al. Aquaporin-4 functionality and virchow-robin space water dynamics: Physiological model for neurovascular coupling and glymphatic flow. Int J Mol Sci, 2017, 18(8): 1798. doi: 10.3390/ijms18081798.
33.	Jennings D, Raghunand N, Gillies RJ. Imaging hemodynamics. Cancer Metastasis Rev, 2008, 27(4): 589-613.
34.	Fukui A, Tamai S, Williams HB. The importance of venous drainage in rat flaps: an experimental study. J Reconstr Microsurg, 1989, 5(1): 19-30.
35.	Lee C, Mehran RJ, Lessard ML, et al. Leeches: controlled trial in venous compromised rat epigastric flaps. Br J Plast Surg, 1992, 45(3): 235-238.
36.	Chiu DT, Hu G, Wu J, et al. Extended rat-ear flap model: a new rodent model for studying the effects of vessel supercharging on flap viability. J Reconstr Microsurg, 2002, 18(6): 503-508.
37.	Zhang W, Zhu W, Li X, et al. Effects of distal arterial supercharging and distal venous superdrainage on the survival of multiterritory perforator flaps in rats. J Invest Surg, 2022, 35(7): 1462-1471.
38.	Huang X, Liu D, Gu S, et al. Augmentation of perforator flap blood supply with vascular supercharge or flap prefabrication: Evaluation in a rat model. Plast Reconstr Surg, 2021, 147(5): 1105-1115.
39.	Wang D, Chen W. Which is the pivotal vessel in vascular dupercharging? An assessment of three forms of vascular supercharging models using indocyanine green fluorescence angiography. J Surg Res, 2020, 251: 16-25.
40.	Wang X, Pan J, Xiao D, et al. Comparison of arterial supercharging and venous superdrainage on improvement of survival of the extended perforator flap in rats. Microsurgery, 2020, 40(8): 874-880.
41.	Xu H, Steinberger Z, Wo Y, et al. Supercharging strategies for prefabricated flaps in a rat model. J Reconstr Microsurg, 2019, 35(8): 568-574.
42.	Fang F, Zhang Z, Wang K, et al. The skin bridge is more important as an additional venous draining route in a perforator-plus flap. J Surg Res, 2019, 234: 40-48.
43.	Zhang Y, Wang T, Wei J, et al. What’s the remedy for the distal necrosis of DIEP flap, better venous drain or more arterial supply? PLoS One, 2017, 12(2): e0171651. doi: 10.1371/journal.pone.0171651.
44.	Xu H, Feng S, Xia Y, et al. Prefabricated flaps: Identification of microcirculation structure and supercharging technique improving survival area. J Reconstr Microsurg, 2017, 33(2): 112-117.
45.	Zheng J, Xi S, Ding M, et al. Effects of venous superdrainage and arterial supercharging on dorsal perforator flap in a rat model. PLoS One, 2016, 11(8): e0160942. doi: 10.1371/journal.pone.0160942.
46.	Xin MQ, Jie L, Dali M, et al. Hemodynamic effect of different kinds of venous augmentation in a pig transmidline flap model of DIEP flap. J Reconstr Microsurg, 2013, 29(6): 379-386.
47.	Gümüş N, Erkan M, Erçöçen AR. Vascular pressure monitorization for necessity of vascular augmentation in a rat extended abdominal perforator flap model. Microsurgery, 2012, 32(4): 303-308.
48.	Fukushima J, Inoue Y, Kiyokawa K, et al. Effects of short-term venous augmentation on the improvement of flap survival: an experimental study in rats. J Plast Reconstr Aesthet Surg, 2012, 65(5): 650-656.
49.	Yamamoto Y, Sakurai H, Nakazawa H, et al. Effect of vascular augmentation on the haemodynamics and survival area in a rat abdominal perforator flap model. J Plast Reconstr Aesthet Surg, 2009, 62(2): 244-249.
50.	Chang H, Minn KW, Imanishi N, et al. Effect of venous superdrainage on a four-territory skin flap survival in rats. Plast Reconstr Surg, 2007, 119(7): 2046-2051.
51.	Groth AK, Campos AC, Gonçalves CG, et al. Effects of venous supercharging in deep inferior epigastric artery perforator flap. Acta Cir Bras, 2007, 22(6): 474-478.
52.	Hallock GG, Rice DC. Efficacy of venous supercharging of the deep inferior epigastric perforator flap in a rat model. Plast Reconstr Surg, 2005, 116(2): 551-555.
53.	Chang H, Nobuaki I, Minabe T, et al. Comparison of three different supercharging procedures in a rat skin flap model. Plast Reconstr Surg, 2004, 113(1): 277-283.
54.	Sano K, Hallock GG, Rice DC. Venous “supercharging” augments survival of the delayed rat TRAM flap. Ann Plast Surg, 2003, 51(4): 398-402. doi: 10.1097/01.SAP.0000068111.83104.7F.
55.	Ueda K, Harashina T, Oba S, et al. Which vessel is more important in the supercharged flap-artery, vein, or both? An experimental study. J Reconstr Microsurg, 1994, 10(3): 153-155.
56.	Li Z, Zhang ZW, Yu SX, et al. The experimental study of shunt-decompression arterialized vein flap. Cancer Cell Int, 2018, 18: 148. doi: 10.1186/s12935-018-0622-z.
57.	Wu H, Zhang C, Chen Z, et al. Distal arterialized venous supercharging improves perfusion and survival in an extended dorsal three-perforasome perforator flap rat model. Plast Reconstr Surg, 2021, 147(6): 957e-966e.
58.	Agarwal P, Sharma D, Kukrele R. Arteriovenous supercharging: A novel approach to improve reliability of the distally based sural flap. Trop Doct, 2021, 51(3): 339-344.
59.	曾秀安, 厉孟, 杨其兵, 等. 二甲基乙二酰基甘氨酸对跨区穿支皮瓣Choke Ⅱ区血管生成的影响机制研究. 中国修复重建外科杂志, 2022, 36(2): 224-230.
60.	严玉勇, 潘新元, 林博杰, 等. 天然水蛭素对大鼠缺血皮瓣血管生成作用的 Micro-CT 观察. 中国修复重建外科杂志, 2020, 34(3): 382-386.
61.	Tu Q, Liu S, Chen T, et al. Effects of adiponectin on random pattern skin flap survival in rats. Int Immunopharmacol, 2019, 76: 105875. doi: 10.1016/j.intimp.2019.105875.
62.	Khavanin N, Yesantharao P, Kraenzlin F, et al. Quantifying the effect of topical nitroglycerin on random pattern flap perfusion in a rodent model: An application of the ViOptix Intra. Ox for dynamic flap perfusion assessment and salvage. Plast Reconstr Surg, 2021, 148(1): 100-107.

1. Taylor GI, Palmer JH. The vascular territories (angiosomes) of the body: experimental study and clinical applications. Br J Plast Surg, 1987, 40(2): 113-141.
2. Koshima I, Soeda S. Inferior epigastric artery skin flaps without rectus abdominis muscle. Br J Plast Surg, 1989, 42(6): 645-648.
3. Low OW, Sebastin SJ, Cheah AEJ. A review of pedicled perforator flaps for reconstruction of the soft tissue defects of the leg and foot. Indian J Plast Surg, 2019, 52(1): 26-36.
4. Blondeel PN, Van Landuyt KH, Monstrey SJ, et al. The “Gent” consensus on perforator flap terminology: preliminary definitions. Plast Reconstr Surg, 2003, 112(5): 1378-1383.
5. Saint-Cyr M, Wong C, Schaverien M, et al. The perforasome theory: vascular anatomy and clinical implications. Plast Reconstr Surg, 2009, 124(5): 1529-1544.
6. Wolff KD. Perforator flaps: the next step in the reconstructive ladder? Br J Oral Maxillofac Surg, 2015, 53(9): 787-795.
7. 赵海福, 方柏荣. choke血管血流动力学及血管重构的研究进展. 中华整形外科杂志, 2022, 38(1): 109-114.
8. 唐茂林, 刘元波. 轴型皮瓣与血管体区及穿支体区的内在联系. 中华整形外科杂志, 2019, 35(9): 847-853.
9. Tutor EG, Auba C, Benito A, et al. Easy venous superdrainage in DIEP flap breast reconstruction through the intercostal branch. J Reconstr Microsurg, 2002, 18(7): 595-598.
10. Ayestaray B, Yonekura K, Motomura H, et al. A comparative study between deep inferior epigastric artery perforator and thoracoacromial venous supercharged deep inferior epigastric artery perforator flaps. Ann Plast Surg, 2016, 76(1): 78-82.
11. Lee KT, Mun GH. Benefits of superdrainage using SIEV in DIEP flap breast reconstruction: A systematic review and meta-analysis. Microsurgery, 2017, 37(1): 75-83.
12. Cao Z, Liu L, Fan J, et al. Different transfer forms of the expanded forehead flap pedicled with superficial temporal vessels to treat chin and submental scar deformities. J Craniofac Surg, 2022, 33(4): 1066-1070.
13. Gan C, Fan J, Liu L, et al. Reconstruction of large unilateral hemi-facial scar contractures with supercharged expanded forehead flaps based on the anterofrontal superficial temporal vessels. J Plast Reconstr Aesthet Surg, 2013, 66(11): 1470-1476.
14. Vinh VQ, Van Anh T, Gia Tiên N, et al. Reconstruction of neck and face scar contractures using occipito-cervico-dorsal supercharged “super-thin flaps”: A retrospective analysis of 82 cases in Vietnam. Burns, 2018, 44(2): 462-467.
15. Herlin C, Bekara F, Bertheuil N, et al. Venous supercharging reduces complications and improves outcomes of distally based sural flaps. J Reconstr Microsurg, 2017, 33(5): 343-351.
16. McGregor IA, Morgan G. Axial and random pattern flaps. Br J Plast Surg, 1973, 26(3): 202-213.
17. Cormack GC, Lamberty BG. Cadaver studies of correlation between vessel size and anatomical territory of cutaneous supply. Br J Plast Surg, 1986, 39(3): 300-306.
18. Chubb DP, Taylor GI, Ashton MW. True and ‘choke’ anastomoses between perforator angiosomes: part Ⅱ. dynamic thermographic identification. Plast Reconstr Surg, 2013, 132(6): 1457-1464.
19. Cormack GC, Lamberty BG. A classification of fascio-cutaneous flaps according to their patterns of vascularisation. Br J Plast Surg, 1984, 37(1): 80-87.
20. Taylor GI, Chubb DP, Ashton MW. True and ‘choke’ anastomoses between perforator angiosomes: part i. anatomical location. Plast Reconstr Surg, 2013, 132(6): 1447-1456.
21. Fang F, Liu M, Xiao J, et al. Arterial supercharging is more beneficial to flap survival due to quadruple dilation of venules. J Surg Res, 2020, 247: 490-498.
22. Gascoigne AC, Taylor GI, Corlett RJ, et al. Increasing perfusion pressure does not distend perforators or anastomoses but reveals arteriovenous shuntings. Plast Reconstr Surg Glob Open, 2020, 8(6): e2857. doi: 10.1097/GOX.0000000000002857.
23. Luo X, Zhao B, Chu T, et al. Improvement of multiterritory perforator flap survival supported by a hybrid perfusion mode: A novel strategy and literature review. J Tissue Viability, 2021, 30(2): 276-281.
24. 牙祖蒙, 陈宗基. 跨区反流轴型皮瓣成活机理的实验研究. 中华整形外科杂志, 2002, 18(4): 197-199.
25. Taylor GI, Gianoutsos MP, Morris SF. The neurovascular territories of the skin and muscles: anatomic study and clinical implications. Plast Reconstr Surg, 1994, 94(1): 1-36.
26. Teo TC. The propeller flap concept. Clin Plast Surg, 2010, 37(4): 615-626.
27. Taylor GI, Corlett RJ, Dhar SC, et al. The anatomical (angiosome) and clinical territories of cutaneous perforating arteries: development of the concept and designing safe flaps. Plast Reconstr Surg, 2011, 127(4): 1447-1459.
28. Nakamura Y, Takanari K, Nakamura R, et al. Correlation between blood flow, tissue volume and microvessel density in the flap. Nagoya J Med Sci, 2020, 82(2): 291-300.
29. Dusseldorp JR, Pennington DG. Quantifying blood flow in the DIEP flap: An ultrasonographic study. Plast Reconstr Surg Glob Open, 2014, 2(10): e228. doi: 10.1097/GOX.0000000000000191.
30. Tao Y, Hu S, Lui KW, et al. Quantitative regression analysis of the cutaneous vascular territories in a rat model. Surg Radiol Anat, 2011, 33(9): 789-799.
31. Tao Y, Ding M, Wang A, et al. Basic perforator flap hemodynamic mathematical model. Plast Reconstr Surg Glob Open, 2016, 4(5): e714. doi: 10.1097/GOX.0000000000000689.
32. Nakada T, Kwee IL, Igarashi H, et al. Aquaporin-4 functionality and virchow-robin space water dynamics: Physiological model for neurovascular coupling and glymphatic flow. Int J Mol Sci, 2017, 18(8): 1798. doi: 10.3390/ijms18081798.
33. Jennings D, Raghunand N, Gillies RJ. Imaging hemodynamics. Cancer Metastasis Rev, 2008, 27(4): 589-613.
34. Fukui A, Tamai S, Williams HB. The importance of venous drainage in rat flaps: an experimental study. J Reconstr Microsurg, 1989, 5(1): 19-30.
35. Lee C, Mehran RJ, Lessard ML, et al. Leeches: controlled trial in venous compromised rat epigastric flaps. Br J Plast Surg, 1992, 45(3): 235-238.
36. Chiu DT, Hu G, Wu J, et al. Extended rat-ear flap model: a new rodent model for studying the effects of vessel supercharging on flap viability. J Reconstr Microsurg, 2002, 18(6): 503-508.
37. Zhang W, Zhu W, Li X, et al. Effects of distal arterial supercharging and distal venous superdrainage on the survival of multiterritory perforator flaps in rats. J Invest Surg, 2022, 35(7): 1462-1471.
38. Huang X, Liu D, Gu S, et al. Augmentation of perforator flap blood supply with vascular supercharge or flap prefabrication: Evaluation in a rat model. Plast Reconstr Surg, 2021, 147(5): 1105-1115.
39. Wang D, Chen W. Which is the pivotal vessel in vascular dupercharging? An assessment of three forms of vascular supercharging models using indocyanine green fluorescence angiography. J Surg Res, 2020, 251: 16-25.
40. Wang X, Pan J, Xiao D, et al. Comparison of arterial supercharging and venous superdrainage on improvement of survival of the extended perforator flap in rats. Microsurgery, 2020, 40(8): 874-880.
41. Xu H, Steinberger Z, Wo Y, et al. Supercharging strategies for prefabricated flaps in a rat model. J Reconstr Microsurg, 2019, 35(8): 568-574.
42. Fang F, Zhang Z, Wang K, et al. The skin bridge is more important as an additional venous draining route in a perforator-plus flap. J Surg Res, 2019, 234: 40-48.
43. Zhang Y, Wang T, Wei J, et al. What’s the remedy for the distal necrosis of DIEP flap, better venous drain or more arterial supply? PLoS One, 2017, 12(2): e0171651. doi: 10.1371/journal.pone.0171651.
44. Xu H, Feng S, Xia Y, et al. Prefabricated flaps: Identification of microcirculation structure and supercharging technique improving survival area. J Reconstr Microsurg, 2017, 33(2): 112-117.
45. Zheng J, Xi S, Ding M, et al. Effects of venous superdrainage and arterial supercharging on dorsal perforator flap in a rat model. PLoS One, 2016, 11(8): e0160942. doi: 10.1371/journal.pone.0160942.
46. Xin MQ, Jie L, Dali M, et al. Hemodynamic effect of different kinds of venous augmentation in a pig transmidline flap model of DIEP flap. J Reconstr Microsurg, 2013, 29(6): 379-386.
47. Gümüş N, Erkan M, Erçöçen AR. Vascular pressure monitorization for necessity of vascular augmentation in a rat extended abdominal perforator flap model. Microsurgery, 2012, 32(4): 303-308.
48. Fukushima J, Inoue Y, Kiyokawa K, et al. Effects of short-term venous augmentation on the improvement of flap survival: an experimental study in rats. J Plast Reconstr Aesthet Surg, 2012, 65(5): 650-656.
49. Yamamoto Y, Sakurai H, Nakazawa H, et al. Effect of vascular augmentation on the haemodynamics and survival area in a rat abdominal perforator flap model. J Plast Reconstr Aesthet Surg, 2009, 62(2): 244-249.
50. Chang H, Minn KW, Imanishi N, et al. Effect of venous superdrainage on a four-territory skin flap survival in rats. Plast Reconstr Surg, 2007, 119(7): 2046-2051.
51. Groth AK, Campos AC, Gonçalves CG, et al. Effects of venous supercharging in deep inferior epigastric artery perforator flap. Acta Cir Bras, 2007, 22(6): 474-478.
52. Hallock GG, Rice DC. Efficacy of venous supercharging of the deep inferior epigastric perforator flap in a rat model. Plast Reconstr Surg, 2005, 116(2): 551-555.
53. Chang H, Nobuaki I, Minabe T, et al. Comparison of three different supercharging procedures in a rat skin flap model. Plast Reconstr Surg, 2004, 113(1): 277-283.
54. Sano K, Hallock GG, Rice DC. Venous “supercharging” augments survival of the delayed rat TRAM flap. Ann Plast Surg, 2003, 51(4): 398-402. doi: 10.1097/01.SAP.0000068111.83104.7F.
55. Ueda K, Harashina T, Oba S, et al. Which vessel is more important in the supercharged flap-artery, vein, or both? An experimental study. J Reconstr Microsurg, 1994, 10(3): 153-155.
56. Li Z, Zhang ZW, Yu SX, et al. The experimental study of shunt-decompression arterialized vein flap. Cancer Cell Int, 2018, 18: 148. doi: 10.1186/s12935-018-0622-z.
57. Wu H, Zhang C, Chen Z, et al. Distal arterialized venous supercharging improves perfusion and survival in an extended dorsal three-perforasome perforator flap rat model. Plast Reconstr Surg, 2021, 147(6): 957e-966e.
58. Agarwal P, Sharma D, Kukrele R. Arteriovenous supercharging: A novel approach to improve reliability of the distally based sural flap. Trop Doct, 2021, 51(3): 339-344.
59. 曾秀安, 厉孟, 杨其兵, 等. 二甲基乙二酰基甘氨酸对跨区穿支皮瓣Choke Ⅱ区血管生成的影响机制研究. 中国修复重建外科杂志, 2022, 36(2): 224-230.
60. 严玉勇, 潘新元, 林博杰, 等. 天然水蛭素对大鼠缺血皮瓣血管生成作用的 Micro-CT 观察. 中国修复重建外科杂志, 2020, 34(3): 382-386.
61. Tu Q, Liu S, Chen T, et al. Effects of adiponectin on random pattern skin flap survival in rats. Int Immunopharmacol, 2019, 76: 105875. doi: 10.1016/j.intimp.2019.105875.
62. Khavanin N, Yesantharao P, Kraenzlin F, et al. Quantifying the effect of topical nitroglycerin on random pattern flap perfusion in a rodent model: An application of the ViOptix Intra. Ox for dynamic flap perfusion assessment and salvage. Plast Reconstr Surg, 2021, 148(1): 100-107.

Chinese Journal of Reparative and Reconstructive Surgery

Further study of hemodynamics in the distal end of multi-territory perforator flap

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