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Lymphatic reconstruction
C H A P T E R
8 Lymphatic reconstruction Annika Mohr, Daniel Palmes, Felix Becker Clinic of General, Visceral and Transplantation Surgery, University Hospital M€ unster, M€ unster, Germany
Introduction Lymphatic reconstruction as a surgical approach is mostly utilized for patients with destructed or obstructed lymphatic vessels who are suffering from secondary lymphedema [1]. The accumulation of abnormal fluid in the interstitium results in an enlargement of the affected area [2]. Due to continued lymphatic stasis, inflammatory activation bay immune cells, cytokines, and microorganisms might lead to inflammation, gradual fibrosis, and thus a decrease in the number of functional lymphatic channels [1]. Underlying reasons for the disruption of the lymphatic drainage system are mostly posttraumatic, postinfectious, or postinflammational due to surgery, radiotherapy, or cancer [3]. However, clinical manifestation may be delayed after the initial incidence by months or even years. Nevertheless if once occurred, adjusted treatment is initiated for providing symptomatic improvement and deceleration of the progressive disease with conservative therapy representing the today’s gold standard [4]. Although for most patients beneficial, major disadvantages are the required compliance of the patient, as well as the lifelong commitment necessary for a prosperous therapy. Thus, surgical treatment options represent an additional option when conservative therapy is unable to control the symptoms of
Lymphatic Structure and Function in Health and Disease https://doi.org/10.1016/B978-0-12-815645-2.00008-3
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Copyright © 2020 Elsevier Inc. All rights reserved.
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8. Lymphatic reconstruction
lymphedema [1]. Specifically, patients with insufficient reduction by medical and physical therapy (less than 50%) and those dissatisfied by the results of conservative methods and willing to proceed with surgical options might benefit from surgical reconstruction approaches of the lymphatic system [5].
History of surgical approaches for lymphatic reconstruction Surgical approaches for lymphatic reconstruction are performed since the 1960s. Niebulowisz et al. performed a lymphdraining anastomosis between a lymph node and a neighboring vein in patients with secondary lymphedema of the lower limb [6]. Subsequent research about the mechanisms of the development of secondary lymphedema mostly due to improvement of imaging systems led to adjustments of surgical methods. Thus, spontaneous lymphatic pulse, stagnation of tissue fluid, and the presence of bacterial flora could be visualized [7–9]. In addition to that, the improvement of microsurgical equipment (e.g., microscope and atraumatic sutures) helped to facilitate lymphatic reconstruction [10,11].
Current options for lymphatic reconstruction Lymphaticovenular anastomosis First anastomoses between lymph vessels and veins were performed in the 1960s due to the introduction of dissection microscopes into surgery [10]. The procedure should imitate the natural communication between lymphatics and veins, thus redirecting the accumulated lymph fluid into the venous system. Since the first approaches, several studies have been conducted leading to a variation of surgical techniques (e.g., end to end, end to side, and side to end) and heterogeneous evidence of treatment effectiveness. Major problems when utilizing this technique are high venous blood pressure and consequently the risk of thrombus formation due to blood coagulation [12].
Current options for lymphatic reconstruction
157
To enhance long-term outcome, the measurement of endolymphatic pressure, lymphatic flow rate, and venous pressure is recommended before the performance of microsurgical anastomosis [3]. Thus, optimal conditions could be created for the best approach. Moreover, whenever possible, lymphatic vessels with contracting ability should be chosen for the anastomosis [13]. In addition to that, patency of the selected vessels should be proven prior surgery [14]. It has also been shown that the absence of blood inside of the venous branch utilized for the anastomosis decreases the risk of thrombosis [15,16]. Most successful results could be accomplished in patients with local, segmental obstructions in the proximal lymph vessels [17]. First results in patients suffering from secondary lymphedema were promising indicating adequate decompression of the limb [18,19]. However, long-term results were less effective in the proximal compared with the distal part of the extremity [18]. The authors concluded the higher degree of destruction of the proximal lymphatic system was responsible for this phenomenon suggesting surgery at an earlier time when lymphatic disruption is less advanced. Consequently, it is generally recommended to treat lymphedema with lymphaticovenular anastomosis as early as possible [15,16], before the development of tissue fibrosis or lymphatic damage due to increasing tissue pressure or infection. Nevertheless, the impact of duration and severity of lymphedema is classified differentially with some surgeons claiming to have found no influence of the length of the condition of the patient on the outcome after surgery [11,20]. Regarding the technique of anastomosis (e.g., end to end, end to side, and side to end), most authors indicated their choice was based on anatomical conditions at the site of operation after isolating lymphatics and veins [3,15,16]. In contrast to the other options, side-to-end anastomosis preserves the original flow of the lymphatic fluids and offers the possibility for further operations at the same vessels if an obstruction of the first anastomosis occurs [21]. Nevertheless, this procedure is more complex, which is why a novel method was introduced to facilitate side-to-end anastomosis. With expanding the lymphatic vessel, shortly before performing the anastomosis, the creation of a lateral window in the lymphatic wall is facilitated, thus improving the success rate
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8. Lymphatic reconstruction
in the performed study [22]. Obstacles still present small lymphatic vessels with a diameter below 0.35 mm where side-toend anastomosis is not recommended even after expansion due to a relatively high failure rate. Follow-up studies indicated beneficial results after lymphaticovenular anastomosis with immediate and long-term significant improvements [11,12,14–16,20,21,23]. In conclusion, lymphaticovenular anastomosis represents a promising approach for decreasing secondary lymphedema. Nevertheless, postoperative compressive therapy still has to be performed. Additionally, it has to be noted that the aforementioned studies utilized different methods and follow-up periods. For the determination of patency, methods varied from circumference measurement to volumetry, lower extremity lymphedema (LEL) index, or lymphoscintigraphy. Thus, a direct comparison between the studies appears to be challenging. Yet, objective and subjective results are indicating a place in the treatment of secondary lymphedema especially when conservative therapy is failing.
Vascularized lymph node transfer Vascularized lymph node transfer represents a relatively novel method where a transfer into regions with dissected lymph nodes (e.g., cancer treatment) or into distal regions of limbs with lymphedema is performed to reestablish lymphatic drainage function [24]. Starting in animal studies, vascularized lymph node transfer showed a complete preservation of the original histological structures [25] in contrast to what has been seen in a vascularized lymph node transfers [26,27]. First attempts in clinical studies in 1982 showed a stable reduction of lymphedema after transferring inguinal lymph nodes to the contralateral inguinal region [28]. Similar results have been reported for the upper extremity with a transfer either into the axillary region [29] or into the wrist area [30]. In general, all studies performed on vascularized lymph node transfer showed favorable outcomes for the patients after surgery including reduction of lymphedematous limb volumes, infections, and improved quality of life [31–34]. Lymph node flap harvest is performed from different areas of the donor including groin,
Conclusion
159
submental, supraclavicular, lateral thoracic, gastroepiploic, jejunal, appendicular, and ileocecal with no general ideal recommendation until now. For better outcomes, lymph nodes may be transferred with a skin paddle containing lymph capillaries, thus facilitating recanalization of the lymphatic system [24]. It has to be noted that only few long-term results are available for vascularized lymph node transfers until now. Moreover, the interaction between transferred lymph node and the lymphatic system in the recipient area still needs to be elucidated. In addition, the risk of causing lymphedema in the region of the donor lymph node might be heightened [35–37]. Despite the promising technique, additional excisional procedures are recommended after vascularized lymph node transfers in patients suffering from secondary lymphedema.
Lympholymphatic graft In contrast to lymphaticovenular anastomosis and vascularized lymph node transfer, only few studies have been conducted evaluating lymphatic grafts in lymphedema treatment. First attempts of harvesting autologous lymphatic grafts to bypass damaged lymphatic vessels resulted in not only volume reduction of 80% but also high risk of donor site morbidity [38]. The bypass should be carried out prior permanent damage of the remainder lymphatic vessels due to back pressure or infection [39]. Alternatively, vein grafts have been used in patients with chronic lymphedema to obtain a lymphatic-venous-lymphatic bypass [15,16] with the result of improvement of both limb function and edema. Most recent studies aimed to develop tissue-engineered grafts to reestablish lymphatic circulation [40], and first studies under culturing conditions offered promising results for future clinical application and as a potential new treatment option for secondary lymphedema [41].
Conclusion Nevertheless, until now, and despite the promising results regarding the surgical approaches of lymphatic reconstruction, it has to be noted that lymphatic reconstruction is still a palliative
160
8. Lymphatic reconstruction
procedure. The creation of a bypass system for lymphatic system offers no elimination of the etiologic factor; thus, obstructions or destructions of the lymphatic vessel and infections leading to decreased transport capacity of lymphatic fluid are still present. In addition to that, in most cases, conservative therapy is still required even though surgical reconstruction was performed. Further improvement of the surgical techniques and a consensus in standardized protocols and reporting of outcome is finally needed to enhance and consolidate lymphatic reconstruction in secondary lymphedema.
References [1] Kung TA, Champaneria MC, et al. Current concepts in the surgical Management of Lymphedema. Plast Reconstr Surg 2017;139(4). [2] Ozturk CN, Ozturk C, et al. Free vascularized lymph node transfer for treatment of lymphedema: a systematic evidence based review. J Plast Reconstr Aesthet Surg 2016;69(9):1234–47. [3] Campisi C, Boccardo F. Frontiers in lymphatic microsurgery. Microsurgery 1998;18(8):462–71. [4] Becker C, Vasile JV, et al. Microlymphatic surgery for the treatment of iatrogenic lymphedema. Clin Plast Surg 2012;39(4):385–98. [5] Boccardo F, Fulcheri E, et al. Lymphatic microsurgery to treat lymphedema: techniques and indications for better results. Ann Plast Surg 2013;71(2):191–5. [6] Nielubowicz J, Olszewski W. Surgical lymphaticovenous shunts in patients with secondary lymphoedema. Br J Surg 1968;55(6):440–2. [7] Olszewski WL. Episodic dermatolymphangioadenitis (DLA) in patients with lymphedema of the lower extremities before and after administration of benzathine penicillin: a preliminary study. Lymphology 1996;29(3):126–31. [8] Olszewski WL. Contractility patterns of human leg lymphatics in various stages of obstructive lymphedema. Ann N Y Acad Sci 2008;010. [9] Olszewski WL, Engeset A, et al. Lymph flow and protein in the normal male leg during lying, getting up, and walking. Lymphology 1977;10(3):178–83. [10] Jacobson II JH, Suarez EL. Microvascular surgery. Dis Chest 1962;41:220–4. [11] Koshima I, Inagawa K, et al. Supermicrosurgical lymphaticovenular anastomosis for the treatment of lymphedema in the upper extremities. J Reconstr Microsurg 2000;16(6):437–42. [12] Winters H, Tielemans HJP, et al. The efficacy of lymphaticovenular anastomosis in breast cancer-related lymphedema. Breast Cancer Res Treat 2017;165(2):321–7. [13] Campisi C, Bellini C, et al. Microsurgery for lymphedema: clinical research and long-term results. Microsurgery 2010;30(4):256–60.
References
161
[14] Demirtas Y, Ozturk N, et al. Supermicrosurgical lymphaticovenular anastomosis and lymphaticovenous implantation for treatment of unilateral lower extremity lymphedema. Microsurgery 2009;29(8):609–18. [15] Campisi C, Boccardo F, et al. Long-term results after lymphatic-venous anastomoses for the treatment of obstructive lymphedema. Microsurgery 2001;21(4):135–9. [16] Campisi C, Boccardo F, et al. The use of vein grafts in the treatment of peripheral lymphedemas: long-term results. Microsurgery 2001;21(4):143–7. [17] Olszewski WL. The treatment of lymphedema of the extremities with microsurgical lympho-venous anastomoses. Int Angiol 1988;7(4):312–21. [18] O’Brien BM, Mellow CG, et al. Long-term results after microlymphaticovenous anastomoses for the treatment of obstructive lymphedema. Plast Reconstr Surg 1990;85(4):562–72. [19] O’Brien BM, Shafiroff BB. Microlymphaticovenous and resectional surgery in obstructive lymphedema. World J Surg 1979;3(1):3–15. [20] Koshima I, Nanba Y, et al. Long-term follow-up after lymphaticovenular anastomosis for lymphedema in the leg. J Reconstr Microsurg 2003;19(4):209–15. [21] Maegawa J, Yabuki Y, et al. Outcomes of lymphaticovenous side-to-end anastomosis in peripheral lymphedema. J Vasc Surg 2012;55(3):753–60. [22] Yamamoto T, Yoshimatsu H, et al. Side-to-end lymphaticovenular anastomosis through temporary lymphatic expansion. PLoS One 2013;8(3):25. [23] Cornelissen AJM, Kool M, et al. Lymphatico-venous anastomosis as treatment for breast cancer-related lymphedema: a prospective study on quality of life. Breast Cancer Res Treat 2017;163(2):281–6. [24] Ito R, Suami H. Overview of lymph node transfer for lymphedema treatment. Plast Reconstr Surg 2014;134(3):548–56. [25] Shesol BF, Nakashima R, et al. Successful lymph node transplantation in rats, with restoration of lymphatic function. Plast Reconstr Surg 1979;63(6):817–23. [26] Jaffe HL, Richter MN. The regeneration of autoplastic lymph node transplants. J Exp Med 1928;47(6):977–80. [27] Tobbia D, Semple J, et al. Experimental assessment of autologous lymph node transplantation as treatment of postsurgical lymphedema. Plast Reconstr Surg 2009;124(3):777–86. [28] Clodius L, Smith PJ, et al. The lymphatics of the groin flap. Ann Plast Surg 1982;9(6):447–58. [29] Becker C, Assouad J, et al. Postmastectomy lymphedema: long-term results following microsurgical lymph node transplantation. Ann Surg 2006;243(3):313–5. [30] Lin CH, Ali R, et al. Vascularized groin lymph node transfer using the wrist as a recipient site for management of postmastectomy upper extremity lymphedema. Plast Reconstr Surg 2009;123(4):1265–75. [31] Cheng MH, Huang JJ, et al. A novel approach to the treatment of lower extremity lymphedema by transferring a vascularized submental lymph node flap to the ankle. Gynecol Oncol 2012;126(1):93–8. [32] Ciudad P, Maruccia M, et al. The laparoscopic right gastroepiploic lymph node flap transfer for upper and lower limb lymphedema: technique and outcomes. Microsurgery 2017;37(3):197–205.
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8. Lymphatic reconstruction
[33] De Brucker B, Zeltzer A, et al. Breast Cancer-related lymphedema: quality of life after lymph node transfer. Plast Reconstr Surg 2016;137(6):1673–80. [34] Gratzon A, Schultz J, et al. Clinical and psychosocial outcomes of vascularized lymph node transfer for the treatment of upper extremity lymphedema after breast Cancer therapy. Ann Surg Oncol 2017;24(6):1475–81. [35] Pons G, Masia J, et al. A case of donor-site lymphoedema after lymph nodesuperficial circumflex iliac artery perforator flap transfer. J Plast Reconstr Aesthet Surg 2014;67(1):119–23. [36] Sulo E, Hartiala P, et al. Risk of donor-site lymphatic vessel dysfunction after microvascular lymph node transfer. J Plast Reconstr Aesthet Surg 2015;68(4):551–8. [37] Viitanen TP, Maki MT, et al. Donor-site lymphatic function after microvascular lymph node transfer. Plast Reconstr Surg 2012;130(6):1246–53. [38] Baumeister RG, Siuda S. Treatment of lymphedemas by microsurgical lymphatic grafting: what is proved? Plast Reconstr Surg 1990;85(1):64–74. [39] Ho LC, Lai MF, et al. Microlymphatic bypass in obstructive lymphoedema. Br J Plast Surg 1988;41(5):475–84. [40] Kanapathy M, Patel NM, et al. Tissue-engineered lymphatic graft for the treatment of lymphedema. J Surg Res 2014;192(2):544–54. [41] Kanapathy M, Kalaskar D, et al. Development of a tissue-engineered lymphatic graft using nanocomposite polymer for the treatment of secondary lymphedema. Artif Organs 2016;40(3):30.
8 Lymphatic reconstruction Annika Mohr, Daniel Palmes, Felix Becker Clinic of General, Visceral and Transplantation Surgery, University Hospital M€ unster, M€ unster, Germany
Introduction Lymphatic reconstruction as a surgical approach is mostly utilized for patients with destructed or obstructed lymphatic vessels who are suffering from secondary lymphedema [1]. The accumulation of abnormal fluid in the interstitium results in an enlargement of the affected area [2]. Due to continued lymphatic stasis, inflammatory activation bay immune cells, cytokines, and microorganisms might lead to inflammation, gradual fibrosis, and thus a decrease in the number of functional lymphatic channels [1]. Underlying reasons for the disruption of the lymphatic drainage system are mostly posttraumatic, postinfectious, or postinflammational due to surgery, radiotherapy, or cancer [3]. However, clinical manifestation may be delayed after the initial incidence by months or even years. Nevertheless if once occurred, adjusted treatment is initiated for providing symptomatic improvement and deceleration of the progressive disease with conservative therapy representing the today’s gold standard [4]. Although for most patients beneficial, major disadvantages are the required compliance of the patient, as well as the lifelong commitment necessary for a prosperous therapy. Thus, surgical treatment options represent an additional option when conservative therapy is unable to control the symptoms of
Lymphatic Structure and Function in Health and Disease https://doi.org/10.1016/B978-0-12-815645-2.00008-3
155
Copyright © 2020 Elsevier Inc. All rights reserved.
156
8. Lymphatic reconstruction
lymphedema [1]. Specifically, patients with insufficient reduction by medical and physical therapy (less than 50%) and those dissatisfied by the results of conservative methods and willing to proceed with surgical options might benefit from surgical reconstruction approaches of the lymphatic system [5].
History of surgical approaches for lymphatic reconstruction Surgical approaches for lymphatic reconstruction are performed since the 1960s. Niebulowisz et al. performed a lymphdraining anastomosis between a lymph node and a neighboring vein in patients with secondary lymphedema of the lower limb [6]. Subsequent research about the mechanisms of the development of secondary lymphedema mostly due to improvement of imaging systems led to adjustments of surgical methods. Thus, spontaneous lymphatic pulse, stagnation of tissue fluid, and the presence of bacterial flora could be visualized [7–9]. In addition to that, the improvement of microsurgical equipment (e.g., microscope and atraumatic sutures) helped to facilitate lymphatic reconstruction [10,11].
Current options for lymphatic reconstruction Lymphaticovenular anastomosis First anastomoses between lymph vessels and veins were performed in the 1960s due to the introduction of dissection microscopes into surgery [10]. The procedure should imitate the natural communication between lymphatics and veins, thus redirecting the accumulated lymph fluid into the venous system. Since the first approaches, several studies have been conducted leading to a variation of surgical techniques (e.g., end to end, end to side, and side to end) and heterogeneous evidence of treatment effectiveness. Major problems when utilizing this technique are high venous blood pressure and consequently the risk of thrombus formation due to blood coagulation [12].
Current options for lymphatic reconstruction
157
To enhance long-term outcome, the measurement of endolymphatic pressure, lymphatic flow rate, and venous pressure is recommended before the performance of microsurgical anastomosis [3]. Thus, optimal conditions could be created for the best approach. Moreover, whenever possible, lymphatic vessels with contracting ability should be chosen for the anastomosis [13]. In addition to that, patency of the selected vessels should be proven prior surgery [14]. It has also been shown that the absence of blood inside of the venous branch utilized for the anastomosis decreases the risk of thrombosis [15,16]. Most successful results could be accomplished in patients with local, segmental obstructions in the proximal lymph vessels [17]. First results in patients suffering from secondary lymphedema were promising indicating adequate decompression of the limb [18,19]. However, long-term results were less effective in the proximal compared with the distal part of the extremity [18]. The authors concluded the higher degree of destruction of the proximal lymphatic system was responsible for this phenomenon suggesting surgery at an earlier time when lymphatic disruption is less advanced. Consequently, it is generally recommended to treat lymphedema with lymphaticovenular anastomosis as early as possible [15,16], before the development of tissue fibrosis or lymphatic damage due to increasing tissue pressure or infection. Nevertheless, the impact of duration and severity of lymphedema is classified differentially with some surgeons claiming to have found no influence of the length of the condition of the patient on the outcome after surgery [11,20]. Regarding the technique of anastomosis (e.g., end to end, end to side, and side to end), most authors indicated their choice was based on anatomical conditions at the site of operation after isolating lymphatics and veins [3,15,16]. In contrast to the other options, side-to-end anastomosis preserves the original flow of the lymphatic fluids and offers the possibility for further operations at the same vessels if an obstruction of the first anastomosis occurs [21]. Nevertheless, this procedure is more complex, which is why a novel method was introduced to facilitate side-to-end anastomosis. With expanding the lymphatic vessel, shortly before performing the anastomosis, the creation of a lateral window in the lymphatic wall is facilitated, thus improving the success rate
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8. Lymphatic reconstruction
in the performed study [22]. Obstacles still present small lymphatic vessels with a diameter below 0.35 mm where side-toend anastomosis is not recommended even after expansion due to a relatively high failure rate. Follow-up studies indicated beneficial results after lymphaticovenular anastomosis with immediate and long-term significant improvements [11,12,14–16,20,21,23]. In conclusion, lymphaticovenular anastomosis represents a promising approach for decreasing secondary lymphedema. Nevertheless, postoperative compressive therapy still has to be performed. Additionally, it has to be noted that the aforementioned studies utilized different methods and follow-up periods. For the determination of patency, methods varied from circumference measurement to volumetry, lower extremity lymphedema (LEL) index, or lymphoscintigraphy. Thus, a direct comparison between the studies appears to be challenging. Yet, objective and subjective results are indicating a place in the treatment of secondary lymphedema especially when conservative therapy is failing.
Vascularized lymph node transfer Vascularized lymph node transfer represents a relatively novel method where a transfer into regions with dissected lymph nodes (e.g., cancer treatment) or into distal regions of limbs with lymphedema is performed to reestablish lymphatic drainage function [24]. Starting in animal studies, vascularized lymph node transfer showed a complete preservation of the original histological structures [25] in contrast to what has been seen in a vascularized lymph node transfers [26,27]. First attempts in clinical studies in 1982 showed a stable reduction of lymphedema after transferring inguinal lymph nodes to the contralateral inguinal region [28]. Similar results have been reported for the upper extremity with a transfer either into the axillary region [29] or into the wrist area [30]. In general, all studies performed on vascularized lymph node transfer showed favorable outcomes for the patients after surgery including reduction of lymphedematous limb volumes, infections, and improved quality of life [31–34]. Lymph node flap harvest is performed from different areas of the donor including groin,
Conclusion
159
submental, supraclavicular, lateral thoracic, gastroepiploic, jejunal, appendicular, and ileocecal with no general ideal recommendation until now. For better outcomes, lymph nodes may be transferred with a skin paddle containing lymph capillaries, thus facilitating recanalization of the lymphatic system [24]. It has to be noted that only few long-term results are available for vascularized lymph node transfers until now. Moreover, the interaction between transferred lymph node and the lymphatic system in the recipient area still needs to be elucidated. In addition, the risk of causing lymphedema in the region of the donor lymph node might be heightened [35–37]. Despite the promising technique, additional excisional procedures are recommended after vascularized lymph node transfers in patients suffering from secondary lymphedema.
Lympholymphatic graft In contrast to lymphaticovenular anastomosis and vascularized lymph node transfer, only few studies have been conducted evaluating lymphatic grafts in lymphedema treatment. First attempts of harvesting autologous lymphatic grafts to bypass damaged lymphatic vessels resulted in not only volume reduction of 80% but also high risk of donor site morbidity [38]. The bypass should be carried out prior permanent damage of the remainder lymphatic vessels due to back pressure or infection [39]. Alternatively, vein grafts have been used in patients with chronic lymphedema to obtain a lymphatic-venous-lymphatic bypass [15,16] with the result of improvement of both limb function and edema. Most recent studies aimed to develop tissue-engineered grafts to reestablish lymphatic circulation [40], and first studies under culturing conditions offered promising results for future clinical application and as a potential new treatment option for secondary lymphedema [41].
Conclusion Nevertheless, until now, and despite the promising results regarding the surgical approaches of lymphatic reconstruction, it has to be noted that lymphatic reconstruction is still a palliative
160
8. Lymphatic reconstruction
procedure. The creation of a bypass system for lymphatic system offers no elimination of the etiologic factor; thus, obstructions or destructions of the lymphatic vessel and infections leading to decreased transport capacity of lymphatic fluid are still present. In addition to that, in most cases, conservative therapy is still required even though surgical reconstruction was performed. Further improvement of the surgical techniques and a consensus in standardized protocols and reporting of outcome is finally needed to enhance and consolidate lymphatic reconstruction in secondary lymphedema.
References [1] Kung TA, Champaneria MC, et al. Current concepts in the surgical Management of Lymphedema. Plast Reconstr Surg 2017;139(4). [2] Ozturk CN, Ozturk C, et al. Free vascularized lymph node transfer for treatment of lymphedema: a systematic evidence based review. J Plast Reconstr Aesthet Surg 2016;69(9):1234–47. [3] Campisi C, Boccardo F. Frontiers in lymphatic microsurgery. Microsurgery 1998;18(8):462–71. [4] Becker C, Vasile JV, et al. Microlymphatic surgery for the treatment of iatrogenic lymphedema. Clin Plast Surg 2012;39(4):385–98. [5] Boccardo F, Fulcheri E, et al. Lymphatic microsurgery to treat lymphedema: techniques and indications for better results. Ann Plast Surg 2013;71(2):191–5. [6] Nielubowicz J, Olszewski W. Surgical lymphaticovenous shunts in patients with secondary lymphoedema. Br J Surg 1968;55(6):440–2. [7] Olszewski WL. Episodic dermatolymphangioadenitis (DLA) in patients with lymphedema of the lower extremities before and after administration of benzathine penicillin: a preliminary study. Lymphology 1996;29(3):126–31. [8] Olszewski WL. Contractility patterns of human leg lymphatics in various stages of obstructive lymphedema. Ann N Y Acad Sci 2008;010. [9] Olszewski WL, Engeset A, et al. Lymph flow and protein in the normal male leg during lying, getting up, and walking. Lymphology 1977;10(3):178–83. [10] Jacobson II JH, Suarez EL. Microvascular surgery. Dis Chest 1962;41:220–4. [11] Koshima I, Inagawa K, et al. Supermicrosurgical lymphaticovenular anastomosis for the treatment of lymphedema in the upper extremities. J Reconstr Microsurg 2000;16(6):437–42. [12] Winters H, Tielemans HJP, et al. The efficacy of lymphaticovenular anastomosis in breast cancer-related lymphedema. Breast Cancer Res Treat 2017;165(2):321–7. [13] Campisi C, Bellini C, et al. Microsurgery for lymphedema: clinical research and long-term results. Microsurgery 2010;30(4):256–60.
References
161
[14] Demirtas Y, Ozturk N, et al. Supermicrosurgical lymphaticovenular anastomosis and lymphaticovenous implantation for treatment of unilateral lower extremity lymphedema. Microsurgery 2009;29(8):609–18. [15] Campisi C, Boccardo F, et al. Long-term results after lymphatic-venous anastomoses for the treatment of obstructive lymphedema. Microsurgery 2001;21(4):135–9. [16] Campisi C, Boccardo F, et al. The use of vein grafts in the treatment of peripheral lymphedemas: long-term results. Microsurgery 2001;21(4):143–7. [17] Olszewski WL. The treatment of lymphedema of the extremities with microsurgical lympho-venous anastomoses. Int Angiol 1988;7(4):312–21. [18] O’Brien BM, Mellow CG, et al. Long-term results after microlymphaticovenous anastomoses for the treatment of obstructive lymphedema. Plast Reconstr Surg 1990;85(4):562–72. [19] O’Brien BM, Shafiroff BB. Microlymphaticovenous and resectional surgery in obstructive lymphedema. World J Surg 1979;3(1):3–15. [20] Koshima I, Nanba Y, et al. Long-term follow-up after lymphaticovenular anastomosis for lymphedema in the leg. J Reconstr Microsurg 2003;19(4):209–15. [21] Maegawa J, Yabuki Y, et al. Outcomes of lymphaticovenous side-to-end anastomosis in peripheral lymphedema. J Vasc Surg 2012;55(3):753–60. [22] Yamamoto T, Yoshimatsu H, et al. Side-to-end lymphaticovenular anastomosis through temporary lymphatic expansion. PLoS One 2013;8(3):25. [23] Cornelissen AJM, Kool M, et al. Lymphatico-venous anastomosis as treatment for breast cancer-related lymphedema: a prospective study on quality of life. Breast Cancer Res Treat 2017;163(2):281–6. [24] Ito R, Suami H. Overview of lymph node transfer for lymphedema treatment. Plast Reconstr Surg 2014;134(3):548–56. [25] Shesol BF, Nakashima R, et al. Successful lymph node transplantation in rats, with restoration of lymphatic function. Plast Reconstr Surg 1979;63(6):817–23. [26] Jaffe HL, Richter MN. The regeneration of autoplastic lymph node transplants. J Exp Med 1928;47(6):977–80. [27] Tobbia D, Semple J, et al. Experimental assessment of autologous lymph node transplantation as treatment of postsurgical lymphedema. Plast Reconstr Surg 2009;124(3):777–86. [28] Clodius L, Smith PJ, et al. The lymphatics of the groin flap. Ann Plast Surg 1982;9(6):447–58. [29] Becker C, Assouad J, et al. Postmastectomy lymphedema: long-term results following microsurgical lymph node transplantation. Ann Surg 2006;243(3):313–5. [30] Lin CH, Ali R, et al. Vascularized groin lymph node transfer using the wrist as a recipient site for management of postmastectomy upper extremity lymphedema. Plast Reconstr Surg 2009;123(4):1265–75. [31] Cheng MH, Huang JJ, et al. A novel approach to the treatment of lower extremity lymphedema by transferring a vascularized submental lymph node flap to the ankle. Gynecol Oncol 2012;126(1):93–8. [32] Ciudad P, Maruccia M, et al. The laparoscopic right gastroepiploic lymph node flap transfer for upper and lower limb lymphedema: technique and outcomes. Microsurgery 2017;37(3):197–205.
162
8. Lymphatic reconstruction
[33] De Brucker B, Zeltzer A, et al. Breast Cancer-related lymphedema: quality of life after lymph node transfer. Plast Reconstr Surg 2016;137(6):1673–80. [34] Gratzon A, Schultz J, et al. Clinical and psychosocial outcomes of vascularized lymph node transfer for the treatment of upper extremity lymphedema after breast Cancer therapy. Ann Surg Oncol 2017;24(6):1475–81. [35] Pons G, Masia J, et al. A case of donor-site lymphoedema after lymph nodesuperficial circumflex iliac artery perforator flap transfer. J Plast Reconstr Aesthet Surg 2014;67(1):119–23. [36] Sulo E, Hartiala P, et al. Risk of donor-site lymphatic vessel dysfunction after microvascular lymph node transfer. J Plast Reconstr Aesthet Surg 2015;68(4):551–8. [37] Viitanen TP, Maki MT, et al. Donor-site lymphatic function after microvascular lymph node transfer. Plast Reconstr Surg 2012;130(6):1246–53. [38] Baumeister RG, Siuda S. Treatment of lymphedemas by microsurgical lymphatic grafting: what is proved? Plast Reconstr Surg 1990;85(1):64–74. [39] Ho LC, Lai MF, et al. Microlymphatic bypass in obstructive lymphoedema. Br J Plast Surg 1988;41(5):475–84. [40] Kanapathy M, Patel NM, et al. Tissue-engineered lymphatic graft for the treatment of lymphedema. J Surg Res 2014;192(2):544–54. [41] Kanapathy M, Kalaskar D, et al. Development of a tissue-engineered lymphatic graft using nanocomposite polymer for the treatment of secondary lymphedema. Artif Organs 2016;40(3):30.