Volume 133, Number 6 • Letters Anuja K. Antony, M.D., M.P.H.
Division of Plastic Surgery University of Illinois at Chicago Hospital and Health Sciences System 820 South Wood Street, CSN 515 Chicago, Ill. 60601 [email protected]
DISCLOSURE The author has no financial interest to declare in relation to the content of this communication.
A Prospective Analysis of 100 Consecutive Lymphovenous Bypass Cases for Treatment of Extremity Lymphedema Sir:
W
e read with great interest the article entitled “A Prospective Analysis of 100 Consecutive Lymphovenous Bypass Cases for Treatment of Extremity Lymphedema” by Chang et al. (Plast Reconstr Surg. 2013;132:1305–1314).1 First, we would like to congratulate them on their successful results of supermicrosurgical lymphaticovenular anastomosis with preoperative indocyanine green lymphography for the treatment of extremity lymphedema. Although supermicrosurgical lymphaticovenular anastomosis is mostly performed in Japan, especially in our institution, their work proved that supermicrosurgical lymphaticovenular anastomosis could be successfully performed not only in Japan but also in the United States. Based on our experience of indocyanine green lymphography and lymphaticovenular anastomosis on more than 1000 cases, we would like to comment about their method of indocyanine green lymphography. The authors reported a new severity staging system based on early-phase findings of indocyanine green lymphography. Their staging system is based on visibility of linear pattern and extension of dermal backflow pattern. We used to use a similar staging system that is determined based on extension of dermal backflow pattern, but abandoned it and developed a modified staging system called dermal backflow stage.2,3 In dermal backflow stage, not only extension of dermal backflow pattern but also differences of dermal backflow patterns are taken into consideration. Dermal backflow patterns are classified into three patterns: splash, stardust, and diffuse. With lymphedema progression, indocyanine green lymphographic findings change from normal linear pattern, to splash (mild dermal backflow), to stardust (moderate dermal backflow), and finally to diffuse (severe dermal backflow) pattern (Fig. 1). As our experience of lymphaticovenular anastomosis and indocyanine green lymphography accumulated, we have recognized that differentiation of dermal backflow pattern is the most important in indocyanine green lymphography. As indocyanine green lymphographic findings progress, lymphatic vessels become smaller and sclerotic, and
Fig. 1. Indocyanine green lymphographic findings and lymphedema progression. Indocyanine green lymphographic pattern changes from normal linear pattern to abnormal dermal backflow patterns in obstructive lymphedema; dermal backflow patterns change from splash pattern, to stardust pattern, and finally to diffuse pattern with progression of lymphedema. Lymph flow obstruction results in lymphatic hypertension, lymphatic vessel dilatation, lymphatic valve insufficiency, sclerosis of lymphatic vessels, and lymph backflow. Indocyanine green lymphography visualizes lymph backflow as dermal backflow patterns. The splash pattern represents dilated superficial lymphatics. The stardust pattern represents lymph fluid extravasation; extravasated lymph is shown as spots on indocyanine green lymphography. Finally, the number of spots visualized on indocyanine green lymphography increases to the point where spots merge and cannot be distinguished from each other (diffuse pattern).
Fig. 2. Early-phase and late-phase images of dermal backflow pattern on indocyanine green lymphography. Lymph dermal backflow is shown as the reticular pattern at an early transient phase of indocyanine green lymphography. The reticular pattern will change to splash, stardust, or diffuse pattern at a late plateau phase.
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Plastic and Reconstructive Surgery • June 2014 the success rate of lymphaticovenular anastomoses deteriorates.4 It is not difficult for a surgeon experienced in performing lymphatic supermicrosurgery to find a lymphatic vessel in obstructive lymphedema cases, because the location of lymphatic vessels suitable for lymphaticovenular anastomosis is anatomically invariable; lymphatic vessels can be found along the greater saphenous vein or the cephalic vein by means of a 2- to 3-cm skin incision. However, it is difficult to predict the condition of lymphatic vessels (whether the vessel is suitable for lymphaticovenular anastomosis or not); thus, differentiation of dermal backflow pattern is very helpful for predicting the condition of lymphatic vessels—linear, splash patterns are good and the stardust pattern is acceptable, but the diffuse pattern is not appropriate for lymphaticovenular anastomosis.4 When a lymphedematous limb shows extensive diffuse pattern on indocyanine green lymphography, vascularized lymph node transfer is better indicated than lymphaticovenular anastomosis. To differentiate dermal backflow patterns, indocyanine green lymphographic findings should be evaluated not at an early transient phase but at a late plateau phase (2 or more hours after injection)2,3,5 (Fig. 2). Thus, we perform indocyanine green lymphography as follows: an examinee is kept still for 5 minutes after indocyanine green injection, and indocyanine green velocity measurement and lymphatic mapping are performed (early phase); then, the examinee is allowed to move freely, and dermal backflow stage is determined 2 or more hours later (late phase).5 This dual-phase or dynamic indocyanine green lymphography allows not only preoperative lymph mapping but also evaluation of lymph pump function (indocyanine green velocity) and lymph circulation (dermal backflow stage) by one injection. DOI: 10.1097/PRS.0000000000000189
Takumi Yamamoto, M.D. Isao Koshima, M.D. Department of Plastic and Reconstructive Surgery Graduate School of Medicine University of Tokyo Tokyo, Japan Correspondence to Dr. Yamamoto Department of Plastic and Reconstructive Surgery University of Tokyo 7-3-1 Hongo Bunkyo-ku, Tokyo 113-8655, Japan [email protected]
DISCLOSURE The authors have no financial interest to declare in relation to the content of this communication. REFERENCES 1. Chang DW, Suami H, Skoracki R. A prospective analysis of 100 consecutive lymphovenous bypass cases for treatment of extremity lymphedema. Plast Reconstr Surg. 2013;132: 1305–1314.
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2. Yamamoto T, Matsuda N, Doi K, et al. The earliest finding of indocyanine green lymphography in asymptomatic limbs of lower extremity lymphedema patients secondary to cancer treatment: The modified dermal backflow stage and concept of subclinical lymphedema. Plast Reconstr Surg. 2011;128:314e–321e. 3. Yamamoto T, Yamamoto N, Doi K, et al. Indocyanine greenenhanced lymphography for upper extremity lymphedema: A novel severity staging system using dermal backflow patterns. Plast Reconstr Surg. 2011;128:941–947. 4. Yamamoto T, Yamamoto N, Narushima M, et al. Lymphaticovenular anastomosis with guidance of ICG lymphography. J Jpn Coll Angiol. 2012;52:327–331. 5. Yamamoto T, Narushima M, Yoshimatsu H, et al. Indocyanine green velocity: Lymph transportation capacity deterioration with progression of lymphedema. Ann Plast Surg. 2013;71:591–594.
Reply: A Prospective Analysis of 100 Consecutive Lymphovenous Bypass Cases for Treatment of Extremity Lymphedema Sir:
We would like to thank Drs. Yamamoto and Koshima for their insightful comments. We agree that what is critically important is to precisely identify functioning lymphatic vessels for lymphovenous bypass. We are aware that the lymphatic vessels do run along the great saphenous and cephalic vein; these are called the median or medial bundle.1 However, these lymphatic vessels are not always detected during indocyanine green lymphography, meaning that they are not always functional in certain lymphedema patients. We speculate that in these patients the associated lymph nodes or the proximal portion of the medial lymphatic bundle were excised or damaged during the axillary or inguinal dissection. Thus, just relying on our knowledge of lymphatic anatomy alone is not sufficient for identifying optimal lymphatic vessels for bypass. We have found that the best way to identify functioning lymphatic vessels for lymphovenous bypass is to perform indocyanine green fluorescence lymphography and mapping of the functioning lymphatic vessels just before surgery. As soon as the indocyanine green is injected, fluorescent images of the functioning lymphatic vessels can be visualized using a Hamamatsu Photodynamic Eye (Hamamatsu Photonics, Hamamatsu, Japan), and the mapping is performed on the skin surface immediately. As time passes, even after just 10 to 15 minutes, indocyanine green dye refluxes into the superficial and subdermal lymphatics of the limb, creating the various patterns of dermal backflow, as described by Drs. Yamamoto and Koshima. Once this occurs, the linear patterns of functioning lymphatic vessels often are no longer visible, as they are overshadowed by dermal backflow. We agree with Drs. Yamamoto and Koshima that the type of dermal backflow is important for staging, but we have found in our experience that the quality and the quantity of functioning lymphatic vessels identified by indocyanine green fluorescence lymphography just before surgery not only facilitate the operation
Division of Plastic Surgery University of Illinois at Chicago Hospital and Health Sciences System 820 South Wood Street, CSN 515 Chicago, Ill. 60601 [email protected]
DISCLOSURE The author has no financial interest to declare in relation to the content of this communication.
A Prospective Analysis of 100 Consecutive Lymphovenous Bypass Cases for Treatment of Extremity Lymphedema Sir:
W
e read with great interest the article entitled “A Prospective Analysis of 100 Consecutive Lymphovenous Bypass Cases for Treatment of Extremity Lymphedema” by Chang et al. (Plast Reconstr Surg. 2013;132:1305–1314).1 First, we would like to congratulate them on their successful results of supermicrosurgical lymphaticovenular anastomosis with preoperative indocyanine green lymphography for the treatment of extremity lymphedema. Although supermicrosurgical lymphaticovenular anastomosis is mostly performed in Japan, especially in our institution, their work proved that supermicrosurgical lymphaticovenular anastomosis could be successfully performed not only in Japan but also in the United States. Based on our experience of indocyanine green lymphography and lymphaticovenular anastomosis on more than 1000 cases, we would like to comment about their method of indocyanine green lymphography. The authors reported a new severity staging system based on early-phase findings of indocyanine green lymphography. Their staging system is based on visibility of linear pattern and extension of dermal backflow pattern. We used to use a similar staging system that is determined based on extension of dermal backflow pattern, but abandoned it and developed a modified staging system called dermal backflow stage.2,3 In dermal backflow stage, not only extension of dermal backflow pattern but also differences of dermal backflow patterns are taken into consideration. Dermal backflow patterns are classified into three patterns: splash, stardust, and diffuse. With lymphedema progression, indocyanine green lymphographic findings change from normal linear pattern, to splash (mild dermal backflow), to stardust (moderate dermal backflow), and finally to diffuse (severe dermal backflow) pattern (Fig. 1). As our experience of lymphaticovenular anastomosis and indocyanine green lymphography accumulated, we have recognized that differentiation of dermal backflow pattern is the most important in indocyanine green lymphography. As indocyanine green lymphographic findings progress, lymphatic vessels become smaller and sclerotic, and
Fig. 1. Indocyanine green lymphographic findings and lymphedema progression. Indocyanine green lymphographic pattern changes from normal linear pattern to abnormal dermal backflow patterns in obstructive lymphedema; dermal backflow patterns change from splash pattern, to stardust pattern, and finally to diffuse pattern with progression of lymphedema. Lymph flow obstruction results in lymphatic hypertension, lymphatic vessel dilatation, lymphatic valve insufficiency, sclerosis of lymphatic vessels, and lymph backflow. Indocyanine green lymphography visualizes lymph backflow as dermal backflow patterns. The splash pattern represents dilated superficial lymphatics. The stardust pattern represents lymph fluid extravasation; extravasated lymph is shown as spots on indocyanine green lymphography. Finally, the number of spots visualized on indocyanine green lymphography increases to the point where spots merge and cannot be distinguished from each other (diffuse pattern).
Fig. 2. Early-phase and late-phase images of dermal backflow pattern on indocyanine green lymphography. Lymph dermal backflow is shown as the reticular pattern at an early transient phase of indocyanine green lymphography. The reticular pattern will change to splash, stardust, or diffuse pattern at a late plateau phase.
887e
Plastic and Reconstructive Surgery • June 2014 the success rate of lymphaticovenular anastomoses deteriorates.4 It is not difficult for a surgeon experienced in performing lymphatic supermicrosurgery to find a lymphatic vessel in obstructive lymphedema cases, because the location of lymphatic vessels suitable for lymphaticovenular anastomosis is anatomically invariable; lymphatic vessels can be found along the greater saphenous vein or the cephalic vein by means of a 2- to 3-cm skin incision. However, it is difficult to predict the condition of lymphatic vessels (whether the vessel is suitable for lymphaticovenular anastomosis or not); thus, differentiation of dermal backflow pattern is very helpful for predicting the condition of lymphatic vessels—linear, splash patterns are good and the stardust pattern is acceptable, but the diffuse pattern is not appropriate for lymphaticovenular anastomosis.4 When a lymphedematous limb shows extensive diffuse pattern on indocyanine green lymphography, vascularized lymph node transfer is better indicated than lymphaticovenular anastomosis. To differentiate dermal backflow patterns, indocyanine green lymphographic findings should be evaluated not at an early transient phase but at a late plateau phase (2 or more hours after injection)2,3,5 (Fig. 2). Thus, we perform indocyanine green lymphography as follows: an examinee is kept still for 5 minutes after indocyanine green injection, and indocyanine green velocity measurement and lymphatic mapping are performed (early phase); then, the examinee is allowed to move freely, and dermal backflow stage is determined 2 or more hours later (late phase).5 This dual-phase or dynamic indocyanine green lymphography allows not only preoperative lymph mapping but also evaluation of lymph pump function (indocyanine green velocity) and lymph circulation (dermal backflow stage) by one injection. DOI: 10.1097/PRS.0000000000000189
Takumi Yamamoto, M.D. Isao Koshima, M.D. Department of Plastic and Reconstructive Surgery Graduate School of Medicine University of Tokyo Tokyo, Japan Correspondence to Dr. Yamamoto Department of Plastic and Reconstructive Surgery University of Tokyo 7-3-1 Hongo Bunkyo-ku, Tokyo 113-8655, Japan [email protected]
DISCLOSURE The authors have no financial interest to declare in relation to the content of this communication. REFERENCES 1. Chang DW, Suami H, Skoracki R. A prospective analysis of 100 consecutive lymphovenous bypass cases for treatment of extremity lymphedema. Plast Reconstr Surg. 2013;132: 1305–1314.
888e
2. Yamamoto T, Matsuda N, Doi K, et al. The earliest finding of indocyanine green lymphography in asymptomatic limbs of lower extremity lymphedema patients secondary to cancer treatment: The modified dermal backflow stage and concept of subclinical lymphedema. Plast Reconstr Surg. 2011;128:314e–321e. 3. Yamamoto T, Yamamoto N, Doi K, et al. Indocyanine greenenhanced lymphography for upper extremity lymphedema: A novel severity staging system using dermal backflow patterns. Plast Reconstr Surg. 2011;128:941–947. 4. Yamamoto T, Yamamoto N, Narushima M, et al. Lymphaticovenular anastomosis with guidance of ICG lymphography. J Jpn Coll Angiol. 2012;52:327–331. 5. Yamamoto T, Narushima M, Yoshimatsu H, et al. Indocyanine green velocity: Lymph transportation capacity deterioration with progression of lymphedema. Ann Plast Surg. 2013;71:591–594.
Reply: A Prospective Analysis of 100 Consecutive Lymphovenous Bypass Cases for Treatment of Extremity Lymphedema Sir:
We would like to thank Drs. Yamamoto and Koshima for their insightful comments. We agree that what is critically important is to precisely identify functioning lymphatic vessels for lymphovenous bypass. We are aware that the lymphatic vessels do run along the great saphenous and cephalic vein; these are called the median or medial bundle.1 However, these lymphatic vessels are not always detected during indocyanine green lymphography, meaning that they are not always functional in certain lymphedema patients. We speculate that in these patients the associated lymph nodes or the proximal portion of the medial lymphatic bundle were excised or damaged during the axillary or inguinal dissection. Thus, just relying on our knowledge of lymphatic anatomy alone is not sufficient for identifying optimal lymphatic vessels for bypass. We have found that the best way to identify functioning lymphatic vessels for lymphovenous bypass is to perform indocyanine green fluorescence lymphography and mapping of the functioning lymphatic vessels just before surgery. As soon as the indocyanine green is injected, fluorescent images of the functioning lymphatic vessels can be visualized using a Hamamatsu Photodynamic Eye (Hamamatsu Photonics, Hamamatsu, Japan), and the mapping is performed on the skin surface immediately. As time passes, even after just 10 to 15 minutes, indocyanine green dye refluxes into the superficial and subdermal lymphatics of the limb, creating the various patterns of dermal backflow, as described by Drs. Yamamoto and Koshima. Once this occurs, the linear patterns of functioning lymphatic vessels often are no longer visible, as they are overshadowed by dermal backflow. We agree with Drs. Yamamoto and Koshima that the type of dermal backflow is important for staging, but we have found in our experience that the quality and the quantity of functioning lymphatic vessels identified by indocyanine green fluorescence lymphography just before surgery not only facilitate the operation
