Keywords
lymph - lymphedema - microsurgery - SCIP flap - lymphatic pattern
The lymphatic system comprises lymphatic organs and vessels which play vital roles in maintaining tissue fluid balance, macromolecule transport, and fat absorption from the intestine, and assists the immune system in ensuring adaptive immune protection and immune surveillance.[1]
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[4] Impaired lymphatic function can lead to lymphedema, a chronic condition characterized by a weakened immune response, fluid accumulation, tissue swelling, and fibroadipose deposition.[2]
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To date, lymphedema has no definitive cure, but many treatments can improve symptoms and quality of life of patients. These techniques are divided into conservative and surgical approaches.[8] Surgical procedures can be classified into two categories: excisional and physiological. Excisional procedures primarily involve tissue volume reduction and the enhancement of aesthetic outcomes, while physiological procedures focus on restoring or reconstructing the natural lymph fluid drainage system.[9]
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Currently, in lymphatic reconstructive surgeries, lymphovenous anastomosis (LVA)[18] and vascularized lymph node transfer (VLNT)[19] are the most valuable surgical options. However, both procedures have several drawbacks: LVA requires supermicrosurgical techniques and healthy, actively contractile lymphatic vessels. Vascularized lymph node transfer entails a potential risk of donor-site lymphedema, and functional lymph node transfer is not consistently feasible.[16]
In recent years, a novel concept, known as lymph-interposition-flap transfer (LIFT), has emerged.[17]
[20] This technique involves the reconstruction of lymphatic pathways by utilizing a flap that includes lymph vessels, but without the need for lymph node transfer or supermicrosurgical lymphatic anastomosis. This underscores its potential in both the treatment and prevention of lymphedema.[17]
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The primary determinant for successful lymph flow restoration is the preservation of lymph axiality and the potential to bridge regions with robust lymphatic transport capacity. In theory, any flap containing deep adipose tissue can be employed for LIFT.[23]
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[25] However, the superficial circumflex iliac artery perforator (SCIP) flap is particularly advantageous as it resides in an area devoid of dominant lymphatic pathways and links to the superficial epigastric lymph nodes. By utilizing this flap, the risk of donor-site lymphedema is minimized, even in the absence of incorporated lymph nodes.[26]
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[33] The aim of this study was to describe the superficial lymphatic vessel anatomy within the SCIP flap zone by using indocyanine green (ICG) lymphography to facilitate the understanding of lymphatic flow and its application as an interpositional flap.
Methods
After obtaining approval from the institutional review board, this cross-sectional study was conducted between September 2022 and November 2022 at Hospital de la Santa Creu i Sant Pau (Barcelona, Spain) and Helsinki University Hospital H.U.S. (Helsinki, Finland).
This multicenter investigation aimed at evaluating and defining superficial lymphatic patterns within the vascular territory of the SCIP flap in a cohort of 19 healthy volunteers of both sexes. Standardized procedures were implemented for all participants in both hospitals.
The study population comprised only individuals aged ≥18 years. Individuals were excluded for the following reasons: pregnancy, history of previous superficial abdominal or inguinal surgeries, or any signs or symptoms of lymphedema. Before the study's commencement, written informed consent was obtained from all participants. Comprehensive demographic information, medical history, and thorough physical examinations were documented. ICG lymphography was employed to evaluate the superficial lymphatic channels and to establish the lymphatic drainage patterns specific to the SCIP area. Despite the inherent limitation of ICG, with a visualization depth restricted to 1.5 mm, it proved adequate for discerning superficial lymphatic vessels in the SCIP area. For each volunteer, a digital video camera equipped with an infrared filter was used to capture and record the ICG contrast (25 mg; Verdye; Diagnostic Green Limited, Westmeath, Ireland). Throughout the study, adverse reactions, if any, were closely monitored.
ICG lymphography entails the subcutaneous administration of ICG, a water-soluble cyanine dye, diluted in a vial containing 2.5 mg/mL of contrast mixed with 5 mL of 10% glucose saline solution. A total volume of 1.2 mL of the diluted solution was injected subcutaneously on the right and left sides (0.6 mL on each side) at three distinct points spaced 6 cm apart (0.2 mL per point). The first injection point was at the level of the iliac crest, the second point was 3 cm above, and the third point was 3 cm below the initial injection site. After injection, the transport of the contrast agent was recorded at three-time points using an infrared camera (Fluobeam [Fluoptics, Grenoble, France][34] and EleVision IR Platform [Medtronic, Minneapolis, MN][35]): 4 minutes (i.e., the early transient phase), 14 minutes (i.e., the plateau phase), and 24 minutes (i.e., the late plateau phase). Several parameters were assessed to qualitatively evaluate the superficial lymphatic patterns, including assessment of the number of lymphatic vessels, their direction, length, and the presence of a normal linear pattern. Both sides SCIP territories were analyzed.
Results
Characteristics of Study Participants
Nineteen healthy volunteers were enrolled in this study. However, four volunteers were excluded because of their medical history, thus 15 individuals were included in the final analysis of the data. Among the analyzed volunteers, 12 were women and 3 were men. The body mass index of the individuals was 23.6 (range, 20.2–27). The mean age was 40.5 years (range, 30–50 years). No adverse reactions occurred after the administration of the ICG in any of the volunteers, all of whom tolerated the procedure well. The analysis of results was stratified for both SCIP sides, based on the hypothesis of possible distinctions in the lymphatic anatomy between both sides, whether in terms of quantity and/or distribution. [Tables 1] and [2] summarize the properties of the right and left sides of the SCIP flap zone.
Table 1
Summary of the results of the SCIP flap zone on the right side
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Linear pattern
(number volunteers [%])
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Median count of lymphatic vessels
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Direction
(number volunteers [%])
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Mean length
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4 minutes
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12 (80%)
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1
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Toward ILN (100%)
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2.8 cm
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Opposite to ILN (0.0%)
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14 minutes
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2
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Toward ILN (100%)
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3.76 cm
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Opposite to ILN (0.0%)
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24 minutes
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3
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Toward ILN (100%)
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5.24 cm
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Opposite to ILN (0.0%)
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Abbreviations: ILN, inguinal lymph node; SCIP, superficial circumflex iliac artery perforator.
Table 2
Summary of the results of the SCIP flap zone on the left side
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Linear pattern
(number volunteers [%])
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Median count of lymphatic vessels
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Direction
(number volunteers [%])
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Mean length
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4 minutes
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11 (73.3%)
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1
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Toward ILN (86.7%)
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2.9 cm
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Opposite to ILN (13.3%)
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14 minutes
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1
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Toward ILN (86.7%)
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3.9 cm
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Opposite to ILN (13.3%)
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24 minutes
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2
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Toward ILN (86.7%)
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5.5 cm
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Opposite to ILN (13.3%)
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Abbreviations: ILN, inguinal lymph node; SCIP, superficial circumflex iliac artery perforator.
(1) Four minutes: the early transient phase on both SCIP sides ([Figs. 1] and [2]).
Fig. 1 Results of contrast agent transport at 4 minutes in the early transient phase on the right side. ICG lymphography shows the dye inoculation points (red asterisks) and lymphatic vessels (red arrowheads). The images on the left represent the ICG visualization in the color-fused and green overlay modes. ICG, indocyanine green.
Fig. 2 Results of contrast agent transport at 4 minutes in the early transient phase on the left side. ICG lymphography shows the dye inoculation points (red asterisks) and lymphatic vessels (red arrowheads). The images on the left represent ICG visualization in the color-fused and green overlay modes. ICG, indocyanine green.
On both sides, the vessels of 12 participants displayed a normal linear pattern, whereas the vessels of the remaining three participants did not exhibit this pattern. The median count of lymphatic vessels observed per individual was one on each side (range, 1). All lymphatic vessels observed in the 15 volunteers exhibited a trajectory toward the inguinal lymph node (ILN) on both sides, except for one of the volunteers, in which the lymphatic vessel on the left side was oriented opposite to the ILN. The mean lengths of the lymphatic vessels on the right and left sides were 2.8 and 2.9 cm, respectively.
(2) Fourteen minutes: the plateau phase in both SCIP sides ([Figs. 3] and [4]).
Fig. 3 Results of contrast agent transport at 14 minutes in the late plateau phase on the right side. ICG lymphography shows dye inoculation points (red asterisks) and lymphatic vessels (red arrowheads). The images on the left represent the ICG visualization in the color-fused and green overlay modes. ICG, indocyanine green.
Fig. 4 Results of contrast agent transport at 14 minutes in the late plateau phase on the left side. ICG lymphography shows the dye inoculation points (red asterisk) and lymphatic vessels (red arrowheads). The images on the left represent the ICG visualization in the color-fused and green overlay modes. ICG, indocyanine green.
The median count of observed lymphatic vessels per individual on the right side was two vessels (range, 1–2), whereas on the left side, only one was observed (range, 1). The directional distribution of the lymphatic vessels was predominantly toward the ILN in all 15 volunteers, whereas one volunteer presented the left side lymphatic vessel oriented in the opposite direction to the ILN. Furthermore, the computed mean lengths of the lymphatic vessels on the right and left sides were 3.76 and 3.9 cm, respectively.
(3) Twenty-four minutes: the late plateau phase on both SCIP sides ([Figs. 5] and [6])..
Fig. 5 Results of contrast agent transport at 24 minutes in the late plateau phase on the right side. ICG lymphography shows the dye inoculation points (red asterisk) and lymphatic vessels (red arrow). The images on the left represent the ICG visualization in the color-fused and green overlay modes. ICG, indocyanine green.
Fig. 6 Results of contrast agent transport at 24 minutes in the late plateau phase on the left side. ICG lymphography shows the dye inoculation points (red asterisks) and lymphatic vessels (red arrowheads). The images on the left represent the ICG visualization in the color-fused and green overlay modes. ICG, indocyanine green.
The median count of observed lymphatic vessels per individual on the right side was three vessels (range, 1–3), and the count on the left side was two vessels (range, 1–2). All lymphatic vessels observed at this stage were oriented toward the ILN in all 15 volunteers, except for one participant in which the left-side lymphatic vessels were oriented in the opposite direction to the ILN. Furthermore, the calculated mean length of the lymphatic vessels on the right and left sides were 5.24 and 5.5 cm, respectively.
The results indicated that the predominant lymphatic pattern observed in the SCIP flap involved lymphatic vessels directed toward the ILN ([Fig. 7]). No lymphatic vessels were observed oriented away from the ILN; however, such patterns were noted only in one volunteer on the left side ([Fig. 8]). The number of lymphatic vessels and their length increased with time bilaterally ([Figs. 9] and [10]). Most patients had a predominantly unidirectional and favorable flow pattern within the lymphatic system.
Fig. 7 Lymphatic pattern toward the ILN on the right side. ICG lymphography shows the dye inoculation points (red asterisks) and lymphatic vessels at 14 minutes (red arrowheads). ICG, indocyanine green.
Fig. 8 Lymphatic pattern observed in the opposite direction to the ILN on the left side. ICG lymphography shows the dye inoculation points (red asterisks) and lymphatic vessels at 14 minutes (red arrowheads). ICG, indocyanine green.
Fig. 9 Temporal variation in the mean length of lymphatic vessels on the right and left sides. The figure presents the mean length of the lymphatic vessels on the right and left sides across different time intervals, which reflects the temporal dynamics of these measurements. ICG, indocyanine green.
Fig. 10 Median count of lymphatic vessels per individual on the right and left sides over time. The figure presents the median counts of observed lymphatic vessels per individual on the right and left sides across different time intervals, which illustrates variations in vessel counts over time. ICG, indocyanine green.
Discussion
The LIFT technique is a corrective physiological procedure employed in lymphatic surgery, in which lymphatic reconstruction is achieved by utilizing a flap that includes superficial lymph vessels in the cutaneous island.[17]
[21] Unlike other techniques such as VLNT[19] or supermicrosurgical LVA,[36] LIFT does not involve the transfer of lymph nodes or the performance of intricate lymphatic anastomoses. Any flap containing subcutaneous fat could theoretically be used for LIFT.[17]
[21] However, the SCIP flap is particularly advantageous as it is situated in an area devoid of major lymphatic pathways. Lymph axiality plays a crucial role in facilitating lymph flow restoration, thereby making it a significant factor to consider in achieving successful outcomes in lymphatic surgery.[25] In the context of VLNT procedures, the primary objective is to establish a novel lymphatic afferent pathway to a specific lymph node. This procedure aims to enhance the lymphatic circulation and to mitigate swelling in the affected region, thereby enhancing the quality of life of the patient. Lymph node transfer is typically performed as a component of vascularized tissue transfer, commonly involving a tissue flap containing arteries, veins, and lymphatic vessels, which is surgically connected to the affected area to provide functional lymphatic flow. The SCIP flap has been effectively utilized for reconstruction across diverse anatomical regions.[37]
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[39] This flap is distinguished by a dual vascular pedicle, typically with one extending vertically through the skin and the other traversing deep within the subcutaneous tissue toward the midaxillary line. Notably, for optimal inclusion of superficial lymphatic vessels and to minimize dissection while avoiding harm to the deeper lymphatic structures beneath the superficialis fascia, preference should be given to the pedicle ascending vertically into the skin over the one advancing deep toward the axillary line.[40] Understanding the lymphatic pattern and its axiality within the SCIP flap is crucial for the effective design of the contiguous skin island and its successful application and orientation.[21]
The aim of this present cross-sectional study was to evaluate and characterize the lymphatic patterns within the vascular territory of the SCIP flap. Lymphography using ICG was used to visualize the lymphatic channels and to assess the lymphatic drainage patterns specific to the SCIP area.[41]
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We assessed the bilateral lymphatic patterns of the SCIP zone at 4-, 14-, and 24-minute intervals after ICG lymphography injection. All injections were administered laterally, aligning with the study's protocol, which did not entail accessing the pedicle of the SCIP flap. Instead, the focus was on delineating the superficial lymphatics within the cutaneous island of the SCIP flap.
We found that most lymphatic vessels within the SCIP flap exhibited a trajectory toward the ILN, except in one volunteer the lymphatic vessels on the left side were observed to be directed opposite to the ILN. Furthermore, the number and length of lymphatic vessels observed increased over time, which indicated good uptake and transport of ICG dye through the lymphatic network. This underscores the importance of assessing the lymphatic pattern in the SCIP flap area preoperatively to ensure proper lymphatic flow.
The findings from this study provide valuable insights into the count, directional distribution, length, and flow dynamics of lymphatic vessels within the examined population. These results enhance our understanding of standard anatomy, possible variations, and their potential impact on lymphatic transport. Furthermore, these findings have significant implications for further research and clinical applications in diverse physiological and pathological scenarios, thereby enabling a deeper exploration of lymphatic function and its role in various contexts.
This study provides valuable insights into the superficial lymphatic patterns within the SCIP flap, consistent with the findings reported by Suami et al.43,
[44] Several studies have previously demonstrated the efficacy of using a simultaneous lymphatic flap in autologous breast reconstruction using the deep inferior epigastric artery perforator flap,[45]
[46] or the SCIP free flap including lymphatic vessels.[23] However, to date, insufficient information exists in the scientific literature to describe all lymphatic patterns in this area for the analysis before surgery.
This study is limited by the fact that only a small number of participants were involved, which makes reaching a standard anatomical conclusion difficult. In addition, the use of different infrared cameras in both hospitals may have influenced the overall sensitivity of lymphatic vessel detection. Moreover, ICG dye is constrained by its maximum visualization depth of up to 1.5 mm, although it was adequate for detecting superficial lymphatics in the SCIP zone. The lateral injection sites may limit visualization of certain medial lymphatics, but such visualization was beyond the scope of this study. Lastly, it is essential to clarify that the study's objective was not to deliberate on the indications of the LIFT flap, rather the focus of the study was to provide evidence that underscored the significance of the LIFT concept, which is predicated on the orientation and axiality of the superficial lymphatic vessels. Notably, the SCIP flap was presented as a representative example of a commonly employed flap for LIFT procedures.
Conclusion
This study delineates the superficial lymphatic pathway patterns within the SCIP flap zone, indicating its suitability for implementing the LIFT principle. These results underscore the significance of lymphatic axiality and compatible lymphatic patterns in accomplishing successful lymphatic flow restoration.
