Original Article
The “Octopus” Lymphaticovenular Anastomosis: Evolving Beyond the Standard Supermicrosurgical Technique Wei F. Chen, MD1
Takumi Yamamoto, MD2
Mark Fisher, MD1
1 Division of Plastic and Reconstructive Surgery, Department of
Surgery, University of Iowa Hospitals and Clinics, Iowa City, Iowa 2 Department of Plastic and Reconstructive Surgery, Graduate School of Medicine, University of Tokyo, Bunkyo-Ku, Tokyo, Japan
Junlin Liao, MD1
Jennifer Carr, MD1
Address for correspondence Wei F. Chen, MD, Division of Plastic and Reconstructive Surgery, Department of Surgery, University of Iowa Hospitals and Clinics, 200 Hawkins Drive, 1537 JCP, Iowa City, IA 52242-1086 (e-mail: [email protected]).
J Reconstr Microsurg 2015;31:450–457.
Abstract
Keywords
► supermicrosurgery ► lymphaticovenular anastomosis ► LVA ► lymphedema surgery
Background Supermicrosurgical lymphaticovenular anastomosis (LVA) is a promising treatment modality for lymphedema. However, its practice is restricted by the surgeon/ equipment-related factors, and its effectiveness limited by technical constraints. We conducted a pilot study to evaluate the feasibility of a modified “octopus” LVA technique in addressing the above problems. Method Nine consecutive lymphedema patients underwent LVA procedure using the “octopus” technique. Six had the upper extremity disease; three had the lower extremity disease. Except for one patient having primary lower extremity lymphedema, all had secondary disease related to cancer treatment. Disease severity ranged from Campisi stage Ib to IV. Qualitative and quantitative assessments were performed preoperatively, at 1, 3, and 6 months. Results A total of 130 lymphaticovenular drainage pathways were created in 39 “octopus” LVAs. All patients experienced prompt relief of lymphedema symptoms during the 1st postoperative week and continued to improve during the study period. None had postoperative complications. All had disease regression as demonstrated by statistically significant decrease in limb measurements (p ¼ 0.0003) and severity downstaging. The modified technique was found to be easier than the standard supermicrosurgical technique and could be performed using a standard surgical microscope. Conclusion The “octopus” technique is a viable, effective technical alternative to the standard LVA technique. It may greatly simplify this technically challenging procedure.
Supermicrosurgical lymphaticovenular anastomosis (LVA) is an advanced surgical modality for lymphedema treatment.1–5 Since the original description by Koshima et al1 its performance remains limited to the major academic centers due to the need for specialized expertise and equipment. The technical constraints of supermicrosurgery also prevent construction of a high number of LVA per case, and thereby limiting the surgical outcome.6–8 We conducted a pilot study to evaluate
received November 20, 2014 accepted after revision February 15, 2015 published online April 13, 2015
the feasibility of a modified “octopus” LVA technique to address the above problems.
Patients and Methods Nine consecutive patients who presented to University of Iowa Hospitals and Clinics for treatment of lymphedema underwent supermicrosurgical LVA with the modified
Copyright © 2015 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel: +1(212) 584-4662.
DOI http://dx.doi.org/ 10.1055/s-0035-1548746. ISSN 0743-684X.
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Patient
Gender
Age (y)
Extremity
Etiology
No. drainage pathways/ octopus LVA
Preoperative Campisi stage
Postoperative Campisi stage
Preoperative UEL/LEL
Postoperative UEL/LEL
p-Value
0.0003
1
F
46
Left arm
Secondary
7 in 4
II
Ia
129
121
2
F
50
Right arm
Secondary
6 in 3
IV
II
139
123
3
F
56
Right arm
Secondary
15 in 5
III
Ia
111
102
4
F
41
Right arm
Secondary
16 in 5
III
II
165
141
5
F
56
Left leg
Secondary
13 in 4
IV
II
312
281
6
M
50
Left leg
Primary
14 in 4
IV
II
378
352
7
F
54
Left arm
Secondary
19 in 6
III
II
135
116
8
F
52
Left arm
Secondary
13 in 4
Ib
Ia
133
129
9
F
56
Right leg
Secondary
27 in 4
II
Ia
254
243
Abbreviations: LEL, lower extremity lymphedema; F, female; M, male; UEL, upper extremity lymphedema.
“octopus” technique between January and April 2014 (►Table 1). Patient ages ranged from 41 to 56 years. Six had upper extremity lymphedema and three had lower extremity disease. Except for one patient having primary lower extremity disease, all had secondary disease related to cancer treatment. The disease severity was classified using the Campisi criteria9 (►Table 2). Indocyanine green lymphography was performed using SPY Elite system (LifeCell Corp., Bridgewater, NJ) to confirm the diagnosis of lymphedema. This was performed by injecting 0.1 mL of 0.25% indocyanine green (ICG) intradermally into the second and third web spaces of the hand or the first and second web spaces of the foot. The injected limb was scanned immediately to visualize the superficial lymphatic vessels (LVs) and at 6 hours following injection to visualize the pathologic dermal backflow patterns. All patients had at least 6 months of decongestive therapy without noticeable improvement before undergoing surgery. After surgery, all patients resumed limb compression for 3 months and discontinued afterward. Qualitative and quantitative assessments were performed before the surgery, at 1, 3, and 6 months postoperatively. Qualitative assessments included serial clinical evaluation
performed by the surgeon and a patient questionnaire (►Fig. 1), assessing the presence and the severity of symptoms of pain, stiffness, numbness, tightness, and functional compromise. Quantitative assessments were performed using the upper and lower extremity lymphedema (UEL and LEL) indices (►Fig. 2).10,11 The UEL and LEL indices combine circumference measurements from five different anatomic levels and the patient’s body mass index, and thus decreased intra- and interrater errors typically associated with the circumference measurement method.12
Surgical Technique ICG lymphography was performed as described above immediately before surgery to delineate the superficial lymphatic anatomy and to guide incision placements. The incisions were preferentially placed over where healthy “linear” lymphographic patterns were seen.13 When no such pattern was seen; the incisions were placed along the courses of the cephalic vein and the greater saphenous vein for upper and lower extremities, respectively. Around 0.1 mL of isosulfan blue (Lymphazurin; United States Surgical Corp., Norwalk, CT) was injected 2 cm distal to each incision to further facilitate identification of the LVs.
Table 2 Campisi staging system Campisi staging 1A
No overt swelling despite impaired lymph drainage
1B
Reversible swelling that subsides with limb elevation
2
Limb elevation only partially reduces swelling
3
Persistent edema; recurrent lymphangitis
4
Fibrotic lymphedema with column limb
5
Elephantiasis with limb deformation including widespread lymphostatic warts
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Table 1 Nine patients underwent LVA with the “octopus” technique during the recruitment period. All experienced disease regression, as demonstrated by the clinical disease down-staging. All demonstrated statistically significant decrease in lymphedema index
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Fig. 1 Qualitative assessments included serial evaluations performed by the surgeon and patient self-assessment questionnaire as the one shown here. The patient filled out the questionnaire before the surgery, at 1, 3, and 6 months postoperatively.
Dissection was performed through 2- to 4-cm incisions under 18 to 20 magnification with a surgical microscope (Pentero 900; Carl Zeiss, Oberkochen, Germany). Supermicrosurgical instruments (S&T Surgical, Neuhausen, Switzerland) were used for the vessel dissection and anastomosis. All the subdermal veins were carefully preserved. All the LVs of sufficient quality between the superficial and deep fasciae were skeletonized in preparation for anastomosis. The “octopus” LVA was performed as followed: Using 12–0 nylon, an out-to-in transluminal suture was placed through a vein of adequate caliber. After transversely grasping the adventitia of each individual LV, an in-to-out transluminal suture was placed through the vein to intussuscept all the LVs into the vein, forming an LVA complex, or an “octopus” (►Fig. 3). Placement of additional reinforcing sutures completed the anastomosis.
Results A total of 130 lymphaticovenular drainage pathways were constructed in 39 “octopus” LVAs. The diameters of the LV ranged from 0.2 to 0.9 mm. The diameters of the veins ranged from 0.4 to 1.8 mm. In all the cases, anastomotic patency was confirmed intraoperatively by observing the movement of lymph–blood interface across the anastomosis. When such movement was not observed, the anastomosis was taken down and redone. The mean operative time was 6.0 (range, 4.8–7.1) hours. The mean follow-up was 7.6 (range, 6–9) months. No patient developed postoperative complication. Journal of Reconstructive Microsurgery
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All were discharged on postoperative day 1. None developed worsening of lymphedema during the study period. All patients experienced prompt relief of lymphedema symptoms starting during the 1st postoperative week, and continued to improve during the entire study period (►Figs. 4 and 5). All experienced disease regression as demonstrated by statistically significant decreases (p ¼ 0.0003) (►Table 1) in the lymphedema indices. The disease regression was further supported by disease severity down-staging in all the patients—four became completely asymptomatic (Campisi stage Ia) and five only experienced mild, intermittent symptoms (Campisi stage II) at the conclusion of the study.
Discussion Supermicrosurgical LVA and microsurgical autologous lymph node transplants (ALNT) are two recently developed surgical modalities for treatment of therapy-refractory extremity lymphedema.14–17 The ALNT has gained a wider acceptance than the LVA because as a free tissue transfer procedure, it utilizes techniques and principles already familiar to microsurgeons. LVA, in contrast, requires the delicate supermicrosurgical technique18,19 and equipment that are not routinely available at most hospitals.3,20 Supermicrosurgical LVA is preferably performed under 25 to 50 magnification.1,3 Powerful magnification is a prerequisite to ensure safe suturing of the minuscule vessels. The microscopes used for the standard microsurgery are frequently insufficiently powered for LVA. The cost of a
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Fig. 2 Calculation of the UEL index. Measurements (in cm) are obtained at 5 cm above the olecranon (C1), at the olecranon (C2), at 5 cm below the olecranon (C3), at the wrist (C4), and at the dorsum of the hand (C5). The sum of the squares of these measurements is divided by the patient’s body mass index (BMI) to obtain the UEL index. For the lower extremity, measurements are taken at 10 cm above the superior edge of the patella, at the superior edge of the patella, and at 10 cm below the superior edge of the patella (C1, C2, C3), at the medial malleolus (C4), and at the foot dorsum (C5). UEL indices of < 130, 130 to 150, > 150 are considered early, intermediate, and advanced UEL, respectively. LEL indices of < 250, 250 to 300, > 300 are considered early, intermediate, and advanced LEL, respectively. LEL, lower extremity lymphedema; UEL, upper extremity lymphedema.
supermicrosurgery-friendly microscope may exclude many surgeons who would otherwise be interested in offering the procedure. The effectiveness of the LVA procedure is proportional to the number of LVAs, or the lymphatic drainage pathways, created.7,8,21,22 Multisurgeon approach had been employed to maximize the number of LVAs constructed per case.22 This approach, however, may not be economically feasible, especially when the procedure is undercompensated or not compensated at all by the insurance carriers due to the procedure being labeled as “experimental.” Economic consideration aside, a given institution may simply not have enough supermicrosurgery-trained surgeons to practice this approach.
Technical Constraints of the Standard LVA Technique Three technical constraints frequently encountered in an LVA procedure are as follows: (1) mismatch between the vein and LV calibers (►Fig. 6A); (2) mismatch between the numbers of
Chen et al.
vein and LV (►Fig. 6B); and (3) the available LVs are severely sclerotic and functionally poor (►Fig. 6C). While the caliber mismatches < 1:2 can be overcome with suture technique, anastomosis of a LV to a larger vein with higher venous pressure risks developing undesirable retrograde vein-tolymphatic flow, making the LVA ineffective. Caliber mismatches > 1:2 cannot be compensated for with suturing technique and we do not recommend performing LVA with these vessels as the risk of retrograde flow is high. The standard end-to-end LVA anastomotic configuration requires equal numbers of LVs and veins. Each LV needs one outflowing vein to establish an LVA. In the situation of differential numbers of LV and vein, the one with the lower quantity becomes the limiting factor, capping the maximal number of LVA possible. Although creative anastomotic configurations6,21,23–25 have been described to tackle this problem, all are more technically complex than the end-to-end anastomosis, making an already challenging procedure impractically challenging. The progressive pathological structural changes in the LV have been described previously.26,27 As lymphedema worsened, the LV wall progresses from initially being thin-walled and transparent, to opaque and thick-walled, and to eventually being sclerotic and having a severely compromised lumen. LVA constructed using qualitatively poor LV is likely to be ineffective, due to the weak lymphatic pressure unable to overcome the venous pressure. This explains the observation of LVA being ineffective in patients with advanced disease,4 as the LVs are likely to be compromised.
Technical Advantages of the “Octopus” Technique This pilot study suggests that the “octopus” technique is less technically demanding, and may address all the limitations of the standard technique described above. A similar technique was previously described by Campisi et al.9 The Campisi technique involves performing the LVA in the proximal limb using the relatively deep and large lymphatics. In addition, the perilymphatic areolar tissues are preserved and telescoped into the vein along with the LVs. In contrast, the “octopus” technique emphasizes (1) recruiting superficial and small LVs (typically < 0.5 mm), (2) thorough skeletonization of the LVs to create a more secured anastomosis, (3) exploring through multiple incisions to maximize the number of LVAs constructed, and (4) preferentially using the distal LVs as they tend be better preserved than the proximal LVs. We previously performed only the standard supermicrosurgical technique described by Koshima et al and Yamamoto et al.1,7,24 While we had success with the standard technique, its technical limitations prompted us to seek an alternative solution. We named the technique “octopus” due to the completed LVA resembling this invertebrate sea creature. The “octopus” technique was notably easier and required less time per anastomosis. The time saving was evident when we compared the operative times and the amount of the lymphatic drainage pathways created using the two different techniques. The need of a high-power microscope was also obviated since the technique does not require direct end-to-end coaptation of the lumens. We Journal of Reconstructive Microsurgery
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Fig. 3 (A) Dissection of the lymphatics and vein. Multiple lymphatic vessels and a single vein are selected for creation of the “octopus” LVA. (B) Division of the lymphatics and vein. The lymphatic vessels and the vein have been divided. All have been skeletonized and aligned in preparation for anastomosis. (C) Creation of anastomosis. A 12–0 nylon suture has been placed transluminally on the vein, and through the adventitia only on the lymphatic vessels. Placing the suture back transluminally through the vein will complete the suture loop and will intussuscept the lymphatic vessels into the vein. (D) Completion of the “octopus.” The lymphatic vessels have been intussuscepted into the vein. Additional reinforcing sutures have been placed. Washout is clearly identified in the vein in this image, indicative of the lymphatic pressure overcoming the venous pressure. LVA, lymphaticovenular anastomosis.
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were able to perform the technique comfortably using our standard surgical microscope that provided only 20 magnification. With this technique, a higher number of LVA or drainage pathways are feasible even with only one operating surgeon because, in contrast to the standard technique that demands only the use of healthy LVs, all the LV of sufficient quality can be recruited to build LVAs. Mihara et al described the sequential pathological changes in the LVs from being normal, to being ectatic, to being contracted, to finally being sclerotic.26 We found that the “octopus” LVA constructed using all except for the “sclerotic” LVs continued to demonstrate venous washout (antegrade movement of the lymph–blood inter-
Fig. 5 Image showing patient 5 who suffered from secondary Campisi stage IV left leg lymphedema. She had 13 LV drainage pathways created in four “octopi.” Her disease severity regressed to stage II and she experienced complete relief of pain and paresthesia associated with prolonged standing. LV, lymphatic vessel.
face). Particularly in the three patients with Campisi stage IV disease, majority of the “octopus” LVAs were constructed using the “ectatic” and “contracted” LVs. Although the mean number of drainage pathways per patient in the current study was only 14, we recently have been able to consistently construct over 20 drainage pathways per patient (►Fig. 7) with similar operative times, reflecting the surgeon moving forward on the learning curve. With the standard technique, we typically created –three to five drainage pathways per limb in similar operative time. A theoretical concern when such a high number of LVs is recruited to build LVA is worsening of the lymphatic drainage function. This was not observed in our series. We speculated that the reason might be the creation of a more effective “octopi” drainage pattern with the bundling of multiple individually suboptimal LVs that would not have drained properly anyway when left in continuity. The preoperative presence of the “linear” pattern during ICG lymphography is not a prerequisite for the performance of the “octopus” technique. The presence of the “linear” pattern indicates the presence of the healthy LVs. However, its absence does not indicate the absence of the healthy LVs. As demonstrated by Hara et al, healthy LVs continue to exist even in patients demonstrating severe pathological lymphographic patterns such as the “stardust” and the “diffuse” patterns, albeit in lower quantities.27 Two patients in this series, patients 5 and 6 failed to demonstrate “linear” pattern (►Fig. 8) but both went on to successfully receive LVA and experienced demonstrable postoperative improvements. The technical issues of caliber and number mismatches are no longer relevant because the technique by design utilizes differential calibers of LVs and veins in differential quantities. Interestingly, we observed a tendency of brisk venous washout after each anastomosis, even when the LVs were of suboptimal qualities. The washout occurred noticeably faster when compared with what we typically observed with the standard end-to-end anastomotic technique. We hypothesized that the collective lymphatic drainage of all the LVs, Journal of Reconstructive Microsurgery
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Fig. 4 Image showing patient 4 who suffered from postmastectomy Campisi stage III right arm lymphedema. She had 16 LV drainage pathways created in five “octopi.” Her disease severity regressed to stage II and she experienced complete relief of stiffness and paresthesia. LV, lymphatic vessel.
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Fig. 6 Technical limitations in standard LVA technique. These three images demonstrate the limitations associated with the standard technique. LVA constructed with the standard technique is either infeasible or ineffective when (A) the sizes of the lymphatic vessel and the vein do not match (left), (B) there are more lymphatic vessels than veins (center), or vice versa, and (C) the available lymphatic vessels are diseased and sclerotic (right). LVA, lymphaticovenular anastomosis.
although each suboptimal, created a stronger, more favorable LV-to-vein pressure gradient, and therefore the more effective drainage. We further hypothesized that, with the “octopus” technique, the LVA may remain a viable treatment modality even in patients with moderate-to-advanced disease, as was supported by the favorable responses of the three-stage IV patients in the series.
Considerations and Future Investigation
Fig. 7 The “octopus” technique facilitates creating a high number of LVAs or drainage pathways. A total of 23 LVAs was created in this patient. LVA, lymphaticovenular anastomosis.
Having demonstrated the feasibility of the “octopus” LVA technique, the next step would be to compare its efficacy with that of the standard technique. Furthermore, while our findings support the consensus that the effectiveness of the surgery correlates with the number of the lymphatic drainage pathways created, we were unable to identify a threshold of diminishing return due to the limited sample size. These will be investigated in our future studies.
Conclusion Our pilot study suggests the “octopus” technique to be a viable technical alternative to the standard LVA technique. It decreases the demand for expensive equipment, decreases the technical complexity of LVA, and allows LVA to be constructed in technically challenging situations.
Fig. 8 Intraoperative ICG lymphographic mapping of the superficial lymphatics in patient 5. The injection sites were rigorously massaged to promote lymphatic uptake. ICG signal concentrated at the injection sites. No “linear” pattern was seen in the foot dorsum and in the leg.
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Financial Disclosure None of the authors has a financial interest in any of the products, devices, or drugs mentioned in this article. Conflict of Interest None.
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Contributions Each person listed as an author has participated in the study to a significant extent.
Note This article represents an original contribution and has not been previously published.
14
15
16
References 1 Koshima I, Inagawa K, Urushibara K, Moriguchi T. Supermicrosur-
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novel severity staging system using dermal backflow patterns. Plast Reconstr Surg 2011;128(4):941–947 Lin C-H, Ali R, Chen S-C, 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):1265–1275 Gharb BB, Rampazzo A, Spanio di Spilimbergo S, Xu E-S, Chung K-P, Chen H-C. Vascularized lymph node transfer based on the hilar perforators improves the outcome in upper limb lymphedema. Ann Plast Surg 2011;67(6):589–593 Cheng M-H, Huang J-J, Nguyen DH, 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):93–98 Cheng M-H, Chen S-C, Henry SL, Tan B-K, Lin MC, Huang J-J. Vascularized groin lymph node flap transfer for postmastectomy upper limb lymphedema: flap anatomy, recipient sites, and outcomes. Plast Reconstr Surg 2013;131(6):1286–1298 Masia J, Olivares L, Koshima I, et al. Barcelona consensus on supermicrosurgery. J Reconstr Microsurg 2014;30(1):53–58 Chen WF, Eid A, Yamamoto T, Keith J, Nimmons GL, Lawrence WT. A novel supermicrosurgery training model: the chicken thigh. J Plast Reconstr Aesthet Surg 2014;67(7):973–978 Mihara M, Hayashi Y, Iida T, Narushima M, Koshima I. Instruments for supermicrosurgery in Japan. Plast Reconstr Surg 2012;129(2): 404e–406e Yamamoto T, Narushima M, Kikuchi K, et al. Lambda-shaped anastomosis with intravascular stenting method for safe and effective lymphaticovenular anastomosis. Plast Reconstr Surg 2011;127(5):1987–1992 Yamamoto T, Koshima I, Yoshimatsu H, Narushima M, Miahara M, Iida T. Simultaneous multi-site lymphaticovenular anastomoses for primary lower extremity and genital lymphoedema complicated with severe lymphorrhea. J Plast Reconstr Aesthet Surg 2011;64(6):812–815 Yamamoto T, Kikuchi K, Yoshimatsu H, Koshima I. Ladder-shaped lymphaticovenular anastomosis using multiple side-to-side lymphatic anastomoses for a leg lymphedema patient. Microsurgery 2014;34(5):404–408 Yamamoto T, Yoshimatsu H, Narushima M, et al. Sequential anastomosis for lymphatic supermicrosurgery: multiple lymphaticovenular anastomoses on 1 venule. Ann Plast Surg 2014;73(1): 46–49 Ayestaray B, Bekara F. π-Shaped Lymphaticovenular Anastomosis: The Venous Flow Sparing Technique for the Treatment of Peripheral Lymphedema. J Reconstr Microsurg 2014;30(8): 551–560 Mihara M, Hara H, Hayashi Y, et al. Pathological steps of cancerrelated lymphedema: histological changes in the collecting lymphatic vessels after lymphadenectomy. PLoS ONE 2012;7(7): e41126 Hara H, Mihara M, Seki Y, Todokoro T, Iida T, Koshima I. Comparison of indocyanine green lymphographic findings with the conditions of collecting lymphatic vessels of limbs in patients with lymphedema. Plast Reconstr Surg 2013;132(6):1612–1618
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The “Octopus” Lymphaticovenular Anastomosis
The “Octopus” Lymphaticovenular Anastomosis: Evolving Beyond the Standard Supermicrosurgical Technique Wei F. Chen, MD1
Takumi Yamamoto, MD2
Mark Fisher, MD1
1 Division of Plastic and Reconstructive Surgery, Department of
Surgery, University of Iowa Hospitals and Clinics, Iowa City, Iowa 2 Department of Plastic and Reconstructive Surgery, Graduate School of Medicine, University of Tokyo, Bunkyo-Ku, Tokyo, Japan
Junlin Liao, MD1
Jennifer Carr, MD1
Address for correspondence Wei F. Chen, MD, Division of Plastic and Reconstructive Surgery, Department of Surgery, University of Iowa Hospitals and Clinics, 200 Hawkins Drive, 1537 JCP, Iowa City, IA 52242-1086 (e-mail: [email protected]).
J Reconstr Microsurg 2015;31:450–457.
Abstract
Keywords
► supermicrosurgery ► lymphaticovenular anastomosis ► LVA ► lymphedema surgery
Background Supermicrosurgical lymphaticovenular anastomosis (LVA) is a promising treatment modality for lymphedema. However, its practice is restricted by the surgeon/ equipment-related factors, and its effectiveness limited by technical constraints. We conducted a pilot study to evaluate the feasibility of a modified “octopus” LVA technique in addressing the above problems. Method Nine consecutive lymphedema patients underwent LVA procedure using the “octopus” technique. Six had the upper extremity disease; three had the lower extremity disease. Except for one patient having primary lower extremity lymphedema, all had secondary disease related to cancer treatment. Disease severity ranged from Campisi stage Ib to IV. Qualitative and quantitative assessments were performed preoperatively, at 1, 3, and 6 months. Results A total of 130 lymphaticovenular drainage pathways were created in 39 “octopus” LVAs. All patients experienced prompt relief of lymphedema symptoms during the 1st postoperative week and continued to improve during the study period. None had postoperative complications. All had disease regression as demonstrated by statistically significant decrease in limb measurements (p ¼ 0.0003) and severity downstaging. The modified technique was found to be easier than the standard supermicrosurgical technique and could be performed using a standard surgical microscope. Conclusion The “octopus” technique is a viable, effective technical alternative to the standard LVA technique. It may greatly simplify this technically challenging procedure.
Supermicrosurgical lymphaticovenular anastomosis (LVA) is an advanced surgical modality for lymphedema treatment.1–5 Since the original description by Koshima et al1 its performance remains limited to the major academic centers due to the need for specialized expertise and equipment. The technical constraints of supermicrosurgery also prevent construction of a high number of LVA per case, and thereby limiting the surgical outcome.6–8 We conducted a pilot study to evaluate
received November 20, 2014 accepted after revision February 15, 2015 published online April 13, 2015
the feasibility of a modified “octopus” LVA technique to address the above problems.
Patients and Methods Nine consecutive patients who presented to University of Iowa Hospitals and Clinics for treatment of lymphedema underwent supermicrosurgical LVA with the modified
Copyright © 2015 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel: +1(212) 584-4662.
DOI http://dx.doi.org/ 10.1055/s-0035-1548746. ISSN 0743-684X.
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Patient
Gender
Age (y)
Extremity
Etiology
No. drainage pathways/ octopus LVA
Preoperative Campisi stage
Postoperative Campisi stage
Preoperative UEL/LEL
Postoperative UEL/LEL
p-Value
0.0003
1
F
46
Left arm
Secondary
7 in 4
II
Ia
129
121
2
F
50
Right arm
Secondary
6 in 3
IV
II
139
123
3
F
56
Right arm
Secondary
15 in 5
III
Ia
111
102
4
F
41
Right arm
Secondary
16 in 5
III
II
165
141
5
F
56
Left leg
Secondary
13 in 4
IV
II
312
281
6
M
50
Left leg
Primary
14 in 4
IV
II
378
352
7
F
54
Left arm
Secondary
19 in 6
III
II
135
116
8
F
52
Left arm
Secondary
13 in 4
Ib
Ia
133
129
9
F
56
Right leg
Secondary
27 in 4
II
Ia
254
243
Abbreviations: LEL, lower extremity lymphedema; F, female; M, male; UEL, upper extremity lymphedema.
“octopus” technique between January and April 2014 (►Table 1). Patient ages ranged from 41 to 56 years. Six had upper extremity lymphedema and three had lower extremity disease. Except for one patient having primary lower extremity disease, all had secondary disease related to cancer treatment. The disease severity was classified using the Campisi criteria9 (►Table 2). Indocyanine green lymphography was performed using SPY Elite system (LifeCell Corp., Bridgewater, NJ) to confirm the diagnosis of lymphedema. This was performed by injecting 0.1 mL of 0.25% indocyanine green (ICG) intradermally into the second and third web spaces of the hand or the first and second web spaces of the foot. The injected limb was scanned immediately to visualize the superficial lymphatic vessels (LVs) and at 6 hours following injection to visualize the pathologic dermal backflow patterns. All patients had at least 6 months of decongestive therapy without noticeable improvement before undergoing surgery. After surgery, all patients resumed limb compression for 3 months and discontinued afterward. Qualitative and quantitative assessments were performed before the surgery, at 1, 3, and 6 months postoperatively. Qualitative assessments included serial clinical evaluation
performed by the surgeon and a patient questionnaire (►Fig. 1), assessing the presence and the severity of symptoms of pain, stiffness, numbness, tightness, and functional compromise. Quantitative assessments were performed using the upper and lower extremity lymphedema (UEL and LEL) indices (►Fig. 2).10,11 The UEL and LEL indices combine circumference measurements from five different anatomic levels and the patient’s body mass index, and thus decreased intra- and interrater errors typically associated with the circumference measurement method.12
Surgical Technique ICG lymphography was performed as described above immediately before surgery to delineate the superficial lymphatic anatomy and to guide incision placements. The incisions were preferentially placed over where healthy “linear” lymphographic patterns were seen.13 When no such pattern was seen; the incisions were placed along the courses of the cephalic vein and the greater saphenous vein for upper and lower extremities, respectively. Around 0.1 mL of isosulfan blue (Lymphazurin; United States Surgical Corp., Norwalk, CT) was injected 2 cm distal to each incision to further facilitate identification of the LVs.
Table 2 Campisi staging system Campisi staging 1A
No overt swelling despite impaired lymph drainage
1B
Reversible swelling that subsides with limb elevation
2
Limb elevation only partially reduces swelling
3
Persistent edema; recurrent lymphangitis
4
Fibrotic lymphedema with column limb
5
Elephantiasis with limb deformation including widespread lymphostatic warts
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Table 1 Nine patients underwent LVA with the “octopus” technique during the recruitment period. All experienced disease regression, as demonstrated by the clinical disease down-staging. All demonstrated statistically significant decrease in lymphedema index
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Fig. 1 Qualitative assessments included serial evaluations performed by the surgeon and patient self-assessment questionnaire as the one shown here. The patient filled out the questionnaire before the surgery, at 1, 3, and 6 months postoperatively.
Dissection was performed through 2- to 4-cm incisions under 18 to 20 magnification with a surgical microscope (Pentero 900; Carl Zeiss, Oberkochen, Germany). Supermicrosurgical instruments (S&T Surgical, Neuhausen, Switzerland) were used for the vessel dissection and anastomosis. All the subdermal veins were carefully preserved. All the LVs of sufficient quality between the superficial and deep fasciae were skeletonized in preparation for anastomosis. The “octopus” LVA was performed as followed: Using 12–0 nylon, an out-to-in transluminal suture was placed through a vein of adequate caliber. After transversely grasping the adventitia of each individual LV, an in-to-out transluminal suture was placed through the vein to intussuscept all the LVs into the vein, forming an LVA complex, or an “octopus” (►Fig. 3). Placement of additional reinforcing sutures completed the anastomosis.
Results A total of 130 lymphaticovenular drainage pathways were constructed in 39 “octopus” LVAs. The diameters of the LV ranged from 0.2 to 0.9 mm. The diameters of the veins ranged from 0.4 to 1.8 mm. In all the cases, anastomotic patency was confirmed intraoperatively by observing the movement of lymph–blood interface across the anastomosis. When such movement was not observed, the anastomosis was taken down and redone. The mean operative time was 6.0 (range, 4.8–7.1) hours. The mean follow-up was 7.6 (range, 6–9) months. No patient developed postoperative complication. Journal of Reconstructive Microsurgery
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All were discharged on postoperative day 1. None developed worsening of lymphedema during the study period. All patients experienced prompt relief of lymphedema symptoms starting during the 1st postoperative week, and continued to improve during the entire study period (►Figs. 4 and 5). All experienced disease regression as demonstrated by statistically significant decreases (p ¼ 0.0003) (►Table 1) in the lymphedema indices. The disease regression was further supported by disease severity down-staging in all the patients—four became completely asymptomatic (Campisi stage Ia) and five only experienced mild, intermittent symptoms (Campisi stage II) at the conclusion of the study.
Discussion Supermicrosurgical LVA and microsurgical autologous lymph node transplants (ALNT) are two recently developed surgical modalities for treatment of therapy-refractory extremity lymphedema.14–17 The ALNT has gained a wider acceptance than the LVA because as a free tissue transfer procedure, it utilizes techniques and principles already familiar to microsurgeons. LVA, in contrast, requires the delicate supermicrosurgical technique18,19 and equipment that are not routinely available at most hospitals.3,20 Supermicrosurgical LVA is preferably performed under 25 to 50 magnification.1,3 Powerful magnification is a prerequisite to ensure safe suturing of the minuscule vessels. The microscopes used for the standard microsurgery are frequently insufficiently powered for LVA. The cost of a
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Fig. 2 Calculation of the UEL index. Measurements (in cm) are obtained at 5 cm above the olecranon (C1), at the olecranon (C2), at 5 cm below the olecranon (C3), at the wrist (C4), and at the dorsum of the hand (C5). The sum of the squares of these measurements is divided by the patient’s body mass index (BMI) to obtain the UEL index. For the lower extremity, measurements are taken at 10 cm above the superior edge of the patella, at the superior edge of the patella, and at 10 cm below the superior edge of the patella (C1, C2, C3), at the medial malleolus (C4), and at the foot dorsum (C5). UEL indices of < 130, 130 to 150, > 150 are considered early, intermediate, and advanced UEL, respectively. LEL indices of < 250, 250 to 300, > 300 are considered early, intermediate, and advanced LEL, respectively. LEL, lower extremity lymphedema; UEL, upper extremity lymphedema.
supermicrosurgery-friendly microscope may exclude many surgeons who would otherwise be interested in offering the procedure. The effectiveness of the LVA procedure is proportional to the number of LVAs, or the lymphatic drainage pathways, created.7,8,21,22 Multisurgeon approach had been employed to maximize the number of LVAs constructed per case.22 This approach, however, may not be economically feasible, especially when the procedure is undercompensated or not compensated at all by the insurance carriers due to the procedure being labeled as “experimental.” Economic consideration aside, a given institution may simply not have enough supermicrosurgery-trained surgeons to practice this approach.
Technical Constraints of the Standard LVA Technique Three technical constraints frequently encountered in an LVA procedure are as follows: (1) mismatch between the vein and LV calibers (►Fig. 6A); (2) mismatch between the numbers of
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vein and LV (►Fig. 6B); and (3) the available LVs are severely sclerotic and functionally poor (►Fig. 6C). While the caliber mismatches < 1:2 can be overcome with suture technique, anastomosis of a LV to a larger vein with higher venous pressure risks developing undesirable retrograde vein-tolymphatic flow, making the LVA ineffective. Caliber mismatches > 1:2 cannot be compensated for with suturing technique and we do not recommend performing LVA with these vessels as the risk of retrograde flow is high. The standard end-to-end LVA anastomotic configuration requires equal numbers of LVs and veins. Each LV needs one outflowing vein to establish an LVA. In the situation of differential numbers of LV and vein, the one with the lower quantity becomes the limiting factor, capping the maximal number of LVA possible. Although creative anastomotic configurations6,21,23–25 have been described to tackle this problem, all are more technically complex than the end-to-end anastomosis, making an already challenging procedure impractically challenging. The progressive pathological structural changes in the LV have been described previously.26,27 As lymphedema worsened, the LV wall progresses from initially being thin-walled and transparent, to opaque and thick-walled, and to eventually being sclerotic and having a severely compromised lumen. LVA constructed using qualitatively poor LV is likely to be ineffective, due to the weak lymphatic pressure unable to overcome the venous pressure. This explains the observation of LVA being ineffective in patients with advanced disease,4 as the LVs are likely to be compromised.
Technical Advantages of the “Octopus” Technique This pilot study suggests that the “octopus” technique is less technically demanding, and may address all the limitations of the standard technique described above. A similar technique was previously described by Campisi et al.9 The Campisi technique involves performing the LVA in the proximal limb using the relatively deep and large lymphatics. In addition, the perilymphatic areolar tissues are preserved and telescoped into the vein along with the LVs. In contrast, the “octopus” technique emphasizes (1) recruiting superficial and small LVs (typically < 0.5 mm), (2) thorough skeletonization of the LVs to create a more secured anastomosis, (3) exploring through multiple incisions to maximize the number of LVAs constructed, and (4) preferentially using the distal LVs as they tend be better preserved than the proximal LVs. We previously performed only the standard supermicrosurgical technique described by Koshima et al and Yamamoto et al.1,7,24 While we had success with the standard technique, its technical limitations prompted us to seek an alternative solution. We named the technique “octopus” due to the completed LVA resembling this invertebrate sea creature. The “octopus” technique was notably easier and required less time per anastomosis. The time saving was evident when we compared the operative times and the amount of the lymphatic drainage pathways created using the two different techniques. The need of a high-power microscope was also obviated since the technique does not require direct end-to-end coaptation of the lumens. We Journal of Reconstructive Microsurgery
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Fig. 3 (A) Dissection of the lymphatics and vein. Multiple lymphatic vessels and a single vein are selected for creation of the “octopus” LVA. (B) Division of the lymphatics and vein. The lymphatic vessels and the vein have been divided. All have been skeletonized and aligned in preparation for anastomosis. (C) Creation of anastomosis. A 12–0 nylon suture has been placed transluminally on the vein, and through the adventitia only on the lymphatic vessels. Placing the suture back transluminally through the vein will complete the suture loop and will intussuscept the lymphatic vessels into the vein. (D) Completion of the “octopus.” The lymphatic vessels have been intussuscepted into the vein. Additional reinforcing sutures have been placed. Washout is clearly identified in the vein in this image, indicative of the lymphatic pressure overcoming the venous pressure. LVA, lymphaticovenular anastomosis.
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were able to perform the technique comfortably using our standard surgical microscope that provided only 20 magnification. With this technique, a higher number of LVA or drainage pathways are feasible even with only one operating surgeon because, in contrast to the standard technique that demands only the use of healthy LVs, all the LV of sufficient quality can be recruited to build LVAs. Mihara et al described the sequential pathological changes in the LVs from being normal, to being ectatic, to being contracted, to finally being sclerotic.26 We found that the “octopus” LVA constructed using all except for the “sclerotic” LVs continued to demonstrate venous washout (antegrade movement of the lymph–blood inter-
Fig. 5 Image showing patient 5 who suffered from secondary Campisi stage IV left leg lymphedema. She had 13 LV drainage pathways created in four “octopi.” Her disease severity regressed to stage II and she experienced complete relief of pain and paresthesia associated with prolonged standing. LV, lymphatic vessel.
face). Particularly in the three patients with Campisi stage IV disease, majority of the “octopus” LVAs were constructed using the “ectatic” and “contracted” LVs. Although the mean number of drainage pathways per patient in the current study was only 14, we recently have been able to consistently construct over 20 drainage pathways per patient (►Fig. 7) with similar operative times, reflecting the surgeon moving forward on the learning curve. With the standard technique, we typically created –three to five drainage pathways per limb in similar operative time. A theoretical concern when such a high number of LVs is recruited to build LVA is worsening of the lymphatic drainage function. This was not observed in our series. We speculated that the reason might be the creation of a more effective “octopi” drainage pattern with the bundling of multiple individually suboptimal LVs that would not have drained properly anyway when left in continuity. The preoperative presence of the “linear” pattern during ICG lymphography is not a prerequisite for the performance of the “octopus” technique. The presence of the “linear” pattern indicates the presence of the healthy LVs. However, its absence does not indicate the absence of the healthy LVs. As demonstrated by Hara et al, healthy LVs continue to exist even in patients demonstrating severe pathological lymphographic patterns such as the “stardust” and the “diffuse” patterns, albeit in lower quantities.27 Two patients in this series, patients 5 and 6 failed to demonstrate “linear” pattern (►Fig. 8) but both went on to successfully receive LVA and experienced demonstrable postoperative improvements. The technical issues of caliber and number mismatches are no longer relevant because the technique by design utilizes differential calibers of LVs and veins in differential quantities. Interestingly, we observed a tendency of brisk venous washout after each anastomosis, even when the LVs were of suboptimal qualities. The washout occurred noticeably faster when compared with what we typically observed with the standard end-to-end anastomotic technique. We hypothesized that the collective lymphatic drainage of all the LVs, Journal of Reconstructive Microsurgery
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Fig. 4 Image showing patient 4 who suffered from postmastectomy Campisi stage III right arm lymphedema. She had 16 LV drainage pathways created in five “octopi.” Her disease severity regressed to stage II and she experienced complete relief of stiffness and paresthesia. LV, lymphatic vessel.
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Fig. 6 Technical limitations in standard LVA technique. These three images demonstrate the limitations associated with the standard technique. LVA constructed with the standard technique is either infeasible or ineffective when (A) the sizes of the lymphatic vessel and the vein do not match (left), (B) there are more lymphatic vessels than veins (center), or vice versa, and (C) the available lymphatic vessels are diseased and sclerotic (right). LVA, lymphaticovenular anastomosis.
although each suboptimal, created a stronger, more favorable LV-to-vein pressure gradient, and therefore the more effective drainage. We further hypothesized that, with the “octopus” technique, the LVA may remain a viable treatment modality even in patients with moderate-to-advanced disease, as was supported by the favorable responses of the three-stage IV patients in the series.
Considerations and Future Investigation
Fig. 7 The “octopus” technique facilitates creating a high number of LVAs or drainage pathways. A total of 23 LVAs was created in this patient. LVA, lymphaticovenular anastomosis.
Having demonstrated the feasibility of the “octopus” LVA technique, the next step would be to compare its efficacy with that of the standard technique. Furthermore, while our findings support the consensus that the effectiveness of the surgery correlates with the number of the lymphatic drainage pathways created, we were unable to identify a threshold of diminishing return due to the limited sample size. These will be investigated in our future studies.
Conclusion Our pilot study suggests the “octopus” technique to be a viable technical alternative to the standard LVA technique. It decreases the demand for expensive equipment, decreases the technical complexity of LVA, and allows LVA to be constructed in technically challenging situations.
Fig. 8 Intraoperative ICG lymphographic mapping of the superficial lymphatics in patient 5. The injection sites were rigorously massaged to promote lymphatic uptake. ICG signal concentrated at the injection sites. No “linear” pattern was seen in the foot dorsum and in the leg.
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Financial Disclosure None of the authors has a financial interest in any of the products, devices, or drugs mentioned in this article. Conflict of Interest None.
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Contributions Each person listed as an author has participated in the study to a significant extent.
Note This article represents an original contribution and has not been previously published.
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